HORTICULTURAL REVIEWS Volume 30
Horticultural Reviews is sponsored by: American Society for Horticultural Science
Editorial Board, Volume 30 Martine Dorais Wilhelmina Kalt Raphael Goren
HORTICULTURAL REVIEWS Volume 30
edited by
Jules Janick Purdue University
John Wiley & Sons, Inc.
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Contents Contributors Dedication: Dale E. Kester
ix xiii
Thomas M. Gradziel
1. Girdling: Physiological and Horticultural Aspects
1
R. Goren, M. Huberman, and E. E. Goldschmidt I. II. III. IV. V. VI.
Introduction Girdling Concepts and Techniques Girdling and Physiological Studies Endogenous Plant Hormones Girdling in Horticultural Practice Concluding Remarks Literature Cited
2. Irrigation Water Quality and Salinity Effects in Citrus Trees
2 7 12 16 19 25 26
37
Yoseph Levy and Jim Syvertsen I. II. III. IV. V. VI. VII.
Introduction Managing Salinity Experimental Methods in Salinity Research Physiological Responses Salinity and Biotic Stresses Benefits of Moderate Salinity Summary Literature Cited
38 39 49 55 68 70 72 72
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CONTENTS
3. Red Bayberry: Botany and Horticulture
83
Kunsong Chen, Changjie Xu, Bo Zhang, and Ian Ferguson I. II. III. IV. V. VI.
Introduction Botany Physiology Environmental Requirements Horticulture Concluding Remarks Literature Cited
4. Protected Cultivation of Horticultural Crops in China
84 87 96 99 101 110 111
115
Weijie Jiang, Dongyu Qu, Ding Mu, and Lirong Wang I. II. III. IV. V. VI.
Introduction The Energy-Saving Greenhouse Vegetable Crops Floriculture Fruit Trees Future Development of Protected Horticulture Literature Cited
5. Greenhouse Tomato Fruit Cuticle Cracking
116 121 126 141 149 158 159
163
Martine Dorais, Dominique-André Demers, Athanasios P. Papadopoulos, and Wim Van Ieperen I. II. III. IV. V. VI.
Introduction Fruit Characteristics Related to the Development of Cuticle Cracking Genetic Aspects of Fruit Resistance to Cuticle Cracking Climatic Factors Related to the Development of Cuticle Cracking Cultural Factors Related to the Development of Cuticle Cracking Conclusion Literature Cited
164 166 170 171 174 178 179
CONTENTS
vii
6. Fresh-Cut Vegetables and Fruits
185
Jeffrey K. Brecht, Mikal E. Saltveit, Stephen T. Talcott, Keith R. Schneider, Kelly Felkey, and Jerry A. Bartz I. II. III. IV. V. VI. VII.
Introduction Physiology Sensory Quality Phytonutrients Microbiology Treatments to Maintain Quality Conclusions Literature Cited
186 190 203 209 217 224 230 231
7. Postharvest Physiology and Storage of Widely Used Root and Tuber Crops
253
Uzi Afek and Stanley J. Kays I. II. III. IV. V.
Introduction Causes of Postharvest Losses Tuber Crops Root Crops Corm and Rhizome Crops Literature Cited
8. Metabolic Control of Low-Temperature Sweetening in Potato Tubers During Postharvest Storage
255 255 259 276 295 299
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R. W. Blenkinsop, R. Y. Yada, and A. G. Marangoni I. II. III. IV. V. VI. VII. VIII.
Introduction Starch Metabolism Sucrose Metabolism Glycolysis Oxidative Pentose Phosphate Pathway Mitochondrial Respiration Metabolic Factors Affecting Chip Color Development Conclusion Literature Cited
318 321 325 335 339 340 342 345 346
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9. Cassava-based Multiple Cropping Systems
355
V. Ravi and C. R. Mohankumar I. II. III. IV. V. VI. VII.
Introduction Growth and Productivity of Cassava Growth and Productivity of Associate Crops Intercropping Cassava Relay Sequential Cropping Cassava Multi-Cropping Management Conclusion and Future Prospects Literature Cited
356 361 374 394 417 420 460 463
Subject Index
501
Cumulative Subject Index
503
Cumulative Contributor Index
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Contributors Uzi Afek, Department of Postharvest Science of Fresh Produce, Agricultural Research Organization, Gilat-Agricultural Research Center, Mobile Post Negev 85280, Israel,
[email protected] Jerry A. Bartz, Plant Pathology Department, University of Florida, Gainesville, FL 32611-0680 R. W. Blenkinsop, Department of Food Science, University of Guelph, Guelph, ON, Canada, N1G 2W1,
[email protected] Jeffery K. Brecht, Horticultural Sciences Department, University of Florida, Gainesville, FL 32611-0690,
[email protected] Kunsong Chen, Department of Horticulture, Huajiachi Campus, Zhenjiang University, Hangzhou, 310029, P. R. China Dominique-André Demers, Agriculture and Agri-Food Canada, Greenhouse and Processing Crops Research Centre, Harrow, ON, Canada, N0R 1G0 Martine Dorais, Agriculture and Agri-Food Canada, Centre de Recherche en Horticulture, Université Laval, Ste-Foy, QC, Canada, G1K 7P4,
[email protected] Kelly Felkey, Food Science and Human Nutrition Department, University of Florida, Gainesville, FL 32611-0370 Ian B. Ferguson, The Horticulture and Food Research Institute of New Zealand, Private Bag 92 169, Auckland, New Zealand, Iferguson@ hortresearch.co.nz E. E. Goldschmidt, Kennedy-Leigh Centre for Horticultural Research, The Institute of Plant Sciences and Genetics in Agriculture, The Hebrew University of Jerusalem, P.O. Box 12, Rehovot, 76100, Israel Raffi Goren, Kennedy-Leigh Centre for Horticultural Research, The Institute of Plant Sciences and Genetics in Agriculture, The Hebrew University of Jerusalem, P.O. Box 12, Rehovot, 76100, Israel, rgoren@ agri.huji.ac.il Thomas M. Gradziel, Department of Pomology, University of California, Davis, CA 95616-8683,
[email protected] ix
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CONTRIBUTORS
M. Huberman, Kennedy-Leigh Centre for Horticultural Research, The Institute of Plant Sciences and Genetics in Agriculture, The Hebrew University of Jerusalem, P.O. Box 12, Rehovot, 76100, Israel Weijie Jiang, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, 12 Zhongguancun S. Street, Beijing, 100081, China,
[email protected] Stanley J. Kays, Department of Horticulture, The University of Georgia, Athens, GA, 30602-7273,
[email protected] Yoseph Levy, Agricultural Research Organization, Department of Fruit Tree Sciences, Gilat Research Center, Mobile Post Negev, 85-280, Israel,
[email protected] A. G. Marangoni, Department of Food Science, University of Guelph, Guelph, ON, Canada, N1G 2W1,
[email protected] C. R. Mohankumar, Central Tuber Crops Research Institute, Sreekariyam, Trivandrum, India, 695 017 Ding Mu, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, 12 Zhongguancun S. Street, Beijing, 100081, China Athanasios P. Papadopoulos, Agriculture and Agri-Food Canada, Greenhouse and Processing Crops Research Centre, Harrow, ON, Canada, N0R 1G0 Dongyu Qu, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, 12 Zhongguancun S. Street, Beijing, 100081, China V. Ravi, Central Tuber Crops Research Institute, Sreekariyam, Trivandrum, India, 695 017,
[email protected] Mikal E. Saltveit, Department of Vegetable Crops, University of California, Davis, CA, 95616-8631 Keith R. Schneider, Food Science and Human Nutrition Department, University of Florida, Gainesville, FL 32611-0370 Jim P. Syvertsen, University of Florida, IFAS, Citrus Research and Education Center, 700 Experiment Station Road, Lake Alfred, FL, 338502299,
[email protected] Stephen T. Talcott, Food Science and Human Nutrition Department, University of Florida, Gainesville, FL 32611-0370 Wim Van Ieperen, Horticultural Production Chains Group, University of Wageningen, Marijkeweg 22, 6709 PG, The Netherlands Lirong Wang, Zhengzhou Fruit Research Institute, Chinese Academy of Agricultural Sciences, Zhengzhou, Henan Province 450009, China
CONTRIBUTORS
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Changjie Xu, Department of Horticulture, Huajiachi Campus, Zhenjiang University, Hangzhou, 310029, P. R. China R. Y. Yada, Department of Food Science, University of Guelph, Guelph, ON, Canada, N1G 2W1 Bo Zhang, Department of Horticulture, Huajiachi Campus, Zhenjiang University, Hangzhou, 310029, P. R. China
Dale E. Kester
Dedication: Dale E. Kester
Volume 30 of Horticulture Reviews is dedicated to the productive career of Dale Emmert Kester, who has been a leader in pomological research and horticultural education at the University of California at Davis. Dale was born July 28, 1922, the third in a family of seven, and grew up on a self-supporting Iowa farm producing corn, small grain, alfalfa, pasture, vegetable gardens, and fruit orchards (apple, mulberry, black walnuts, sour cherry, plums, and seedling peaches). He still retains vivid memories of cultivating corn behind a team of horses, haying, shocking grain, picking corn by hand, and milking cows each morning and evening. Dr. Kester’s education included grade school at a rural school that included a daily walk of one mile between home and the school house and later, at high school in Audubon, Iowa. Early on, Dale developed a passion for birds, perhaps nurtured by the fact that the county in which he grew up, Audubon County, was an oasis for bird life of all kinds. His parents were conservative politically but very progressive in farming practices. They pioneered soil conservation practices and the use of improved seeds such as hybrid corn. They were also strong supporters of 4-H and Future Farmer programs, as well as Farm Bureau and Iowa State College sponsored programs. After High School, Dale spent a year as a farm worker both at a neighboring farm and at his parents’ farm. Then, with the help of a Sears and Roebuck scholarship, he entered Iowa State College in the Fall of 1941, majoring in Horticulture. He supported himself by working in the greenhouses of the Department of Horticulture at Ames, by waiting tables in the girls’ dormitory, and by summer work in the pea canneries in DeKalb, Illinois. During World War II, he joined the Air Force Reserve and was called into service in February 1943. He flew 28 missions, flying P-40s and P-51s, escorting bombers from Italy to Central Europe. Immediately after the war he returned to Iowa State to complete his degree. In July 1946, Dale married Daphne Dougherty, whom he met in Baton Rouge, Louisiana, during his Air Force training. They have two children, William Kester and Nancy Kester Baysinger, and three grandsons.
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DEDICATION: DALE E. KESTER
In December 1947, the Kesters moved to Davis, California, where he entered graduate school as a Masters Candidate in Pomology. Dr. Kester’s work consisted, in part, of collecting fruit samples of peaches, plums, and apricots for Dr. Claron Hesse, the newly hired plant breeder in the Department. His Ph.D. thesis examined the requirements of in-vitro peach embryo development following cotyledon removal. He was awarded a Ph.D. in Plant Physiology in June, 1951. At that time, Dale was hired by the Department of Pomology, UC Davis, as an Instructor in Pomology and a Junior Pomologist in the Experiment Station. Subsequently, he advanced to the rank of Assistant Professor, Associate Professor, and Professor in the College of Agriculture, with corresponding titles in the Experiment Station of Assistant Pomologist, Associate Pomologist, and Pomologist. Dale retired as emeritus Professor in 1991. Dr. Kester’s professional interests can be divided into three principal areas: the genetics and physiology of almond, the identification and characterization of clone degeneration with vegetative propagation, and teaching. The immediate requirement of the Pomology Departmental position was to take control of a long-term (1923–1948) almond breeding project that had existed previously as a cooperative project with the USDA. The University/USDA programs were separated in 1948, after two cultivars, ‘Jordanolo’ and ‘Harpareil’, were released in 1938. Although initially commercially successful, within five years the two cultivars both developed symptoms of a genetic disorder subsequently identified as noninfectious bud-failure. The prevalence of this disorder was so pronounced and widespread that commercial production of both cultivars was quickly abandoned. A further responsibility of the almond breeding project was to complete the evaluation of advanced selections and of the several thousands of almond seedlings from controlled crosses. ‘Davey’ was jointly released in 1953 from this project. A second program to develop a smaller-sized version of the major almond cultivar ‘Nonpareil’ led to the release of ‘Kapereil’ (1963) and ‘Milow’ (1975). While all three cultivars met the requirements for which they were selected, none became widely planted. This early experience convinced Dr. Kester that successful cultivar breeding depended upon a comprehensive understanding of the entire range of biological, cultural, and marketing characteristics of almond. His subsequent efforts to achieve this breadth of understanding has led to his recognition today as a world authority on almond genetics, culture, and improvement. Dr. Kester’s rootstock evaluation and selection programs also included studies on almond/Marianna plum incompatibility and the develop-
DEDICATION: DALE E. KESTER
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ment of peach × almond hybrids rootstocks. Three hybrid clones, ‘Hansen 2168’, ‘Hansen 536’, and ‘Nickels’ have been released, with the last two attaining important commercial use. In collaboration with statewide county extension personnel, a comprehensive system of cultivar evaluations in Regional Variety Trial plots was established throughout California. These have facilitated the more recent testing and introduction of new almond cultivars, including ‘Solano’, ‘Sonora’, ‘Padre’, and ‘Winters’. The identification of pollen incompatibility alleles was also carried out in a series of controlled hand-pollination studies replicated over a period of many years. The majority of established almond cultivars were shown to belong to a single family arising from natural crossings between the two principal founding cultivars: ‘Nonpareil’ and ‘Mission’ (syn. ‘Texas Prolific’). These studies, in turn, have served as the basis for subsequent molecular characterization of the pollen self-incompatibility factor in almond, making this species an important model for pollination studies in the Rosaceae. Transfer of self-fertility to almond from peach, Prunus mira, and later Prunus webbii was accomplished in related research. The extensive gene introgression involved in these transfers demonstrated that wild almond species originating in southwest Asia and southeast Europe could be valuable sources of new germplasm. Large numbers of interspecific hybrids and backcross breeding lines were also established. Studies were carried out on the inheritance of time of bloom, the correlations between bloom time and germination requirements, and heritability of numerous other almond genetic traits including pioneering work on isozyme analysis. A major effort begun in 1954 and continuing through the rest of Dr. Kester’s career was a series of genetic and physiological studies of noninfectious bud-failure. These eventually led to the critical distinction between the potential for occurrence and the actual level of phenotypic expression of this epigenetic disorder that increases with time and clonal age (cycles of propagation). Subsequent studies of clone variability within individual cultivars resulted in his strategies of clonal source selection for low bud-failure potential. Promising clonal sources (i.e., foundation sources for subsequent nursery vegetative propagation of true-to-type cultivars) were identified by a combination of individual tree source selection and subsequent vegetative progeny testing. In 1969, California’s clean tree stock program was thrown into turmoil because of the unexpected occurrence of early and severe noninfectious bud-failure in the Foundation Plant Material source of the principal almond cultivar ‘Nonpareil’ that accounts for half of the almond crop area in California and over half of the world’s production. The following years were dominated
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by genetic, physiological, and epidemiological research on this problem. Related research examined another clonal variability problem in ‘Mission’ involving nonproductivity in commercial nursery source material. By the time of retirement in 1991, new low bud-failure potential clone sources of essentially all almond cultivars except for ‘Carmel’ were identified and made available through the UC Foundation Plant Material Service. In addition, the protocols utilized in source maintenance had showcased procedures to stabilize low potentials for noninfectious bud-failure in individual clones, although this accomplishment was not recognized at the time. In 1989, a series of research initiatives in collaboration with department and extension colleagues not only detailed a comprehensive model for the development of noninfectious bud-failure in almonds, but also defined measures for its control. Key findings include the demonstration of the existence of two periods of seasonal dormancy in almond species; the discovery of an epigenetic, somaclonal decline of genes controlling high temperature summer dormancy, and the demonstration of predictable distribution patterns for this epigenetic factor following sexual and asexual reproduction. Nursery management practices introduced to control the resulting noninfectious bud-failure disorder include the identification and evaluation of elite source clone selections, and cultural management procedures for stabilizing source clones in subsequent propagations. Specific source clones developed by these methods account for approximately 70% of the 550,000 acres of almond presently planted in California. Dr. Kester has been a major professor to 16 M.S. and Ph.D. students and is remembered as a patient mentor whose keen insights and sanguinity were always available. He has published over 111 papers in refereed journals and conference proceedings, and has coauthored 76 reports. Dr. Kester’s first teaching assignment in the Department of Pomology was a course on Plant Propagation and he later taught General Pomology, Species and Environmental Aspects of Pomology Crops, and Nut Crops of California. In the early 1970s, Dr. Kester started a lifelong collaboration with Dr. Hudson Hartmann, who had also been teaching plant propagation. In 1979, this collaboration resulted in the preparation of a textbook, Plant Propagation, Principles and Practices. This publication has now gone through seven editions and has become the world standard text and reference in this field, having been translated into Spanish, Russian, and Italian. Following the death of Dr. Hartmann, Dr. Kester has coauthored later editions with Dr. Fred T. Davies and Dr. Robert L. Geneva, thus keeping this important reference current with emerging technologies.
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Dr. Kester helped found the Western Region of the International Plant Propagator Society, and he has served that organization in many capacities including Western Region President in 1997. He also served as the first Chair of the Propagation Working Group of the American Society of Horticultural Sciences. He has been a participant in many international symposia on almond, tissue culture, and breeding and has been recognized throughout the world for his expertise in those areas. In 1997, Dr. Kester became a fellow of the American Society for Horticultural Sciences, and in 1980 he received the Stark Award for pomological research. In recognition of his lasting contributions to pomological research and the education of horticulturalists throughout the world, he was honored as the Spencer Ambrose Beach Lecturer at Iowa State University in 1998. Dale Kester is truly a scholar and a gentleman who has devoted his life to science and who continues to contribute to horticultural progress in California and the world. Thomas M. Gradziel Department of Pomology University of California Davis, CA 95616-8683
1 Girdling: Physiological and Horticultural Aspects R. Goren, M. Huberman, and E. E. Goldschmidt* Kennedy-Leigh Centre for Horticultural Research The Institute of Plant Sciences and Genetics in Agriculture The Hebrew University of Jerusalem P.O. Box 12, Rehovot 76100, Israel
I. INTRODUCTION II. GIRDLING CONCEPTS AND TECHNIQUES A. Site of Girdling B. Morphology of the Girdle C. Damage D. Healing III. GIRDLING AND PHYSIOLOGICAL STUDIES A. Phloem Transport B. Assimilate Accumulation C. Translocation D. Source-Sink Investigations E. Flowering IV. ENDOGENOUS PLANT HORMONES V. GIRDLING IN HORTICULTURAL PRACTICE A. Rooting and Vegetative Growth B. Floral Induction and Juvenility C. Fruit Set D. Fruit Size E. Yield F. Fruit Maturity and Quality VI. CONCLUDING REMARKS LITERATURE CITED
*The valuable comments and suggestions for improvement of the manuscript by J. A. Barden, F. Bangerth, F. G. Dennis, and T. Robinson are gratefully acknowledged. Special thanks are due to J. Janick for his help with specific sections of the article. Horticultural Reviews, Volume 30, Edited by Jules Janick ISBN 0-471-35420-1 © 2004 John Wiley & Sons, Inc. 1
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R. GOREN, M. HUBERMAN, AND E. GOLDSCHMIDT
I. INTRODUCTION Farmers have practiced the use of girdling and related techniques in horticulture for thousands of years in order to increase crop production. Theophrastus (285 B.C.E.) refers to root pruning, girdling the stems, and driving iron pegs into the trunks of pear and other methods of “punishing trees” to hasten bearing. Girdling has been mentioned by Albertus Magnus (1193–1280), and is also described in a French apple growth manual from the 16th century (Spiegel-Roy 1976). In Maison Rustique (1616), the use of lead for pre-blossom girdling to improve both flowering and apple fruit quality is described (Janick 1972). An early mention of girdling can be also found in Shakespeare’s writings: . . . [We] at time of year Do wound the bark, the skin of our fruit-trees, Lest being over-proud in sap and blood, With too much riches it confound itself; . . . (Richard II, Act III, Scene IV, lines 57–60)
The culture of fruit trees is geared toward production of a high-value crop, integrating quantity and fruit quality. This is achieved by various techniques, including breeding, nutrition, pest control, and bioregulators as well as direct manipulations of the plant itself. Direct plant manipulations leading to the desired yield consist of two kinds of horticultural agrotechniques: (1) removal of certain tree organs (e.g., pruning, fruit thinning); and (2) interference with translocation between major tree organs (e.g., girdling, ringing, scoring [Table 1.1]; branch bending, which modifies auxin distribution, may be included in this second category). Fruit trees might be viewed as a system of sinks and sources (leaves, reproductive organs, and roots) interconnected via vascular organs (trunk, branches, scaffold roots). Girdling is basically an intervention in the phloem transport between canopy and roots, in an attempt to manipulate the distribution of photosynthate, mineral nutrients, and plant bioregulators. Girdling and similar techniques (Table 1.2) have also been used in physiological investigations of translocation processes in higher plant systems. Girdling has immediate and long-term effects, and local, as well as whole-plant, effects. Horticultural and physiological studies have addressed various direct and indirect aspects of girdling with numerous plant systems. The general response of the tree to girdling follows a wellknown pattern. Botanists have conducted many variations of girdling
1. GIRDLING: PHYSIOLOGICAL AND HORTICULTURAL ASPECTS Table 1.1.
3
A glossary for girdling and related techniques.
Cincturing
Cutting a very narrow wound completely around the trunk or target branch.
Girdling
A procedure by which a ring of bark (or, in some cases, bark and sapwood) is removed from the trunk or branch of a tree or a ligature is tied tightly.
Hacking or frilling
A single line of overlapping downward axe cuts, leaving a frill into which toxic materials may be poured.
Notching
A shallow cut into the wood directly above a bud.
Nicking
A shallow cut into the wood directly above a bud (Syn. to notching).
Ringing
A form of girdling in which a cut is made with a pruning knife or a similar instrument around the circumference of a trunk or branch, with or without removal of a ring of bark.
Scoring
A form of girdling in which a narrow cut is made with a pruning knife or a similar instrument around the circumference of a trunk or branch.
Strangulation
Depressing the bark of the trunk or branches using a steel wire.
Stripping
Peeling off a band of bark completely around the tree.
Wiring
Depressing of the bark of the trunk or branches using a steel wire (Syn. to strangulation).
experiments for over 200 years and the conclusions have been essentially the same. Namely, the primary effect is the blocking of the downward flow of photosynthetic products at the girdle, while water and mineral transport from roots to the canopy is not directly affected. The use of girdling in forestry and its implications has been discussed extensively by Noel (1970). Two main factors limit the extensive application of girdling: (1) difficulties related to determining the optimal timing and environmental conditions for each species and location; and (2) uncertainties concerning the effect of girdling on trees, and fear of causing severe or even lethal damage by single or repeated treatments. In spite of these reservations, girdling is widely used even today with grapes, citrus, apple, peach, and other fruit tree crops, mainly in order to improve fruit set, size, and quality (Tables 1.3 and 1.4). The development of other agrotechnical practices, such as growth regulator treatments, has not always provided an efficient substitute for girdling in commercial horticulture. There is a vast horticultural literature on girdling. The purpose of the present review, however, is to provide a conceptual analysis, pointing out areas of comprehension as well as gaps in current knowledge. We
4 Table 1.2.
R. GOREN, M. HUBERMAN, AND E. GOLDSCHMIDT Description of girdling techniques.z
Cincturing Girdling
Double girdling Guillotine girdling Ring-girdling Chemical girdling Hot girdling (Steam) Hot girdling (wax collar) Cold girdling
Hacking or frilling Notching Ringing
Scoring
Strangulation Stripping
Wiring
Cutting a very narrow wound completely around the trunk or target branch Complete removal of a bark cylinder, either narrow or wide, around the trunk or individual branches Usually in different sites of the tree Two opposing, deep horizontal chain-saw cuts made one-third the diameter of the tree trunk, separated vertically 20 cm Two opposing half-circle cuts on the trunk of the tree separated vertically 20 cm Painting a ring of chemical solution (i.e., of morphactin) around the trunk Encircling the petiole or stem by a flash of steam Hot wax (80–85°C) poured into a wooden collar sealed around the petiole A cold jacket applied around the petiole, cooled (1–3°C) by circulation of an ethanol/water mixture A single line of overlapping downward axe cuts, leaving a frill into which toxic materials may be poured Removing a piece of bark from directly above a bud, cut into the sapwood A form of girdling in which a cut is made with a pruning knife or a similar instrument around the circumference of a trunk or branch, with or without removal of a ring of bark Severing the bark tissue with a knife, by a single thin cut completely encircling the trunk, without removal of bark Depressing the bark using a steel wire, depth and tension as required Peeling off a band of bark completely around the tree. Synonymous with girdling, although it was pointed out that penetration of the sapwood might be involved Depressing the bark using a steel wire, depth and tension as required (synonymous to strangulation)
George et al. 1993 General literature
Winkler et al. 1974 Hoying and Robinson 1992 Hoying and Robinson 1992 Shulman et al. 1986 Moing et al. 1994 Goldschmidt and Huber 1992 Ntsika and Delrot 1986 Noel 1970
Hoying 1993 General literature
Powell and Howell 1985 Yamanishi et al. 1994 Kumar and Chhonkar 1974
Kim and Chung 2000
z A representative reference article is given for each technique; text of the table is not a quotation from the article.
1. GIRDLING: PHYSIOLOGICAL AND HORTICULTURAL ASPECTS
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Table 1.3. Effect of girdling on fruit yield (selected references). Intensity of response is indicated by number of (+) signs. Crop
Effect
Comments
Reference
Apple (Malus × domestica)
++ ++ +
Second and third years Reduced tree size Restricted tree growth
Greene and Lord 1983 Williams 1985 Wang and Zheng 1997
Avocado (Persea americana)
++ +++ +++
Increased no. of fruits/tree Increased no. of fruits/tree Reduced shoot growth
Hackney et al. 1995 Kohne 1992 Ibrahim and Bahlool 1979
Citrus (Citrus spp.)
+++ +++
Increased fruit set Decreased no. of fruits/tree the following year Increased no. of fruits/tree
Agusti et al. 1990 Huberman and Goren 1996
+++ ++ +++ ++
Increased fruit splitting
Koller et al. 2000 Monselise et al. 1981 Rabe et al. 1996 Tuzcu et al. 1992
Grape (Vitis vinifera)
+ ++ ++ +++
Mango (Mangifera indica)
+++ ++ ++
Reduction of vegetative growth
Leonardi et al. 1999 Maiti et al. 1981 Rabelo et al. 1999
Nectarine (Prunus persica)
++
Yields were enhanced both years by all ringing treatments Fruits from girdled trees were significantly larger at harvest
Agenbag et al. 1992b
++ Olive (Olea europaea)
++ + ++ ++
Peach (Prunus persica)
+++
Persimmon (Diospyrus spp.)
+++ ++ ++
+++ +++
Increased bunch weight Increased fruit mass Delayed ripening
Increased no. of panicles/ shoot, fruit/panicle
Young branches more responsive Larger fruit, reduced shoot growth Reduced shoots growth Consistently advanced harvest Doubled flowers Fewer and shorter lateral branches
Botiyanski et al. 1998 Jawanda and Vij 1973 Ramming and Tarailo 1998 Wolf et al. 1991
Wand et al. 1991a Barut and Eris 1993 Ben-Tal and Lavee 1985 Gezerel 1984 Lavee et al. 1983 Allan et al. 1993 Perez and Rodriguez 1987 Powell and Howell 1985 Aoki et al. 1977 Blumenfeld 1986 Hasegawa and Nakajima 1991
6 Table 1.4.
R. GOREN, M. HUBERMAN, AND E. GOLDSCHMIDT Effect of girdling on fruit quality (selected references).
Crop
Effects
Reference
Apple
Increase TSS and acidity, reduced Ca content Improved fruit color Improved fruit color
Arakawa et al. 1998
Reduced peel suberizing and uneven softening Various fruit parameters
Adato 1979
Citrus
Improved fruit color, TSS/acid Various fruit parameters Increased TSS/acid and sucrose
Peng and Rabe 1996 Simoes et al. 1999 Yamanishi 1995
Grape
Accumulation of anthocyanin Increased TSS Increased TSS and sugar/acid ratio Improved fruit color, dry matter, storage quality Improved fruit color, dry matter, storage quality Increasing dry matter and pulp color
El-Hammady and Abdel Hamid 1995 Jawanda and Vij 1973 Kim and Chung 2000 Kumar and Chhonkar 1974 Kumar and Chhonkar 1979 Simmons et al. 1998
Nectarine
Various fruit parameters Enhanced fruit coloring, early harvest Early ripening TSS, reduced in Ca content
Agenbag et al. 1992a Agusti et al. 1998 Vaio et al. 2001 Zhang 1997
Olive
Increased oil content
Proietti et al. 1999
Peach
Increased sugar content Increase in TSS and firmness Improved fruit color and TSS
Allan et al. 1993 El-Sherbini 1992 Yoshikawa 1988
Persimmon
Reduced no. of seeds/fruit, improved color Increase in TSS Improved fruit color and TSS
Hasegawa and Nakajima 1991 El-Shaikh et al. 1999 Hasegawa and Sobajima 1992
Avocado
Williams 1985 Wilton 2000
Trochoulias and O’-Neil 1976
intend to discuss practical and physiological aspects of fruit-tree girdling, and to evaluate the possible effects of girdling on various endogenous systems of fruit trees.
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II. GIRDLING CONCEPTS AND TECHNIQUES A series of synonymous, slightly overlapping terms can be found in the literature. Table 1.1 contains definitions of most girdling terms, mainly following the horticultural glossary of Soule (1985). Careful review of the literature indicates that slightly different meanings have been assigned to specific girdling terms by different authors. Nevertheless, throughout the present review, the terms used by the cited authors have been adopted. Table 1.2 lists the most frequently used girdling techniques in some detail. Some girdling instruments are pictured in Fig. 1.1. The various methods of girdling range from mechanical wounding techniques, through pressure by steel wires, to chemical girdling by application of morphactin solutions. Also, girdling has been used and is still being used in physiological investigations, mainly with herbaceous plants. In such studies, girdling is applied either to stems or to leaf petioles. One major technique used in physiological studies is heat girdling, which involves application of steam or a wax collar, causing phloem necrosis. A more delicate, non-damaging technique is cold girdling, which is discussed in detail in Section III. The type of girdling applied, especially its width, is very important and should be selected according to the desired effects (Krezdorn and Wiltbank 1968). Neither cambium nor deeper tissues should be damaged in regular horticultural girdling procedures (Noel 1970; Goren and Monselise 1971; Winkler et al. 1974; Jensen et al. 1975). Damage to the cambium prevents the formation of callus bridges over the exposed surface and xylem damage interferes with water and mineral supply to the canopy. Moreover, a cut in the xylem will prevent a complete recovery of the severed surface (Heinicke 1933; Winkler et al. 1974). Shulman et al. (1986) compared chemical (morphactin) and mechanical girdling (ringing) in grapevine and reported that neither method caused any visible damage in the year of treatment or in the following year. Using the criteria of berry size and total soluble solids (TSS) accumulation, Shulman et al. (1986) concluded, nevertheless, that chemical girdling was generally less effective than mechanical girdling. A. Site of Girdling The question often arises whether girdling of the trunk and girdling of the main branches have identical effects. In grape, cane girdling gave better results than arm or trunk girdling (Bhujbal and Chaudhari 1973) but, in general, all sites of girdling give comparable results. The susceptibility
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R. GOREN, M. HUBERMAN, AND E. GOLDSCHMIDT
Fig. 1.1. Girdling instruments. A. “The Great Girdler©”, produced by Juran Works Ltd. Rishon LeZion, Israel, adapted from the original instrument developed by the late Dr. A. Cohen, Volcani Center, Israel. B. “Spanish” girdling scissors.
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9
of the tree to girdling must, however, be taken into account. Whenever there is a danger of causing severe damage to the tree, girdling should be applied to the main limbs, and one or two limbs should be left ungirdled (Krezdorn and Brown 1970; Lahav et al. 1971). This part-tree girdling prevents root starvation and reduces potential damage. In shy-bearing avocado trees, the common practice is to girdle only half of the limbs every year (Lahav et al. 1971). B. Morphology of the Girdle Classical botanical literature describes the morphology of the girdle and its healing. As mentioned above, girdling basically consists of a cut through the phloem; in most cases it involves the removal of a strip of bark from the circumference of the trunk or scaffold branch (Schneider 1954 and Fig. 1.1). For a schematic illustration of the anatomy of the girdle, see Fig. 1.2. Morphological responses to girdling were observed in
Fig. 1.2. Schematic illustration of a girdle, cutting through the bark in the trunk of a citrus tree (after Schneider 1954).
