Cell Biology of Metals and Nutrients (Plant Cell Monographs, Volume 17)

Plant Cell Monographs Volume 17

Series Editor: David G. Robinson Heidelberg, Germany

For further volumes: http://www.springer.com/series/7089

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Ru¨diger Hell

l

Ralf-Rainer Mendel

Editors

Cell Biology of Metals and Nutrients

Editors Prof. Dr. Ru¨diger Hell Universita¨t Heidelberg Heidelberger Institut fu¨r Pflanzenwissenschaften Im Neuenheimer Feld 360 69120 Heidelberg Germany [email protected]

Prof. Dr. Ralf-Rainer Mendel Technische Universita¨t Braunschweig Institut fu¨r Pflanzenbiologie Humboldtstr. 1 38106 Braunschweig Germany [email protected]

Series Editor David G. Robinson Ruprecht-Karls-University of Heidelberg Heidelberger Institute for Plant Sciences (HIP) Department Cell Biology Im Neuenheimer Feld 230 69120 Heidelberg Germany

ISSN 1861-1370 e-ISSN 1861-1362 ISBN 978-3-642-10612-5 e-ISBN 978-3-642-10613-2 DOI 10.1007/978-3-642-10613-2 Springer Heidelberg Dordrecht London New York Library of Congress Control Number: 2009940401 # Springer-Verlag Berlin Heidelberg 2010 This work is subject to copyright. All rights are reserved, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilm or in any other way, and storage in data banks. Duplication of this publication or parts thereof is permitted only under the provisions of the German Copyright Law of September 9, 1965, in its current version, and permission for use must always be obtained from Springer. Violations are liable to prosecution under the German Copyright Law. The use of general descriptive names, registered names, trademarks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. Cover photo: The upper part of the cover was created by Steffen Rump. It shows a mitochondrion which is essential for the biosynthesis of two metal-containing prosthetic groups: the molybdenum cofactor (left) and iron sulfur clusters (middle). Cover design: WMXDesign GmbH, Heidelberg, Germany Printed on acid-free paper Springer is part of Springer Science+Business Media (www.springer.com)

About the Editors

Ru¨diger Hell studied Biology at the Technical University of Darmstadt, Germany, and completed his PhD at the University of Cologne, Germany, in 1989. From 1990 to 1992, he worked at the University of California in Berkeley as a postdoctoral researcher. After returning to Germany, he completed his postdoctoral thesis at the University of Bochum, in 1998, and held a position at the Leibniz Institute for Plant Genetics and Crop Plant Research in Gatersleben. During that time, he developed his ongoing interest in molecular mechanisms of plant nutrition, especially in sulfur metabolism and cellular redox control. In 2003, he was appointed chair at the Heidelberg Institute for Plant Sciences. He served as Dean of the Faculty of Biosciences at Heidelberg University from 2005 to 2007, and is currently the managing director of the university’s Plant Sciences Institute. Ralf-Rainer Mendel studied biochemistry at the Humboldt University in Berlin, completed his PhD at the Martin-LutherUniversity Halle in 1979 and his postdoctoral thesis, in 1985. During that time he held a position at the Institute for Plant Genetics and Crop Plant Research in Gatersleben. In 1992, he was appointed as Full Professor of Botany at the (now) Institute of Plant Biology of the Braunschweig University of Technology, Germany. He has been the director of the Institute since 1993 and also served as Dean of Biosciences at Braunschweig from 1997 to 1999. His research focuses on the cell biology and biochemistry of molybdenum in plants and humans.

v

Preface

Plants are composed of 17 essential elements and these must be taken up as nutrients to allow for growth and cell division. Macronutrients are defined by their large amounts in plants (>0.1% of dry mass), while micronutrients are much less abundant (10,000 mg/g d.w., i.e. more than 100-fold that of “normal” plants

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(Baker 1989). Obviously, such hyperaccumulators are Zn hypertolerant as well. Zn hyperaccumulation – which is a constitutive trait displayed even on sites with average Zn levels in the soil – has over the past years been intensively studied in two model systems closely related to A. thaliana, A. halleri and Thlaspi caerulescens, and has been fueled by the concept of biofortification (see above). Comparative transcriptome studies revealed constitutive high expression of metal homeostasis genes in A. halleri and T. caerulescens relative to nonhyperaccumulators such as A. thaliana (Weber et al. 2004; Becher et al. 2004; van de Mortel et al. 2006). This finding suggested that an altered regulation of metal homeostasis is underlying the evolution of hyperaccumulation. The genes more strongly expressed encode, for instance, metal transporters (HMAs, MTPs, ZIPs, Nramps) and enzymes involved in chelator synthesis (NAS). Indeed, for one of the candidate genes (HMA4) a major role of its elevated expression level in Zn hyperaccumulation was proven recently (Hanikenne et al. 2008). Efficient translocation of Zn to the shoot is dependent on strong Zn efflux activity around the xylem. Other postulated differences between hyperaccumulators and nonhyeraccumulators are: possibly more efficient uptake into the root, reduced sequestration in root cells, stronger buffering capacity to detoxify excess Zn, higher storage capacities in leaf cell vacuoles (Kra¨mer et al. 2007; Verbruggen et al. 2009). Binding partner in vacuoles could be malate (Sarret et al. 2002). Transgenic approaches involving RNAi-mediated intervention in Zn hyperaccumulators will be required to dissect the actual relevance of these processes.