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R. GOREN, M. HUBERMAN, AND E. GOLDSCHMIDT
citrus (Schneider 1954) and peach (Schneider 1945) in the trunk both above and below the girdle and in the roots below the girdle. Degeneration of sieve tubes and companion cells was accompanied by hypertrophy near the girdle (4 cm), followed by similar damage further from the wound (Schneider 1954). Phloem degeneration appeared within two weeks when girdling was performed in July but only after nine months when done in October (Schneider 1954). Another factor to be considered is the width of the ring. A ring of 3 mm caused partial death of summer branches in pistachio because the closing rate of the girdled area was too slow (Crane and Nelson 1972). Scoring was significantly less effective for increasing grape berry weight than 4.8 mm wide girdling (Jensen et al. 1981). Girdles up to 5 mm in width did not damage Shamouti orange trees treated at five dates during the year (Wallerstein et al. 1973). As a rule, a wider ring provides a more prolonged effect, but increases the risk of damage to the tree (Fernandez-Escobar et al. 1987). Relatively wide ringing should therefore be applied only to strong and vigorous trees that are capable of surviving the treatment (Krezdorn and Brown 1970; Goren and Monselise 1971; Lahav et al. 1971; Cohen et al. 1972). C. Damage Growers often regard girdling as a dangerous technique; indeed, damage or even the death of trees is occasionally observed. Sometimes, the growth of the trunk and the overall development of the tree may be retarded even though no external damage is apparent (Shamel and Pomeroy 1944; Winkler et al. 1974). The most common symptom of damage is leaf chlorosis, followed by leaf drop, which may occur even several months after girdling (Noel 1970). The rate of leaf drop determines the ability of the tree to recover. If leaf drop is intensive, the tree degenerates rapidly. Girdling damage is more pronounced in cases where the trees are weak and are grown under unfavorable conditions (Goren and Monselise 1971). Wounding can induce ethylene evolution and/or resin secretion. In some cases, the damage in the girdled area is related to diseases, mostly virus diseases (Krezdorn and Brown 1970). In extreme cases, branches dry up and the whole tree collapses (Lahav et al. 1971; Cohen et al. 1972). Root starvation is a serious problem when a complete trunk girdle is performed. In young citrus seedlings, the respiration rate of roots decreased immediately after girdling, accompanied by a gradual decrease in starch content of the main roots (Wallerstein et al. 1978a). Nematode-induced ethylene evolution may play a role in root damage
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and pathogenesis (Glazer et al. 1984). The most serious damage is done by the larvae, which bore into the bark and along the cambium of roots and often cause girdling of single roots or even the root collar (Kozlowski 1973). Trees can be severely injured or even killed if their trunks, taproots, or large lateral roots are partially encircled by other roots so that movement of water and nutrients through them is severely impeded or cut off. The strangling effect, similar to that caused by a wire tied tightly around a branch and left for a few years, does not cause sudden death, but results in deterioration evidenced over a period of a few years by weak growth and dying back of branches that normally would be supplied by the girdled root. Excess accumulation of carbohydrates in the canopy has been observed in girdled citrus and apple trees (Schaffer et al. 1986; Nii 1989). The damage due to excess carbohydrates is particularly striking in the absence of fruits or other sinks in the canopy. Ultrastructural studies indicated that leaf chlorosis, which is typically observed under these conditions, results from an unusual increase in the size of starch granules, causing a degeneration of the chloroplasts (Schaffer et al. 1986; Nii 1992). Additional causes of damage may be associated with disturbance of bi-directional transport of plant hormones, nutrients, and metabolites. D. Healing Healing of the wound and reestablishment of regular contact between root and canopy is critical for the future of the branch or tree. Healing consists of the regeneration of the vascular connection, which depends on cambial activity. For this reason, special care should be exercised to avoid any damage to the cambium. Persistence of effect of girdling depends on the length of time required for the formation of new callus bridges across the ring. New callus is formed at the margin of the cut surface, spreading gradually over the entire exposed surface (Sharples and Gunnery 1933). In peach, callus growth from the upper edge of the girdle downward was most prominent (Dann et al. 1985). In apple, very little callus is formed on the distal end of the girdle. The cambium begins to develop in this callus. Callus cells change into cambial cells wherever the intact vascular cambium impinges upon them. Thus, the callus cambium differentiates from all margins of the wound toward the center, the process being comparable to the closing of a diaphragm (Esau 1953). The new vascular cambium forms xylem and phloem in continuity with the same tissues in the uninjured portion of the stem. A periderm develops in the outer portion
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R. GOREN, M. HUBERMAN, AND E. GOLDSCHMIDT
of the callus in line with the original stem periderm, if present (Sharples and Gunnery 1933). In citrus, the new callus bridges are formed about three weeks after ringing, at the time when the respiration level starts to recover and the decrease in starch level ceases (Wallerstein 1976). In grapes, callus bridges start to develop 16 days after ringing and a few days later phloem elements can already be detected in the callus (Sidlowski et al. 1971). In sugar maple, the rate of xylem and phloem element formation in the cambium surface of the girdled area depends on the season at which trees were girdled (Evert et al. 1972). Since differentiation of vascular elements in the callus depends on cambial activity, it takes longer for elements to form when girdling is performed during dormancy than when it is applied at a time of high cambial activity. It is advisable, therefore, whenever possible, to girdle during periods of intensive growth, when the time required for the formation of callus bridges is relatively short. Humidity is another factor that determines the rate of recovery. Wrapping the girdle with plastic strips can control humidity. If the cambium is not allowed to dry out, it should immediately start to produce callus and replace the phloem.
III. GIRDLING AND PHYSIOLOGICAL STUDIES A. Phloem Transport Girdling has been used for decades, and is still being used, as a major tool in physiological studies of translocation and source/sink relationships. This includes immediate, short-term as well as long-term effects (Curtis and Clark 1950). The main problems investigated using girdling techniques are phloem transport, metabolite distribution, and photosynthesis of source leaves. The preferable technique in physiological studies is “cold girdling” that consists of cooling of the stem or the petiole. Cold girdling causes a transient block of phloem transport without physical damage, unlike mechanical and heat girdling (Neales and Incoll 1968). Some investigators used temperatures of 1° to 3°C (Swanson and Geiger 1967; Ntsika and Delrot 1986), while others used temperatures up to 5°C (Krapp and Stitt 1995). Temperatures above 7°C are considered ineffective (Neales and Incoll 1968). A one- to three-centimeter length of petiole or stem was usually exposed to the low temperature treatment (Swanson and Geiger 1967; Ntsika and Delrot 1986; Krapp and Stitt 1995). In cold girdle of sugar beet, following the immediate decrease of transport there is a gradual recovery of transport, even while the stem
1. GIRDLING: PHYSIOLOGICAL AND HORTICULTURAL ASPECTS
13
is being cooled. Such rapid reversal of low temperature transport inhibition may not apply to all plant species (Swanson and Geiger 1967). Cold girdling is the major method enabling direct study of the translocation processes per se. Inhibition of translocation apparently results from physical blockage of sieve plates rather than from inhibition of metabolic processes (Giaquinta and Geiger 1973). When cold girdling blocked the export of photosynthates, Gamalei et al. (2000) reported that in coleus, cucurbits, pea, and sunflower the endoplasmic reticulum of intermediary cells collapsed, and the vacuoles of transfer cells enlarged. These changes were accompanied by starch accumulation in the mesophyll cells of all species studied. The condensation of the cytosol observed in the transfer cells (reminiscent of plasmolysis) was probably an osmotic response to cold girdling in the case of symplastic species. The possibility that cold-induced callose formation in the sieve plates is involved in blocking transport has been ruled out in sugar beet and bean (Swanson and Geiger 1967). B. Assimilate Accumulation One of the best-known effects of girdling is the accumulation of assimilates above the girdle (Mason and Maskell 1928; Ticho 1963; Greene 1937; Engard 1939; Murneek 1941; Weaver and McCune 1959; Zimmermann 1960; Stoltz and Hess 1966; Plaut and Reinhold 1967; Amir and Reinhold 1971; Little and Louch 1973; Wallerstein et al. 1974; Goldschmidt et al. 1985; Mataa et al. 1998). Assimilates may accumulate directly above the girdle, but generally increased levels of carbohydrates can be found throughout the canopy (Weaver and McCune 1959). Leaves that are the primary source organ store large amounts of carbohydrates, since their export is inhibited for a relatively long period (Engard 1939). Increased carbohydrates levels in the leaf are often associated with reduced photosynthesis. Trunk girdling of grapevine reduced the net CO2 assimilation rate by approximately 30%, and increased stomatal resistance, as compared with ungirdled control, 13 days after treatment. The reduction of photosynthetic rates due to girdling was smaller when vines were also sprayed with GA3 (Harrell and Williams 1987). Foliar carbohydrates were higher in girdled vines four weeks after the girdling treatment was imposed and, concomitantly, root carbohydrate concentrations were lower than in the untreated control (Roper and Williams 1989). Accumulation of sucrose and starch has been detected within 30 min. in heat-girdled bean leaves (Ntsika and Delrot 1986) and a rise in apoplastic sucrose within 60 min. (Ntsika and Delrot 1986; Voitsekhovskaja et al. 2000). Sorbitol, which is a major storage carbohydrate in woody Rosaceae
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R. GOREN, M. HUBERMAN, AND E. GOLDSCHMIDT
(Wallaart 1980), accumulated within 60 min. in steam-girdled peach leaves (Moing et al. 1994). Longer response times (several hours or even days) may be expected when branch or trunk girdling is employed. The accumulation of those assimilates in the leaves apparently results from inhibition of phloem loading (Ntsika and Delrot 1986; Voitsekhovskaja et al. 2000). According to Jordan and Habib (1996), girdling of three-year-old peach seedlings mainly affected the accumulation of insoluble carbohydrates (starch?) in leaves and shoots above the girdle and their depletion in roots and rootstock-trunk bark. Soluble carbohydrate levels were not significantly affected, above or below the girdle. In a subsequent study, Jordan et al. (1998) showed that girdling strongly reduced nitrogen uptake in peach to 19% of that of non-girdled trees. However, almost all absorbed nitrate was reduced in the roots in both the girdled and non-girdled trees. They suggest that nitrogen uptake is strongly dependent on the continuous supply of photosynthates from shoots to the roots and that girdling modifies the nitrogen balance at the whole plant level. Girdling affected the activity of key enzymes involved in carbohydrate metabolism of the growing apple fruit (Beruter et al. 1997). When fruit-bearing wood was girdled during the period of active starch synthesis, sucrose and sorbitol content declined to 20–30%. Fructose concentration was unaffected and starch level decreased continuously with a concomitant rise in glucose content. Girdling increased the activities of hexokinase, fructokinase, phospho-fructo-phospho-transferase, and pyruvate kinase, suggesting that girdling activates glycolysis as a means of meeting the increased energy requirements (Beruter et al. 1997). C. Translocation Even with a mechanical girdle, certain components of translocation may by-pass the girdle. A study of the translocation of sucrose in one-yearold sour orange seedlings revealed two transport systems that responded differently to girdling. One is responsible for the slow (mass-flow) transport of sucrose in the phloem and is affected by girdling. The other is very rapid (2,040 m/hr), involves a minor amount of sucrose, and is unaffected by girdling (Wallerstein et al. 1978b). In the first, slow system, assimilates accumulate in the leaves as a result of girdling. Several hours later, assimilates start to migrate from the leaves and their accumulation is evident throughout the canopy (Wallerstein 1976; Wallerstein et al. 1978b). In mature trees, this is probably the system responsible for the beneficial effect of girdling on the reproductive organs. The other, rapid system supplies constant, although small, quantities of assimilates to the root during the immediate period after girdling. This movement is influ-
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15
enced by water tension, and might be related to movement on molecular surfaces (Hardy and Possingham 1969; Wallerstein et al. 1978b). Assimilates carried in the fast transport system appear to by-pass the girdled area. Experiments involving the application of 14C-sucrose to leaves revealed no differences in levels of radioactivity in the roots of girdled vs. non-girdled plants, supporting the assumption that girdling does not inhibit transport via the fast system (Wallerstein et al. 1978b). Assimilates in the form of sugars, glutamine and malic acid are known to bypass the girdle via the xylem in grapes (Harel and Reinhold 1966; Hardy 1969). In annual plants, too, sugars are capable of by-passing girdled areas (Zucconi et al. 1980), indicating that this ability is widespread in the plant kingdom. This is further demonstrated by a study of Stebbins and Dewey (1972), designed to determine the role of xylem and phloem in the accumulation of calcium in leaves. Girdling of apple seedlings indicated that the phloem was the primary route of 45Ca translocation. However, calcium appeared to leak into the xylem at increasing rates in the young stem and near the growing apex. D. Source-Sink Investigations The interruption of phloem transport and the ensuing accumulation of assimilates further influences the activity of source leaves. Girdling has been instrumental in attempts to verify the “sink feedback inhibition of photosynthesis” hypothesis (Neales and Incoll 1968). Girdling of grapevines eliminates the roots as a sink for assimilates, leading to assimilate build-up in leaves and causing a consistent reduction in photosynthesis (Kriedemann and Lenz 1972; Harrell and Williams 1987). Sink feedback inhibition builds up gradually following carbohydrate accumulation. Excess carbohydrates may interfere with photosynthesis through several mechanisms: (1) enlarged starch granules damaging the chloroplasts (Schaffer et al. 1986); (2) closure of stomata (Goldschmidt and Huber 1992); (3) accumulation of phosphorylated intermediates and depletion of inorganic phosphate (Krapp and Stitt 1995); and (4) indirect action by repressing the expression of genes that encode proteins needed for photosynthesis (Krapp and Stitt 1995). In a study aimed to explore the effect of crop load and girdling on apple fruit and leaf characteristics (Schechter et al. 1994a,b), fruit on mature girdled trees had higher dry weight and dry-matter concentration than fruit on nongirdled trees. In fruiting trees, leaves on girdled limbs had slightly lower photosynthetic rates but, in nonfruiting trees, leaves of the girdled limbs had 70% lower photosynthetic rates, high stomatal resistance, and high leaf internal CO2 concentration. The authors concluded, nevertheless,
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R. GOREN, M. HUBERMAN, AND E. GOLDSCHMIDT
that the results do not necessarily support the concept of feedback inhibition of photosynthesis, and propose alternative explanations for the relationship between leaf activity and excessive carbohydrate accumulation in leaves. Similar conclusions were reached by Harrell and Williams (1987) in a study of girdling-induced depression of photosynthesis in grapevine. It may still be argued, however, that the data of these studies are best interpreted through the “feedback inhibition of photosynthesis” concept. Girdling is also used in long-term source/sink experiments in fruit trees, as a means for isolating a fruit-bearing branch from the rest of the tree (Fishler at al. 1983; Bustan et al. 1995; Laing and Clark 1996). Such an experimental system has also been used for modeling of fruit development (Genard et al. 1998; Lescourret et al. 1998). E. Flowering The elusive florigen, nowadays more often called “floral stimulus,” is believed to move via the phloem. Girdling has been used extensively in flowering research, as a means for interrupting the movement of the floral stimulus, as well as for determination of the precise timing and velocity of this movement (Lang 1965). Among fruit trees, girdling has been most frequently used with mango, to demonstrate the role of leaves in supplying the floral stimulus (Reece et al. 1949; Davenport and Nunez-Elisea 1997). In a recent study of flowering in Sinapis alba, Havelange et al. (2000) showed that girdling interfered with the movement of sucrose into roots and at the same time reduced the export of cytokinins from the roots to the shoots. Girdling seems therefore to remain an efficient tool for physiological studies in both herbaceous and perennial plants.
IV. ENDOGENOUS PLANT HORMONES Girdling-induced interruption of phloem transport should affect not only assimilates but also other organic compounds. Among these, plant hormones may be of special interest since they are known to play regulatory roles in various processes of growth and development. Changes in the distribution of plant hormones may therefore be anticipated, as well as effects on their biosynthesis in distant organs. Contrary to the rather consistent horticultural effects of girdling (promotion of floral induction, fruit set and enlargement, fruit quality, yield), the picture
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emerging from girdling-related endogenous hormone studies is fragmentary and somewhat confusing. Dann et al. (1985) found in peach a transient accumulation of IAA above the girdle, that peaked within 24 hr after girdling. This might be causally related to the often-observed thickening of the branch above the girdle (Chalmers 1985; Dann et al. 1985). Girdling-induced thickening of the branch above the girdle of a young citrus tree is shown in Fig. 1.3. In addition, Dann et al. (1984) suggest that lower cytokinin and/or gibberellin synthesis/activation by the roots may be a secondary effect of
Fig. 1.3. Thickening of the branch above the girdle of a young ‘Murcott’ tangerine hybrid citrus tree.
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R. GOREN, M. HUBERMAN, AND E. GOLDSCHMIDT
girdling, resulting from the diminished supply of phloem-borne substances to the roots. This hypothesis was substantiated by Cutting and Lyne (1993). They found a significant reduction in the concentration of the cytokinin, zeatin-riboside, and gibberellin A1 and A3 in the xylem sap of peach shoots above the girdle that persisted for 7 weeks, and a corresponding reduction in shoot growth. Trunk girdling of apple trees at full bloom also reduced the content of zeatin riboside above the girdle (Skogerbo 1992). A similar decrease in cytokinins above the girdle was found by Skene (1972) in grape vine shoots and by Havelange et al. (2000) in Sinapis alba. These observations presumably indicate a depression of hormone biosynthesis in roots, which might be associated with carbohydrate depletion and reduced root growth. Weaver and Pool (1965) reported an increase of gibberellin-like substances in some fractions of grape berry extracts in girdled vines, while other fractions showed a decrease. Trunk girdling of citrus trees induced an increase of gibberellin-like substances in bark and leaves above the ring (Goren et al. 1971). On the other hand, Wallerstein et al. (1973) found a decrease in gibberellin-like substances in young citrus fruitlets above the girdle. In a seasonal study, ringing caused in most cases an increase in gibberellin-like substances in new lateral shoots, while the opposite trend was found in rootlets. Attempts to establish a relationship between citrus’s floral induction and endogenous IBA, IAA, ABA, and gibberellins in leaves of ringed branches did not lead to conclusive results (Koshita et al. 1999). Various modes of girdling had little effect on the distribution of endogenous ABA in grape vines (During 1978). Girdling reduced IAA and ABA levels in sitka spruce branches (Little and Wareing 1981). Girdling reduced the level of auxin above the girdle in hibiscus (Stoltz and Hess 1966). Dann et al. (1985) reported that girdling did not entirely deplete the IAA immediately below the girdle; it reduced it by 75% and severely reduced growth and cell division of the cambium. The decrease in IAA concentration below the girdle strongly indicated that girdling interrupts the basipetal transport of auxin (Little and Wareing 1981; Dann et al. 1985). Wilson (1968) reported an increase in radial cell number in white pine up to 310 cm above the girdle. He suggested that this might be explained by the effect of girdling in blocking the polarized auxin transport as well as the non-polarized phloem transport system. Girdling of nectarine trees two weeks before pit hardening increased the rate of endogenous IAA accumulation during stage II of fruit development, when the growth rate was also higher. Thereafter, the IAA concentration fell to control levels, but total pericarp IAA content remained
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higher. Reducing IAA transport by applying 2,3,5-triiodo-benzoic acid (TIBA) reduced the amount of calcium entering the fruit. On the other hand, girdling reduced the calcium concentration during stage II, but increased it during stage III so that fruits from girdled trees had a much higher calcium content at harvest (Wand et al. 1991b). Similar results, showing that both TIBA and girdling decreased calcium concentration, were obtained in fruits of certain apple cultivars (Tomala and Dilley 1989). Girdling of young ‘Red Fuji’ apple trees resulted in increased contents of zeatin riboside and IAA in spur buds (Li et al. 1996).
V. GIRDLING IN HORTICULTURAL PRACTICE The use of girdling as a horticultural technique requires consideration of tree age, health and vigor, as well as growing conditions. The grower must take into account the anticipated benefits as against the risks involved. The success of girdling depends upon careful execution of this delicate manipulation. The accumulation of carbohydrates in the canopy provides a rich source of energy for all the stages of reproductive development; flowering, fruit set, fruit enlargement, and ripening. The most common purpose of girdling is to increase fruit set by reducing fruitlet drop. Girdling is also performed to increase fruit size. In alternate-bearing trees, girdling increases the carbohydrate level in the canopy during “off” years, following the intensive utilization of carbohydrate reserves during “on” years (Crane and Nelson 1972). Weaver and McCune (1959) argue that the increase in carbohydrates following girdling is not the only reason for the increase in fruit set and fruit size in grapes. They base their argument on the fact that thinning, which also increases the availability of carbohydrates to the cluster, has only a slight effect on fruit size. A. Rooting and Vegetative Growth Girdling is being used to promote rooting of hardwood cuttings (Noel 1970; Hartmann and Kester 1975). Girdling shoots before their removal from stock plants presumably blocks the downward translocation of carbohydrates, hormones, and other root-promoting factors, leading to an increase in root initiation (Hartmann and Kester 1975). In some cases, girdling promotes rooting even without addition of synthetic auxins (Wood 1989). Details of this technique have received considerable attention (Evert and Smittle 1990; Oliveira et al. 2000).
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Girdling has often been observed to reduce canopy shoot growth (Dennis and Edgerton 1966; Priestly 1976; Greene and Lord 1983; Cutting and Lyne 1993). Some restriction of vegetative growth is desirable in vigorous apple cultivars. Notching, scoring, and ring girdling have been used successfully to reduce apple shoot growth (Hoying 1993). Both ring girdling and the related “guillotine girdling” (Table 1.2) reduce trunk cross-sectional area, average shoot length, and average number of shoots per tree (Hoying and Robinson 1992). Notching is used to ensure scaffold development in young trees (Hoying 1993) by stimulating lateral shoot growth (Greene and Autio 1992). Notching above apple vegetative buds was most effective when performed with buds on the top of the branch 2 to 4 weeks prior to full bloom (Greene and Autio 1992). The mechanism is presumably hormonal; the notch (Fig. 1.2) blocks basipetal flow of auxin, which normally inhibits lateral shoot growth (Greene and Autio 1992). Another facet of the same phenomenon, though mostly undesirable, is the formation of water sprouts directly below the girdle, generally known as basal sprouting (Noel 1970). B. Floral Induction and Juvenility Girdling and similar techniques have been used in attempts to induce earlier flowering of seedling apple trees (Zimmerman 1972; Meilan 1997). Maximum response was obtained with trees that were on the verge of flowering or had already produced a small number of flowers. Way (1971) reported that scoring 4- to 7-year-old apple seedlings was more effective in inducing flowering than scoring 3-year-old seedlings. Girdling branches of mature apple trees significantly increased flower bud formation (Dennis and Edgerton 1966). Ringing between May 30 and July 30 inhibited flower formation in the following year (Jona and Casale 1976). Induction of flower formation was found to be a fairly gradual process that culminated in mid-June and was complete by late July. Scoring ‘Delicious’ apple for three consecutive years consistently reduced terminal growth and increased yield during the second and third years (Greene and Lord 1983). Li et al. (1996) reported an increased flower bud formation in 5-year-old ‘Red Fuji’ apple with girdling (+534%), girdling plus paclobutrazol (+648%), and paclobutrazol alone (+154%). Ringing hastened flowering of juvenile citrus seedlings. More than 60% of 7-year-old trees flowered the year after ringing, but only 3% of 3-year-old trees flowered (Furr et al. 1947). Autumn girdling increased flower number of ‘Murcott’ citrus three-fold and markedly intensified
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the flowering of ‘Shamouti’ orange (Goldschmidt et al. 1985) and ‘satsuma’ mandarin (Erner 1990; Iwahori et al. 1990; Garcia-Luis et al. 1995). Girdling shortened the juvenile period of avocado seedlings (Lahav et al. 1986). Girdling before bloom, at full bloom, and after full bloom did not significantly affect the yield of ‘Fuerte’ avocado (Gregoriou 1989). In avocado trees girdled several months before flowering, only the timing of floral expression seemed to be altered, not the number of flowers or inflorescences (Ibrahim and Bahlool 1979). In some cases, girdling had no apparent effect on flowering of avocado (Lahav et al. 1971). Girdling induced formation of pistillate flowers on juvenile pecan clones (Thompson 1986). Girdling was ineffective in induction of flowering in sweet cherry (Oliviera and Browning 1993). Ben-Tal and Lavee (1984) report a significant increase of flowering following girdling of biennial bearing olive trees during their “off” year. Girdling has an inconsistent effect on flowering in mango, as noted by Davenport and Nunez-Elisea (1997), who summarized numerous earlier reports. The promotion of flowering by girdling may reflect the need for threshold levels of carbohydrate in the canopy for flower formation (Goldschmidt et al. 1985). Bernier and co-workers assign a role for sucrose in the floral induction of Sinapis alba (Bodson and Outlaw 1985; Havelange et al. 2000). However, girdling also interfered with the transport of plant hormones (Cutting and Lyne 1993) and other metabolites. Thus, a specific role played by carbohydrates in the initiation of flowering has not been unequivocally demonstrated (Davenport and Nunez-Elisea 1997). C. Fruit Set Fruit set is a critical process in cropping. Persistence of the young fruitlets or their abscission is a major physiological event resulting from a variety of endogenous and environmental factors (Goldschmidt 1999). Girdling, close to or during bloom, increases fruit set in numerous tree crops, mostly by reducing fruitlet abscission as in: citrus (Monselise et al. 1972; Cohen 1981; Barry and Bower 1997), apple (Dennis and Edgerton 1966; Dennis 1986; Kyun et al. 1997), olive (Fortanazza et al. 1987), and persimmon (Hasegawa and Sobajima 1992). Similar effects were also found after strangulation of citrus in early spring (Yamanishi et al. 1994). In avocado, on the other hand, girdling in order to increase fruit set is commonly employed during the preceding autumn (Tomer 1977). Carbohydrate level is one of the factors limiting fruit set (Garcia-Luis et al. 1988; Caspari et al. 1998; Goldschmidt 1999). Since girdling causes accumulation of carbohydrates in the canopy, the effect of girdling on
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fruit set may be a result of increased supply of carbohydrates to the reproductive organs. In avocado, girdling increases the level of carbohydrates in the pistil (Tomer 1977). In cultured flowers, addition of sugars to the medium enhanced the growth of the pollen tube and its penetration into the ovule. This suggests that, at least in avocado, girdling affects fruit set by increasing the level of carbohydrates in the pistil, which causes faster growth of the pollen tubes (Tomer 1977). The involvement of plant hormones in fruit set processes is recognized (Crane 1964; Monselise 1986), thus the effect of girdling on fruit set may also involve changes in hormonal balance. Indeed, application of gibberellins is often combined with girdling to ensure adequate fruit set in grape (Winkler et al. 1974) and citrus (Goren et al. 1992; El-Otmani et al. 2000). Girdling may lead to higher yield in citrus, even when performed during the fruitlet abscission period due to reduction of the last stages of fruitlet drop (Koller et al. 2000; A. A. Schaffer and E. E. Goldschmidt, unpublished data). D. Fruit Size The positive effect of girdling on fruit size is well documented and girdling for this purpose is widely used in grape (Weaver and McCune 1959; Jawanda and Vij 1973; Peruzzo 1994; Dokoozlian et al. 1995; Kim and Chung 2000). Girdling-induced increase in fruit size has also been reported in peach (El-Sherbini 1992; Allan et al. 1993; Agusti et al. 1998), nectarines (Fernandez-Escobar et al. 1987; Villiers 1990; Agusti et al. 1992), mango (Bhattacharyya and Mazumdar 1990; Simmons et al. 1998), avocado (Davie et al. 1995), olive (Lopez Rivares and Suarez Garcia 1990; Barut and Eris 1993; Proietti et al. 1999), and persimmon (Hasegawa and Sobajima 1992; El-Shaikh et al. 1999). Less effect of girdling on fruit size was found in apple (Arakawa et al. 1998; Miller 1995; Wilton 2000). Grape vines are girdled after the termination of fruit set in order to avoid effects on fruit number. Girdling when 50% of the berries were 4–5 mm in diameter reduced the incidence of berry shatter and improved berry size (Wolf et al. 1991). Girdling-induced increase in grape berry size is commonly combined with GA3 treatment (Weaver and McCune 1959). In peach and nectarine, girdling is most effective prior to stage II of fruit growth (pit hardening). Girdling at this stage shortened stage II and caused peak fruit growth rate to occur earlier in the season (Day and DeJong 1990; Agusti et al. 1998). It increased fruit weight by 22 to 25%, and more than doubled the percentage of fruit in the larger fruit size category (Day and DeJong 1990). Similar results were obtained in an earlier study of apricot (Lilleland and Brown 1936).
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Ringing of apple trees 3 weeks after full bloom caused slight fruit elongation (Webster and Crow 1969). Girdling of grapefruit trees during anthesis may increase fruit set but eventually reduce fruit size (Cohen 1981). Girdling at different times during fruit growth invariably increased fruit size; early summer girdling was most effective (Hochberg et al. 1977; Fishler et al. 1983; Cohen 1984). Up to 100% increase in fruit weight was obtained in grapefruit following girdles in late May (Cohen 1984). Girdling combined with fruit thinning had a dramatic effect on fruit size (Goldschmidt 1999). Double girdling (15 cm below the scaffold branches junction level, and a second girdling 5 cm above it) at 75% petal fall markedly increased fruit size and yield of clementine citrus (Tuzcu et al. 1992). Girdling-induced increase in fruit size is most probably caused by improved supply of photosynthates to the developing fruit. This is indicated by the fact that, in citrus, girdling is effective throughout fruit development (Fishler et al. 1983), while auxins (and other plant growth substances), are effective only during the early stage of fruit development (Ortola et al. 1997).
E. Yield Increasing yield is one of the main goals in fruit tree culture. Since yield is a product of fruit number and fruit weight, an increase in yield may result from either an increased number of fruit units or from larger fruit (or their combination). Girdling often increases yield in various tree crops (Table 1.3), especially when yield of controls is low, as in young trees or in alternate bearing orchards. Excessive numbers of fruit units may produce a large crop of small, low-price fruit, which requires adjustment by thinning. This situation is often encountered with grapes and with tangerine hybrids; girdling may be necessary to secure adequate fruit set, but fruit thinning is subsequently applied to ensure reasonable fruit size (Winkler et al. 1974; Galliani et al. 1975).
F. Fruit Maturity and Quality While fruits approaching maturity are still actively growing, additional processes that are characteristic of maturity occur, primarily changes in sugars, acids, and pigmentation, all of which are highly dependent upon the supply of photosynthates. Girdling enhances maturation in various crops, particularly in grape and peach. Effects of girdling on grape maturation and quality have been described by Winkler et al. (1974). Girdling for hastening of maturation and improving quality is performed
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in grape at the beginning of ripening (veraison), or combined with earlier girdling after fruit set (double girdling) (Winkler et al. 1974; Carreno et al. 1998). Jacob (1931) recommended that girdling be done when the berries are about half-grown and that the wound be kept open during the ripening period. In one experiment, Weaver (1952) showed that the best coloration resulted from girdling ‘Red Malaga’ grapes when total soluble solids (TSS) reached about 13 or 14%, and that TSS increased more rapidly with early girdling. In a later study, Weaver (1955) reported that early girdling, when TSS content of ‘Red Malaga’ and ‘Ribier’ grapes was only 5 or 6%, usually resulted in the most rapid maturation. He suggested that girdling at this time coincides with decreased vegetative activity of the vine. Girdling of ‘Italia’ grape at the beginning of ripening significantly increased soluble solids and maturity index, and improved berry color, reduced titratable acidity, and advanced fruit ripening by five days (Carreno et al. 1998). Girdling table grapes after fruit set in cool climate growing areas markedly increased yield but consistently reduced soluble solids concentration, presumably due to dilution of the photosynthates (Zabadal 1992). Girdling or scoring consistently advanced peach harvest (Powell and Howell, 1985). In nectarine, girdling during the beginning of stage two of fruit development increased TSS concentration by about a half (Day and DeJong 1990), but girdling during stage three did not affect fruit maturation or quality (El-Sherbini 1992). In another study, fruit coloration was also enhanced (Bakr et al. 1981; Agusti et al. 1998). Girdling increased total phenolic content and high-molecular-weight phenols of peach fruit (Kubota et al. 1993a) as well as L-phenylalanine-ammonia-lyase activity (Kubota et al. 1993b). Enhanced ripening of peach and nectarine on girdled branches was associated with an earlier climacteric, resulting in higher ACC, ACC oxidase, and ethylene values (Agusti et al. 1998). Some investigators found that girdling sometimes increases the frequency of pit splitting (Kubota et al. 1993a), while others did not detect such an effect (Day and DeJong 1990; Allan et al. 1993; Agusti et al. 1998). Girdling of olives in mid-August increased fruit dry weight by 15% and oil content from 5 to 10% (Proietti et al. 1997). Fruit on girdled cherry trees were higher in soluble solids and color (Roper et al. 1987). Trunk strangulation of pummelo citrus tree increased sucrose and citric acid content in juice (Yamanishi et al. 1995). In apple, girdling as late as three weeks before harvest increased fruit firmness and TSS concentration (Elfving et al. 1991). Girdling and bark inversion of apple trees improved the eating quality of the fruit by increasing TSS content, while reducing water and calcium content (Arakawa et al. 1998). In apple
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flowers, girdling suppressed nectar production and reduced the sugar concentration of the remaining nectar (Campbell et al. 1991). More details are presented in Table 1.4.
VI. CONCLUDING REMARKS Girdling has a broad range of horticultural effects. As discussed above, all stages of reproductive development are influenced: flowering, fruit set and development and, in many instances, fruit maturity and quality as well. A model describing the effects of girdling on the distribution of photosynthate, feedback inhibition of leaf activity, and the transport of plant hormones is illustrated in Fig. 1.4. However, mechanism(s) through which girdling operates are not yet fully understood. The supply of water and mineral nutrients via the xylem is not generally affected by girdling. Logically, therefore, girdling must affect phloem-transported components. Two major candidates are apparent: photoassimilates (carbohydrates) and plant hormones. Evidence for involvement of carbohydrates in girdling effects is extensive and detailed (Weaver and McCune 1959; Priestley 1976; Goldschmidt and Huber
Fig. 1.4. A model illustrating the effects of girdling on the flow of carbohydrates and hormones in fruit trees. Arrows indicate the direction of transport and not the vascular site of transport.
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1992). Numerous studies have reported the accumulation of carbohydrates in canopy organs above the girdle and a simultaneous decline in carbohydrates below the girdle, often resulting in root starvation (Weaver and McCune 1959; Noel 1970). The multitude of carbohydrates in the canopy provides additional dry matter and energy for reproductive processes, that have a high energy and dry matter demand (Bustan and Goldschmidt 1998). This involves all of the reproductive stages mentioned above, thereby providing an explanation for the positive effects of girdling in all these stages. The evidence supporting the involvement of endogenous plant hormones in girdling effects, on the other hand, is somewhat equivocal and incomplete. Nevertheless, the following relationships can be portrayed. Auxins, known to be transported basipetally, seem to accumulate above the girdle (Dann et al. 1985), stimulating, in many cases, excessive growth immediately above the girdle (Fig. 1.3). At the same time, girdling seems to reduce the supply of cytokinins to the canopy (Skogerbo 1992; Cutting and Lyne 1993; Havelange et al. 2000). This may be responsible for the often-observed inhibition of shoot growth (Priestley 1976; Cutting and Lyne 1993). Other lines of circumstantial evidence also point to the role of cytokinins as regulators of shoot growth (Hall 1973). Since cytokinins are presumably produced in roots and transported upward via the xylem, the reduced supply of cytokinins to the canopy in girdled trees does not seem to result from blockage of transport but, rather, from an indirect effect on cytokinin production (Cutting and Lyne 1993), brought about perhaps by root starvation. In general, the effect of girdling on root-associated processes needs closer attention. The advance of plant science in recent years has indicated that plant responses to agrotechnical manipulations are likely to involve molecular up- and down-regulation of gene activity. It may, therefore, be assumed that responses to girdling also include changes in gene expression. Future girdling research will undoubtedly address this assumption, leading to more focused insight into the multiple far-reaching effects of girdling.
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Agenbag, H., and I. du Toit. 1992b. Girdling as an aid to harvest scheduling. Deciduous Fruit Grower 42:410–412. Agusti, M., V. Almela, and J. Pons. 1992. Effects of girdling on alternate bearing in citrus. J. Hort. Sci. 67:203–210. Agusti, M., V. Almela, and A. M. Mingo-Castel. 1990. Effect of kinetin and ringing on fruit set in the orange cultivar ‘Navelate’ (Citrus sinensis (L.). Osbeck). Investigacion Agraria, Produccion, Proteccion-Vegetales 5:69–76. Agusti, M., I. Andreu, M. Juan, V. Almeta, and L. Zacarias. 1998. Effects of ringing branches on fruit size and maturity of peach and nectarine cultivars. J. Hort. Sci. Biotech. 73:537–540. Allan, P., A. P. George, R. J. Nissen, and T. S. Rasmussen. 1993. Effects of girdling time on growth, yield, and fruit maturity of the low chill peach cultivar ‘Flordaprince’. Austral. J. Expt. Agr. 33:781–785. Amir, S., and L. Reinhold. 1971. Interaction between K-deficiency and light in C14-sucrose translocation in bean plants. Physiol. Plant 24:226–231. Aoki, M., K. Tanaka, and N. Okada. 1977. Effects of nitrogen fertilization and ringing treatment on initial yield of persimmon (Diospyros kaki), cv. ‘Wasejiro’. Research Bul. Aichi Ken Agr. Res. Center, Horticulture 9:119–130. Arakawa, O., A. Kanetsuka, K. Kanno, and Y. Shiozaki. 1998. Effects of five methods of bark inversion and girdling on the tree growth and fruit quality of ‘Megumi’ apple. Japan. Soc. Hort. Sci. 67:721–727. Bakr, E. I., K. M. Abdalla, M. A. Meligi, and I. A. Ismail. 1981. Floral differentiation in mango as affected by growth regulators, ringing and defoliation. Egyptian J. Hort. 8:161–166. Barry, G. H., and J. P. Bower. 1997. Manipulation of fruit set and stylar-end fruit split in ‘Nova’ mandarin hybrid. Scientia Hort. 702:243–250. Barut, E., and A. Eris. 1993. Research on the effects of girdling, thinning and plant growth regulators on yield, quality and alternate bearing in olive cv. ‘Gemlik’. Doga,Turk Tarim ve, Ormancilik-Dergisi. 17:953–970. Ben-Tal, Y., and S. Lavee. 1984. Girdling olive trees, a partial solution to biennial bearing. II. The influence of consecutive mechanical girdling, on flowering and yield. Riv. Ortoflorofrutt. It. 68:441–451. Ben-Tal, Y., and S. Lavee. 1985. Girdling olive trees, a partial solution to biennial bearing. III. Chemical girdling: its influence on flowering and yield. Riv. Del. Ortoflorofrutt. It. 69:1–11. Beruter, J., M. Feusi, and E. Studer. 1997. The effect of girdling on carbohydrate partitioning in the growing apple fruit. J. Plant Physiol. 151:277–285. Bhattacharyya, A. K., and B. C. Mazumdar. 1990. Quality of mango fruits due to ringing of fruit bearing shoots and auxin application on leaves of ringed shoots. Agr. Res. 5: 75–78. Bhujbal, B. G., and K. G. Chaudhari. 1973. Yield and quality of ‘Thompson seedless’ grape (Vitis vinifera L.) as influenced by girdling and gibberellins. Res. J. Mahatma Phule Agr. Uni. 4:108–112. Blumenfeld, A. 1986. Improving productivity of ‘Triumph’ persimmon. Alon Hanotea 40:539–544. Bodson, M., and W. H. Outlaw, Jr. 1985. Elevation in the sucrose content of the shoot apical meristem of Sinapis alba ay floral evocation. Plant Physiol. 79:420–424. Botiyanski, P., T. Mokreva, and V. Roichev. 1998. Biometric characteristics of seed-buds and grapelets, formed after girdling of seedless grapevine varieties. Bulgarian J. Agr. Sci. 4:605–611.
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Heinicke, A. J. 1933. The assimilation of carbon dioxide by apple leaves as affected by ringing the stem. Proc. Am. Soc. Hort. Sci. 29:225–229. Hochberg, R., S. P. Monselise, and J. Costo. 1977. Summer girdling and 2,4-D effects on grapefruit size. HortScience 12:3, 228. Hoying, S. A. 1993. Benefits and pitfalls of nicking, notching, ringing, girdling and root pruning apple trees. Compact Fruit Tree 26:66–68. Hoying, S. A., and T. L. Robinson. 1992. Effects of chain saw girdling and root pruning of apple tree. Acta Hort. 322:167–172. Huberman, M., and R. Goren. 1996. Effects of plant growth regulators and girdling on yield of ‘Sweetie’ (‘Oroblanco’) (in Hebrew with English abstr.). Alon Hanotea 50:194–199. Ibrahim, I. M., and S. El D. Bahlool. 1979. The effect of girdling on flowering, fruiting and vegetative growth of avocado trees. Agr. Res. Rev. Hort. 57:55–66. Iwahori, S., A. Garcia-Luis, P. Santamarina, C. Monerri, and J. L. Guardiola. 1990. The influence of ringing on bud development and flowering in ‘Satsuma’ mandarin. Expt. Bot. 41:1341–1346 Jacob, H. E. 1931. Girdling grape vines. Calif. Agr. Exp. Service Circ. 56. Janick, J. 1972. Biological control. p. 248–256. In: Horticultural science. San Francisco, CA. Jawanda, J. S., and V. K. Vij. 1973. Effect of gibberellic acid and ringing on fruit set, cluster and berry characters and fruit quality of ‘Thompson seedless’ grape. Indian Agr. Sci. 43:346–351. Jensen, F., H. Andris, and R. Beede. 1981. A comparison of normal girdles and knife-line girdles on ‘Thompson seedless’ and Cardinal grapes. Am. Enol. Vitic. 32:206–207. Jensen, F., F. Swanson, W. Peacock, and G. Leavitt. 1975. The effect of width of cane and trunk girdles on berry weight and soluble solids in table ‘Thompson seedless’ vineyards. Am. Enol. Vitic. 26:90–91. Jona, R., and L. Casale. 1976. Studies on the time of flower induction in ‘Golden delicious’ apple. Fruticoltura 38:39–41. Jordan, M. O., and R. Habib. 1996. Mobilizable carbon reserves in young peach trees as evidenced by trunk girdling experiments. J. Expt. Bot. 47:79–87. Jordan, M. O., R. Habib, and M. Bonafous. 1998. Uptake and allocation of nitrogen in young peach trees as affected by the amount of photosynthates available in roots. Plant Nutr. 21:2441–2454. Kim, W. S., and S. J. Chung. 2000. Effect of GA3, ethephon, girdling and wiring treatment on the berry enlargement and maturity of ‘Himrod’ grape. J. Korean Soc. Hort. Sci. 41:75–77. Kohne, J. S. 1992. Increased yield through girdling of young ‘Hass’ trees prior to thinning. Yearb., South-African Avocado Growers’ Assoc. Vol. 15 issue 68. Koller, O. L., E. Soprano, A. C. Z-da. Costa, O. C. Koller, and O. K. Yamanishi. 2000. Flowering induction and fruit production in oranges cv. ‘Shamouti’. Laranja 21:307–325. Koshita, Y., T. Takahara, T. Ogata, and A. Goto. 1999. Involvement of endogenous plant hormones (IAA, ABA, GAs) in leaves and flower bud formation of ‘Satsuma’ mandarin (Citrus unshiu Marc.). Sci. Hort. 79:185–194. Kozlowski, T. T. 1973. Shedding of plant parts. p. 560. Academic Press, New York. Krapp, A., and M. Stitt. 1995. An evaluation of direct and indirect mechanisms for the “sink-regulation” of photosynthesis in spinach: Changes in gas exchange, carbohydrates, metabolites, enzyme activities and steady-state transcript levels after coldgirdling source leaves. Planta 195:313–323. Krezdorn, A. H., and H. D. Brown. 1970. Increasing yields of the ‘Minneola’, ‘Robinson’ and ‘Osceola’ varieties with gibberellic acid sprays and girdling. Proc. Fla. Sta. Hort. Soc. 83:29–34. Krezdorn, A. H., and W. J. Wiltbank. 1968. Annual girdling of ‘Orlando’ tangelos over an eight-year period. Proc. Fla. Sta. Hort. Soc. 81:17–23.
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2 Irrigation Water Quality and Salinity Effects in Citrus Trees* Yoseph Levy Agricultural Research Organization Department of Fruit Tree Sciences Gilat Research Center, Mobile Post Negev, 85-280 Israel Jim Syvertsen University of Florida, IFAS, Citrus Research and Education Center 700 Experiment Station Road Lake Alfred, Florida 33850-2299, USA
I. INTRODUCTION II. MANAGING SALINITY A. Irrigation and Salinity B. Rootstocks and Scions III. EXPERIMENTAL METHODS IN SALINITY RESEARCH A. Leaf Analysis B Juice Analysis C. Seed Mineral Content D. Biochemical Indicators E. Seed Germination F. Solution Culture vs. Soil Culture G. Seedling Rootstocks vs. Budded Trees H. Greenhouse vs. Field Studies I. Tissue Culture vs. Whole Plant IV. PHYSIOLOGICAL RESPONSES A. Amino Acids Accumulation B. Net Gas Exchange of Leaves C. Salinity Interactions with Physical Environmental Factors *We thank Drs. G. Albrigo and M. Talon for helpful comments. Horticultural Reviews, Volume 30, Edited by Jules Janick ISBN 0-471-35420-1 © 2004 John Wiley & Sons, Inc. 37
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D. Osmotic Stress E. Toxic Ions F. Vegetative Growth G. Fruit Yield and Quality H. Phytochemicals V. SALINITY AND BIOTIC STRESSES A. Phytophthora B. Rio Grande Gummosis C. Nematodes D. Mycorrhizae VI. BENEFITS OF MODERATE SALINITY A. Chilling and Freezing Tolerance B. Leaching C. Increase Flowering, Yield VII. SUMMARY LITERATURE CITED
I. INTRODUCTION Most worldwide citrus production at least partially depends on irrigation for economic production (Shalhevet and Levy 1990). Irrigation is inevitably associated with the deterioration of water quality of run-off or ground water, especially due to increases in soluble salts. Poor water quality unavoidably leads to increased soil salinity. Excess salts from irrigation water must be removed from the root zone by leaching from rainfall or irrigation if agriculture is to be sustainable (Shannon 1997). Citrus trees, and most other fruit trees with the exception of date, pistachio, pomegranate, and perhaps olive trees (Gucci and Tattini 1997), are relatively sensitive to salinity stress. Unlike deciduous fruit trees, world citrus production is limited to a relatively small climatic belt where frosts are not too severe. The best citrus is produced, however, where winter cold is adequate to induce uniform flowering and the development of good fruit color. Human immigration to these mild-climate zones and concomitant urban development competes with citrus for both land and water resources. This trend began in Southern California and is now also evident in the citrus producing areas of Arizona, Texas, Florida, and the Mediterranean coasts. Increased consumptive use of water also results in the degradation of ground water quality all over the world (Jensen et al. 1990). In many coastal areas, demand for water exceeds the annual renewable supply and this over-exploitation of groundwater can lead to salt water intrusion into aquifers (Bosch et al. 1992). Any future rise in sea level may further threaten coastal ground water quality. However, salinization is caused not only by overuse of ground water, but also from slowing the
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rate of natural drainage to the sea. This process increases salts in ground water, that is already being replenished by increasingly saline irrigation water. Such salinization of the aquifer is not only limited to arid areas but is also evident in higher rainfall humid regions, such as parts of Florida, where salinity of well water increased at a rate of 12 mg L–1 per year (Calvert 1982) long before the more recent drought years. Urban requirements for high-quality water will ultimately require citriculture to depend on alternate poorer-quality water sources, including recycled wastewater and brackish water. The quality of domestic wastewater is also likely to deteriorate. Ironically, as water conservation reduces per capita domestic water use and increases water-use efficiency, effluent is diluted with less fresh water even though the total salt output may not change. The toxic ion content of domestic wastewater can be reduced by replacing the Na+ with K+ in water softeners and cleaning agents and also by limiting the use of boron (B) in cleaning agents. The quality of industrial wastewater can be improved by modifying industrial processes to use less-harmful pollutants. The amount of NO3– and/or NH4+ can be reduced by effluent treatment procedures. Soluble chlorides will continue to be a problem since it is not possible to significantly reduce Cl– in domestic effluent, nor is there an effective way of removing Cl– from solution apart from expensive desalination of wastewater. This review summarizes effects of irrigation water quality and salinity on citrus trees. We have tried to focus on cultural practices that are used to deal with poor-quality irrigation water, especially with respect to salinity, along with physiological responses of rootstocks and scions to salinity stress. Although this review concentrates on information that has become available since the review by Maas (1993), it was often necessary to review older work to develop the appropriate context in which to discuss experimental results. Conclusions about negative and positive aspects of salinity stress and their interaction with other environmental stresses are developed along with contrasting different experimental approaches in the laboratory, greenhouse, and field.
II. MANAGING SALINITY A. Irrigation and Salinity. All irrigation water contains salts; moderately saline water containing 200 mg Cl– L–1 will add 1000 kg Cl– ha–1 when applied at 500 mm per annum. If only part of that amount accumulates from year to year, soil
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will become non-productive. Even if the overall salt content does not increase from year to year because of adequate leaching, salinity may become high enough to cause damage during rain-free periods, between irrigations, or in portions of the soil that are inadequately leached. Leaching, of course, requires good drainage. In poorly drained soils, finetextured soils, or when the ground-water table is shallow, leaching requirements may necessitate the construction of an effective drainage system. The effects of irrigation and salinity on perennial tree crops are cumulative (Hoffman et al. 1989), particularly for citrus (Shalhevet and Levy 1990). In humid areas with high rainfall, injury symptoms on citrus trees from saline irrigation water may be transitory. However, even temporarily affected trees may remain stunted compared with trees not exposed to saline water, especially if young trees are salinity-stressed. The concentration of salts in a soil is a function of the total salts present and the soil water-content. Soil salinity is related to the electrical conductivity of standard saturated aqueous extract (ECe). Managing irrigation and fertilization with high-salinity irrigation waters requires routine monitoring of the electrical conductivity of the irrigation water (ECi) and ECe. If excess salts accumulate in the soil, it is best to keep the soil near field capacity moisture content so as not to further concentrate the salts. Without adequate rain, it may become necessary to apply irrigations with excess water in order to leach salts from the root zone (leaching fraction). The required frequency of leaching varies with the degree of salinization and evaporative demand. Leaching may be required no less frequently than every other week in some environments and irrigation must be excessive. Areas with compacted soils or poor drainage may need special attention when managing salinity, such as flood leaching or other ways to handle slow percolation and poor aeration. The method of irrigation and its interactions with the amount of rainfall throughout the season have important effects on responses of citrus trees to salinity. The amount of leaching depends on the amount of rainfall during the wet season and on the volume of soil wet by the irrigation water. Under dry summer conditions in Mediterranean climates, most of the active roots concentrate in the soil volume that is wet by the irrigation water since roots cease to develop at low soil temperatures when the soil is wet by winter rains. In summer-rainfall areas, however, roots grow beyond the irrigated zone. ECe measurement standardizes the amount of salts in the soil to conditions when the soil is saturated, but depending on soil moisture content, the actual salinity level in the vicinity of the tree roots may be several times greater than the ECe. In sandy soils where salts are easily
2. IRRIGATION WATER QUALITY AND SALINITY EFFECTS IN CITRUS TREES
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leached, using ECe alone to evaluate soil salinity may not be sufficiently accurate. The ECe of these soils is only an indication of soil salinity at the time of measurement and can change rapidly following irrigation or rainfall. Without proper water and nutrient management, citrus irrigated with high-salinity water can suffer reduced growth and production. Salt concentrations in the soil solution can be monitored effectively with ceramic suction cups or soil salinity probes after proper calibration to approximate ECe (Boman 2000). Monitoring of soil solution is important where saline conditions may result from intentional deficit irrigation (Gonzalez-Altozano and Castel 1999) or from water-conserving irrigation scheduling based on soil moisture sensors (Boman et al. 2000) such as tensiometers or capacitance sensors (Fares and Alva 2000). When irrigation amounts do not exceed evapotranspiration, all the dissolved salts in the irrigation water that are not taken up by roots will remain in the root zone. Since the decreasing soil osmotic potential (Ψπ) reduces water uptake by roots, soil moisture sensors will indicate that the soil water content is high, thereby reducing the amount of water per irrigation. Such a scenario can result in a spiraling increase in soil salinization even with comparatively good-quality water. The soil ECe, which is linearly correlated to Ψπ, should be monitored to prevent such problems from developing. Microirrigation, especially drip irrigation, results in a relatively small soil volume that is routinely wet and leached by irrigation water. In arid climates, this comparatively small soil volume may be surrounded by a saline border and can be underlain by a salinized soil zone. Although drip irrigation can be beneficial for leaching salts away from localized root zones, a light rain may move the salts that accumulated on the surface or at the border of the wetted zone into the root zone. This necessitates the operation of drip irrigation (even during an initial rain event) until adequate rains have occurred to leach out accumulated salts. Salts can also accumulate in the periphery of furrows that are irrigated with saline water. 1. Irrigation Methods Gravity Irrigation. If adequate water is available, flood or basin irrigation can have an advantage over microirrigation due to the high downward movement of soil water. This leaching depends on soil permeability, drainage, and on the depth to ground water. The interval between irrigations is usually relatively long with these methods, so when the water tables are shallow, ground water salinity can affect soil salinity if the net flow of water is upward for a significant period of time in the absence
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of sufficient irrigation or rainfall to maintain downward water flow (Boman 2000). This method usually will depend on skilled labor to maintain uniform irrigation. Thus, basin irrigation is becoming less popular in new large-scale plantings because of the soil grading and skilled labor needed to maintain the system and because it requires a high volume of water. With good drainage, flood irrigation is still an excellent way to leach saline soils before planting. Furrow irrigation with saline water may cause salt buildup in the periphery of the wetted zone as mentioned above. The necessary soil grading, greater need for weed control, and skilled labor to operate such systems make it less feasible than other methods for many locations. Sprinkler. Overhead irrigation is still practiced in some parts of the world. This method requires comparatively high pressure, high volume, and good-quality water. If used with reclaimed water, there is also the hazard of biological contamination of the fruit. Citrus leaves easily absorb Cl– and Na+ from direct contact with water droplets (Eaton and Harding 1959; Ehlig and Bernstein 1959). Salt accumulation is a function of the evaporation rate, which increases the salt concentration of the water film on leaves. Damage can also develop from windblown salt water near the sea. Severe damage to leaves located in low canopy positions of under-thecanopy sprinkler-irrigated trees or in canopies of overhead-irrigated citrus has been described (Harding et al. 1958; Lundberg 1971; Nakagawa et al. 1980; Spurling 1981; Calvert 1982). Nighttime irrigation was recommended for overhead irrigation with comparatively high salinity (1200 mg L–1 TDS; Tucker 1978), since the accumulation of dissolved salts is greater from daytime than nighttime irrigation because of the different evaporative demand. Pulsed irrigation is dangerous, since salt absorption is greater from intermittent than from continuous wetting. The sensitivity of a citrus scion/rootstock combination to injury through direct foliar contact bears no relationship to its general tolerance to soil salinity that will be discussed later. Leaf Cl– and Na+ toxicity from direct contact with saline water has different symptoms from toxicity of Cl– that was absorbed by roots. Contact damage, consisting of burned necrotic, or dry-appearing tips on leaves, is one of the most common visible salt injury symptoms. In some cases, overhead irrigation, particularly at low humidity, will cause ring-shaped lesions on fruit where irrigation water evaporated. There are reports of Cl– and Na+ concentrations in leaves from low positions in the canopy that were about four times greater than those of the upper leaves (of grapefruit, ‘Valencia’ and ‘Washington
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Navel’ orange). The lowest concentration of either Na+ or Cl– generally associated with leaf burn is about 0.25% of leaf dry weight. Young trees (1–2 years) on ‘CTRM’ (see Table 2.1 for rootstock abbreviations) seem to be more susceptible to saline irrigation water spray and can develop brown “blisters” of dead tissue on their trunks (Boman 1999). Using overhead irrigation with poor-quality water for evaporative cooling (Brewer et al. 1979) during conditions of high evaporative demand can be especially dangerous and can lead to rapid concentration of the remaining salt solution on the leaves. Under-the-canopy sprinklers, especially microsprinklers, lessen the danger of salt damage to wetted leaves. The use of microsprinklers has become popular in Florida due to water-use restrictions, and because it prevents frost damage better than overhead sprinklers or drip irrigation (Boman and Parsons 1999). Microirrigation systems usually do not wet the entire soil volume. This occurrence is a benefit in arid climates, since more leaching of water usually occurs during irrigation of the limited volume and salts will not accumulate on the soil surface. However, the same increased leaching may also leach nutrients from the soil and increase nitrate concentration in ground water, especially in rainy areas with sandy soils.
Table 2.1. CARZ CLEO CTRM CTRN FA13 FA5 MACR RANG RL SB812 RT803 GT SO SwL SwO TRIF TROY VOLK X639
Abbreviations for names of Citrus and Citrus relatives. Carrizo citrange (C. sinensis [L.] Osbeck. × Poncirus trifoliata L.) Cleopatra mandarin (C. reshnii Hort ex Tan.) Swingle citrumelo (C. paradisi × P. trifoliata) citron (C. medica L.) Cleopatra mandarin (C. reshnii × P. trifoliata) Cleopatra mandarin (C. reshnii × P. trifoliata) Alemow (C. macrophylla Westr.) Rangpur lime (C. limonia Osbeck.) rough lemon (C. jambhiri Lush.) Sunki × Beneke (C. sunki × P. trifoliata L.) RANG × TROY [C. limonia × (C. sinensis × P. trifoliata)] Gau Tau (C. aurantium × ?) sour orange (C. aurantium L.) sweet lime (C. aurantifolia L.) sweet orange (C. sinensis [L.] Osbeck.) trifoliate orange (Poncirus trifoliata L) Troyer citrange (C. sinensis × P. trifoliata) Volkameriana (C. volkameriana Chapot) CLEO × TRIF (C. reshni × P. trifoliata)
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Drip. This irrigation method has become common in arid areas and Mediterranean climates. The popularity of drip is not only due to the water savings gained by reducing evaporative losses, but also due to the advantage of this system for irrigation with saline water that was described above. Successful use of a drip system depends on good water filtration and water treatment to prevent bacterial or mineral clogging. The utility of a drip system can be improved by fertigation. Dripper improvement and chemical prevention of root penetration into the drippers make underground drip systems feasible in citrus orchards. The advantage of this system over regular drip is that the water does not usually reach the surface, so it does not leave salts behind. This system is also advantageous when using reclaimed water that may be contaminated with harmful bacteria. Additionally, underground systems are less prone to damage from orchard operations and from pests like rodents or woodpeckers. Among the disadvantages of subsurface drip systems is the difficulty in monitoring the proper operation of the system. Also, if water does wet the soil surface by capillary action, salts may accumulate there. 2. Fertilizer and Salinity. The frequency of applying fertilizer has a direct effect on the concentration of total salts in the soil solution. A fertilization program that uses frequent applications with relatively low concentrations of salts will normally result in less salinity stress than programs using only two or three applications per year. As described above, light rain can aggravate salinity damage by the leaching of any residual dry fertilizer that was applied in the non-irrigated soil areas between the rows. Relatively expensive controlled-release fertilizers or frequent fertigations are ways to minimize salt stress when using highsalinity irrigation water. Selecting nutrient sources that do not add potentially harmful ions to already high levels in irrigation water can also avoid compounding salinity problems. The Cl– in KCl or Na+ in NaNO3 materials adds more toxic salts to the soil solution. Repeated fertilizer application with sources like (NH4)2SO4 can alter soil pH and cause soil nutrient imbalances. Specific ions can also add to potential nutrient imbalances in soil and trees. For example, Na+ can displace K+ and lead to K+ deficiencies. The displacement of Ca2+ by Na+ in the soil cation exchange complex can lead to decreased permeability and destroy soil structure. Such nutrient imbalances can compound drainage problems and aggravate the effects of salinity stress. Salinity problems can be minimized if sufficient soil nutrient concentrations are maintained, especially those of K+ and Ca2+. Preliminary results suggest that continuous application of nitrates like
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KNO3 under saline conditions can reduce Cl– accumulation in scions grafted on susceptible rootstocks, and can increase yield (Bar et al. 1996, 1997; Levy et al. 1999a, 1999c, 2002; Levy and Lifshitz 2000a, 2000b). This effect might be due to competitive exclusion of Cl– by NO3– at the soil-root interface, or, in young trees, a dilution effect due to increased growth. There are marked differences in the salt index (the salt content per unit nutrient) of particular formulations of fertilizer nutrients. Choosing nutrient sources with a relatively low salt index can reduce salinity problems from fertilizer salts. With high-salinity irrigation water, fertilizer formulations should have low salt index. It may be necessary to increase the frequency of fertilizations, thereby making it possible to reduce the salt content of each application and aid in preventing excess salt accumulation in the root zone. The nutrient storage capacity of citrus trees tends to buffer the different seasonal demands for nutrients associated with specific growth demands. Leaf or fruit analysis should be used to detect excessive Na+ and Cl– concentrations, or deficient concentrations of other elements caused by nutrient imbalances from salt stress.
B. Rootstocks and Scions 1. Rootstock Abbreviations. The abbreviations for different rootstocks (Table 2.1) are based on nomenclature of Hodgson (1967). 2. Salt Tolerance. It has been known for many years that citrus rootstocks differ in their ability to absorb the toxic ions, Cl–, Na+, and B, and to translocate ions to the canopy (Oppenheimer 1937; Cooper et al. 1951, 1952; Cooper and Gorton 1952; Cooper 1961; Embleton et al. 1973; Wutscher et al. 1973). Most of these studies were from short-term, comparatively high salinity trials, but results have been corroborated more recently for many rootstocks under field conditions (Levy and Shalhevet 1990, 1991; Garcia Lidon et al. 1998; Levy et al. 1999a,b,c). Because of the relative importance of Cl– toxicity in citrus (detailed below), salinity tolerance of rootstocks is most often based on the ability of the root system to limit the transport of Cl– to the leaves. In general, the decreasing order of salinity tolerance (most tolerant to most sensitive) in citrus rootstocks is: ‘CLEO’, ‘RANG’, ‘SB812’, ‘X639’, ‘GT’, ‘VOLK’, ‘SO’, ‘MACR’, ‘CTRM’, ‘RL’, ‘CARZ’, and ‘TROY’, ‘C35’ citrange, ‘CTRN’ (see Table 2.2 for details). The above ranking may differ somewhat, however, depending on the specific ions, effects of scion,
46 Table 2.2.
Ranking of rootstock tolerance to Cl– in different studies.
Susceptible
Medium
Tolerant
Scion
500
Reference
SwL
SO
CTRN>CTRM>RL
SwO>SO
CLEO>RANG
grapefruit
1800
Cooper and Gorton 1952
SO
CLEO
grapefruit
1200
Cooper et al. 1958
MACR>CARZ>TROY
SwL>SO>CTRM
CLEO>RANG>SUNKI
grapefruit
1200
Peynado and Young 1962
CARZ
CLEO
FA5=FA13
seedlings
4690
Forner et al. 2000
RL>TRIF
CARZ>TROY>SwO
RANG>CLEO>MACR
seedlings
1775
Grieve and Walker 1983
MACR
SO*
CLEO*
lemon
1490
Nieves et al. 1990
RL
SwO
Max Cl– Range
SO>CLEO
grapefruit
SO
VOLK
MACR
lemon
3550
Garcia Legaz et al. 1992
TROY
SO>CITR
CLEO
grapefruit
3400
Boman 1994
CARZ=TROY
RL
VOLK
seedlings
1147
Combrink et al. 1995
SO
CLEO
RANG>VOLK
seedlings
3000
El Hammady et al. 1995
SO
SB812
RT803>GT>CLEO
seedlings
1680
Levy et al. 1999
TROY
SO>SB812>GT
VOLK>RANG>CLEO
grapefruit
880
Levy et al. 2000
*SwO interstock
680
Oppenheimer 1937
Levy and Shalhevet 1990
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conditions of incompatibility, and with disease status (viruses, viroids, root infections, or pests). Many citrus rootstocks with low growth vigor have good Cl– exclusion characteristics, whereas some of the vigorous citrus rootstocks exhibit poor Cl– tolerance (Castle and Krezdorn 1993). Since faster-growing trees always use more water than slower-growing trees, leaves on highvigor trees would be exposed to relatively more Cl– in the transpiration stream from saline water than low-vigor trees. Thus, at least part of the mechanism underlying the accumulation of relatively low leaf Cl– in some citrus rootstocks may be related to their low growth vigor (Moya et al. 1999). However, there are many exceptions to this rule: ‘RANG’ is a fast-growing rootstock with good salt tolerance and ‘VOLK’, another fast-growing rootstock, exhibits some salt tolerance, at least as a young tree (Levy and Lifshitz 2000a). It is important to remember that due to osmotic effects, growth and yield of citrus trees can be reduced by excessive salts regardless of rootstock. The critical salinity level for salt damage varies with the buffering capacity of the soil (soil type, organic matter), climatic conditions, and the soil moisture status. Salinity-induced symptoms such as nonspecific chlorosis, smaller leaf size, and impaired shoot growth are often difficult to assess. Cl– toxicity can be diagnosed by leaf analysis (taking care to sample leaves that were not wet by irrigation water, when only a part of the canopy is wet by irrigation water) and at harvest time by juice analysis (Levy and Shalhevet 1990). Na+ toxicity symptoms such as tip-burn seldom distinctly appear. Boron toxicity symptoms are usually visible in leaves. Without leaf ion analysis, however, boron toxicity can be confused with other microelement deficiency or herbicide damage symptoms. Salinity interacts with many horticultural issues when choosing a rootstock. The comparatively high salinity tolerance of ‘SO’ and its other desirable horticultural characteristics make it a good rootstock to choose to cope with salinity problems. This fact places growers all over the world in a dilemma because trees grafted on ‘SO’ are susceptible to tristeza. Many tristeza-tolerant rootstocks such as ‘RL’, ‘TRIF’, ‘CARZ’, and ‘CTRM’ are sensitive to salinity. In addition, recent research indicates that drip-irrigated young trees on ‘SO’ may be more susceptible to salinity than mature trees (Hamou et al. 1999; Levy et al. 2000). A goal of many plant breeding programs is to develop a substitute rootstock for ‘SO’ that has similar growth, fruit quality, disease tolerance, and salinity tolerance, but is also tolerant to tristeza. Poncirus sp. and its hybrids are popular rootstocks in many areas but are susceptible to lime-induced chlorosis in calcareous soils. When
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salinity is also a potential problem, the grower is presented with an additional dilemma. Deficit irrigation can prevent lime-induced chlorosis (Levy 1998; Boman et al. 1999), but since these rootstocks are also very susceptible to salinity, it increases the hazard of salinity damage if leaching is reduced with reduced irrigation. The fact that rootstocks differ in their ability to extract water from saline soil affects the leaching pattern in the soil. For example, salinity stress increased N leaching (Lea-Cox and Syvertsen 1993). Since salinity reduces water use and transpiration differently in different rootstocks, rootstocks can actually affect soil salinity (Levy and Shalhevet 1991). Most of the breeding work done on citrus rootstocks is aimed at producing dwarfing and disease tolerance (tristeza, phytophthora, and nematode), but not for salinity tolerance (J. R. Furr and J. B. Carpenter, pers. commun. 1975; Hutchison 1985; C. M. Anderson, pers. commun. 2000; G. W. Grosser, pers. commun. 2001). Some new rootstocks have been evaluated for salinity tolerance. Rootstocks released by Forner et al. (2000) include ‘F&A13’ (‘CLEO’ × ‘TRIF’) that accumulated half the amount of Cl– compared with ‘CLEO’ and only 16% of the amount of Na when irrigated for 7 months with saline water in the greenhouse. The hybrid rootstock ‘FA517’ (C. nobilis Lour × ‘TRIF’), was similar to ‘CLEO’ and much better than ‘CARZ’ in the same experiment. Two other hybrids, ‘020324’ (‘TROY’ × ‘CLEO’) and ‘030131’ (‘CLEO’ × ‘TRIF’) were also noted as Cl– and Na+ excluders. ‘CLEO’, which is one of the best Cl– excluding rootstocks, was recognized as a salt-tolerant rootstock even though it was never selected intentionally because of its salt tolerance, but rather as an ornamental (Chapman 1968). Future research should evaluate citrus crosses that were produced in different parts of the world and evaluated for disease tolerance or cold hardiness (Hutchison 1985; Dunaway and Dunaway 1996). There is hope that crosses of ‘CLEO’ with ‘RANG’ or ‘VOLK’ or even ‘TRIF’ may produce a rootstock that is better than ‘CLEO’ in terms of salt tolerance, vigor, and yield. Another direction to take may be to try to induce beneficial mutations in ‘CLEO’. 3. Ranking of Salinity Tolerance. Table 2.2 summarizes the Cl– tolerance ranking reported in different studies during the last seven decades. 4. Effect of Scion Cultivars. Just as growth and yield responses of citrus scions and rootstocks differ in sensitivity to salinity (Cooper et al. 1951, 1961; Levy 1986, 1997; Levy and Shalhevet 1990, 1991; Levy et al. 1992, 1999a,b; Levy and Lifshitz 2000a), there are scion differences in salt sensitivity of leaf gas exchange physiology that may be attributed to genetic
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differences. Net gas exchange of CO2 in ‘Marsh’ grapefruit leaves was more sensitive to salt stress than in ‘Navel’ or ‘Valencia’ orange regardless of the rootstock on which they were grafted (Lloyd et al. 1990). This observation was attributed to the higher accumulation of Na+ in grapefruit leaves than in orange leaves even though grapefruit leaves also accumulated the most Cl–. However, salinity experiments with mature grapefruit and ‘Washington Navel’ oranges also indicated that grapefruit growth and yield were more susceptible than orange to salinity (Levy and Shalhevet 1991). In this case, salinity effects were manifested by Cl– accumulation in the leaves and yield reduction of grapefruit grafted on salt-sensitive ‘RL’ (Levy and Shalhevet 1991; Levy et al. 1992). There are also differences in the susceptibility of different citrus scions to salt damage from overhead irrigation. Similar to the report above, ‘Marsh’ grapefruit had more leaf damage than ‘Temple’ or ‘Valencia’ orange trees when irrigated with water containing 2800 mg L–1 total salts (about 1000 mg Cl– L–1; Calvert and Reitz 1965). This may be related to differences in cuticular permeability to Cl–, as well as to the sensitivity of the different cultivars to salinity. Such genetic differences of scion types may also be attributable to different sensitivities to Cl– or to an ability of salt-tolerant types to compartmentalize toxic ions in the vacuoles away from the physiologically active cytoplasm. However, x-ray analysis could not detect such compartmentation in citrus under salinity stress (M. Talon, pers. commun. 2001). It is interesting to note that leaves containing high Cl– levels from saline foliar sprays did not have the same reductions of photosynthetic assimilation of CO2 that would be expected from similar leaf Cl– levels that accumulated from salinized soil (Romero-Aranda and Syvertsen 1996). Future research should focus on such potential differences (and others) with a goal to achieve an understanding of the underlying mechanisms of salinity tolerance. This understanding may lead to breeding salt-tolerant scions that will continue to yield commercial crops in spite of Cl– or Na+ accumulation in their leaves. Breeding of such halophytic-like cultivars, however, seems to be a distant prospect today (Yeo 1998; Barkla et al. 1999).
III. EXPERIMENTAL METHODS IN SALINITY RESEARCH Reliable data on the yield response of citrus or any other commercial crop to salinity can be obtained only from carefully controlled and wellreplicated field experiments conducted across a range of salinity treatments (Shannon 1997). Tests should include mature yielding trees during a long time span (years) in order to evaluate possible cumulative
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effects of salinity on tree development and yield. Such experiments are expensive and thus rare (Hoffman et al. 1989). Young seedlings often provide indications as to the anticipated response of the trees to salinity and, as such, seedlings as early indicators may be tools in testing new breeding materials and cultural practices even though in many cases they may fail as rootstocks for mature trees. A. Leaf Analysis Leaf analysis was developed as a tool for assessing the nutritional needs of citrus. Some of the standards developed in Riverside, California (Chapman 1968; Embleton and Jones 1964; Embleton et al. 1973) were based on hydroponics along with some actual nutrition field experiments and field observations. The work of Cooper et al. (Cooper et al. 1951, 1955; Cooper and Gorton 1952; Cooper 1961) also contributed to the establishment of tolerances for Cl–, Na+, and B concentrations in citrus leaves. There are some disadvantages in using leaves for assessment of salt accumulation. Mineral concentrations depend on leaf age, so leaves should be sampled carefully to ensure that they are of the same age (Embleton et al. 1962a). Leaves exposed to saline irrigation water may absorb salt directly through the epidermis (Stolzy et al. 1966) or have non-washable salt residues adsorbed on the leaf surface. Therefore, leaf analysis may not always be indicative of ion uptake by roots. Another serious problem is the tendency of leaves most affected by salinity to abscise before the usual summer/autumn sampling date, resulting in the sampled leaves not being representative. B. Juice Analysis Juice analysis can give a better ranking of the susceptibility of citrus rootstocks to salinity (Levy and Shalhevet 1990; Levy et al. 1992, 2000; Levy and Lifshitz 1995, 2000a). Juice analysis has several advantages over leaf analysis. A much more uniform tissue is used and the sample can be much larger. There can be 3 to 6 kg fresh weight of fruit per juice sample vs. about 50 g for leaves. As a rule, in most citrus cultivars (except summer lemon) all the fruits are of a similar calendar age and it is easy to eliminate surface contaminants from the juice. There is no need for extensive preparation of juice samples for analysis since fresh citrus juice can be analyzed directly for Cl–, Na+, and K+. Analysis results can be obtained shortly after the juice is extracted (Levy and Shalhevet 1990). The concentration of Cl– and particularly Na+ in juice is often lower than that of
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tap water, so care should be exercised to prevent contamination of juice with tap water during juice extraction. Since variability is lower than with leaf analysis, juice analysis can give a better ranking on the uptake of Cl– and Na+ by the different rootstocks (Levy and Shalhevet 1990; Levy et al. 1992, 2000; Levy and Lifshitz 1995, 2000a). C. Seed Mineral Content Seed tissue of eleven citrus species revealed significant differences in Cl– concentration calculated on a dry weight basis (Altman and Goell 1970). This result correlated well with the Cl– concentrations in the leaves of the same plants. However, there was no significant difference in Cl– concentrations of seeds from 10-year-old ‘Clemantine’ mandarin grafted on different rootstocks and watered with non-saline water. Increasing the Cl– concentration of irrigation water from 130 to 1800 mg L–1 did not affect the Cl– concentration of the seeds of ‘Shamouti’ orange trees grafted on salt susceptible ‘Palestine SwL’ rootstock. Thus, it does not appear that seed Cl– concentrations can be a reliable indicator of salinity tolerance, nor is it conveniently sampled tissue. D. Biochemical Indicators An intriguing possibility is to identify an indicator of membrane permeability to Cl– and, thus, an indicator Cl– tolerance. Treatment with high salinity increased free sterols in the young fibrous roots of salttolerant ‘RANG’, and reduced free sterols in the non-tolerant ‘Kharna khatta’ rootstock of India (C. karna Raf.) (Douglas and Walker 1983). A significant correlation was found between the ratio of the “more planar” cholesterol and campesterol to “less planar” sterols in the free sterol fraction. In the absence of salt stress, this ratio was lowest in ‘RANG’, intermediate in ‘Kharna khatta’, and highest in ‘Etrog’ citron, correlating to their Cl– exclusion. This finding was interpreted as a potentially useful indicator of membrane permeability of the different genotypes. Another study suggested that the phospholipid to free sterol ratio could be used to assess Cl– exclusion ability in citrus (Douglas and Sykes 1985). Unfortunately, these studies have not been continued. E. Seed Germination Salinity reduces seed germination initially through the osmotic effect of the solution, but there was no evidence that the tolerance to salinity during germination was correlated with the tolerance of the plant to
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salinity (Zekri 1993). This finding was confirmed in a recent study (Zekri 2001). ‘CARZ’, which is a Cl– accumulator, was the first to germinate at high salinity, ‘SO’ the last, and ‘CLEO’, the best Cl– excluder, was intermediate. The author suggested that stem analysis of seedlings germinated at high salinity could serve as an indicator of Cl– tolerance. F. Solution Culture vs. Soil Culture Much of the early work on the salt tolerance of citrus rootstocks to salinity was based on hydroponics or sand culture. These studies ranked ‘RL’ and ‘SO’ as moderately tolerant to salinity (Cooper et al. 1952; Bernstein 1969, 1980). Later, under field conditions, it was found that ‘SO’ could tolerate salinity (Bielorai et al. 1983, 1985) and that ‘RL’ was much more sensitive to salinity than ‘SO’ (Shalhevet and Levy 1990; Levy and Shalhevet 1990, 1991). Thus, ion uptake by roots in solution culture can be different from that by roots growing in soil. Irrigation method can also interact with the response of field-grown rootstocks to salinity (Wutscher et al. 1973). Roots growing in an aqueous environment encounter entirely different solute gradients than roots in soil. In soil, the mass flow of solution toward the root by transpiration is much greater than the diffusion away from the root unless there is continuous leaching of salts by rainfall or irrigation (Yeo 1998). If a root in soil excludes Na+ or Cl– ions, they will not move away from the root. Thus, roots may actually increase soil salinity by salt exclusion. In addition, salinity-tolerant citrus rootstocks can increase the soil salinity because they do not limit water uptake as salinity increases compared with non-selective rootstocks (Levy and Shalhevet 1991). This condition is very different from flowing or stirred hydroponic solutions. In this respect, sand culture may be similar to hydroponics since sand is usually frequently irrigated with an excess of nutrient solution. Roots also interact with soil microflora such as vesicular arbuscular mycorrhizae (VAM), that are missing in water culture and may be altered or absent in sand culture. Roots develop a different anatomy when grown in solution-culture than when grown in soil. In addition, since nutrient solutions have different aeration and usually a different pH than the soil, salinity responses of solution culture plants are usually different from that of trees in soil. There are examples, however, of short-term, high-salinity hydroponic culture of citrus hybrids where leaf analysis was coupled to plant development and gave a rapid indication of their possible Cl– tolerance when used as rootstocks under real field situations (Sykes 1985).
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G. Seedling Rootstocks vs. Budded Trees The majority of commercial citrus trees are composed of a rootstock and a scion, which are two different Citrus (or Poncirus) species or their hybrids. Exceptions may be lime trees (C. aurantifolia L.) that are vegetatively propagated from cuttings or ‘Emperor’ (‘Empress’) mandarin trees grown as seedlings. The rootstock develops the root system that absorbs water, nutrients, and salts from the soil; the scion develops the branch system and leaves, transpires water, fixes CO2, flowers, and develops the fruit. It is the scion that suffers most from the stress caused by salinity. Many rootstocks behave differently when scions are budded on them than when grown as unbudded seedlings. For instance, ‘MACR’ as a rootstock produces a large and prolific tree for virus-free scions in Israel (Levy et al. 1980; Levy and Lifshitz 1995), Arizona (Fallahi and Rodney 1992; Wright 1999), and Spain (A. Garcia Lidon pers. commun. 2001), but on its own roots, ‘MACR’ will remain a relatively small tree with only a few fruit. To have practical significance, studying physiological processes in un-budded rootstock seedlings should be augmented by studies with grafted scions in order to distinguish between the effect of the rootstock as a root system and the possible effects of shoot anatomy and physiology. Shoot and leaf characteristics of a seedling of a rootstock species have no practical significance once it is grafted. Physiological responses of shoots and leaves (including photosynthetic responses) of rootstock seedlings, however, can yield valuable information about physiological functions of the root system that can have practical significance for understanding underlying mechanisms in the root systems of commercial trees. The compound genetic system of a citrus tree presents other potential complications that do not occur in seedlings. The specific scion can influence ion uptake by the rootstock (Cooper et al. 1952). The budunion itself may affect the transfer of nutrients and toxic elements from root to canopy. This is especially true of some specific rootstock/scion combinations that are partially incompatible. In addition, the bud-union is the part of the grafted tree that may be first affected by several virus diseases, further complicating the response of the whole tree to the environment variables.
H. Greenhouse vs. Field Studies Most of the knowledge about the salinity tolerance of rootstocks comes from water-culture or container experiments. These experiments are usually short-term, and comparatively high salinities are used in order
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to measure results quickly. Often the response of mature, grafted trees was different from that of young seedlings in pots (Levy et al. 1992). As with seedlings vs. budded tree studies, pot experiments with confined root systems should be corroborated in long-term orchard experiments before recommendations based on results are adopted in commercial practices. Obviously, long-term field experiments are more difficult and less common than shorter-term pot experiments in fruit trees (Hoffman et al. 1989). I. Tissue Culture vs. Whole Plant Much of our physiological knowledge at the molecular level comes from bacterial or animal systems, which are very different from whole plants. Animal cells and respiring plant tissues absorb O2 and release CO2. The O2 concentration in air is about 21%, while the CO2 that the green plant tissues combine with water to make sugars is only present at a concentration of about 0.03%. Plant leaves unavoidably transpire a relatively huge volume of water while acquiring CO2 for photosynthesis. Plant cell suspensions do not transpire and in vitro plants from tissue cultures transpire very little water, so there is relatively little exchange of water and ions with their environment. Toxic ions that are not absorbed by cell or tissue cultures will remain uniformly distributed in the culture media and not accumulate in the media near cells (Yeo 1998). This situation is very different from the accumulation of excluded ions in the rhizosphere of roots growing in soil. Thus, in vitro cultured cells and tissues can tolerate much higher external salinity in the media than a transpiring plant growing in soil. Variant cell lines selected from cultured somatic cells can exhibit a level of tolerance to salinity (Ben Hayyim and Kochba 1983; Ben-Hayyim and Goffer 1989; Kochba et al. 1982). As stated by Kochba et al. (1982), the salt tolerance of selected cell lines will be of agronomic value only if the tolerance achieved is maintained in all stages of plant development. The major limitation of tissue culture is that the selected salinity tolerance character often cannot be maintained during the regeneration process and tolerance mechanisms that depend on the integrated function of the differentiated tissues cannot readily be identified in cell culture (Shannon 1997; Yeo 1998). Thus, salinity tolerance for terrestrial agriculture is a whole plant function that can best be studied in intact plants in the field. Induction of natural genetic mutations may offer improvements in salinity tolerance. Flowers and Yeo (1995) state that mutation works best with factors likely to be controlled by a single gene. Tolerance to abiotic stresses is usually a function of a group of complex quantitative genetic
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characters and, thus, very few successes have been reported in breeding plants with increased stress tolerance. Garcia-Agustin and Primo-Millo (1992, 1995) treated unfertilized TROY ovules with the mutagen ethylmethyl-sulphonate, and selected three lines that accumulated little Cl– and Na+ along with high concentration of K+ in leaves when subjected to increasing NaCl in the culture medium. However, two of the selected lines partially lost this characteristic when they were vegetatively propagated from cuttings and grown in the absence of saline selection pressure. Since only a true mutant continues to carry a stable trait in the absence of selection pressure (Garcia-Agustin and Primo-Millo 1992, 1995), these lines apparently were only phenotypically acclimated to salinity and lost this characteristic when propagated. Cervera et al. (2000) transformed plants of ‘CARZ’ with the halotolerance gene HAL2, which confers Li+ and Na+ tolerance in yeast and so was implicated in salt-tolerance mechanisms. The transgenic nature of these plants was confirmed by Southern and Northern analyses, and was the first time that a gene from yeast had been stably integrated and expressed in citrus plants. However, when whole plants were tested in the greenhouse, the transformed ‘CARZ’ plants did not differ in their susceptibility to salinity from control ‘CARZ’ plants (L. Peña and M. Talon, pers. commun. 2001). These contrast with results with tomato plants that were transformed with the HAL1 gene from yeast (Gisbert et al. 2000), which reduced both root and leaf Na+ and increased K+. Cervera et al. (2000) concluded that salt tolerance is a multigenic and quantitative trait, and both improvement and evaluation of this characteristic is difficult. This is especially true for Cl– toxicity tolerance in citrus, which is not well understood and apparently is not governed by a single gene. Introduction of transgenic genes for salinity tolerance into commercial rootstocks or preferably directly into commercial scion cultivars could result in the production of “halophytic” citrus. This prospect seems remote at the present time due to our lack of basic knowledge about salinity tolerance in citrus. However, progress is rapid in yeast molecular genetics for improvement of salt tolerance in plants (Matsumoto et al. 2002) and a breakthrough is possible.
IV. PHYSIOLOGICAL RESPONSES A. Amino Acids Accumulation Non-protein amino acids like proline, often reported as a stress metabolite, increase with drought stress (Levy 1980; Yelenosky 1979) and also with salt stress (Dunn et al. 1998). Proline has been reported to have a
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role in stressed plants (Syvertsen 1984; Syvertsen and Smith, Jr. 1984), where it acts as an osmoticum and/or a storage source of N. Arginine concentration in ‘VOLK’ feeder roots (percent of total amino acids) was doubled by salinity, while phenylalanine ammonia lyase (PAL) was reduced (Dunn et al. 1998). These may reduce the chemical defenses of the plant to nematodes as discussed below. Free proline increased with salinity in the leaves of lemon grafted on the relatively salt-tolerant ‘SO’, but not when grafted on the more salt-susceptible ‘MACR’ (Nieves et al. 1991). In another study (Walker et al. 1993), proline increased significantly only in lemon leaves on ‘RANG’ exposed to Na2SO4 but not when irrigated with NaCl. Its increase with salt stress supports its role in stressed plants where it acts as an osmoticum. Betaine levels in leaf tissues of ‘CARZ’ were also positively related to soil salinity (Duke et al. 1986). These compounds are considered as osmo-protectants, which may be “engineered” into citrus for better total salt (osmotic and drought) tolerance (Nolte et al. 1997) but not for reduction of specific mineral toxicity. B. Net Gas Exchange of Leaves There have been several studies comparing stomatal conductance (gs) and photosynthetic assimilation of CO2 (ACO2 ) in leaves from salinized trees with gas exchange values from non-salinized controls. It is clear that salt stress reduces water use and ACO2 but the underlying mechanisms are still debatable. Much of the controversy surrounding salinityinduced limitations on net gas exchange follows the same argument as the relative importance of osmotic stress vs. toxic ion stress of Na+ and Cl–. Osmotic stress from saline soils undoubtedly reduces water use and gs, but the magnitude of this reduction depends on the rate at which salinity stress develops and the duration over which it exists. Leaf proline concentration (Syvertsen and Yelenosky 1988) and proline-betaine levels (Lloyd et al. 1990; Banuls and Primo-Millo 1992) increased with salinity-induced osmotic stress. Potentially negative osmotic shock effects on plant-water relations usually do not occur if there are ample cations available to gradually allow leaf tissues to lower osmotic potential (Ψπ) to compensate for losses of turgor. For example, long-term moderate salinity stress lowered leaf Ψπ such that turgor was maintained and leaves suffered little or no drought stress-like symptoms (Syvertsen et al. 1988). Turgor can be even higher in salt-stressed trees than in nonstressed control trees (Behboudian et al. 1986). This is why controlled salinity studies often gradually build up salt concentrations in the irrigation water to avoid osmotic shock and defoliation.
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Patterns in gs usually follow patterns in ACO2, which has caused some researchers to mistakenly link declines in ACO2 to salinity-induced reductions in gs. This speculation is probably not the case, however, since low gs probably only directly limits ACO2 at very low leaf water potential (Ψw) or at large vapor pressure deficits (Farquhar and Sharkey 1982). In most cases, including moderate salinity stress, changes in ACO2 cause changes in gs. Lloyd et al. (Lloyd and Howie 1989b; Syvertsen and Lloyd 1994) examined effects of salinity on the relationship between ACO2 and internal CO2 concentrations and concluded that reductions in ACO2 were due to a direct biochemical inhibition of mesophyll photosynthetic capacity followed by reductions in gs. Thus, other than osmotic shock responses, most decreases in net gas exchange attributable to salinity are probably caused by ion toxicity responses. Since the most common source of salt stress is NaCl and both ions often accumulate together, it is difficult to determine the relative importance of Na+ vs. Cl– ions in reducing ACO2. There are many reasons why decreases in the net gas exchange of leaves in response to salinity are complicated by salinity-induced variations in leaf nutrition and by leaf chlorophyll. Increases in leaf Na+ interact with Ca2+ and K+, whereas leaf Cl– interacts with the anions NO3– and SO42–. Many problems associated with toxic levels of Na+ are probably due to deficiencies of K+ and Ca2+. These deficiencies explain why salinity effects can be ameliorated with Ca amendments (Cooper et al. 1958; Banuls et al. 1991; Banuls and Primo-Millo 1992). Ca2+ amendments also help remove Na+ from soil colloids and free Na+ to be leached. There can also be direct effects of leaf Cl– on other ions. For example, high Cl– reduces N uptake (Syvertsen et al. 1993) and decreases NO3– N use efficiency (Lea-Cox and Syvertsen 1993). There are direct effects of salinity on leaf chlorophyll concentrations that are reflected in variations in ACO2. In the field or in high-light greenhouses, leaf chlorophyll concentration usually decreases with salinity stress in well-watered trees (Syvertsen et al. 1988; Romero-Aranda et al. 1998). Interestingly, surviving leaves from drought-stressed salinized trees did not suffer losses of chlorophyll. In low-light growth chamber studies, however, leaf chlorophyll is affected little by salinity (Lloyd et al. 1987a) and can even be higher in salinized leaves than in nonsalinized control leaves (Lloyd et al. 1987b). Several studies describe decreases in citrus leaf ACO2 in response to elevated leaf Cl– (Syvertsen and Lloyd 1994; Storey and Walker 1999). Although citrus has been considered to be sensitive to Cl– toxicity, Syvertsen et al. (1988) found no effect of salinity on gas exchange of remaining leaves on ‘Valencia’ orange trees on both ‘SwO’ and ‘TRIF’ rootstocks despite foliar concentrations (cell sap basis) of Cl– as high as
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400 mol m–3 (mM). These trees had already sustained some salinityinduced defoliation such that whole tree-water relations were dramatically affected. Defoliation can actually increase ACO2 of the surviving leaves (Syvertsen 1994; M. Talon, pers. commun. 2001). As leaf canopies became thinner, salinity responses of retained leaves were affected little. The inhibition of citrus leaf photosynthesis by high Cl– concentrations (Walker et al. 1982; Lloyd and Howie 1989a) appears especially prominent when rates of Cl– entry into foliage are rapid. If rapid salinity stress in the field induces leaf abscission, physiological responses to salt stress can only be characterized in the remaining relatively young leaves, that have relatively low concentrations of Cl–. This occurrence can lead to a misinterpretation of the relative importance of leaf Cl– relative to leaf Na. Nonetheless, high correlations between net gas exchange and salinity in two orchard sites in Australia (Syvertsen et al. 1988; Lloyd and Howie 1989a) were attributed to a Na+ rather than a Cl– effect on citrus leaf gas exchange. Reductions in ACO2 can be attributed to high Na+, especially when there are relatively low Ca and K+ concentrations in leaves. Although leaf injury can be correlated with Cl– concentrations, studies have shown that reductions in ACO2 depend on the relative sensitivity of the scion type rather than on the absolute concentration of Na+ or Cl– (Banuls and Primo-Millo 1995). Salinity caused a progressive loss in variable fluorescence under strong irradiance. Adaxial (upper) surfaces were especially vulnerable to this apparent photoinhibitory damage, which coincides with the apparent bronzing that is typical of Cl toxicity. Predawn increases in maximal fluorescence correlated with leaf Cl– (Lloyd et al. 1986). Rootstock differences in Cl– exclusion characteristics also are reflected in salinity effects on ACO2 (Lloyd et al. 1987a,b). ‘Valencia’ orange trees on TRIF rootstock had a less rapid decline in leaf gas exchange when exposed to 1775 mg Cl– L–1 (50 mol m–3) NaCl than did equivalent foliage on ‘CLEO’ despite much higher Cl– concentrations in leaves on scions budded to ‘TRIF’. Although this rootstock effect was attributed to higher Na+ levels in scion foliage budded on ‘CLEO’, underlying levels of leaf Cl– were much higher in trees on ‘TRIF’ than in those on ‘CLEO’. In spite of high levels of Na+ in NaNO3 treated leaves, there were no reductions in ACO2 that could be attributed to Na+ (Banuls et al. 1997). C. Salinity Interactions with Physical Environmental Factors 1. High Temperature and Evaporative Demand. There are direct interactions between salinity, leaf water relations, irradiance, leaf temperature, and atmospheric evaporative demand that are impossible to
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separate in the field. Physiological mechanisms underlying environmental interactions with salinity can only be studied in controlled environments. Such studies may provide insights into cultural practices or environmental conditions that can improve production under salinity stress. Citrus leaves growing in full sun can experience temperatures that exceed air temperature by as much as 10°C (Syvertsen and Albrigo 1980). Leaf temperatures up to 45°C not only exceed optimum temperature for photosynthesis, but also lead to large vapor pressure differences (VPD) between leaves and air. Since citrus stomata are sensitive to evaporative demand, a large VPD can reduce gs and ACO2. Transpirational water use is also a function of VPD, and large VPDs can result in very low water use efficiency (WUE). Decreasing VPD by lowering leaf temperature or increasing humidity can increase gs, ACO2, and WUE. Misting tree canopies with high-quality water may improve salinity tolerance and decrease accumulation of toxic ions as found in tomatoes (RomeroAranda et al. 2001). Since salinity stress is greater for sun-exposed than for shaded leaves, additional shade may improve salinity tolerance. Artificial shade screens during the warmest season reduced citrus leaf temperature and improved WUE (Jifon and Syvertsen 2001) and likely would decrease salt stress. 2. Elevated CO2. Growing plants at elevated CO2 usually increases growth and ACO2 but at the same time, high CO2 decreases stomatal conductance. Elevated CO2 almost always leads to higher WUE, so it can disconnect rapid tree growth from high water use. Thus, elevated CO2 offers a tool to study mechanisms of salinity tolerance. If salt uptake is coupled with water uptake, then leaves grown at elevated CO2 should have lower salt concentrations than leaves grown at ambient CO2 (Ball and Munns 1992). In greenhouse studies using twice ambient elevated CO2, all citrus rootstock species studied increased growth and WUE in response to CO2, but ‘RANG’ and ‘CLEO’ were less affected by salinity stress than were ‘SO’ and ‘SwO’ (Syvertsen and Grosser, unpublished). Generally, the salinity-induced accumulation of Na+ in leaves was less when seedlings were grown at elevated CO2 than at ambient CO2, implying that the lower Na+ accumulation was linked to increased WUE. Na+ accumulation, however, was unaffected by elevated CO2 in ‘RANG’. In addition, ‘RANG’ also had the lowest leaf Cl– concentrations. The accumulation of leaf Cl– in salinized ‘SO’ was greater at elevated CO2 than at ambient CO2. Cl– concentrations were less at elevated CO2 in ‘CLEO’, but unaffected by CO2 in ‘RANG’. The decrease in Cl– accumulation at elevated CO2 in ‘CLEO’ was related to the increase in WUE, whereas the
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increase in leaf Cl– in ‘SO’ was not. Thus, relationships between salt ion accumulation and water use differed depending on the specific ions and citrus species. The growth increases in response to elevated CO2 in salt-tolerant ‘RANG’ were less under salt stress than without salt stress and there was little interaction between CO2 level and salinity for growth responses of ‘SO’ and ‘CLEO’. Seedlings of these three Citrus species, therefore, differed from other C3 non-halophytic species in which the enhancement of growth in response to elevated CO2 was greater when plants were exposed to salt stress (Ball and Munns 1992). Non-salinized plants were relatively less responsive to elevated CO2 than salt-stressed plants because non-salinized plants were growing near their maximum growth capacity, whereas salt-stressed plants had a greater potential for growth. This result differed for relatively slow-growing, salt-tolerant ‘SO’ and ‘CLEO’, where growth was enhanced by elevated CO2 similarly at high and low salinity (Syvertsen and Grosser, unpublished). In ‘RANG’, the adverse effects of salinity on growth were worse at elevated CO2. Thus, the salinity tolerance of ‘RANG’ may be reflected in the near maximum growth response of salinized seedlings at elevated CO2, whereas nonsalinized seedlings at elevated CO2 may have a greater potential for growth. D. Osmotic Stress Salinity affects citrus in two ways: osmotic stress and toxic ion stress. Dissolved salts exert an osmotic effect that reduces the availability of free (unbound) water through physical processes. This situation is analogous to drought stress and is discussed in detail below. The effect of osmotic stress is different when stress increases gradually and the plant can adjust to it compared with the situation when the Ψπ of the soil solution decreases abruptly. 1. Gradual Osmotic Stress. The osmotic effect from dissolved salts in the soil solution reduces the availability of free (unbound) water through the physical processes of lowering the energy of the soil solution. More free energy is required to overcome the lower Ψπ exerted by salts in solution, so there is less water available to roots. The energy required for roots to extract that water is referred to as osmotic stress. Osmotic stress can result in a reduction in root growth followed by a decline of canopy development and yield. When salinity stress is gradual, salt-tolerant rootstocks, that limit the translocation of the toxic ions Cl– and Na+ into the leaves, will acclimate
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to the lower Ψπ in the root zone by closing stomata and reducing transpiration (Syvertsen and Smith, Jr. 1983; Nieves et al. 1991). Ψπ can decrease in the plant by accumulating sugars and other osmoticum such as proline (Banuls and Primo-Millo 1992). Under saline conditions, Ψw reached values near –1.8 MPa. This reduction was offset by a decrease in the leaf Ψπ so that turgor was maintained at or above control values. The changes in Ψπ were closely correlated with changes in leaf proline concentration (Syvertsen and Smith, Jr. 1983; Rabe 1990; Eissenstat 1998; Nolte et al. 1997). Under osmotic stress caused by high nutrient concentrations (Syvertsen and Yelenosky 1988), ‘CLEO’ accumulated more proline than ‘SwO’ and ‘TRIF’ seedlings. This response may contribute to the relatively high tolerance of ‘CLEO’ to salinity. Enhanced accumulation of proline was considered to be a good indicator of superior salinity stress tolerance in breeding programs (Deng et al. 1993; Nolte et al. 1997), especially if the new lines also limit the uptake of Cl– and Na+. 2. Osmotic Shock. Osmotic shock can occur from excessive fertilization and from a drastic increase in water salinity in the soil solution. A rapid shock can occur as a result of light rain leaching accumulated salts into the root zone. The first apparent symptom of such an osmotic shock is abrupt leaf abscission, which may occur within days after the rain event or application of the salt. Typically, the lamina (leaf blade) separates at the abscission zone between the lamina and the petiole. The petiole may remain green and attached to the stem for some time. Leaf analysis of the abscised leaves may not reveal an increase in their Cl– or Na+ content. Such leaf drop can be prevented by irrigation during the initial rain period until sufficient rain leaches the previous accumulated salts. Similar leaf abscission is common for situations of sudden drought stress such as that caused by desiccating winds (Schneider 1968). Typically, citrus leaves will not abscise during drought but abscise only when irrigation (or rain) follows a severe drought. Ethylene production may be involved, since elevated ethylene is produced within 2 hours after rehydration (Tudela and Primo Millo 1992). Osmotic shock, induced either by a sudden salt increase or severe drought stress, increased abscisic acid (ABA) and aminocyclopropane1-carboxylic acid (ACC) in roots, xylem fluid, and leaves (GomezCadenas et al. 1996, 1998). Under salinity, the pattern of change of ABA, ACC, and proline followed a two-phase response: an initial transient increase (10 to 12 days) overlapping with a gradual and continuous accumulation. This biphasic response appears to be compatible with the proposal that the transitory hormonal (ethylene) rises are first induced
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by the osmotic component of salinity and then by Cl– accumulation (Gomez-Cadenas et al. 1998). Thus, osmotic shock induced ABA, ethylene production, and leaf abscission. E. Toxic Ions In addition to osmotic stress, part of the salt sensitivity in citrus is related to the specific toxic effects of accumulation of Cl–, Na+, B, and other ions in leaves (Bernstein 1980). One of the main differences between the effect of salinity on annual plants and trees is the gradual accumulation of toxic elements in the leaves and other plant parts in trees. These elements are transported by the transpiration stream and remain in the plant after transpired water has evaporated. 1. Chloride. Chloride toxicity in woody species is generally more severe and observed in a wider range of species than is Na+ toxicity (Shannon 1997). Citrus provides a good example. Since Cl– ion is more toxic to citrus than Na+, the concentration of Cl– in water is an important parameter in deciding the suitability of water for citrus irrigation (Bernstein 1980; Shalhevet and Levy 1990; Levy and Shalhevet 1991; Levy et al. 1992; Maas 1993; Storey and Walker 1999). Cl– can reduce leaf chlorophyll concentration (Zekri 1991), and cause bleaching or bronzing of sunlit leaves. There is ample evidence that Cl– can reduce photosynthesis in citrus leaves as discussed previously. Under warm, dry, summer conditions in Australia, a yield decrease of about 20% was calculated for each increase of 35.5 mg L–1 (1 mol m–3) of Cl– concentration in the irrigation water above a threshold concentration of about 152 mg L–1 Cl– (4.3 mol m–3). The yield decrease was attributable to Cl– toxicity rather than osmotic stress (Cole 1985). A similar negative correlation was found between leaf Cl– and yield under similar climatic conditions in Israel (Levy et al. 1992). 2. Sodium. Na+ is a toxic element that is perhaps a greater salinity problem in other plant species than it is in citrus. The significance of Na+ toxicity in citrus and other fruit trees is often overshadowed by the effect of Cl–. Na+ can be harmful through its effect on the absorption of other nutrients, especially K+. The amount of Na+ found in citrus leaves and juice is comparatively low; in lemon juice, it amounts to 0.1 g kg–1 fresh weight compared with 10 g kg–1 for K+ and 6 g kg–1 for Ca++ (Sinclair 1984). The application of NaNO3 was compared with Ca(NO3)2 for 9 years. The NaNO3 increased leaf Na+ concentration from 0.1 to 0.2 g kg–1 and reduced the yield of ‘Washington Navel’ orange by 25%. In the
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same experiment, feeder root Na+ concentration increased from 0.2 to 0.7 g kg–1. However, it is not clear if all the Na+ was inside the roots or just adsorbed on the root surface (Jones et al. 1952). In most situations, salinity problems are almost always caused by NaCl. The relatively greater importance of Cl– than Na+ is not unique to citrus. In stone fruits, Cl– was found to be the main damaging ion, whereas Na+ accumulated in leaves only after membranes had already been damaged by Cl– (Shannon 1997). This is probably true also for citrus, however, in situations where salinity is caused by non Cl– salts (mainly sulfates), Na+ toxicity can appear. As described for Cl–, rootstocks can have a significant effect on the amount of Na+ absorbed from the soil and transported to the leaves. Among the rootstocks, ‘CLEO’ absorbed more Na+ than most other rootstocks (Cooper et al. 1958; Taylor and Dimsey 1993; Azab 1998; Levy 1998; Levy et al. 2000). Poncirus sp. and its hybrids usually absorb less Na+ than other rootstocks. 3. Boron. A toxic element of great concern for citriculture is boron. Boron is unique among the toxic elements since the range between deficiency and toxicity is narrow; B deficiency and toxicity can appear in the same orchard. Leaf concentrations of B of 50 to 200 mg kg–1 dry weight was considered optimum, and above 200 mg kg–1 (Chapman 1968) or 250 mg kg–1 (Embleton et al. 1973) was considered to be in the excess range. Toxicity can be caused by high concentrations of available B in the soil, even when the total B concentration is low, such as in some desert sandy soils (Elseewi et al. 1977). Salinity caused an increase in leaf injury of cucumber due to B toxicity (Alpaslan and Gunes 2001). High B soils can be found in some semi-arid regions, including the lower Rio Grande Valley of Texas (Cooper and Gorton 1952), around the Mediterranean, in some fine-textured soils in Victoria, Australia (Penman and McAlphin 1949) and the internal valleys of Israel. Boron excess can occur in some natural water sources. It is usually higher in reclaimed water (Reboll et al. 2000) and may increase in desalinized water produced by reverse-osmosis of seawater. Natural seawater contains 4 to 5 mg L–1 B, but the water that is desalinized by reverse osmosis may still contain more than 1.8 mg L–1 B (Nadav 1999) and membranes cannot deliver less than 1 mg L–1 B (Taniguchi et al. 2001). Such a level of B may prohibit the utilization of reclaimed water derived from desalinized water for the irrigation of citrus or other Bsensitive plants. A multistage reverse osmosis membrane sea desalination process and a low pressure reverse osmosis process can be recommendable for B management with a reasonable additional cost in drinking water supply (Magara et al. 1998). Scofield and Wilcox (1931)
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concluded that irrigation waters containing more than 0.5 mg L–1 of B might injure sensitive crops such as lemons or walnuts. Since irrigation water containing more than 1 mg L–1 may injure other plants, the 1 mg L–1 threshold is probably a safe upper level for B in irrigation water for citrus (Parsons et al. 2001). Under severe B toxicity, typical symptoms appear in the summer, with leaf abscission in winter leading to completely leafless trees, before they flush in the spring. This can result in branch dieback and sun damage to branches. B toxicity is often accompanied by Cl– toxicity. The orange-yellow mottling of B toxicity is often difficult to distinguish from the bronzing symptoms of Cl– toxicity (Cooper et al. 1955). The nutrition status of the tree has an effect on the appearance of B toxicity symptoms. High rates of N fertilizer, especially Ca (NO3)2 (but not (NH4)2SO4), reduced the severity of the B-toxicity symptoms, although the concentration of B in leaves was not reduced (Cooper et al. 1958; Cooper and Peynado 1959). CaSO4 had no effect on B-toxicity. In high-B soils in Israel, a common practice has been to apply chicken manure to sprinklerirrigated citrus to counteract B toxicity. The chicken manure may act like a high organic, slow-release fertilizer, thereby improving overall mineral nutrition. The shift from high volume sprinkler to microirrigation along with continuous proportional fertigation also mitigated B toxicity. This effect was probably because of better N and P fertilization and because of increased leaching of the smaller soil volume with water low in B. Swietlik (1995) described a link between the appearance of B-toxicity symptoms and Zn deficiency. Apparently, Zn-deficient citrus seedlings were more sensitive to B toxicity, as only Zn-deficient seedlings reduced growth in response to high B. The B toxicity symptoms could be reduced with foliar applications of chelated Zn even though the B concentrations in leaves, stems, and roots of the foliar-sprayed seedlings were not reduced. This observation is important since B toxicity and Zn deficiency may occur simultaneously in some soils and Zn deficiency is relatively easy to correct by foliar application. The susceptibility of different rootstocks to B toxicity and their interaction with scions has a large effect on the development of B toxicity. In grapefruit grafted on different rootstocks, the highest B levels recorded for ‘ SwL’, ‘SO’ and ‘RL’ were intermediate, and ‘SwO’ had the lowest B uptake (Embleton et al. 1962b). In a rootstock trial for ‘Nova’ mandarin, B was highest in trees on ‘Yuma citrange’ and C. taiwanica and lowest on ‘SO’ (Georgiou 2000). Outstanding tolerance to B was reported for grapefruit and ‘Valencia’ orange grafted on Severinia buxifolia (Poir)
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Tenore (Cooper et al. 1955). Graft incompatibility may rule out this combination, which also causes abnormal concentrations of other leaf nutrients. ‘MACR’ was also among the most tolerant rootstocks to high B (Embleton et al. 1962b; Peynado and Young 1962). This may be associated with the fact that scion leaves on this rootstock usually have higher N concentration than other rootstocks (Caro et al. 1977; Levy et al. 1993). ‘SO’ was much more tolerant to B than ‘SwL’ and ‘RL’ in the Negev area of Israel (Levy et al. 1980). Among the scions, lemon was more sensitive than other cultivars, and ‘Shamouti’ orange was more sensitive than ‘Valencia’ orange to B toxicity. ‘Emperor’ mandarin had the lowest B levels regardless of rootstock (Taylor and Dimsey 1993). 4. Lithium. There are some reports that excessive lithium can become toxic in arid areas of California and Arizona (Aldrich et al. 1951; Bradford 1961; Hilgeman et al. 1970). Symptoms included necrotic lesions in grapefruit leaves and defoliation. Injury became evident after the trees were 10 years old and increased in severity as the trees aged. Hilgeman et al. (1970) reported marked differences between citrus species and varieties in either tolerance to Li+ or their influence on Li+ uptake. Grapefruit and lemon seem to be more susceptible than orange, and ‘Kinnow’ mandarin topworked on severely affected grapefruit did not show any symptoms. Toxicity may be linked to the effect of Li on Ca uptake (Epstein 1960) or to an inhibition of myo-inositol monophosphatase (IMP) that is required for de novo inositol synthesis (Gillaspy et al. 1995). This compound has been related to salinity tolerance in plants (Nelson et al. 1998). The threshold for toxicity was estimated to be 12 mg kg–1 in leaf dry weight (Bradford 1961) or between 50 and 90 mg kg–1 in leaf dry weight (Embleton et al. 1973). Such a high range may be related to the fact that Li+ may concentrate at lesions in leaves (Hilgeman et al. 1970). Bradford (1961) noted that Li+ toxicity symptoms were similar in many respects to B symptoms and soils that have an excess of Li+ usually are also high in B. There are no recent reports on Li toxicity in citrus. 5. Interaction between Salinity and Nutrient Ions. Salinity can cause nutrient imbalances in various ways. K+ can be leached from the soil exchange complex if excessive Na+ is present, and Na+ may also compete with K+ at the soil-root interface. This can result in K+ deficiency under saline conditions. Interestingly, some of the Cl–-tolerant rootstocks, such as ‘CLEO’, ‘Sunki’, and ‘Emperor’ mandarins, tend to suffer
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from K+ deficiency coupled with an increase in tissue Na+ content under saline conditions (Behboudian et al. 1986). One way to observe the interrelations of Cl– and Na+ is to use these ions with different anion combinations. Banuls and Primo-Millo (1992) compared the effect of NaCl, KCl, and NaNO3 on citrus photosynthesis, and concluded that NaCl and KCl increased Cl– leaf content and reduced photosynthesis. NaNO3, however, did not affect photosynthesis though it increased leaf Na+ content. These results were confirmed by RomeroAranda et al. (1998), who found that decreases in photosynthesis were highly correlated with increases in leaf Cl–. F. Vegetative Growth Growth of all plants is reduced by decreased leaf water potential (Maas 1986). The effect of salinity on plant growth is not always related to the accumulation of toxic elements in citrus leaves if toxic concentrations are not reached. For example, the growth of ‘SO’ and ‘CLEO’ was similar even though ‘SO’ accumulated more Cl– (Zekri 1991). Salinity also increases the succulence of citrus leaves (Cerda et al. 1977) and the thickness of the leaf lamina. Comparative anatomical observations indicated that the mesophyll increased in volume by simultaneous division and expansion of the cells as spongy parenchyma cells became larger and more rounded (Romero-Aranda et al. 1998; Nastou et al. 1999). In a short-term experiment, Sykes (1985) reported that salinity increased leaf water contents acropetally in only some of the rootstocks tested. G. Fruit Yield and Quality 1. Yield. Many salinity tolerance comparisons have been based on relative reductions in fruit yield. ‘Verna’ and ‘Fino’ lemons, on ‘SO’ and ‘MACR’ rootstocks, had reduced yields as salinity increased (Nieves et al. 1992). Fruit yields decrease about 13% for each 1.0 dS m–1 increase in electrical conductivity of the saturated-soil extract (ECe) once soil salinity exceeds a threshold ECe of 1.4 dS m–1 (Maas 1993). In Australia (Cole and McCloud 1985), regression analysis during the period 1945–1979 on data from irrigated orchards showed that yield was negatively associated with salinity at the locations with highest salinity. Fruit yield of ‘Washington Navel’ orange decreased with increasing salinity due to a reduced number of fruits per tree rather than reduced average fruit weight (Haggag 1997). Increased salinity of ground water caused by seawater intrusion reduced the yield of ‘Satsuma’ mandarins
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grafted on trifoliate orange rootstocks in Western Turkey (Aksoy et al. 1996). ‘Shamouti’ orange on ‘SO’ did not absorb much Cl– after 6 years of salinization (up to 0.44% Cl leaf dry weight) with water up to 462 mg Cl– L–1 (13 mol m–3 Cl–). The 14% reduction in yield was mainly due to osmotic stress (Dasberg et al. 1991). However, continued exposure to salinity could have caused accumulation of Cl– to toxic levels. 2. Internal Quality. Although drought stress can have a profound effect on citrus internal quality, the effect of salinity is usually very subtle. Most salinity studies report a slight increase in juice solids, sometimes accompanied with a similar increase in acidity, which causes the TSS to acid ratio to remain unchanged (Boman 2000; Levy et al. 1978, 1979). This observation implicates a reduced water movement into the fruit due to the osmotic effect of salinity. The production of more solids in fruit may have a significant importance in fruit for processing. H. Phytochemicals Citrus fruits contain several phytochemicals and/or nutraceuticals such as carotenoids (lycopene and β-carotene), limonoids, flavonones (naringin and naringin rutinoside), folate, and vitamin C that have important medical benefits in human diets. Phenolic compounds have been used to establish taxonomic relationships among fruit cultivars (Berhow et al. 1998) and many phytochemicals vary with rootstocks (Kefford and Chandler 1970). This fact implies that the accumulation of these materials in fruit is subject to variations in water relations, mineral nutrition, and/or plant growth regulators that are attributable to rootstock. There are data indicating that several phytochemicals can be enhanced by preharvest factors such as cultivar and season (Patil 2000). Red and pink grapefruit cultivars have higher lycopene and total carotenoids than white-fleshed ones and concentrations of most phytochemicals change as seasonal maturity progresses. In addition, there are a few studies on effects of soil moisture status, temperature, and freezing on juice constituents (Kefford and Chandler 1970). Flavonones and liminoids increase during post-harvest storage (Patil et al. 2000). Undoubtedly, such responses in fruit are related to dehydration and/or dilution of juice. It is tempting to speculate that just as rootstocks affect salinity tolerance, salinity stress may affect the accumulation of phytochemicals. Controlled salinity stress might enhance the concentration of phytochemicals in juice. We know of no data, however, to support this speculation, but this is an area that may merit future research work.
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V. SALINITY AND BIOTIC STRESSES A. Phytophthora Multiple stresses can have synergistic effects on plants. Much of the work on interactions between salinity and pathogens has been done using seedlings. In field trees, however, the scion can affect the susceptibility of the rootstock to root rot (Shaked et al. 1984). In greenhouse experiments, irrigation with high-salinity water with a Cl– concentration of 1670 mg L–1 predisposed citrus rootstocks to attack by root pathogens (Combrink et al. 1996). Rootstock seedlings of ‘TROY’, ‘CARZ’, ‘VOLK’, and ‘RL’ were most affected by the treatment consisting of three root pathogens in combination (Phytophthora nicotianae, Fusarium solani, and Tylenchulus semipenetrans) under saline conditions. Growth of these seedlings subjected to both Phytophthora and salinity together was significantly less than that of seedlings subjected to the pathogens either singly or with Cl– stress alone. Phytophthora infection and Fusarium root rot were always more severe in combination with Cl–. ‘VOLK’ and ‘RL’ were more severely affected by the three pathogens than ‘TROY’ and ‘CARZ’. In addition, ‘TROY’ and ‘CARZ’ citranges, with known tolerance to P. nicotianae and T. semipenetrans, became more susceptible to these pathogens when irrigated with high-salinity water. Salinity also affected stem infection. Stems of ‘SO’, ‘RL’, and ‘TROY’ were inoculated with a fungus identified as P. citrophthora, and regardless of rootstock, NaCl (but not Na2SO4) increased stem gummosis (El Guilli 2000), pointing again to the detrimental effect of the Cl– ion on citrus. Increased disease could have resulted from increased tissue susceptibility in response to salinity stress, inhibition of plant defense (Afek and Sztejnberg 1993), and/or decreased root regeneration. Phytophthora isolates cultured from diseased citrus growing in the saline soils of the Coachella valley in California tolerated salinity more than a culture isolated from citrus growing in non-saline soil (Blaker and MacDonald 1985). The ability of Phytophthora to tolerate high levels of salinity could significantly diminish the resistance of Phytophthora-tolerant rootstocks such as ‘TROY’ under saline conditions (Blaker and MacDonald 1986).
B. Rio Grande Gummosis Rio Grande gummosis, a disease of unclear etiology, was attributed to irrigation with high-salinity water and to applications of KCl or CaCl2 but not to K2SO4 (Childs 1978). Although the Cl– levels in the leaves were
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similarly normal in infected and non-infected locations, Cl– levels in the bark and wood were about 10 times higher than those in the roots and almost four times higher in an orchard infected with Rio Grande gummosis than in the non-infected orchard (Russo et al. 1993). However, analysis of grapefruit trees on different rootstocks in Florida indicated no relationship between rootstock tolerance to salinity and incidence of Rio Grande gummosis (Sonoda and Pelosi 1990). In a long-term salinity experiment at Gilat, Israel (Y. Levy and J. Shalhevet, unpublished results), there was no correlation between the salinity of the irrigation water and appearance of Rio Grande gummosis in ‘Marsh’ grapefruit. There was adequate disease pressure present, however, as trees at different salinities were infected at random. In Israel, Rio Grande gummosis commonly affects grapefruit trees on ‘TROY’ or on ‘SO’ that suffer from lime-induced chlorosis. The problem can be corrected by the application of chelated iron and by modifying the irrigation system from sprinkler to drip. This occurrence leads us to the conclusion that Rio Grande gummosis may be related to soil aeration, to lime-induced chlorosis, or to just general stress that may be caused by different factors and not only salinity. C. Nematodes The citrus nematode (Tylenchulus semipenetrans) can reduce the salt tolerance of citrus roots and increase Cl– uptake (Willers and Holmden 1980). Leaf Cl– levels of severely affected trees varied between 1.75 and 2.00% compared with 0.50–0.90% in less-infected trees under the same conditions; this was true for salinity-tolerant rootstocks and for salinitysensitive rootstocks, however. At the same experiment, nematodes increased more than three-fold the Cl– concentration in leaves but decreased the Cl– concentration in roots (Mashela and Nthangeni 2002). Salinity increased nematode egg production, with the largest number of eggs recovered from ‘CLEO’ and ‘SO’ roots, where salinity doubled the number of eggs. Salinity also increased the number of nematode eggs and females on rootstocks with better tolerance to nematodes, such as ‘TRIF’, ‘CTRM’, and ‘TROY’. However, the nematode number remained small, suggesting that salt-tolerant rootstocks are more susceptible to nematodes and nematode-resistant rootstocks lack salt tolerance (Mashela et al. 1992a). On the other hand, sudden reductions in soil salinity by rain or irrigation offered nematodes a suitable non-osmotic habitat that increased their population densities (Mashela et al. 1992b). Soil salinity increased the susceptibility of citrus roots to attack by the citrus nematode (Dunn et al. 1998). Thirty days of a high-salinity (0.1 M
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NaCl) treatment 6 months after inoculation with nematodes, increased the nematode infection rate by 54%. Phenylalanine ammonia lyase (PAL) activity was inversely correlated with salinity level and with increase in arginine concentration, suggesting that salinity caused a breakdown in root chemical defenses. D. Mycorrhizae Citrus trees interact with microorganisms that belong to various groups, including bacteria, fungi, and nematodes. Soil-borne pathogens constitute only a very small fraction of the total population of soil organisms (Katan 1996). These range from true parasites that always harm the roots to microorganisms that may exist in harmony with the plant or even benefit the plant. Citrus is very dependent on vesicular arbuscular mycorrhizae (VAM) colonization, especially under conditions of low soil P concentration or sterilized soils (Kleinshmidt and Gerdemann 1972; Krikun and Levy 1980; Menge et al. 1978). The ability of VAM to increase tree growth particularly under saline conditions and thus alleviating salinity stress has been reported. However, there have been some reports that VAM can increase Cl– uptake by plants, just as VAM increases P uptake. VAM plants of ‘CARZ’ and ‘SO’ accumulated more Cl– in leaves than non-mycorrhizal plants. Cl– was higher in non-mycorrhizal roots of ‘SwO’ and ‘CARZ’ than in mycorrhizal roots (Hartmond et al. 1987). Graham and Syvertsen (1989) reported that VAM increased the concentrations of Cl– in leaves and roots of ‘SwO’ and ‘SO’ seedlings irrigated with high-salinity water. This increase could not be attributed to increased transpiration in the VAM plants. Na+ concentrations, on the other hand, were not affected by VAM. There were no significant growth or physiological interactions between mycorrhizae and salinity. Natural VAM in relatively saline soils may be sensitive to salinity and its population decreased with increased soil salinity (Levy et al. 1983). VAM strains that originated in soils of different salinities may differ in this respect (Copeman et al. 1996; Juniper and Abbott 1993).
VI. BENEFITS OF MODERATE SALINITY Other than the benefits from moderate applications of fertilizer salts, salinity is usually not beneficial for citrus in the long run. Since citrus can tolerate moderate salinity and produce a profitable yield using
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proper cultural practices and tolerant cultivars, there may be some shortterm benefits from salinity. A. Chilling and Freezing Tolerance Moderate salinity at levels of 1065 to 2130 mg Cl–1 L–1 (30 to 60 mol m–3 of NaCl) applied for 2 months, reduced growth and total plant transpiration but enhanced cold hardiness of ‘SwO’ and ‘CLEO’ seedlings (Syvertsen and Yelenosky 1988) even though leaf Ψπ and leaf proline concentration did not change significantly. Thus, controlled salinity stress under greenhouse conditions can substitute for cool temperature-induced freeze tolerance in seedlings by reducing physiological activity and growth. However, when freeze injury was determined for young grapefruit trees on different rootstocks, trees with high Cl– content were more susceptible to freeze injury than those with low Cl– (Peynado 1982). B. Leaching Du Plessis (1985) suggested that reduced transpiration from salinity stress could potentially be a benefit in reducing the accumulation of soil salinity, since the lower water uptake should increase the leaching fraction. This scenario implies that an increase in the leaching fraction occurs when irrigating with increasingly saline water when water applications are scheduled similarly to those for non-saline conditions. However, soil salinity can increase proportionally to the salinity in the irrigation water and thereby reduce growth and yield. C. Increase Flowering, Yield Just as drought stress can substitute for cool wintertime temperatures to enhance flower induction (Nir et al. 1972; Southwick and Davenport 1986), it is possible that moderate salinity stress will also increase flowering. In a warm, wet climate with inadequate chilling or drought stress to maximize flower induction, controlled salinization might offer a substitute to induce flowering as is practiced for inducing flowering of litchi in Thailand (E. Tomer, pers. commun. 2001). If saline irrigation water could be applied during induction followed by adequate rainfall or irrigation with good-quality water during fruit set, yields might be increased. The successful economic use of such a practice, however, remains to be tested. As discussed above, effects of moderate salinity on fruit quality are usually subtle (Boman 2000).
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VII. SUMMARY Since decreases in the quality of the world’s water resources are inevitable, it is important that growers continue to improve production practices and genetic varieties to deal with poor-quality water to sustain production. Citrus can use reclaimed water better than other crops since fruit are either processed for juice or thoroughly washed and disinfected in the packinghouse prior to peeling (Parsons et al. 2002). However, reclaimed waters are higher in salinity than unused water and salinity will increase as urban water use efficiency improves. There are many things citrus growers can do to ameliorate problems associated with salinity stress, from choosing the best rootstock and scion cultivars to appropriately managing irrigation and fertilizer application methods. To help citrus growers cope with salinity problems, researchers should not only understand the mode of action of salinity stress but also understand the underlying mechanisms of salinity tolerance. Salinity reduces water use thorough osmotic effects but the gradual accumulation of Cl–, Na+, and B to toxic levels are equally or even more important in citrus trees. Fortunately, the different species of Citrus and their relatives differ in susceptibility to salinity, and future breeding may produce better rootstocks than are available today. Salinity tolerance is a whole plant phenomenon that requires an appreciation of citrus rootstock/scion interactions in the field. Such relationships are complicated by interactions between salinity and physical environmental factors as well as between salinity, pests, and diseases. The study of interactions between salinity, drought, and elevated CO2 can yield insights into salt exclusion/uptake, growth, and plant water use. New rootstocks or even salttolerant cultivars, together with improved cultural practices, such as nutrition, irrigation, drainage, and perhaps altering the physical environment, such as shading or raising humidity, may enable future citriculture to utilize lower-quality water. Not all effects of salinity are negative, however, as moderate osmotic stress can reduce physiological activity and growth, allowing citrus seedlings to survive cold stress. Short-term salinity can even enhance flowering after the salinity stress is relieved. LITERATURE CITED Afek, U., and A. Sztejnberg. 1993. Temperature and gamma irradiation effects on scoparone, a citrus phytoalexin conferring resistance to Phytophthora citrophthora. Phytopathology 83:753–758.
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Combrink, N. J. J., N. Labuschagne, R. O. Barnard, and J. M. Kotze. 1995. The effect of chloride on four different citrus rootstocks. South African J. Plant Soil 12:95–98. Cooper, W. C. 1961. Toxicity and accumulation of salts in citrus trees on various rootstocks in Texas. Proc. Fla. State Hort. Soc. 74:95–104. Cooper, W. C., and B. S. Gorton. 1952. Toxicity and accumulation of chloride salts in citrus on various rootstocks. Proc. Am. Soc. Hort. Sci. 59:143–146. Cooper, W. C., B. S. Gorton, and C. Edwards. 1951. Salt tolerance of various citrus rootstocks. Proc. Rio Grande Valley Hort. Soc. 5:46–52. Cooper, W. C., B. S. Gorton, and E. O. Olson. 1952. Ionic accumulation in citrus as influenced by rootstock and scion and concentration of salts and boron in the substrate. Plant Physiol. 27:191–203. Cooper, W. C., and A. Peynado. 1959. Chloride and boron tolerance of young-line citrus trees on various rootstocks. J. Rio Grande Valley Hort. Soc. 13:89–96. Cooper, W. C., A. Peynado, and A. V. Olson. 1958. Response of grapefruit on two rootstocks to calcium additions to high-sodium, boron contaminated and high salinity water. Soil Sci. 86:180–189. Cooper, W. C., A. Peynado, and A. V. Shull. 1955. Boron accumulation in citrus as influenced by rootstock. J. Rio Grande Val. Hort. Soc. 9:86–94. Copeman, R. H., C. A. Martin, and J. C. Stutz. 1996. Tomato growth in response to salinity and mycorrhizal fungi from saline or nonsaline soils. HortScience 31:341–344. Dasberg, S., H. Bielorai, A. Haimowitz, and Y. Erner. 1991. The effect of saline irrigation water on ‘Shamouti’ orange trees. Irrigat. Sci. 12:205–211. Deng, Z. N., W. C. Zhang, and S. Y. Wan. 1993. In vitro induction and protoplast plant regeneration from NaCl-tolerant lines in citrus. Acta Hort. Sinica 20:127–132. Douglas, T. J., and S. R. Sykes. 1985. Phospholipid, galactolipid and free sterol composition of fibrous roots from citrus genotypes differing in chloride exclusion ability. Plant, Cell, Environ. 8:693–699. Douglas, T. J., and R. R. Walker. 1983. 4-Desmethylsterol composition of citrus rootstocks of different salt exclusion capacity. Physiol. Plant. 58:69–74. Du Plessis, H. M. 1985. Evapotranspiration of citrus as affected by soil water deficit and soil salinity. Irrig. Sci. 6:51–61. Duke, E. R., C. R. Johnson, and K. E. Koch. 1986. Accumulation of phosphorus, dry matter and betaine during NaCl stress of split-root citrus seedlings colonized with vesicular-arbuscular mycorrhizal fungi on zero, one, or two halves. New Phytol. 104: 583–590. Dunaway, J. K., and K. W. Dunaway. 1996. The development of new citrus rootstocks. Proc. Fla. State Hort. Soc. 109:104–105. Dunn, D. C., L. W. Duncan, and J. T. Romeo. 1998. Changes in arginine, PAL activity, and nematode behavior in salinity-stressed citrus. Phytochemistry 49:413–417. Eaton, F. M., and R. B. Harding. 1959. Foliar uptake of salt constituents of water by citrus plants during intermittent sprinkling and immersion. Plant Physiol. 33:22–26. Ehlig, C. F., and L. Bernstein. 1959. Foliar absorption of sodium and chloride as a factor in sprinkler irrigation. Proc. Am. Soc. Hort. Sci. 74:661–670. Eissenstat, D. M. 1998. Responses of fine roots to dry surface soil: A case study in citrus. p. 224–237. In: H. E. Flores, J. P. Lynch, and D. Eissenstat (eds.), Radical Biology: Advances and perspectives in the function of plant roots. Current Topics Plant Physiology. Vol. 17. Am. Soc. Plant Physiol., Rockville, MD. El Guilli, M., H. Benyahia, A. Jrifi, and M. Besri. 2000. Effect of irrigation water salinity on trunk gummosis symptom severity for citrus affected with Phytophthora citrophthora. Fruits 55:181–186.
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Gomez-Cadenas, A., F. R. Tadeo, M. Talon, and E. Primo-Millo. 1996. Leaf abscission induced by ethylene in water-stressed intact seedlings of Cleopatra mandarin requires previous abscisic acid accumulation in roots. Plant Physiol. 112:401–408. Gonzalez-Altozano, P., and J. R. Castel. 1999. Regulated deficit irrigation in Clementina de Nules’ citrus trees. I. Yield and fruit quality effects. J. Hort. Sci. Biotechnol. 74: 706–713. Graham, J. H., and J. P. Syvertsen. 1989. Vesicular arbuscular mycorrhiza increase chloride concentration in citrus seedlings. New Phytol. 113:29–36. Grieve, A. M., and R. R. Walker. 1983. Uptake and distribution of chloride, sodium, and potassium ions in salt-treated citrus plants. Austral. J. Agr. Res. 34:133–143. Gucci, R., and M. Tattini. 1997. Salinity tolerance in olive. Hort. Rev. 21:177–214. Haggag, L. F. 1997. Response of Washington Navel orange trees to salinity of irrigation water. Egypt. J. Hort. 24:67–74. Hamou, M., Y. Levy, O. Sagee, D. Hisdai, A. Dahan, J. Lifshitz, and A. Shaked. 1999. Effect of salinity and rootstock on the easy peeling cultivar ‘Winola’ (in Hebrew). Alon Haotea 53:242–247. Harding, R. B., M. Miller, and M. Fireman. 1958. Absorption of salts by citrus leaves during sprinkling with water suitable for surface irrigation. Proc. Am. Soc. Hort. Sci. 71:248–256. Hartmond, U., N. V. Schaesberg, J. H. Graham, and J. P. Syvertsen. 1987. Salinity and flooding stress effects on mycorrhizal and nonmycorrhizal citrus rootstock seedlings. Plant Soil 104:37–43. Hilgeman, R. H., W. H. Fuller, L. F. True, G. C. Sharples, and P. F. Smith. 1970. Lithium toxicity in Marsh grapefruit in Arizona. J. Am. Soc. Hort. Sci. 95:248–252. Hodgson, R. L. 1967. Horticultural varieties of Citrus. p. 431–591. In: W. Reuther, H. J. Webber, and L. D. Batchelor (eds.), The citrus industry, Vol. 1. Univ. California, Berkeley. Hoffman, G. J., P. B. Catlin, R. M. Mead, R. S. Johnson, L. E. Francois, and D. Goldhamer. 1989. Yield and foliar injury response of mature plum trees. Irrig. Sci. 10:215–229. Hutchison, D. J. 1985. Rootstock development screening and selection for disease tolerance and horticultural characteristics. Fruit Var. J. 39:21–25. Jensen, M. E., W. R. Rangeley, and P. J. Dieleman. 1990. Irrigation trends in world agriculture. p. 31–67. In: A. R. Stewart, and D. R. Nielsen (eds.), Irrig. Agr. Crops, Vol. 30. Am. Soc. Agron., Crop Sci. Soc. Am. Soil Sci. Soc. Am., Madison. Jifon, J. and J. P. Syvertsen. 2001. Effects of moderate shade on citrus leaf gas exchange, fruit yield and quality. Proc. Fla. State Hort. Soc. 114:177–181. Jones, W. W., H. E. Pearson, E. R. Parker, and M. R. Huberty. 1952. Effect of sodium fertilizer and irrigation water on concentration in leaf and root tissues in citrus trees. Proc. Am. Soc. Hort. Sci. 60:65–70. Juniper, S., and L. Abbott. 1993. Vesicular-arbuscular mycorrhizas and soil-salinity. Mycorrhiza 4:45–57. Katan, J. 1996. Interaction of roots with soil-borne pathogens. p. 811–822. In: Y. Waisel, A. Eshel, and U. Kafkafi (eds.), Plant roots: The hidden part, 2nd ed. Marcel Dekker Inc., NY. Kefford, J. F., and B. V. Chandler. 1970. The chemical constituents of citrus fruits. Acad. Press, NY, p. 246. Kleinshmidt, G. D., and J. W. Gerdemann. 1972. Stunting of citrus seedlings in fumigated nursery soils related to the absence of endomycorrhizal. Phytopathololy 62:1447–1453. Kochba, J., G. Ben-Hayyim, P. Spiegel-Roy, S. Saad, and H. Neumann. 1982. Selection of stable salt-tolerant callus cell lines and embryos in Citrus sinensis and Citrus aurantium. Z. Planzenphysiol. 106:111–118.
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3 Red Bayberry: Botany and Horticulture* Kunsong Chen, Changjie Xu, and Bo Zhang Department of Horticulture Huajiachi Campus, Zhejiang University Hangzhou, 310029, P. R. China Ian B. Ferguson The Horticulture and Food Research Institute of New Zealand Private Bag 92 169 Auckland, New Zealand I. INTRODUCTION A. History B. Distribution C. Commercial Production II. BOTANY A. Taxonomy B. Morphology and Anatomy III. PHYSIOLOGY A. Vegetative Growth B. Flowering and Fruit Set C. Fruit Development IV. ENVIRONMENTAL REQUIREMENTS A. Temperature B. Water C. Soil D. Light E. Elevation and Exposure *This review was supported by the State Key Basic Research and Development Plan (G2000046806), the National Natural Science Foundation of China (30170660), and Zhejiang Natural Science Foundation (ZD0004), and was also a part of a cooperative program between The Horticulture & Food Research Institute of New Zealand and Zhejiang University. We thank Dr. Grant Thorp for critically reading the manuscript. Horticultural Reviews, Volume 30, Edited by Jules Janick ISBN 0-471-35420-1 © 2004 John Wiley & Sons, Inc. 83
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V. HORTICULTURE A. Propagation B. Field Cultivation C. Pests and Diseases D. Harvest and Handling E. Storage and Transportation F. Processing VI. CONCLUDING REMARKS LITERATURE CITED
1. INTRODUCTION Red bayberry (Myrica rubra Sieb. & Zucc., Myricaceae) is a subtropical fruit tree native to China and other Asian countries, bearing a delicious, berry-like fruit (Fig. 3.1). Gengmin Wu, founder of modern Chinese horticulture, praised it as a “precious Southern Yangtze fruit of early summer ” (Wu 1995). The fruit ripens in June and early July in the main Chinese production areas of Zhejiang and Jiangsu provinces, earlier than most other local fruits. The rich red colors and appealing flavor make this juicy fruit popular with consumers; it is eaten like a cherry.
Fig. 3.1. Red bayberry (Myrica rubra) fruit and trees. A and B: mature fruit showing (B) the segmented juicy flesh and the hard stone. C: fruit growing on the outer space of the canopy. D: trees growing on hillsides, a common cultivation practice in China. Photos by Jiangguo Xu.
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In addition to being consumed fresh, various products such as juice, canned fruit, jam, wine, sweets and salted fruit are produced. Presentday commercial cultivation is still largely restricted to China. The fruit and roots of red bayberry have been used as important components of traditional Chinese medicines for more than 2000 years (Li 1578), the fruit being beneficial for treating congestion, coughs, digestive problems, and diarrhoea. The root also has wound healing properties. In recent years, a number of pharmaceutically active compounds have been identified from the various plant parts (Zhang et al. 1993; Chi et al. 2000; Yi and Liu 2000; Zhong et al. 2000). The evergreen tree has a bushy, round canopy and grows well in soils of low fertility, having an association with the nitrogen-fixing bacterium Actinomyces frankia. The tree is used in China to increase the organic matter content of soil, reduce soil erosion, and to enhance the landscape (Wang and Chen 1989). Red bayberry is often interplanted with existing vegetation such as pine or other natural forest trees (Wang et al. 2001). While the fruit is well known throughout China, where there is a considerable body of literature on various aspects of production, it is little known elsewhere. There is a short general review on red bayberry available in English (Li et al. 1992), and a review of research progress in China has recently been published (Li et al. 1999). This review will cover the botany and horticulture of red bayberry, most of it based on Chinese publications. A. History In China, red bayberry has been known by a variety of names. Yangmei is the most common name in Chinese. Shizheng Li, in Compendium of Materia Medica (1578), wrote: “The shape of the tree is similar to poplar (Yang), and the taste of the fruit is somewhat like mume (Mei), thus it is named Yangmei.” Shumei (strawberry tree) is used in Taiwan. Zhuhong is a common name in Fujian province and, elsewhere in China, names such as Shanyangmei and Zhurong are used. The English names for this fruit include red bayberry, Chinese bayberry, and waxberry. The fruit has a very long history in Chinese civilization. The earliest records come from the Neolithic site at Hemudu, Zhejiang province, indicating that the fruit has existed as a foodstuff for more than 7,000 years (Yu 1979; Wu 1984). Red bayberry fruit and stones have also been found in the Mawangdui tumulus of the Western Han Dynasty (206 B.C.E.–25 C.E.) in Hunan province and the Luobowan tumulus in Guangxi Zhuang Autonomous Region (Yu 1979). Nan Fang Cao Mu Zhuang, a book on the properties of various plants from southern China, written by Ji Han during the Jing Dynasty (265–420), recorded the cultivation of red bayberry
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and its use in wine making (Ji 304). By the Song Dynasty (960–1279), the Wu-Yue area (Jiangsu and Zhejiang provinces today) was well known for red bayberry production and the fruit recognized for its quality and quantity; locations close to Ningbo and Taizhou in Zhejiang province are still the most important production areas. B. Distribution Red bayberry originated in southeastern China, where it is still found in the wild and is the source of seed for rootstocks. It is now distributed south of the Yangtze River and north of Hainan Island, approximately 97° to 122°E longitude, and 20° to 31° N latitude. This distribution is similar to that of citrus, loquat, tea, and bamboo, except that red bayberry can withstand lower temperatures (Maio and Wang 1987; Maio et al. 1995). The major commercial production area is concentrated in Zhejiang, Fujian, Jiangxi, Jiangsu, Guangdong, and Guizhou provinces. There is some production in Yunnan, Guangxi, Sichuan, Hunan, Shanxi, and Taiwan, from semi- or wholly wild trees (Wang 1995). Outside of China (Yu 1979; Wang 1987) the crop is grown in Thailand, although fruit quality is often poor and the area limited. In Japan, it is grown in Tokushima, Kochi, Ehime and the western part of Honshu. In Europe and America, red bayberry trees are used mainly for ornamental purposes. There are a number of closely related species (described below) that are cultivated. Myrica integrifolia Roxb. is distributed in India, Sri Lanka, Burma, and Vietnam, where it is confined to home gardens, producing small and acid fruit, usually used for jam or medicine. Myrica esculenta Buch.-Ham. is found in India, Nepal, and Vietnam as well as in southwest China. Myrica faya Ait. has fruit suitable for fresh consumption and is grown in the Canary Islands. C. Commercial Production Production of red bayberry has increased dramatically; the cultivated area in China in 1995 was 130,000 ha. The crop has become one of the most important fruit tree crops in south China (Liu 2000; Wang et al. 2001). In Zhejiang province, the cultivated area and production were 4,400 ha and 26,500 tonnes (t) in 1959, 17,500 ha and 46,200 t in 1985, and 38,378 ha and 129,750 t in 2000 (Wang et al. 2001). As a result, red bayberry is second only to citrus among the fruit crops of the province, and the yield is expected to continue to increase. Most production is consumed locally, but an increasing proportion is being exported both within and outside of China.
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II. BOTANY A. Taxonomy 1. Species. The Myricaceae are widespread in tropical, subtropical, and temperate areas of the world. They consist of two genera, Comptonia and Myrica, both of which are cultivated. The genus Myrica Linn contains more than 50 species of which six are found in China (Yu 1979; Maio and Wang 1987; Qu and Sun 1990; Wang 1995; Li et al. 1999). More recently, RAPD (Random Amplified Polymorphic DNA) markers have been successfully used in classification and identification of Myrica species (Lin et al. 1999). Myrica cerifera L. originating from North America was clearly distinguished from three Chinese species (Myrica adenophora Hance, Myrica esculenta Buch. -Ham, and Myrica rubra Sieb. & Zucc.), which clustered together. Myrica rubra Sieb. & Zucc. Red bayberry (2n = 16) is an evergreen tree growing to a height of 5 to 10 m, distributed in southern China, but also found in Japan, South Korea, and The Philippines. The bark of young trees is smooth and yellow-green, while that of old trees is grey-brown with white spots and narrow cracks. The canopy is uniform and round or slightly flattened. The branches are frail and easily broken, and the leaves alternate and simple, with blades 5–14 cm long and 1–4 cm wide, usually with smooth margins, although sometimes serrated. The upper and lower leaf surfaces are smooth without hairs, the upper lustrous and dark green and the lower light green. The plant is dioecious, although occasionally monoecious, with the inflorescence forming in axillary buds. The staminate inflorescence is a compound catkin, 1–3 cm long, columnar, and yellow-red; the pistillate inflorescence is a simple catkin and shorter and thinner, filaceous, bright red, with two longitudinal grooves along the stigma. The fruit is a small drupe and consists of a fleshy pericarp comprising individual segments and a hard endocarp protecting a single seed. It is red, purple, white, or pink when ripe, depending on the cultivar. Flowers bloom during February to April and fruit ripen during May to July. Myrica esculenta Buch.-Ham. This is also known as Yangmei Dou in Guizhou. It is mainly distributed in mountains at elevations of 1,500–2,500 m in southwest China (Sichun, Yunnan, Guizhou, Guangdong, and Guangxi), and in India, Nepal, and Vietnam. The tree is 4–15 m high, with light-colored bark. The shoots are thin and covered with numerous hairs. The leaves are thick, hairless, and oval, 3–12 cm long
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and 1.2–4.5 cm wide, with few or no marginal indentations and sparse yellow glands on the lower surface. The petiole is covered with white hairs. The plant is dioecious and the inflorescences are catkins, the flowers having two bright red, thin stigmas. The fruit are ovoid, about 1 cm long and 0.8 cm in diameter, with an average weight of about 0.5 g, and with red flesh. The edible portion constitutes about 80% of the fruit weight and, when ripe, the soluble solids concentrations are about 12.5% and total acids 1.3%. Flowers bloom during September to October and fruit ripen during the following March to April. There are seven subspecies or variants of this species, which can endure high humidity and temperatures down to –6°C, and which will also grow well in dry areas. Myrica nana Cheval. This species is variously known as Yunnan Yangmei and Dian Yangmei and is mainly distributed in subtropical and temperate zones of Yunnan, Guizhou, and Xizhang in China. The plant is a shrub 0.5–1.0 m high, with thick, strong shoots. The bark is rich in tannin, and the olive green leaves are narrowly obovate or occasionally elliptic. The upper leaf surface usually has small depressions associated with yellow glands and sunken venation; the lower leaf surface has glands and protruberant venation. Petioles are short and covered with short soft hairs. Fruit are round to oblate, about 2 cm long and 2 cm in diameter, with an average weight of 3.5–5 g. Ripe fruit are red, with an 80% edible proportion and soluble solids levels of 9–10% and total acids of nearly 4%. Flowering may last 1 month from February to March, and fruit normally ripen about 4–6 months after flowering. The species has four variants and two derivatives: M. nana var. integra Cheval., M. nana var. luxurians Cheval., M. nana Cheval, var. humifusa N. Liu et Z. F. Li, var. sp. nov., M. nana Cheval, var. alba N. Liu et Z. F. Liu et Z. F. Li var. sp. nov., M. nana cheval, f. cerea N. Liu et Z. F. Li, f. niv. and M. nana Cheval, f. gracilifolia N. Liu et Z. F. Li, f. onv. Myrica integrifolia Roxb. This species is mainly distributed in the mountains of South Asia at an elevation of 900–1,400 m in countries such as India, Sri Lanka, Burma, and Vietnam, and also in the western part of Yunnan in China. It is a large evergreen shrub or tree, 8–10 m high with dense shoots covered with dense soft hair. Leaves are lanceolate, bright green, with smooth margins, but sometimes undulate. The plant is dioecious, with oval, red, acid fruit when ripe, weighing about 2.4–3 g, with 10.5% soluble solids and an edible portion of about 85%. Flowers bloom during February to March, and fruit ripen from April to May. The species prefers an acid soil and high humidity, and usually grows in forests together with deciduous plants.
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Myrica arborescens. S. R. Liet X. L. Hu, sp. nor. The species is distributed in the south and southwest part of Yunnan in China, and in Burma, growing in the mountains at an elevation of 900–1,400 m. Plants prefer an acid soil and humid climate. It is an evergreen tree, about 15 m in height, with a trunk of more than 300 cm in circumference. Shoots have long white hairs and few glands, and the leaves are larger than for other species, with blades 8–19 cm long and 2–4 cm wide, elongated lanceolate or ellipsoidal in shape, and having obvious sharp sawtooth edges on the abaxial sides. The upper venation of young leaves is covered with white soft hair, while yellow glands cover the lower surface, and the secondary veins are also covered with long white soft hair. Plants are dioecious, with an ovary surrounded by long hairs and the fruit are round or ovoid, 2.5–3 cm in diameter and yellow-white or green-white when ripe. Flowers bloom during February to March, and the fruit ripen from April to May. Myrica adenophora Hance. Known variously as Xiyeyangmei, Pomei, and Qingmei, it is mainly distributed in Hainan province, the southern part of Guangdong province and southwestern Guangxi province. The variant M. adenophora var. kusanoi Hayata is grown in Taiwan. It is a shrub or small tree, 1–6 m high. The bark is gray and the young thin shoots are covered with short soft hair and yellow glands. Leaves are obovate, both sides with numerous glands. The medial vein has short soft hair, as does the petiole. Staminate and pistillate inflorescences form in axillary buds. The red fruit are oval, small, and less than 1 cm in diameter. Flowers bloom from October to November, and the fruit ripen during February to May. 2. Cultivars. There is little agreement on cultivar classification. Fruit color and ripening date have been used to identify different groups of cultivars (Yu 1979; Wu 1984; Maio and Wang 1987; Qu and Sun 1990). Guo and Li (1994) sorted the cultivars into five groups and nine types based on physical characters of the stone, fruit, and leaves, while Chen (2000) divided them into two types based on soft and hard fruit flesh. The Chinese Red Bayberry Cooperation Association has established three types based on the fruit ripening date (Chen 2000). Recently, peroxidase isozyme analysis, chromosome banding, and karyotypic analysis have been introduced into varietal classification (Lin et al. 1999). Ripe fruit color is one of the more useful criteria used (Qu and Sun 1990; Li et al. 1992), and this has resulted in four cultivar groups described as follows:
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Wild. This group, also called wild black, is found growing in the wild and is used as rootstocks. The fruit are red and acid, with small flesh segments, and ripen earlier than other types, in Zhejiang at about the beginning of June. Red. Fruit of this group are red when ripe, and usually larger and of better quality than other types. Representative cultivars include ‘Shuimei ’, ‘Chise’ , ‘Dongkui’ in Zhejiang, and ‘Dayexidi ’ in Jiangsu. Black. This group has the best fruit quality, with large flesh segments and a stone that can be easily separated from the flesh. The fruit turns from red to red-black during ripening. Representative cultivars include ‘Biqi’ in the Cixi-Yuyao district, ‘Wandao Yangmei’ in Dinghai, ‘Ding-ao Mei’ in Wenzhou, ‘Datanmei’ in Yuhang in Zhejiang, ‘Wumei’ in the Dongting area in Jiangsu, and ‘Shanwu’ and ‘Wuhesu’ in the Chaoyang area in Guangdong. White. The ripe fruit of this group are various shades of white. Yield and fruit quality is less than for fruit of the black or red groups, and it is not so widely planted. ‘Shuijing Yangmei’ (crystallooking) in Shangyu is the best cultivar of this type grown in Zhejiang province. Zhang and Miao (1999) distinguished 268 cultivars in China. Fruit characteristics vary widely among these cultivars, as shown by the percentage of cultivars in different groups on the basis of ripening date, fruit color, and fruit weight (Table 3.1). The cultivars in Zhejiang province can be sorted by ripening date into three groups (Table 3.2).
Table 3.1. Distribution of fruit attributes among different Chinese cultivars of red bayberry. Source: Zhang and Miao (1999). Ripening Date
Month April May Early June Mid June Late June Early July
Distribution (%) 1.1 6.3 13.7 18.7 47.8 12.4
Flesh
Fruit Size
Color
Distribution (%)
Weight (g)
Distribution (%)
White Pink Red Deep red Purple Deep purple Purple black Jet black
9.3 5.6 17.2 7.8 37.3 3.4 13.8 5.6
15
6.3 25.8 46.6 14.9 6.3
Table 3.2. Ripe fruit attributes of early-, medium-, and late-maturing cultivars of red bayberry grown in Zhejiang. Data are averages from unpublished sources. Fruit Characteristics
Ripening date Early (<June 20) Mid (June 20–July 5) Late (>July 5)
Cultivar
Width (cm)
Length (cm)
Weight (g)
Zaodamei Zaoqimimei Biqi Ding-aomei Dongkui Wandaoyangmei Wanqimimei
3.2 2.6 2.7 2.7 3.7 2.8 2.8
2.9 2.5 2.6 2.9 3.9 2.7 2.7
15.7 9.7 10.7 20–25 11.20 12.50
Edible portion (% wt)
Soluble solids (%)
Total sugars (%)
Acidity (%)
Stone (g)
94 94 95 94 96 95 95
11.7 11.5 12.5 11.7 12.7 12.7 12.8
8.7 9.7 9.5 9.7 9.5 9.7 10.7
1.1 1.7 0.9 0.9 1.4 0.9 0.9
1.7 0.5 0.6 0.6 0.8 0.6 0.6
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B. Morphology and Anatomy 1. Roots and Nitrogen Fixation. The trees have a shallow, fibrous root system, usually occupying the top 5 to 40 cm of the soil, and typically one- to twofold greater than the diameter of the canopy. The plants form an association with Actinomyces frankia, a nitrogen-fixing bacterium. The nodules are usually greyish yellow, fleshy, and randomly distributed on the roots (Miao and Wang 1987; Wang 1995). In transverse section, the nodules are round and symmetric, and their color changes from oyster white to yellow brown with maturation, and dark brown with senescence (Wang and Huang 1990). Nitrogenase activity of mature nodules is higher than that of the young ones, with two peaks of activity observed in June and October. The lowest activity is found in January, and can be inhibited by nitrate (Wang and Huang 1990; Wu and Gu 1994). Measurements by Z. Li et al. (1993) have shown that the average nodulation mass in a 7-year-old red bayberry sapling was 52 g/tree with 460 kg/ha of nitrogen fixed per year. There are clear advantages in this nitrogen-fixing capacity in terms of fertilizer use and soil fertility. 2. Shoots. The bark color varies with development stages, from pale yellow-green in young trees to grey-brown in mature trees. The mature branches, which have very visible lenticels, are weak and easily broken by wind. There are four types of shoots: rapidly growing extension shoots (water shoots), vegetative shoots, bearing shoots, and staminate flowering shoots (Miao and Wang 1987; Wang 1995). Water shoots are usually longer than 30 cm and vegetative shoots shorter than 30 cm, with longer internodes. Well-developed axillary buds on vegetative shoots are the potential fruiting shoots. New leaf and shoot growth generally arises from buds near the shoot apex (Miao and Wang 1987). The season of growth affects leaf size: The spring leaves are the biggest, followed by those produced in the summer, and then the autumn. Leaf color also varies with the season; the spring leaves are deep green, in the summer a lighter green, and autumn leaves are pale green. These characters are also used to estimate nutritional status. Leaves remain on the tree usually for 12–14 months, with a marked peak in abscission just prior to the spring growth flush. 3. Flowers. Flower buds of red bayberry are simple, forming in axillary buds and never in terminal buds, where only vegetative (leaf) buds occur. The flower bud is larger than the leaf bud, and can be distinguished in winter before budbreak. New growth in spring occurs from axillary buds on shoots grown in the previous season. Flower bud differentiation has been well studied, mainly on ‘Xiyeqing ’and ‘White’ cul-
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tivars (Li and Dai 1980). Only apical buds and 4–5 axillary buds can develop into leaf or flower primordia; the other buds remain latent for quite some time and can be stimulated to develop into shoots. This character is useful when replacement of the canopy and fruiting shoots is needed. Leaf buds break about 20 days later than flower buds, and leaf unfurling occurs about 15 days after that. Red bayberry is a typical dioecious fruit tree, but it is difficult to identify sex before flowering. G. Li et al. (1993) established a method based on isozymes patterns and composition of phenolic compounds. The flower is small, unisexual, without perianth, and is wind-pollinated. Each staminate flowering shoot can contain 2–60 inflorescences, normally between 15 and 20, and is part of a compound inflorescence that bears 15–36 catkins, each catkin composed of 4–6 staminate flowers. Staminate inflorescences form in the leaf axil, and are cylindrical or long conical in shape, with the color changing from garnet in young flowers to yellow-red or bright red in mature ones. The distal staminate flowers open first, and the flowering period can be as long as 40–50 days for a whole tree. Staminate flowers are arranged as a corymb, without pedicel or receptacle, and are surrounded by greenish white bracts. Each staminate flower has two stamens, and unequal filament length (Fig. 3.2). The filaments are yellowish red or bright red, and usually bear anthers at the apex. Anthers are kidney-shaped, bright red, fused at the base, and
Fig. 3.2.
Morphology of staminate floral structure of red bayberry (from Wang 1995).
1. Staminate flowering shoot. 2. Staminate compound catkin. 3. Individual staminate catkin. 4. Bract for compound catkin. 5. Bract. 6. Stamen.
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release yellow pollen through longitudinal splits. The pollen grains are small (20 µm diameter) and can be carried as far as 1000 m by wind (Miao and Wang 1987). Each anther holds more than 7,000 pollen grains, and each staminate inflorescence contains 200,000–250,000 pollen grains. Each pistillate flower shoot has 2–60 pistillate inflorescences, the average being 15 to 20. The catkins contain 7–26 flowers (average 14). The ovary is unilocular, and the style bright red, 0.5–1 cm in length, with a Y-shaped stigma with 2, sometimes 3–4 sites of dehiscence. Terminal flowers of the pistillate inflorescence usually flower earlier than others (Fig. 3.3), and the flowering period for a whole tree may last for about 30 days. Occasionally, mixed inflorescences occur with pistillate flowers at the top and staminate flowers at the base (Fig. 3.4). Staminate flowers open after 2–3 pistillate flowers have opened in the same inflorescence. However, pistillate flowers in a staminate inflorescence have only been reported once (Miao and Wang 1987). 4. Fruit. The fruit have stones like peach and plum, with an edible part more like a berry (Fig. 3.1). The fruit is usually spherical, and the skin has a waxy coat (Miao and Wang 1987). Fruit size varies among cultivars (Table 3.2), generally being greater than 2 cm in diameter, with some reaching 3 cm or more. Fruit of the wild types are less than 2 cm in diameter, and fruit of Myrica nana Cheval grown in Guizhou, China, are the smallest, measuring less than 1 cm in diameter.
Fig. 3.3.
Morphology of pistillate floral structure of red bayberry (from Wang 1995).
1. Pistillate flowering shoot. 2. Pistillate inflorescence. 3. Pistillate flower. 4. Bract for inflorescence. 5. Bract. 6. Pistil. 7. Longitudinal section of fruit. 8. Flesh segment.
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Fig. 3.4.
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Inflorescences of red bayberry (from Liu 2000).
1. Staminate inflorescence. 2. Bisexual inflorescence. 3. Pistillate inflorescence.
The epicarp of the fruit consists of thin-walled parenchyma cells, in which the vascular bundles are arranged like a cup. The parenchymatous mesocarp makes up the edible portion. The endocarp consists of a hard stone with small, round, thick-walled sclerenchyma cells, most of which are flattened. The stone includes a seed coat, embryo, and large, soft, waxy cotyledon (Fig. 3.5). The epicarp and mesocarp (flesh segments) develop from the outermost layers of endocarp and usually consist of 1,100–1,300 flesh segments. The length, thickness, pointedness, and hardness of the flesh segments varies with cultivars. Tree age, yield, soil nutrition, humidity, degree of maturation, and position of fruit on the tree influence fruit quality (Li et al. 1992). More mature trees, heavier fruit loads, more abundant nutrition, drier climates, and sun exposure will result in fruit with more pointed flesh segments. In some cultivars, a single fruit may contain both round and pointed segments. The former would be located
Fig. 3.5.
Morphology of the fruit of red bayberry (from Miao and Wang 1987).
1. Epicarp. 2. Mesocarp (flesh segment). 3. Endocarp. 4. Seed coat. 5. Seed (cotyledon).
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in the middle of the fruit, with the latter in the outer parts. Fruit with round flesh segments are usually more succulent and taste better, while those with sharper flesh segments tend to have a longer storage life. III. PHYSIOLOGY A. Vegetative Growth Root growth usually commences in late February, and the root system has three major growth peaks, in late May, mid-July, and early October (Miao and Wang 1987). Vegetative growth has up to three growth flushes each year. Summer shoots are the most abundant, accounting for 60–70% of the total shoots each year, and these make up most of the bearing shoots in the following season; spring shoots, summer shoots, and sometimes autumn shoots will become flowering branches. Winter shoots can develop into bearing shoots depending on weather and nutrition (Miao and Wang 1987). Spring shoots occur from late March to late June, developing from the spring shoots or summer shoots of the previous year; summer shoots, from June to August, developing from the spring shoots of the same year and bearing shoots of the previous year; autumn shoots, from early August to October, developing mainly from the spring and summer shoots of the same year (Li 2001). Except for the cultivars ‘Biqi’ and ‘Ding-ao’, autumn shoots do not become bearing shoots, as they form too late (Miao and Wang 1987). As might be expected, spring shoots are the longest and autumn shoots the shortest. Leaves unfurl during late March to early April, and develop rapidly in May. Old leaves begin to abscise at the beginning of May, and reach an abscission peak when spring shoots stop growing. Leaf abscission is influenced by both the growing environment and the cultivar. Trees growing on clay soils, attacked by pathogens, or generally weak trees, usually shed leaves earlier, and abscission is postponed in late maturing cultivars such as ‘Wandao Yangmei’. B. Flowering and Fruit Set Flower-bearing shoots develop from the strong spring and summer shoots of the previous year. Although spring shoots are the best shoots for bearing fruit, they are not sufficient for adequate crop loads, and since summer shoots are the most abundant, they become the most important source of fruit and the key factor influencing yield in the next year (Li 2001). The fruit capacity of a bearing shoot varies with shoot length, and shoots are divided by length in the ‘Biqi’ cultivar into four types: extended, long,
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medium, and short shoots (Miao and Wang 1987). Extended shoots are more than 30-cm long with limited flower buds at the end and most of the buds will be shed after flowering. Long shoots are thin, 20–30 cm in length, with 5–6 flower buds at the end, and a low rate of fruit set. Medium shoots are 10–20 cm long, with a heavy load of flower buds except at the apex; these shoots bear the highest fruit load. Short shoots, 1–10 cm in length, some as short as 1–2 cm, carry many flower buds, with high rates of fruit set. When flowering shoots constitute about 40% of the total shoots, a high, steady yield can be predicted (Chen et al., pers. comm.), but when this ratio is more than 60%, alternate bearing may develop. Flower bud differentiation begins shortly after the cessation of summer shoot growth (Li and Dai 1980). Physiological differentiation of inflorescence primordia of the ‘Xiyeqing’ and ‘White’ cultivars occurs in early or mid-July. During the early stage of flower bud differentiation, abortive pistillate inflorescences emerge and these will be shed rather than open in the next spring. Inflorescences that differentiated after early August normally develop fruit. Morphological differentiation of the primordia of pistillate inflorescences begins in mid-July, and the first small flower primordium forms in late July. The formation of primordia of the staminate inflorescences begins at the end of the same month. Flower bud differentiation stops at the beginning of December. Physiological differentiation of the flower buds develops 2–4 weeks earlier than morphological differentiation, and takes about 3 months to complete. Autumn shoots are unable to develop flower primordia in time for the normal flowering period. Flowering date varies according to cultivar and growing conditions (Miao and Wang 1987). Some staminate flowers open in late January, some during February and March, reaching full bloom in March to April. This also happens with pistillate flowers and, as a result, individual pistillate inflorescences commonly carry fruit and opening flowers at the same time. Flowering can be divided into six stages: bud break, inflorescence break, first bloom, full bloom, end of bloom, flower drop (Miao and Wang 1987). Usually, the first bloom stage is when 5% of anthers or stigmas are exposed, full bloom stage is at 75%, and end of bloom when the anther exposes pollen and becomes yellowish-brown or the stigma wilts (Miao and Wang 1987). The period of flowering can span 39 days for staminate flowers and 27 days for pistillate flowers. Though pistillate flowers open later and last for a shorter time than the staminate ones, full bloom stage is longer (13 days) than that of the staminate flowers (5–7 days), and this benefits pollination (Miao and Wang 1987). The highest fruit set occurs in the uppermost five inflorescences on bearing shoots, but the first inflorescence is the predominant one, bearing
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20–45% of the total fruit. The rate of fruit set is only 2–4% for the whole tree (Wang 1995). The main peak in abscission of inflorescences and fruitlets is late April to early May. Additional peaks occur in the middle of May and just prior to harvest in some cultivars such as ‘Shuimei’ and ‘Hunanzhong’, but not in the cultivars ‘Dongkui’ and ‘Wandao Yangmei’ (Miao and Wang 1987). C. Fruit Development The time from fruit set to maturation is 60–70 days (Miao and Wang 1987). The fruit of leading cultivars in Guangdong and Fujian ripen during late May to early June, the early-maturing cultivars in Zhejiang and Jiangsu during middle to late June, and the late-maturing cultivars in early July. Fruit on trees in inland areas ripen earlier than in coastal areas because of greater diurnal temperature differences in inland climates. Fruit growth follows a double sigmoid curve in both fruit size (diameter; Fig. 3.6) and fruit weight. For example, ‘Biqi’ and ‘Dongkui’ fruit (Miao and Wang 1987; Gong 1995) develop rapidly and reach the max-
Fig. 3.6. Changes in length, diameter, and ratio of length to diameter during fruit development of ‘Donkui’ red bayberry (from Gong, 1995).
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imum of the first growth stage (about 20 days) just after the first peak of fruit abscission in early May. This period of rapid growth is followed by a pit hardening stage (15–20 days) and a second burst in fruit growth, characterized by increases in water content, weight, and color of fruit just prior to fruit ripening on the tree. Fruit size increases synchronously with fruit weight and there is a strong correlation between the size of the seed and the fruit. Water content of the fruit increases from the fruitlet to the pit hardening stage, then decreases gradually, before increasing again as the fruit matures (Miao and Wang 1987). The daily increment in fresh weight of the fruit flesh during the maturation stage is three times that at the first rapid growth stage; there is no similar difference in dry weight increase. The length of the pit hardening stage is influenced by fruit size as well as cultivar—the bigger the fruit, the shorter the length of the stage. Total soluble solids (TSS) contents increase with fruit maturation to the point of harvest, with sugars accumulating rapidly during the final 2–3 weeks (Chen et al. 1992). Larger fruit are commonly sweeter than smaller ones, and there is a positive correlation between TSS content and degree of pigmentation. Citric acid is the most abundant of the fruit organic acids, accounting for 97% of the total, with malic, oxalic, succinic, isocitrate, fumaric and other acids making up the remaining 3%. Chen et al. (1992) found that total acidity increased rapidly from about 40 days before harvest, but then decreased as the fruit began to ripen on the tree. Smaller fruit tend to have higher acidity than larger ones (Chen et al. 1992). The pigments responsible for the fruit flesh color (red, and purple to black) are anthocyanins, the levels of which vary with cultivar, fruit development, and environmental factors, especially light. Cyanidin-3glucoside has been identified as the principal fruit pigment, with pelargonin-3-monoside and delphinidin-3-monoside as minor components (Lin 1984; Ye et al. 1994). Chlorophyll contents decrease during fruit maturation.
IV. ENVIRONMENTAL REQUIREMENTS A. Temperature The tree performs well in tropical, subtropical, and temperate zones, with optimum temperatures of 15–20°C. It can endure winter freezing with average temperatures of more than 2°C and an absolute minimum
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above –9°C. However, the trees can be damaged and the yield for the following year reduced by more than 20% if the minimum temperature falls below –9°C and a maximum temperature of less than 0°C lasts longer than about three consecutive days. Because the flowering period is quite late, unlike peach and apricot, flower or fruit freezing seldom occurs. To get high yields and quality, the growing conditions should include an annual average temperature >14°C and accumulated temperature (>10°C) of more than 4,500 degree days. Outside these conditions, small, very acid and poor-tasting fruit are likely to be produced. High temperatures during May and June, during the second fast growth phase, also may result in fruit with high acid and low sugar contents. For example, one study has shown that when the mean May–June temperature was 20–22°C, the acid content was 0.7–1.3% and the ratio of soluble solids to acids was 9–16, but when the mean temperature was raised by 2°C, the acid content increased to 1.4–1.9% and the ratio decreased to 6–7 (Miao and Wang 1987). High temperatures (e.g., a mean temperature higher than 28°C) can cause damage, particularly to young, newly transplanted trees, and affect the development of flower buds and fruit-bearing shoots. The optimum temperature for photosynthesis of red bayberry is less than 20°C (Ruan and Wu 1991). B. Water High humidity and a plentiful water supply assures high cropping and high-quality fruit (Chen et al. 1992). In China, most trees are planted on hills and slopes without artificial irrigation (Fig. 3.1). Annual precipitation and its seasonal distribution are the most important factors influencing tree growth and fruit production. In Zhejiang, precipitation of more than 1000 mm is usually required (Li et al. 1992), and the optimum is between 1300–1700 mm. Low humidity results in poor pollination and reduced yields. Rainfall of more than 260 mm during February and April favors the growth of the root system, leaf development, blossoming, and fruit set. The period May to June is of particular importance for fruit maturation, warmth and light being needed to enhance fruit color. Rainfall of more than 160 mm is required in June, since less than 100 mm will result in small, poor-quality fruit, and a reduction in yield. Having sunny days during late summer to early autumn is beneficial for the accumulation of carbohydrates and flower bud differentiation. Most of the important commercial areas of red bayberry production in China do not have extremes of temperature and humidity.
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C. Soil A deep, fertile, acid soil with a pH of 4–5.5 is the optimum for cultivation. In mountainous areas, successful growth of plants such as Dicranopteris pedata (Houtt.) Nakaike, Rhododendron simsii Planch., pines, firs, bamboos, Cyclobalanopsis glauca (Thunb.) Oerst., Quercus acutissima Carruth., or Castanopsis sclerophylla (Lindl.) Schott. indicate suitable conditions for bayberry cultivation (Li et al. 1992). Red bayberry is tolerant of shade and can be planted in less-fertile soils and fine sandy loams. Planting in clay or sandy soils can result in weak and/or dwarfed trees. The presence of nitrogen-fixing root nodules allows the trees to perform well on infertile but well-drained slopes. In fertile flat soils, trees may have excess vegetative growth and consequently shed flowers and fruit. The species is susceptible to boron deficiency, which can result in small leaf size. D. Light Although tolerant of shade, sufficient light is needed for cropping. Ruan and Wu (1991) found that the tree had significant winter photosynthetic rates, although the net rate was usually below 1.5 mg CO2 d–1m–2. Fruit of poor quality and small size may be produced on south-facing slopes where direct light and heat is excessive (Li et al. 1992). E. Elevation and Exposure Flowering and fruiting have been shown to be delayed by up to 20 days with an increase in elevation from 50 to 600 m (Chen et al. 1989). Trees grown at between 200 and 400 m produce fruit of high quality, with soluble solids levels of 9.9–10.1% and acidity 1.8–1.55% (Chen et al. 1992). Elevations greater than 500 m are unsuitable for cultivation since annual temperatures are usually below 15°C. The trees are not tolerant of strong winds because of a shallow root system, dense branches and leaves, large canopy, and brittle shoots. V. HORTICULTURE A. Propagation The most widely used methods for propagation include seeds, grafting, and layering (Wang 1995). Propagation from seed has been the traditional practice in many areas in China, especially for rootstocks. Seeds need to
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be stratified, and are generally sown in November. The soil should be deep, well drained, and with reasonable organic matter. Soils previously used for citrus, peach, pine, cypress and red bayberry itself are usually unsuitable for sowing, probably because of nutrient depletion, with soils used for annual crops such as rice, vegetables and leguminous plants being preferred. The seeds are sown at a density of about 1.2–1.5 kg⋅m–2, and they germinate in the following spring. In April, seedlings can be transplanted to nurseries when about 7 cm high. By the time of the next spring after transplanting, the saplings are suitable for grafting. Seedlings with a stem diameter over 0.5 cm can be used as rootstocks for grafting. For scions, one- to two-year-old shoots are cut from trees over 10 years old with a history of good yields, and these are cut into several 7-cm segments after removing the leaves. The optimum time for grafting is between late March and early April in Zhejiang. A survival rate of over 70% can be achieved with cleft grafting. The growers in Xiaoshan and Lanxi in Zhejiang province often propagate red bayberry by layering, which is usually performed before bud break in spring. This method speeds up the time to production of a fruiting tree. However, the root systems of such plants are often shallow, and the growth weak. B. Field Cultivation Red bayberry is a long-lived tree and can remain productive for more than 30 years (Wang 1995). The optimum time for planting varies with regions. To avoid freezing injury in winter, planting takes place during late February to mid-March in Zhejiang, Jiangsu, Hunan, and Jiangxi. In regions with a relatively warm winter, such as in Guangdong, Fujian, Yunnan, Guizhou, and Sichuan, planting is carried out during early October to early December or from mid-February to mid-March. Planting density is about 600 trees/ha. Since the tree is dioecious, it is necessary to interplant staminate trees, at a frequency of about 1–2% (Wang 1995). Pollen grains are small and can be carried some distance by wind, and if an orchard has staminate plantings nearby, then interplanting is not always necessary. Organic fertilizer applications are commonly made in October, and green manure crops, usually leguminous plants, are often interplanted with young trees to improve soil structure and provide another source of income. For plantings on slopes, mounding up can prevent exposure of roots and promote root growth. According to Zhang (1999), a tonne of ‘Dongkui’ fruit contains 1.4 kg N, 0.07 kg P, 1.8 kg K, 0.06 kg Ca, and 0.28 kg Mg, with a ratio of N: P:
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K=20:1:26. The nutrient contents of fruit (Table 3.3) are generally lower than in many fruit crops, especially levels of P and Ca. Since nodulated roots supply part of the N requirements of the tree, K is the most important major nutrient that must be supplied from the soil. Excess P application can be harmful because of possible boron, zinc, and molybdenum deficiencies. The kinds of fertilizers used and application rates are related to plant age and soil nutrient status. For example, at a density of 270 trees/ha, fertilizers applied annually to young trees (5 years old) should contain 3.5 kg N, 0.9 kg P, and 3.0 kg K, and for adult trees (12 years old) 9.2–10.6 kg N, 2.3 kg P, and 12.3 kg K. Fertilizers should be applied three times a year: during February or March to promote spring flush growth, blossoming, and fruit set; late May for promoting fruit development; and a further application just after harvest. The trees are upright and will grow too tall if not trained, and the recommended practice throughout China is to create a tree with a low canopy and open center (Fig. 3.1). Pruning is carried out in February to March (spring) and September to October (autumn). Unwanted branches are removed or cut back to allow light penetration into the canopy to promote fruit set and increase fruit quality. For example, training of ‘Dongkui’ trees involves establishing a trunk with 3–4 primary scaffold limbs, with angles between the trunk and the limbs greater than 45°, and the height of the canopy less than 2.5–3.0 m. Groups of fruiting branches, rather than secondary scaffold limbs, should be allowed to develop on the main limbs, and these should be replaced by new groups about every 4 years (Wang 1999).
Table 3.3. The content of mineral elements in different organs of red bayberry trees (data from Zhang 1999). Fruit Nutrient Content (% dry weight) Tree age Non-bearing (5 year old)
Bearing (12 year old)
Organs
N
P
K
Ca
Mg
Leaves Shoots Roots
1.33 0.31–0.67 0.57
0.08 0.03–0.04 0.03
0.95 0.24–0.76 0.53
0.46 0.12–0.31 0.15
0.14 0.02–0.08 0.07
Leaves Fruit Shoots Roots
1.27 1.01 0.24–0.82 0.55
0.07 0.02 0.02–0.03 0.03
1.02 1.10 0.25–0.08 0.57
0.38 0.03 0.11–0.28 0.17
0.13 0.12 0.02–0.09 0.06
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Alternate bearing has been the target of recent research. Li et al. (2001) showed that spraying bayberry trees with 250 g/L GA3 in June and July inhibited the activities of PAL, POD, and PPO, and hence slowed down the biosynthesis of lignin, suppressed the differentiation of flower buds, and as a result, greatly reduced flowers in the following year. These results confirm those of Lavee (1989), who found that phenylalanine ammonia lyase (PAL), peroxidase (POD), polyphenol oxidase (PPO), and lignin were related to formation of flower buds. GA3 treatment promoted the emergence of spring shoots by 133%, increased the size of flower buds on spring shoots, and increased fruit weight by 3.8 g, soluble solids by 3.4%, and advanced maturity by 3 days (Liang et al. 2000). Paclobutrazol (PP333), an inhibitor of GA biosynthesis, applied in autumn or spring to arrest the vigorous growth of young trees, accelerates the formation of flower buds. However, Luo and Huang (1997) reported that spraying trees with PP333 at 500 mg/L in spring decreased fruit size and sugar content while increasing acid levels. Trunk spiral girdling also effectively promotes flower formation (Luo et al. 1999). In China, growing red bayberry in greenhouses was first carried out in Wenzhou, Zhejiang in 1999–2000 with ‘Ding-ao’ (Huang and Zhao 2001). The system has proved to be profitable, with fruit in the market early in the season realizing higher prices. The plastic house, 20 m × 10 m × 4.5 m, resulted in average temperatures being increased by 4.5°C, humidity by 7.5%, the ripening date being advanced by 14–16 days, and yields being increased by 11.5%. However, the time from fruit set to full maturation did not change, remaining at about 106 days. C. Pests and Diseases There are important disease and pest problems in red bayberry (listed in Table 3.4), and although studies on these are generally limited, there is some information available in the literature. Pseudomonas syringae pv. myrigae is one of the most widely distributed pathogens, infecting 2- to 3-year-old shoots and resulting in a tumor-like growth known as red bayberry ulcer or sore (Li 2002). Smooth, milky tubercles arise at the infected sites, and then develop into larger, rough, brown or black tumors, 1.5–2 cm in diameter. The symptoms become apparent about 30 days after infection. The disease develops in late April to May, and protective methods involve removal and burning of infected shoots followed by a 0.5% Bordeaux spray. Brown leaf spot results from infection of Mycosphaerella myricae Saw. The round or irregular spots are 4–8 mm in diameter, with brown
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Table 3.4. Major pathogens and pests of red bayberry (data from Chen 1994; Cai 2000; Rao et al. 2001). Disease or pest Disease Brown leaf spot Root rot Rust Tumor-like growth Red mould Stem blight Shoot rot Nematode Root-knot Insect Leaf wilt moth
Scale insect Leaf rolling moth Scale insect Fruit fly White ant White ant
Affected tissue
Production area
Mycosphaerella myricae
Leaves
Zhejiang
Botryosphaeria dothidea Caeoma makinoi Kusano Pseudomonas syringae pv. myricae Corticium saimonicolor Myxosporium corticola
Roots Leaves Shoots, trunk
Valsa coronata
Cortex of shoot
Zhejiang Fujian Zhejiang, Japan Zhejiang All producing areas Zhejiang
Meloidogyne spp.
Roots
Fujian
Lebeda nobilis
Leaves
Lepidosphes cupressi Homona spp.
Spring leaves Young leaves
Jiangsu, Zhejiang, Fujian Zhejiang Zhejiang
Fiorinia myricae Drosophila melanogaster Odontotermes formosanus Macrotermes barneyi
Fruit Fruit Trunk, root Trunk, root
Japan Japan Zhejiang Zhejiang
Binomial
Branches Trunk
or greyish-brown borders and reddish-brown or greyish-white centers. The spots can coalesce and may result in leaf wilting and abscission. Control is through use of fungicides such as a 0.5% Bordeaux spray, and 70% thiophanate methyl and 50% carbendazol wettable powders, sprayed onto foliage one month before full fruit ripening, two weeks prior to harvest, and after harvest (Li 2002). Root rot is an important disease in Zhoushan Island of Zhejiang Province. The pathogen has been identified as Botryosphaeria dothidea (Moung ex Fr.) Ces. & de. Not. (Li et al. 1995), with infection spreading through the root system, resulting in wilting and tree death. Control is through soil applications of carbendazol at 0.25–0.5 kg/tree or thiophanate at 0.25–0.5 kg/tree (Ren et al. 2000).
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Scale insects are common and important pests resulting in severe yield losses and decline in fruit quality; they include Lepidosaphes cupressi Borchsenius in Zhejiang and Jiangsu areas of China, and Fiorinia myricae Targioni in Japan (Xu et al. 1995; Mao 2000). Lepidosaphes cupressi feed on foliage and have two reproductive cycles per year, egg-laying being in mid-April and late July. Insecticides such as buprofezin are used for control, in combination with agriculture practices and native predators such as Chilocorus kuwanae Silvestri and Prospaltella spp. (Xu et al. 1995). D. Harvest and Handling Bayberry fruit are picked when eating ripe. Fruit maturation and time of ripening on the tree varies greatly with growing region. The fruit ripen in early April in Guizhou, from mid- to late May in Fujian, Guangdong, and Sichuan, and from early June to mid-July in Zhejiang, Anhui, Jiangsu, Hunan, and Jiangxi. In most regions, high temperatures and rain are common at the time of fruit ripening, making them susceptible to preharvest drop and rots, resulting in a comparatively short harvest time (Liu 2000). Fruit maturation also varies with cultivars, and since unripe fruit are excessively acid, estimation of maturity and the appropriate harvest time is important. Flesh color is a useful indicator of ripeness and is used as a harvest index. For example, color changing from red to purple or black indicates ripeness for the black type, from bluish green to white for the white type, and from green to deep red for the red type. The soluble solids contents increase in the fruit with ripening, while total acid levels decrease. The optimum acid content for harvest is between 1–1.2% for ‘Biqi’ fruit (Miao and Wang 1987). Individual fruit on a tree ripen at different times, and fruit often have to be picked as frequently as every day. Since the fruit are susceptible to mechanical injury, careful handling is necessary. The optimum times for picking are early morning and evening, when the field heat is least. The flesh is susceptible to damage from pickers, and current recommendations are that fruit should be picked with stalk attached, and packed in 3–5 kg bamboo baskets with leaves or weeds to reduce damage. Fruit shaken from the trees can only be used for processing. E. Storage and Transportation Red bayberry is a delicate fruit and has a short storage life, made shorter by enhanced flesh softness resulting from high temperatures and rain at harvest. The storage life of the fruit is 9–12 days at 0–2°C, 5–7 days at
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10–12°C, and 3 days at 20–22°C (Xi et al. 1993). There is a need for more research on extending the storage and shelf life of the fruit, particularly if it is to be used more widely as an export crop. As the fruit ripens, the total soluble solids (TSS) contents increase and acid levels decrease, resulting in higher ratios of TSS to acids. Sugars are the main constituents of TSS, and sucrose is the principal sugar, accounting for about 60% of the total. Citric acid is the predominant acid, with oxalic acid as the next most abundant; acetic and malic acids are minor components. Fruit quality declines rapidly during storage. For example, after storage at 0–2°C for 12 days, fruit TSS decreased by 10.5%, total acids by 41.4%, sucrose by 49.1%, and vitamin C by 36%, from 432 µmol/L to 277 µmol/L (Xi et al. 1993). These decreases can be retarded by treatment with salicylic acid, an inhibitor of plant senescence (Gao et al. 1989). Cell membrane permeability, measured by changes in electrical conductivity of tissue, increases during fruit storage, and is greater at higher temperatures (Xi et al. 1994). These permeability changes, along with increased respiration and ethylene production, increase under vibrational stress, such as may occur during postharvest handling and transport (Ying et al. 1993; Zheng et al. 1996). There are different views on the respiration pattern of ripening red bayberry fruit. Xi et al. (1994) classified it as nonclimacteric, whereas Hu et al. (2001) regarded it as climacteric because they detected a small ethylene production peak both at 21°C and 1°C. Ethylene production during storage may be dependent on fruit maturity at harvest, since less mature ‘Biqi’ fruit (picked at the pink stage) showed some increase in ethylene production after harvest (Fig. 3.7; K. Chen et al., unpublished data). The activity of superoxide dismutase (SOD), a free radical scavenger and thus a protectant against oxidative stress, gradually increases in the fruit during the first 6 days after harvest, and then decreases rapidly, following a pattern familiar in senescing tissues. High storage temperatures and vibration stress accelerate this decline in SOD activity (Xi et al. 1994; Zheng et al. 1996). The levels of SOD in vibration-stressed fruit were less than those in control fruit, supporting the observation that such stress can promote fruit senescence (Zheng et al. 1996). Malondiadehyde (MDA), a product of membrane peroxidation, which itself can further damage membrane structure and function, has been followed during storage. Fruit stored at 1°C or under high nitrogen (85%) had substantially lower contents of MDA and a longer storage life (Xi et al. 2001). Another group of metabolites, polyamines including spermidine, spermine, and putrescine, share the same precursor as ethylene in their biosynthetic pathway. In a study of vibration stress on bayberry
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Fig. 3.7. Changes in ethylene production of ‘Biqi’ red bayberry fruit of different maturity (K. Chen et al., unpublished data).
fruit, synthesis of spermidine increased whereas ethylene production decreased during the initial post-vibration storage period, suggesting a possible protective metabolic system (Zheng et al. 1996). At a later stage, spermine content decreased while ethylene was produced at a higher rate than in control fruit, suggesting that vibrational stress ultimately accelerated the overall senescence process. Putrescine accumulated during the final storage period, and may be detrimental to fruit storage. Storage life of the fruit can be extended up to two weeks if fruit are stored at 0–1°C, with a relative humidity of 85–90% (Xiao et al. 1999; Xi et al. 2001). Postharvest treatments such as sodium sorbate, 1% salicylic acid, or 0.5% CaCl2 together with 7.5 mg/L NAA (Liu 2000) increased storage life, although 1-MCP (the inhibitor of ethylene reception) had little effect (K. Chen et al., unpublished data). Modified atmosphere packaging and controlled atmospheres have not been studied to any great extent.
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In China, red bayberry is traditionally picked from the tree directly into bamboo baskets, and then transported to the market. Because of the increasing commercial production and value of the crop, packaging of the fruit has greatly improved. Fruit are graded by size and color to provide uniform packs. In Yuyao, Zhejiang province, high-quality ‘Biqi’ fruit are selected and packed in 500-g plastic boxes, then in 3-kg cartons, and shipped to Hong Kong. ‘Dongkui’ fruit, being larger and of higher quality, are packed 10 to a plastic box. Good results have also been achieved with other cultivars by changing the number of fruit in a box (Lu et al. 1999). In Japan, red bayberry are packed in 400-g polyethylene bags and then into 1.6-kg wooden or plastic boxes (Miao and Wang 1987). Because they are susceptible to rots, fruit should be precooled before packing and transported carefully to avoid vibration and high temperatures. Since the short storage life limits the period of supply to the market, there are benefits in freezing. Fresh fruit can be blast-frozen at –25 to –30°C for 15 minutes, and then stored and transported at –18°C. F. Processing Red bayberry fruit can be processed into jam, juice, wine, or as candied products, and canned red bayberry fruit is exported from China, particularly to Southeast Asian countries. Recent annual production of the canned product in Zhejiang has reached 1,800 t, about a third of which is exported. Ye and Zhang (2000) have shown that the fruit pigments can be used as food additives, although they are readily affected by pH, ultraviolet light, and reducing agents. Rapid and simple carbon dioxide supercritical extraction technology is needed for pigment extraction. The pigments have good potential uses so long as stability can be assured. Juice can be extracted with 2% saline at 70–80°C, and the preferred product contains 40% original extract, 10.5% sugar, and 0.45% acid (Zheng and Chen 2000). Red bayberry wine is also an important product of the fruit. Relatively high pectin and cellulose contents are largely responsible for the existence of methanol in the wine, and this needs to be kept at levels less than 0.08 mg/100 ml (Huang 1999). The composition of red bayberry fruit is summarized in Table 3.5. In addition, three flavonoids have been isolated from the fruit stone and identified by spectral analysis as quercetin, myricetin, and quercetin-3-O-αD-glucopyranosyl-(6→1)-α-α-L-rhamnopyranoside (Zou 1995). These compounds, especially quercetin and myricetin, are active antioxidants.
110 Table 3.5.
K. CHEN, C. XU, B. ZHANG, AND I. FERGUSON Chemical composition of ripe red bayberry fruit. Content (fresh weight basis)
Component
Reference
Total soluble solids Total sugars Sucrose Glucose Fructose Total acids Citric acid
11.6–13.4% 9.8–11.7% 46.6 mg/g 13.5 mg/g 13.8 mg/g 0.42–1.28% 0–10.3 mg/g
Tartaric acid Malic acid Succinic acid Acetic acid Oxalic acid Minerals Potassium Trace elements (Fe, Mn, Zn, Cu, Mg) Vitamins Vitamin C (ascorbic acid) Vitamin B1 Vitamin B6 Vitamin E Vitamin A Protein
1.2–4.5 mg/g 1.3–1.7 mg/g 1.2–3.1 mg/g 0.5–2.0 mg/g 1.9 mg/g
Wang et al. 2001 Wang et al. 2001 Zhang et al. 1991 Zhang et al. 1991 Zhang et al. 1991 Wang et al. 2001 Zhang et al. 1991; Wang et al. 2001 Wang et al. 2001 Wang et al. 2001 Wang et al. 2001 Wang et al. 2001 Zhang et al. 1991
1.41 mg/g 0.075 mg/g
Wang et al. 2001 Miao and Wang 1987
0.11–1.14 mg/g
Wang et al. 2001
0.054 mg/g 0.008–0.016 mg/g 0.0007–0.0016 mg/g 0.00004–0.0005 mg/g 0.33%
Wang et al. 2001 Wang et al. 2001 Wang et al. 2001 Wang et al. 2001 Zhang et al. 1991
There are also some unknown compounds in the stones that can arrest the growth of cancer cells or induce cell death (Zhang et al. 1993).
VI. CONCLUDING REMARKS China has a rich genetic resource in red bayberry, with a wide range of cropping and fruit properties that should be exploited for breeding purposes. Some wild species fruit early, resist high temperature, are dwarfing, and have excellent postharvest properties. Many contain compounds of medical importance. These resources are in danger of being destroyed; species such as Myrica esculenta Buch are on the edge of extinction.
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There are 268 cultivars planted in China, of which about two-thirds ripen in mid- to late June (Zhang and Miao 1999). There are some earlymaturing cultivars such as ‘Zaoxingmei’ grown in Huangyan and Wenling, Zhejiang province, that ripen in May, but the fruit is small and acid. The storage life of almost all cultivars is very limited, resulting in severe losses each season. It is imperative that further breeding work be carried out to create new early-maturing cultivars of high fruit quality and longer storage potential. Only 9.3% of total cultivars are white fleshed (Miao and Wang 1987), and only one, ‘Shuijingyangmei’ or ‘Crystal’, has been commercially planted, in Shangyu, Zhejiang province, its place of origin. There is a need for more effort in breeding new white-fleshed cultivars adapted to different climates. Alternate bearing has a major impact on production; in years of high yield, the price of fruit may be low, while in low years there may be insufficient fruit to meet consumer demand. Furthermore, compared with other fruit crops, the yield of red bayberry is quite low. This means that there is a need to increase yield and reduce cropping variability. The short storage life, together with other cultivation, harvesting, and handling problems has inhibited the development of the crop. Red bayberry is a candidate for international markets provided that storage and shelf life of the fruit can be extended. The crop has potential outside of China in warm-temperate and sub-tropical growing conditions. With current limitations on storage life, production would need to be aligned with easily accessible markets.
LITERATURE CITED Cai, H. 2000. Occurrence and control of rust on red bayberry (in Chinese). South China Fruits 29:28–29. Chen, F. Y. 2000. Survey, evaluation and utilization of bayberry resources in Zhejiang (in Chinese). Guangxi Hort. 31:16–17. Chen, Y. B. 1994. Study of advances in occurrence and control of diseases and pests on red bayberry (in Chinese). Subtrop. Plant Res. Commun. 23:64–68. Chen, Z. Y., S. Y. Li, M. E. Ye, and S. C. Qin. 1992. A study on the relationship between climatic ecological factors and fruit quality of red bayberry (in Chinese). J. Zhejiang Agr. Univ. 18:97–103. Chen, Z. Y., S. Y. Li, M. E. Ye, and Z. W. Yu. 1989. Effects of altitude on flowering and fruit quality of red bayberry (in Chinese). J. Zhejiang Agr. Univ. 15:302–304. Chi, W., J. Xu, L. Y. Guo, and Y. S. Zheng. 2000. Effects of polyphenols from red bayberry on protection of blood cells and hemopoietic tissues from injuries (in Chinese). Traditional Chinese Drug Research & Clinical 11:20–22.
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Gao, J. C., M. Y. Yuan, W. L. Gu, and R. J. Xu. 1989. Effects of salicylic acid (SA) on physiological processes and quality of red bayberry fruit (in Chinese). Food Sci. (6):42–43. Gong, J. Q. 1995. An investigation on growth of fruit and shoots of ‘Dongkui’ red bayberry (in Chinese). Fujian Fruits (1):24–25. Guo, S., and S. Y. Li. 1994. Preliminary study on utilization of karyotype analysis in classification of red bayberry (in Chinese). Shu Guo’s Corpus on Citrus Research. p. 129–137. Hu, X. Q., X. Yu, and L. G. Chen. 2001. Studies on some physiological characters of Chinese bayberry fruit during storage (in Chinese). J. Zhejiang Univ. (Agr. & Life Sci.). 27:179–182. Huang, J. Z., and Y. G. Zhao. 2001. Studies on protected culture of Ding-ao Yangmei (in Chinese). South China Fruits 30:33. Huang, Y. D. 1999. The formation of methanol in red bayberry wine and the analysis of the toxicity of methanol (in Chinese). Liquor-making Sci. & Technol. 92:60–61. Ji, H. 304. Nan Fang Cao Mu Zhuang (A prospect of the plants and trees of the southern regions). Commercial Press, Beijing, P. R. China. (Printed in 1955.) Lavee, S. 1989. Involvement of plant growth regulators and endogenous growth substances in the control of alternate bearing. Acta Hort. 239:311–322. Li, G. L., B. N. Lin, and D. X. Shen. 1993. Sex identification of horticultural dioecious plants by phenolic analysis (in Chinese). Acta Hort. Sin. 20:397–398. Li, H. Y., R. B. Gao, and Y. M. Hu. 1995. The symptoms and pathogen of the bayberry (Myrica rubra) root rot (in Chinese). J. Zhejiang Agr. Univ. 21:398–402 Li, J. 2001. Practical techniques of pruning and top grafting of South China fruits (in Chinese). China Agr. Press, Beijing, P. R. China. Li, S. Y. 2002. Encyclopedia of Zhejiang agriculture—Red bayberry (in Chinese). China Agr. Sci. & Technol. Press, Beijing, P. R. China. Li, S. Y., and S. Z. Dai. 1980. A study on flower bud differentiation of red bayberry (in Chinese). Acta Hort. Sin. 7:9–16. Li, S. Z. 1578. Compendium of Materia Medica (in Chinese). People’s Medical Publishing House. Beijing, P. R. China. (Printed in 1978.) Li, X. J., J. L. Lu, and S. Y. Li. 1999. Advances in bayberry research in China (in Chinese). J. Sichuan Agr. Univ. 17:24–229. Li, X. J., S. Y. Li, J. L. Lu, and G. Y. Wang. 2001. Effects of gibberellic acid on leaf lignin levels, related enzymes and flower formation in bayberry (in Chinese). Acta Hort. Sin. 28:156–158. Li, Z. L., S. L. Zhang, and D. M. Chen. 1992. Red bayberry (Myrica rubra Sieb. & Zucc.): A valuable evergreen tree fruit for tropical and subtropical areas. Acta Hort. 321:112–121. Li, Z. Z., J. B. Huang, L. C. Yang, Z. Q. Li, and F. G. Xie. 1993. Nitrogen-fixing activities of Myrica rubra root nodules and evaluation of the amount of nitrogen-fixation (in Chinese). Fujian Res. Inst. Forestry 20:36–38. Liang, S. M., S. L. Miao, and B. S. Jin. 2000. Effects of gibberellins on flowering control in red bayberry (in Chinese). Acta Agr. Zhejiang 12:147–150. Lin, B. N., L. J. Xu, and C. L. Jia. 1999. Studies on identification and classification of genomic DNA in Myrica by RAPD analysis (in Chinese). Acta Hort. Sin. 26:221–226. Lin, D. Y. 1984. Study on the pigments of red bayberry (in Chinese). China Fruits 4:47–49. Liu, Q. 2000. Handbook for cultivation of special local fruits in South China (in Chinese). China Agr. Press. Beijing, P. R. China. Lu, D. H., X. Z. Lin, and Z. G. He. 1999. Study on fruit storage of red bayberry (in Chinese). Fujian Fruits 100:11–12.
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Luo, Z. Y., and J. H. Huang. 1997. Effects of PP333 on growth and fruit set of young trees of ‘Dongkui’ red bayberry (in Chinese). J. Hubei Inst. National (Nat. Sci. Ed.) 15:13–16 Luo, Z. Y., J. H. Huang, T. Y. Xiang, and D. H. Wang. 1999. Effects of spiral girdling on maintaining flowers and fruit of ‘Dongkui’ red bayberry (in Chinese). South China Fruits 28:25–26. Mao, Q. M. 2000. Main pests endangering Myrica rubra in Ningbo and their prevention and control (in Chinese). J. Zhejiang Sci. & Technol. 20:66–68. Miao, S. L., S. B. Huang, S. M. Liang, and Y. J. Zhang. 1995. Study on ecological regionalization of Myrica rubra in China (in Chinese). J. Zhejiang Agr. Univ. 21:366–372. Miao, S. L., and D. X. Wang. 1987. Red bayberry (in Chinese). Zhejiang Sci. & Technol. Press, Hangzhou, P. R. China. Qu, Z. Z., and Y. W. Sun. 1990. Fruit species (in Chinese). China Agr. Press, Beijing, P. R. China. Rao, J. S., C. G. Ding, L. H. Chen, and Y. C. Zhu. 2001. Occurrence and control of Corticium saimonicolor on red bayberry (in Chinese). Plant Protect. Technol. & Exten. 21:23–33. Ren, R. H., Y. M., Hu, H. Y. Li, and L. B. Cao. 2000. Studies on red bayberry root rot and control. South China Fruits (in Chinese) 29:32–33. Ruan, Y. L., and L. M. Wu. 1991. Studies of photosynthetic characteristics of wintering loquat and bayberry (in Chinese). Acta Hort. Sin. 18:309–312. Wang, B. B., Y. P. Zheng, Z. J. Li, and W. W. Yu. 2001. Utilization of Myrica rubra resources in Zhejiang and their ecological effects (in Chinese). J. Zhejiang Forestry College 18:155–160. Wang, D. X. 1987. Cultivation of red bayberry in Japan (in Chinese). China Fruits 32:57–59. Wang, H. Y., and W. N. Huang. 1990. Observations on the structure and ultrastructure of root nodules and nitrogenase activity in Myrica rubra (in Chinese). Acta Phytophysiol. Sin. 16:152–157. Wang, J. B. 1995. Pomology of individual fruits (for Southern China, Second Edition) (in Chinese). China Agr. Press, Beijing, P. R. China. Wang, P. L. 1999. Growth characters of ‘Dongkui’ red bayberry and techniques for high yield (in Chinese). Fujian Fruits 1:45–47. Wang, W. M., and Y. B. Chen. 1989. Effects of planting red bayberry on infiltration and erosion control of deteriorated soil (in Chinese). Sci. & Technic. Info. Soil & Water Conserv. 1:18–20. Wu, G. M.1984. Taxonomy of temperate fruits in China (in Chinese). Agr. Pub. House, Beijing, P. R. China. Wu, G. M. 1995. Precious southern Yangtze fruits (in Chinese). Dept. Hortic., Zhejiang Agr. Univ., Hangzhou, P. R. China. Wu, X. L., and X. P. Gu. 1994. A study on the characteristics of nodulation and nitrogen fixation in Myrica rubra (in Chinese). Forest Res. 7:206–310. Xi, Y. F., Z. S. Luo, D. Cheng, X. Cheng, and Y. G. Wang. 2001. Effect of CA storage on active oxygen metabolism in Chinese bayberry fruit (Myrica rubra) (in Chinese). J. Zhejiang Univ. (Agr. & Life Sci.) 27:311–313. Xi, Y. F., Y. H. Zheng, D. M. Qian, and T. J. Ying. 1993. Effects of storage temperature on changes in nutritional composition and decay rates in fruit of red bayberry (in Chinese). Bul. Sci. Technol. 9:254–256. Xi, Y. F., Y. H. Zheng, T. J. Ying, J. F. Ying, and Z. L. Chen. 1994. Senescence physiology of Chinese bayberry fruit during storage (in Chinese). Acta Hort. Sin. 21:213–216. Xiao, Y., J. C. Huang, and H. B. Li. 1999. Study of the effect of calcium and NAA treatments on the storage of red bayberry (in Chinese). J. Southwest Agr. Univ. 21:307–310.
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Xu, C. M., D. R. Zhou, and X. Y. Wu. 1995. Studies on occurrence and control of Lepidosaphes cupressi Borchsenius on Myrica rubra. J. Nanjing Agr. Univ. 18:57–62. Ye, R. Y., and J. Zhang. 2000. The analysis of physical and chemical characters of red bayberry (in Chinese). Exploit. Agr. & Pastur. Product. 1:11–12. Ye, X. Q., J. C. Chen, and P. Shu. 1994. Identification of the constituents of Yangmei (Myrica rubra cv. Biqi) (in Chinese). J. Zhejiang Agr. Univ. 20:188–190. Yi, Y., and N. Liu. 2000. Comparison of the quercetin contents in leaves of different types of Myrica nana Cheval (in Chinese). J. Plant Resour. & Environ. 9:59–60. Ying, T. J., C. R. Chen, Y. F. Xi, and Y. H. Zheng. 1993. Respiration reactions and cell membrane permeability changes in red bayberry (Myrica rubra) fruit under vibration stress (in Chinese). J. Zhejiang Agr. Univ. 19:80–81. Yu, D. J. 1979. Taxonomy of fruits in China (in Chinese). Agr. Pub. House, Beijing, P. R. China. Zhang, W. M., L. M. Wang, S. R. Zhang, and J. Y. Xu. 1993. A preliminary study on use of red bayberry stones to kill or constrain gastric cancer cells (in Chinese). Acta Chin. Medicine & Pharmacol. (3):38. Zhang, Y. J. 1999. The analysis of mineral nutrient absorption of Chinese bayberry (Myrica rubra) Dongkui over a whole year (in Chinese). Acta Agr. Zhejiang. 11:208–211. Zhang, Y. J., and S. L. Miao. 1999. Resources of red bayberry and its utilization in China. South China Fruits (in Chinese) 28:24–25. Zhang, Y. J., S. L. Miao, D. X. Wang, X. J. Qi, S. M. Liang, and Z. L. Chen. 1991. Alteration of pigments and the major endogenous components of fruits of colored bayberry (Myrica rubra) varieties during pigment development stage (in Chinese). J. Zhejiang Agr. Univ. 3:198–201. Zheng, M. F., and X. H. Chen. 2000. Red bayberry fruit extraction and the production of its juice (in Chinese). Light & Textile Indust. Fujian 130:9–11. Zheng, Y. H., T. J. Ying, Y. F. Xi, L. C. Mao, and Z. L. Chen. 1996. Effects of vibrational stress on postharvest senescence physiology of Chinese bayberry fruit (in Chinese). Acta Hort. Sin. 23:214–234. Zhong, Z. X., J. P. Qin, X. F. Chen, and G. F. Zhou. 2000. Hypoglycemic effect of ampelopsin on diabetic rats induced by steptozotocin (in Chinese). Guangxi Sci. 7:203–205. Zou, Y. H. 1995. Study on the antioxidant ingredients of edible oils in the fruit kernel of Myrica (in Chinese). Chem. & Indust. Forest Product. 15:13–17.
4 Protected Cultivation of Horticultural Crops in China* Weijie Jiang, Dongyu Qu, and Ding Mu Institute of Vegetables and Flowers Chinese Academy of Agricultural Sciences 12 Zhongguancun S. Street, Beijing 100081 China Lirong Wang Zhengzhou Fruit Research Institute Chinese Academy of Agricultural Sciences Zhengzhou, Henan Province 450009 China I. INTRODUCTION II. THE ENERGY-SAVING GREENHOUSE A. General Information B. Structure C. Advantages and Disadvantages III. VEGETABLE CROPS A. Mechanization of Vegetable Seedling Production B. Soil-less Systems C. Nutrient Solution and Substrate D. Disease and Insect Control IV. FLORICULTURE A. Present Situation B. Facilities and Equipment C. Commercial Flower Production V. FRUIT TREES A. Present Situation B. Cultivars C. Cultural Techniques VI. FUTURE DEVELOPMENT OF PROTECTED HORTICULTURE LITERATURE CITED *Acknowledgment: The authors thank Professor Guanghua Zheng for his valuable contribution to the preparation of the manuscript. Horticultural Reviews, Volume 30, Edited by Jules Janick ISBN 0-471-35420-1 © 2004 John Wiley & Sons, Inc. 115
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I. INTRODUCTION Protected horticulture production has a long history in China. In the Hanshu, a history written in the Han Dynasty (206–23 B.C.E.), China had begun to grow alliums such as Welsh onion and leek in heated structures during the winter. In the Tang Dynasty (618–907 C.E.), natural hot springs were used for vegetable growing in winter. In the Song Dynasty (960–1279 C.E.), a simple greenhouse covered with translucent paper had been developed to grow vegetables, and flowers, and in the Ming Dynasty (1368–1644 C.E.), these greenhouses were used to grow flowers during winter around Beijing (Fig. 4.1). Horticultural production within glass greenhouses occurred in Shanghai at the end of the 19th century, and commercial greenhouses for special pot production for species such as Gloxinia and Begonia tuberosa had started at the beginning of the 20th century (Zhang 2001). Windbreaks (Fig. 4.2) and solar, lean-to greenhouses (Fig. 4.3) were constructed in Northern China in the 1950s. At the beginning of 1960, polyvinyl chloride (PVC) and polyethylene (PE) film were produced for agricultural use in the Beijing and Shanghai areas, which promoted the development of medium-high (0.8–1.5 m) and low (2.0 m high) was built to grow spring cucumber very successfully in Jilin province, where winter temperatures reach –30°C. In 1980, low-density polyethylene film was produced and galvanized steel pipe was used to build plastic high tunnels in the Beijing area, but the area of primary protected horticulture was only 16,000 ha. Protected horticulture developed very rapidly in China after 1981, especially during the 1990s. The total area of protected horticultural crops reached 1,401,000 ha in 1999. China is now the leading country in the world for protected horticulture, including multi-span greenSunlight Roof
Paper Ground Wall
Figure 4.1 A special type of greenhouse for growing flowers during the Ming Dynasty. Oiled paper is also used.
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Figure 4.2
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Windbreak used in China in the 1950s.
houses, solar, lean-to greenhouses, and plastic tunnels (Zhang and Li 1999; Jiang et al. 2000). Solar, lean-to greenhouses, with or without heating systems, and large, plastic high tunnels developed very rapidly in China. In 1995, solar, lean-to greenhouses and large high tunnels accounted for about 45% of the total area of protected horticulture, and by 1999 the proportion had increased to 59%. Low tunnels decreased from 55% to 41% of total area from 1995 to 1999 (Zhang and Li 1999) due to low production efficiency, inconveniences, and a higher labor input requirement. Plastic high tunnels and low tunnels are widely used for commercial horticultural crop production all over China (Fig. 4.4). In the north, where winter is cold, plastic tunnels are used mainly in early spring and late autumn. In the south, where winter is mild, plastic tunnels can be used all year (Zhang 2001). In the mid-1980s, a new type of “energy-saving, solar, lean-to greenhouse” was developed in Liaoning province of Northeast China that was adapted for producing cucumber, tomato, eggplant, and watermelon without heating during the winter season. This “energy-saving” greenhouse has been extended to the whole of North China from latitude 33°N to 47°N, and has made a great contribution to the vegetable supply of cities. The area of energy-saving greenhouses was 104,413 ha in 1995 and 200,000 ha in 1999, a 92% increase (Zhang and Li 1999; Chen 2001). All types of protected horticulture have developed rapidly since 1990,
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Figure 4.3
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Solar lean-to greenhouse used in China in the 1950s.
especially in the last 5 years, but the proportion of each type has changed (Table 4.1). Modern greenhouses in China started in the late 1970s, with 21 ha of metal-frame greenhouses imported from 1978 to 1994. On the basis of this introduced technology, China developed its own technology in the late 1980s. This includes large-size tunnels, single-span glasshouses, and double-pitched glasshouses, mainly with a gate-type steel frame structure. In the 1990s, and especially after 1995, the large-scale introduction of foreign greenhouse facility and cultivation technology stimulated
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Figure 4.4
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Plastic tunnel for sinuatum production.
the rapid development of protected horticulture. As of 1995 the total area of the multi-span greenhouse was only about 45 ha. In 1999, it was 588 ha, a 12-fold increase over 1995, of which 180 ha were imported (Table 4.2) and 408 ha were locally made. Modern greenhouse coverings include glass, poly-carbonate (PC), and polyethylene (PE). Glasshouse structures include gate-type steel frame and Venlo-type. The structure of the PC house is similar to the glasshouse, but the glazing material is PC sheet or a combination of PC sheet and PE film. Plastic house structures include arch roof, saw-tooth type, double-pitched roof, Table 4.1.
Area of protected horticultural production in China. Greenhouse area (ha)
Year
High tunnel
Low tunnel
Heated
Solar lean-to
Energy-saving solar lean-to
Total (ha)
1981 1985 1990 1995 1997 1999
1,253 11,766 30,273 186,620 190,580 459,773
4,940 46,473 98,213 333,893 424,160 568,586
300 2,296 3,800 4,793 6,806 14,660
706 6,760 18,380 69,413 78,200 152,293
— 420 8,286 104,413 141,340 200,000
9,180 69,700 160,942 701,127 843,083 1,397,311
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W. JIANG, D. QU, D. MU, AND L. WANG Table 4.2. Greenhouse imports to China from overseas. Country or region France Spain Netherlands Israel Korea U.S.A Japan Canada Total
Area (ha) 60.7 33.9 28.5 25.0 10.0 6.2 3.2 2.8 180.3
and double-deck structure (Zhou and Cheng 1998; Zhou and Wang 2001). Modern multi-span greenhouses (Fig. 4.5) have been increasingly researched by Chinese horticulturists, due to the high technology, capi-
Figure 4.5 Multi-span greenhouse for tomato production in eco-organic type soil-less culture system.
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tal, and energy inputs required. Generally, the height of the greenhouse is 4.3–6.0 m and the span is 8–11 m. It has roof and side ventilation, automatically controlled temperature and irrigation systems, and it is covered with glass, PC sheet, plastic film, or double-layer plastic film. Usually, the greenhouse area is 3,000 to 10,000 m2. The cost of constructing this type of greenhouse is US$50–$120/m2, depending on the covering material used and how the greenhouse is equipped. For production of high-quality horticultural crops, the greenhouse requires systems for heating, shading, fertigation, ventilation, and light supplementation. In recent years, due to the expanding greenhouse market in China, many greenhouse enterprises have been established, including those owned by foreign companies [FatDragon (USA), Richel (France), Ach-Olive (Spain)] as well as domestic companies (Jing-peng and Shanghai Long-march). Although the area of the modern greenhouse in China has been increasing sharply, the outputs are unsatisfactory due to poor equipment in the greenhouses, lack of essential knowledge by growers, and lack of adaptation of foreign greenhouses to local conditions. As a consequence, the market proportion of domestic greenhouse companies has been rising continuously in the past three years. Nets for shading and insect control had been used for raising seedlings derived from tissue culture before 1987. In 1988, shading nets were used for commercial production of vegetables, and have expanded rapidly since the 1990s. In 1999, the area of shading net was 16,000 ha, and use of insect net was 73,000 ha. The development of protected horticulture has increased vegetable production in China, especially in winter. The annual consumption of protected vegetables increased from 0.2 kg per capita in 1981, to 24 kg in 1995 (Zhang and Li 1999), and 52 kg in 2000. At present, only 7% of the protected horticulture area (100,000 ha in 1999) is planted to tree and vine fruits (peach, nectarine, grape, cherry, strawberry, and melon), and to flowers. These crops are more profitable than vegetables, so an increase can be expected in the future. II. THE ENERGY-SAVING GREENHOUSE A. General Information Since the mid-1980s, the energy-saving greenhouse (also referred to as an “energy-saving, solar, lean-to greenhouse”) has developed very rapidly in North China (33°N to 47°N). The total area of this type of greenhouse reached 200,000 ha in 1999 (Zhang and Li 1999). The energy-saving greenhouse (Fig. 4.6) was developed from the Chinese
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Figure 4.6
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Basic structure of a typical energy-saving greenhouse.
traditional lean-to greenhouse in Anshan, Liaoning province of North China in the mid-1980s (Chen 1991, 1994, 2001). It is composed of a north (or back) wall, and east and west gable walls for insulation against the cold outside wind. The walls are constructed with bricks and thermal-preservation materials. The front roof has a transparent plastic film for receiving sunlight. During the night, the plastic film is covered by a mat made of insulating materials. In the morning, once the air temperature inside the greenhouse rises, the mat is rolled up. In the afternoon, when the air temperature inside greenhouse goes below 17°–18°C, the mat is rolled down over the front roof to prevent heat loss. A “coldproof” ditch (0.5–1.0 m deep, filled with insulating materials, such as straw and manure) reduces heat exchange through the soil between the inside and outside of the greenhouse. The ridge of the greenhouse is usually 3 to 4 m high, the span is 6 to 8 m wide, and the length is 40 to 100 m long. The back wall is 0.5 to 1.2 m thick. The unit area is about 300–800 m2. The energy-saving greenhouse is a special type of structure. The heat energy resource comes from the solar radiation and depends on structural and heat-conservation technology (Sun 1993; Yang and Chen 1994). Even in the severe cold winter season of North China, air temperature inside the greenhouse, even without supplemental heating, is sufficient for cool-season leafy vegetables such as celery and Chinese chive and also warm-season vegetables such as tomato, cucumber, sweet pepper, eggplant, and even watermelon (Fig. 4.7). In general, capital costs and
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Figure 4.7
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Energy-saving greenhouse for vegetable production in winter.
operational expenses are much lower than that of a modern multi-span greenhouse. In the winter on a clear day, the greenhouse can receive sunlight for 6 hr with light intensity averaging 20–40 klx. The maximum temperature inside the greenhouse can be higher than 25°C, sometimes even up to 30°C, and can last 3–5 hr. Temperatures at night are not lower than 10°C, and on cloudy days, not lower than 6°C. Night temperature differences between the inside and outside of the greenhouse can reach 30°C. In this microclimate condition, certain cultural practices improve plant growth. These include adoption of low temperature resistant cultivars, grafting to cold resistant rootstocks, multi-layer PE film covering, irrigation, and temporary supplementary heating for warm-season crops such as tomato and cucumber. Leafy vegetables perform well in the greenhouse, even in unexpected cold and cloudy days. Why can the energy-saving greenhouse without a heating system grow vegetables when outside winter temperatures drop to –20° to –10°C, even –25°C, in the north of China? The answer is that the continental, monsoon climate of China receives high solar radiation in winter despite the very low temperatures in northern zones. While winter sunlight intensity is only 50%–60% of summer radiation, the solar radiation
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provides enough heat so that it can be stored by heat-conservation strategies (Chen 2001). B. Structure In the earlier developing stage of the energy-saving greenhouse, the greenhouse was built based on farmers’ experiences only, using cheap and simple materials. In the Beijing district, the internal growing space of the greenhouse was small, with a span of 5.0–6.0 m at a ridge height of 2.6–3.0 m. The wall was built of dry earth, brick, and concrete; the front roof frames were made of bamboo or wood, and the outside covering mat made of straw or cattail. Since the late 1980s, considerable research work has been conducted to improve heat preservation and progress has been rapid. As a result, horticultural crop production in the energy-saving solar greenhouse is rapidly increasing. 1. Dimensions. Based on 20 years of research, the span of the greenhouse has been gradually enlarged, based on local climatic conditions. In Northeast and Northwest China, the span is 6.0–7.0 m where the lowest winter temperature is below –17°C. In North China the span is 6.5–7.5 m where the lowest winter temperature is between –17° and –12°C. However, if the lowest temperature does not reach –12°C, the span can be 7.5–8.0 m. Greenhouse length is site dependent. The back (north) wall is about 2.0–2.4 m high, and the ridge is 3.2–3.5 m high; they depend on the span and local climate. At latitude 40°N, the span can be 7.0, 7.5, or 8.0 m, and the ridge 2.9, 3.2, or 3.5 m, respectively. In warmer locations, the span and ridge are wider and higher. 2. Front Support and Wall Body. The front support is made of bamboo or steel pipe covered with 0.1-mm thick PE film. The east, west, and north walls of the greenhouse are 0.5 to 1.2 m thick and made of bricks. During temperature warm-up during the day inside the greenhouse, the wall is an endothermic body, and during temperature cool-down at night, the wall body is exothermic. Therefore, the reasonable structure of the wall is a double layer. Between the two brick layers is a thermalprotective insulation material such as perlite, coal cinder, sawdust, or polystyrene in order to prevent heat loss. 3. The Back Roof. The back roof of the greenhouse is a multi-layered structure composed of wood, straw, coal cinder, polystyrene, and
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cement board. The roof consists of water-resistant, load-bearing, heatpreserving and water-resistant layers from the bottom to top. The elevation angle of the back roof is 35° to 40°, and is more than the local solar elevation angle at noon on the winter solstice to ensure that sunshine can reach the back wall throughout the winter. 4. Covering Materials. During the day, sunlight is transmitted into the greenhouse through PE film in the front (south) roof of the greenhouse. At night the PE film is covered with a 5 cm thick mat in order to keep the greenhouse warm in cold seasons. When the sun rises in the morning, the mat is rolled up and kept on the back roof. Before the mid-1990s, the mats were made of straw or cattails but these were very heavy and difficult to roll up manually. At present, new kinds of mats made from chemical fibers that are waterproof, heat-conserving, and easily carried are widely used as covering materials. Mats made of synthetic fibers can be easily handled by machine.
C. Advantages and Disadvantages The advantages of this type of greenhouse are twofold: (1) it has good thermal-preservation properties, and makes the cost of energy for growing horticultural crops quite low during the cold season; and (2) the cost of greenhouse construction is only US$6 to $18/m2, much less than that of a modern multi-span greenhouse, making it affordable for most Chinese farmers. However, the disadvantages of this type of greenhouse cannot be ignored. The first is the difficulty of controlling environmental conditions in the greenhouse. The second is that the land-utilization ratio is rather low, because this type of greenhouse usually needs 0.5 to 1.0 m thick walls for thermal preservation, and there must be a space between the two greenhouses (Fig. 4.8). The width of the space is at least twice the height of the greenhouse ridge in order to ensure that the front greenhouse will not block sunlight entering the one behind it. Thus, the land between the two greenhouses cannot have good crops due to the shortage of sunlight. The third disadvantage is that the non-standardized structure of the energy-saving greenhouse makes it difficult to install modernized facilities for controlling conditions within the structure. Starting in the early 1990s, many vegetable growers began to switch to flower production because greater profits could be achieved. By 1998, there were over 1230 ha of energy-saving greenhouses used for growing flower crops in China.
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Figure 4.8 The layout of energy-saving greenhouses, showing the space required between greenhouses to avoid shadow interference from adjacent structures.
III. VEGETABLE CROPS China has a long history of growing vegetables, especially those crops originating in China. About 209 taxonomic species of vegetables, belonging to 31 botanical families, are grown in China. The most important 15 vegetables in terms of total production and growing area are Chinese cabbage, radish, potato, chili pepper, cabbage, tomato, cucumber, pok choi, eggplant, green Chinese onion, celery, garlic, Chinese chive, mustards, and spinach. At the present time, vegetables take first place among China’s protected crops. A. Mechanization of Vegetable-Seedling Production Until 1987 there was little commercial vegetable-seedling production in China, and farmers raised their own vegetable seedlings from seed. Most farmers had only one or two energy-saving greenhouses of 500–700 m2, which made it difficult to grow good seedlings. In 1999, the protected area in China was 1.4 million ha, requiring tremendous amounts of seedlings for commercial production. As a consequence, the establish-
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ment of mechanized vegetable-seedling production nurseries receives high priority. In 1987, China established the first mechanized vegetable-seedling production farm in Beijing, a plug-seedling production system imported from the United States. The majority of trays had 72 and 128 cavities mainly used for tomato, pepper, cabbage, and cauliflower. The medium was 70% peat and 30% vermiculite mixed with NPK fertilizers. Good results were obtained in the first 10 years, and many large cities began building their own mechanized vegetable-seedling production farms with facilities imported from the United States, France, Holland, and Israel. At the same time, China developed and produced some small facilities to produce plug trays and planters for vegetable-seedling production, but not enough to meet the demands of the market. At present the scale of mechanized vegetable-seedling production in China is small, and the efficiency is low as compared with Western Europe and North America, but it has raised efficiency tenfold compared with older vegetable-seedling production systems, and costs have been reduced one third. Mechanized seedling production is expected to develop rapidly. B. Soil-less Systems Though soil is still the predominant growing medium in China, continuous cropping in greenhouses results in soil-borne diseases. This problem is difficult to solve using conventional rotations because the greenhouse is a high-investment facility and should not be used to grow low-value crops such as onion, carrot, and cabbage. Tomato, cucumber, pepper, eggplant, and melon can achieve good returns, but these crops require plant rotation. As a result, protected cultivation for vegetable production in greenhouses is gradually changing from soil to soil-less systems (Zheng and Wang et al. 1990; Jensen and Malter et al. 1994; Jiang et al. 1996, 1998b). The commercial soil-less culture in China began in 1941. A farm for soil-less vegetable production was built in Shanghai but the operation failed because of the high cost of production and commercial soil-less vegetable production was discontinued for over 30 years. In 1976, Shandong Agricultural University began to produce hydroponic vegetables in a small area, but there was only 0.1 ha of soil-less culture in 1981. Since then, soil-less culture has developed steadily. In 1993, China had 43 ha of different types of soil-less culture systems, mostly for vegetables. By 2000, there were 365 ha of soil-less culture area in China (Table 4.3) (Jiang et al. 2000, 2001a).
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W. JIANG, D. QU, D. MU, AND L. WANG Table 4.3. Distribution of soil-less culture in mainland China (2000). Location Shanxi Liaoning Shanghai Xingjiang Hebei Beijing Shenzhen Guangzhou Nanjing Hangzhou Tianjin Wushi Zhuhai Daging Shenli Hainan Changzhou Others Tota1
Area (ha) 130 50 30 25 15 15 10 7 6 6 4 4 3 3 3 2 2 50 365
Soil-less culture systems such as nutrient film technique, deep-flow hydroponics, rockwool culture, and bag culture were all learned from western countries. Recently, China has developed new soil-less systems, including eco-organic and floating capillary hydroponics, which are low cost and more suitable for local conditions. These systems have now been widely extended to different parts of China (Jiang et al. 2001a). 1. Nutrient Film Technique (NFT). NFT is mainly used in Nanjing. In the past 10 years, this system was used to grow lettuce and tomato. Normally, NFT systems (Fig. 4.9) use plastic, iron, or concrete troughs, with gravity flow nutrient solution (Jensen and Collins 1985; Jensen and Malter 1994). The depth of nutrient solution in the trough is only 0.5–1.0 cm. Problems of the NFT system are that it cannot withstand unexpected power loss, temperature fluctuations of the nutrient solution are not easily controlled in summer, and the technique results in high nitrates in plant tissues, and often low oxygen in the nutrient solution. We do not expect this system to be expanded rapidly in China (Jiang et al. 2001a).
4. PROTECTED CULTIVATION OF HORTICULTURAL CROPS IN CHINA
Figure 4.9
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The basic feature of a nutrient film technique (NFT) system (Cooper 1979).
2. Deep-Flow Hydroponics (DFH). The system is a trough system, but the depth of nutrient solution is 5–8 cm. The system can keep temperature and oxygen more stable and is resistant to an unexpected power failure (Fig. 4.10). It has now expanded to tropical and subtropical areas in China, such as Guangdong province. 3. Bag Culture. The common bag size is 70 × 35 cm, which contains 18 L of substrate and normally is used for tomato or cucumber production with 2 plants/bag (Fig. 4.11). This method was popularly used in commercial soil-less vegetable production until 1995, but has gradually decreased. 4. Rockwool Culture. Rockwool culture is the same as bag culture except that the substrate is rockwool, an excellent substrate for vegetables and flowers. Because the cost is high, it is not popular in China. Since 1996, China has imported 30 ha of greenhouses from the Netherlands, which mostly utilize rockwool for vegetable production. 5. Shandong-Soilless Culture (Lu-SC). This system was developed by Shandong Agricultural University (Fig. 4.12). The trough is V-shaped, made of iron, cement, or earth with a 0.5% slope covered by PE film with
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Figure 4.10 A deep-flow hydroponics system for lettuce cultivation, A: top view, B: side view (1=valve, 2=pump, 3=flow pipe, 4=filter, 5=solution level adjustment, 6=catchment pipe, 7=catchment tank, 8=plastic film, 9=transplanting pot, 10=nutrient solution, 11=transplanting plate, 12=culture bed).
Figure 4.11 Bag-culture system for fruit and/or vegetable cultivation (1=nutrientsolution tank, 2=filter, 3=inlet tube, 4=dripper, 5-6-7=flow pipe).
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Figure 4.12 Lu-SC type soil-less culture system (1=trough, 2=flow pipe, 3=catchment pipe, 4=timer, 5=pump, 6=tank, 7=trough structure).
each side 20-cm in width. Water enters one end of the trough and is drained at the opposite end with a siphon pipe. An iron screen covered by palm fiber is set 5 cm above the bottom of the trough and filled with 10 cm vermiculite substrate. Irrigation is carried out 3–4 times each day. The system is mainly used in Shandong province. 6. Floating Capillary Hydroponics (FCH). FCH was first developed by the Zhejiang Academy of Agricultural Sciences and Nanjing Agricultural University. The growing beds are connected with preformed units and laid out in parallel on the leveled greenhouse floor (Fig. 4.13). The growing bed, planting plate, and floating board are made of polystyrene board. The size of each unit is 40 cm wide, 10 cm high, and 100 cm long. The planting board containing holes for plants is 39 cm wide, 100 cm long, and 2.5 cm thick and covers the growing bed. A lining of polythene film (about 80 cm wide) makes the bed leak-proof. The floating board is 12 cm wide, 100 cm long, and 1.25 cm thick. The floating board is covered with a piece of capillary mat (non-woven fiber, 25 cm in width) and floats on the nutrient solution in the culture bed. Through capillary action, the floating plate and non-woven fiber can be kept wet, and the root system grows up and down around the floating plate and takes up both oxygen and nutrients to meet crop demand. The depth of solution in culture beds is 3–6 cm and can be adjusted at the outlet (Zhang and Xu 1993; Xu and Zhang 1994).
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Figure 4.13
W. JIANG, D. QU, D. MU, AND L. WANG
Floating capillary hydroponics system.
7. Eco-organic, Soil-less Culture Development. The traditional soil-less culture systems using nutrient solution to irrigate the plant have high initial capital and production costs and are difficult to operate for Chinese growers. To solve this problem, an eco-organic-type soil-less culture system using solid organic fertilizer instead of nutrient solution was developed in the early 1990s by the Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences and has been adopted rapidly in recent years, reaching over 232 ha at the end of 2000. It accounts for over 60% of total area of soil-less culture in China. This sustainable system combines organic agriculture with soil-less culture (Jiang et al. 1996, 1998b, 2000). Structure. Eco-organic soil-less culture is a trough system using locally available substrates (coal cinder, peat moss, vermiculite, coir, sawdust, perlite, sand, rice husks, sunflower stems, maize stems, and mushroom waste) to reduce the initial investment. These materials have buffering
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Figure 4.14
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Eco-organic type soil-less culture system.
ability and can be used successfully with good results. A mixture of two or three kinds of substrates improves the physical and chemical properties. The system consists of a trough, PE film, irrigation pipe and tape, and substrate (Fig. 4.14). The trough is made of three layers of brick (5 × 12 × 24 cm), 15 cm high and 48 cm wide with varying length of trough depending on the greenhouse. In the traditional Chinese solar, lean-to greenhouse, the trough length is 5–7 m, but in modern, multi-span greenhouses the trough length is around 30 m. The bottom of the trough is covered with 0.1 mm PE film to prevent soil-borne pests and diseases. Only solid manure rather than nutrient solution is used. The bed is irrigated only with fresh water. Development of the eco-organic system decreased initial investment up to 60–80%, and fertilizer cost 60% as compared with nutrient-solution hydroponics. Operations are simplified, vegetable quality is improved, and yields exceed those from soil culture (Table 4.4). Furthermore, crop nitrate levels in eco-organic systems were reduced from 30 to 67%, depending on the crop, as compared to soil-less culture systems with nutrient solutions (Table 4.5). Vitamin C and titrable acidity were also increased (Jiang et al. 2000). Fertilization. Fertilization in eco-organic soil-less culture is quite different from nutrient-film technique, deep-flow hydroponics, or rockwool
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W. JIANG, D. QU, D. MU, AND L. WANG Table 4.4. The average yield of tomato and cucumber production. Average Annual Yield (kg/m2)
Year
Soil culture
Eco-organic soil-less culture
8 10 19
9 19 30
1989–1990 1994–1995 1999–2000
Table 4.5.
NO–3 content of vegetables in different soil-less culture systems. NO–3 Content of Vegetables (ppm)
Vegetables
Eco-organic system
Liquid hydroponics
NO–3 reduction using eco-organic (%)
Melon Bean Cucumber Pok choi Lettuce
29.8 41.8 17.8 2437.0 1339.0
89.7 90.8 35.4 3855.0 2028.0
–66.7 –54.0 –49.7 –36.8 –34.0
systems (Fig. 4.15). The eco-organic soil-less culture system with combined macro- and micro-elements uses solid organic fertilizers, mostly chicken manure, instead of nutrient solution. Growers need only to consider whether the NPK are sufficient and need not be concerned with micro-element deficiency. In any organic fertilizer, micro-elements are sufficient for plant nutrition and are not harmful to plants because of the buffering effect of the substrate. The amount of base organic fertilizer applied to tomato or cucumber, one-year one-crop (long-term crop), or one-year two-crops, is 15 kg/m3 substrate before transplanting (Fig. 4.16). It is unnecessary to add additional organic fertilizer for the first month. Afterward, a top-dressing of 3 kg/m3 of organic fertilizer is applied every two weeks. For melons or lettuce and other leaf vegetables, 25 kg/m3 of organic fertilizer are added as base fertilizer and further fertilization is unnecessary thereafter. Irrigation. Fresh water is used for irrigating horticultural crops instead of nutrient solution. The frequency and amount of irrigation depends on the phase of plant growth and development, and on season and climate. In general, irrigation is carried out in the morning of clear days and is
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Figure 4.15 Eco-organic soil-less culture for sweet pepper production in multi-span greenhouse.
unnecessary on cloudy or rainy days. In the summer, plants are irrigated two times per day, once in the morning and once in the afternoon. When plants are mature and heavily fruited, the amount of daily irrigation is 1.2 L/plant for tomato, 2 L/plant for cucumber, and 0.9 L/plant for melon. Crop Quality. The producers of organic food are not permitted to use any chemical fertilizers and pesticides, only organic fertilizers and biological control for pests and diseases. About 80% of nitrate in the human body comes from eating vegetables. Excess nitrates can induce stomach cancer. Applying different types of fertilizers lead to different nitrate levels. For example, even if the same amount of NPK were applied in the
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Figure 4.16 Eco-organic soil-less culture for muskmelon production in energy-saving greenhouse.
soil-less culture systems, the contents of nitrate in pok choi and lettuce fed by nutrient solutions were much higher than those using organic manure (Table 4.5). At the same time organic manure can reduce titratable acidity and increase vitamin C content (Jiang et al. 2000). Organic Fertilizer Production. The fundamental raw materials for production of organic fertilizers are oil cakes and animal manure. Soybean, peanut, rapeseed cakes are rich in macro- and micro-elements (Table 4.6). In the suburbs of larger cities in China, there is extensive animal agriculture providing manure for eco-organic soil-less systems. However, as in oil cakes and manure, K content is less than N content, and K supTable 4.6.
Nutrient element content of oil cakes. Macro-element (%)
Crops Soybean Peanut Rapeseed
Trace Elements (mg/kg)
N
P
K
Fe
Zn
B
6.68 6.92 5.25
0.44 0.54 0.79
1.19 0.96 1.04
400 392 621
84.9 64.3 86.7
28.0 25.4 14.6
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plementation is required (Table 4.7). The contents of trace elements are sufficient to meet crop needs. Organic fertilizer production requires composting, drying to 15% moisture, testing, and packaging (Jiang et al. 1996). Composting. Composting is the fermentation of organic wastes under controlled conditions in the presence of oxygen to degrade carbohydrates and to eliminate diseases and weed seeds. Temperature first rises rapidly to 40–45°C due to the respiration of aerobic mesophilic microorganisms fermenting sugars and starch. Temperatures then rise to 60–70°C, leading to the replacement of mesophilic microorganisms by thermophilic and thermo-tolerant ones. Microorganism respiration exhausts the oxygen of the composting mass and makes the environment anaerobic. The development of anaerobic organisms responsible for the emission of volatile compounds leads to a fall in temperature as their metabolism is less thermogenic. High temperatures destroy pathogens, parasites, and weed seeds, and foul-smelling odors are prevented. Fermentation is complete when the temperature stops rising after aeration. The progression from the initial materials to humus depends on numerous external factors such as the dimension of the particles, the kinds and structures of the nutrient present, humidity level, aeration, and pH. Aeration is an essential factor in the composting process. Air should occupy at least 50% of the heap volume. An aerobiosis begins when the oxygen level inside the heap is lower than 10% (air = 21% O2). High levels of water further decrease the quantity of air available in the compost. The heat released by fermentation causes the evaporation of a great quantity of water. Thus, the fermenting mass should be watered to maintain humidity at 50–70% of the fresh mass. The compost pile should be protected from heavy rains and from excessive evaporation by the sun. The materials to compost generally present a pH ranging between 5 and 7. The pH decreases during the first day, then rises and becomes neutral or slightly alkaline. Table 4.7.
Nutrient element content in animal manure. Macro-elements (%)
Trace Element (mg/kg)
Manure
N
P
K
Fe
Zn
B
Cow Horse Poultry Sheep
1.66 1.47 2.33 2.01
0.42 0.46 0.92 0.49
0.90 1.30 1.60 1.32
405 498 812 541
100 163 159 105
13 10 13 22
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The carbon form greatly influences the speed of decomposition of the compost. Simple glucose, starch, hemicelluloses, pectin, and amino acids are easily degraded, but cellulose, a more voluminous polymer, is more resistant. Lignin and other aromatic polymers, extremely strong, will be degraded later, slower, and incompletely (leading to the formation of humus). Too low a C/N ratio (i.e., lower than 15) leads to leakage of nitrogen; too high a C/N ratio slows decomposition. The quantity of nitrogen to be added is difficult to assess, as the degree of carbon fermentation must be taken into account. The speed and efficiency of composting is linked to the presence of an adequate microbial population. Adding effective microorganisms into the compost accelerates fermentation. EM are now widely used for organic fertilizer production in China. A good compost is a product in which organic constituents have stabilized through biological conversion. At the end of fermentation, this compost can be used as organic fertilizer or as a growth medium. A simple way to follow the development of the composting process is to use thermometric probes that go deep into the fermenting materials that are used to evaluate the stage of fermentation. Instruments cannot measure maturity level of the compost, so growers must use their own experience to determine that. C. Nutrient Solution and Substrate 1. Nutrient Solution. The hydroponic systems irrigate with nutrient solutions. The nutrient formulas in Table 4.8 are popularly used for tomato and lettuce production. The nutrient solutions for other
Table 4.8.
Nutrient formulae for tomato and lettuce. Concentration (g/1000 L)
Chemical formulae
Tomato
Lettuce
Ca(NO3)2 KNO3 KH2PO4 MgSO4⋅7H2O Fe EDTA MnSO4⋅4H2O H3BO3 CuSO4⋅5H2O ZnSO4⋅7H2O (NH4)6Mo7O24⋅4H2O
680 525 200 250 15 1.8 2.4 0.1 0.28 0.13
1200 799 20.7 1366 30 5 4.1 0.9 1.1 0.9
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crops differ mainly in nitrogen and potassium; microelements are quite similar. In China, fertilizers for making nutrient solution are quite expensive. Furthermore, Chinese growers, who were not well educated, found it difficult to operate and adjust the nutrient solution. Thus the use of hydroponic systems increased very slowly in China. 2. Substrates. Soil-less substrates had a number of advantages over soil: (1) a better control of water content and fertility; (2) reduced losses by leakage of nutritive elements; (3) control of air porosity; (4) more intensive utilization of cultivation area; (5) easier supervision of pests and disinfection; (6) absence of weeds; (7) high success rate in transplantation; (8) easier transport of young plants; and (9) higher buffering than liquid hydroponics. The physical behavior of the substrate is of fundamental importance and is difficult to correct during cultivation. Ideal substrate properties include: (1) high porosity; (2) sufficient particles size to ensure good drainage; (3) high stability; and (4) substrates that do not shrink when drying and are easy to rewet (Zheng and Wang 1990; Jiang et al. 1996). Using local resources for soil-less substrates can decrease costs. Peat, a highly fibrous material, is a good substrate for horticultural crops with high total porosity and high water holding capacity, but it is an unregenerated natural resource and often difficult to wet. Because the price of peat has increased each year, farmers have gradually decreased the use of peat and changed to other substrates. In North China, popular substrates include coal cinder, sawdust, ground maize and sunflower stalks, and perlite. Two or three substrates are often mixed to improve physical and chemical properties. Sawdust is widely used for soil-less culture in China and is always mixed with sand, coal cinder, and other materials to maintain good physical properties. Sawdust from western red cedar (Thuja plicata) is toxic to plant roots, particularly when fresh, and cannot be used in soilless systems. In Hainan island, South China, there is an abundance of coir, which if used properly can last up to ten years, even though organic. Coir is now considered one of the best substrates worldwide and is regenerable. The advantages of coir include good porosity, high available water, good drainage, good absorbtion ability when reused, low volume weight for easy transport, slow degradation, and good chemical properties (Table 4.9). Plant stalks, such as maize and sunflower stems, if well composted can replace peat as a substrate (Table 4.10) (Jiang et al. 1998a, 2000, 2001a). Mushroom waste is a good substrate for soil-less culture of vegetables and flowers and can be mixed with sand, vermiculite, and other
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W. JIANG, D. QU, D. MU, AND L. WANG Table 4.9.
Element N-NO3 N-NH4 Cu Na Fe P K Mg Mn
Chemical properties of coir. Content (mg/kg dw)