9 Regulation of Zn Homeostasis Plants are exposed to extreme fluctuations in Zn availability. In agriculture, Zn deficiency is far more relevant than Zn toxicity. Large areas of agricultural soils are micronutrient-deficient because of low concentrations or low availability of micronutrients. Zn deficiency is at least among cereals the most serious mineral deficiency. It is common, for example, in soils in the Middle East, India and in parts of Australia, America and Central Asia. Many of the regions with Zn-deficient soils are also the regions where Zn deficiency in the human population is widespread (Cakmak 2008). Coordination of transport activities and chelator synthesis for the various metals is essential. Changes in micronutrient availability have to be integrated with growth and developmental processes. Transcriptional responses to both micronutrient deficiency and excess are well-documented. Under Zn-deplete conditions ZIP genes are induced (see above). Since these early reports, microarray studies have identified numerous additional genes that specifically respond to micronutrient deficiencies at the transcript level (Wintz et al. 2003; Talke et al. 2006; van de Mortel et al. 2006). Many of them encode metal homeostasis factors previously mentioned including ZIP metal transporters, MTP gene family, P1B-type ATPase

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transporters (HMA gene family), nicotianamine synthases (NAS), and Yellow Stripe1-like proteins (YSLs). Metal sensing and signal transduction pathways mediating such transcriptional responses have to be postulated. For Zn, these pathways are completely unknown in plants. There is, for instance, no indication that a Zn-sensing transcription factor similar to S. cerevisiae ZAP1 exists. Similarly, no cis elements have been identified yet in genes up- or down-regulated upon changes in Zn supply. Another possible level of regulation is posttranslational modification of metal homeostasis protein stability and/or subcellular localization. Again, evidence in plants is missing when considering Zn. ZIP transporters in S. cerevisiae and mammalian cells have been demonstrated to undergo Zn-stimulated endocytosis upon resupply of Zn to Zn-deficient cells (Eide 2006). Analogous processes appear very likely for plant cells given the documented posttranslational modification of IRT1 (Connolly et al. 2002).

10

Perspectives

Interest in fundamental biological questions of metal homeostasis has been rapidly increasing over the past 10–15 years. During this period many potential factors of plant Zn metabolism have been identified. The majority of these are transporter proteins. Large families are implicated in metal homeostasis. Physiological functions of individual components, however, are understood at the molecular detail only in a few cases. For example, we do not know precisely which protein(s) mediate(s) the uptake of Zn(II) from the rhizosphere into the root symplast. Our insight into cell specificity of Zn accumulation or other aspects of Zn homeostasis such as re-mobilization is extremely limited. Also, an unknown but certainly significant number of molecular players are yet to be discovered. We can only make predictions about Zn-dependent proteins and their metal requirements. Structural information is missing as well as knowledge about the process of Zn insertion into proteins. Regulation of Zn homeostasis is practically not understood at all. These huge gaps are at least partly due to the fact that Zn homeostasis is genetically underexplored. Very few mutants showing defects in Zn tolerance or distribution have been isolated. Natural diversity is – with the exception of seed mineral content (Vreugdenhil et al. 2004) – scarcely documented. Poor genetic dissection can probably be explained by a lack of good, i.e. sensitive and easily scorable, markers for metal status. A major question is speciation of metal ions in the cytoplasm and in other compartments of plant cells as well as in the extracellular space. Moreover, we have only a very limited understanding of whether and how metal specificity is achieved by plants. A number of metal transporters appear to transport multiple metals. Metal chelators such as nicotianamine are not specific, but form complexes of different stability with a range of metal ions. Many examples of apparent competition between metal ions are known. We need to know binding affinities

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of all players in Zn homeostasis and to perform in vivo imaging of Zn-chelate complexes. Only then will we be able to undertake any quantitative description and possibly manipulation of Zn fluxes.

References Adam Z, Rudella A, Van Wijk KJ (2006) Recent advances in the study of Clp, FtsH and other proteases located in chloroplasts. Curr Opin Plant Biol 9:234–240 Andreini C, Banci L, Bertini I, Rosato A (2006) Zinc through the three domains of life. J Proteome Res 5:3173–3178 Andreini C, Bertini I, Cavallaro G, Holliday GL, Thornton JM (2008) Metal ions in biological catalysis: from enzyme databases to general principles. J Biol Inorg Chem 13:1205–1218 Arrivault S, Senger T, Kra¨mer U (2006) The Arabidopsis metal tolerance protein AtMTP3 maintains metal homeostasis by mediating Zn exclusion from the shoot under Fe deficiency and Zn oversupply. Plant J 46:861–879 Baker AJM (1989) Terrestrial higher plants which hyperaccumulate metallic elements – a review of their distribution, ecology and phytochemistry. Biorecovery 1:81–126 Becher M, Talke IN, Krall L, Kra¨mer U (2004) Cross-species microarray transcript profiling reveals high constitutive expression of metal homeostasis genes in shoots of the zinc hyperaccumulator Arabidopsis halleri. Plant J 37:251–268 Benes I, Schreiber K, Ripperger H, Kircheiss A (1983) Metal complex formation by nicotianamine, a possible phytosiderophore. Experientia 39:261–262 Berg J, Shi Y (1996) The galvanization of biology: a growing appreciation for the roles of zinc. Science 271:1081–1085 Bertinato J, L’Abbe MR (2004) Maintaining copper homeostasis: regulation of copper-trafficking proteins in response to copper deficiency or overload. J Nutr Biochem 15:316–322 Black RE (2003) Zinc deficiency, infectious disease and mortality in the developing world. J Nutr 133:1485S–1489S Briat J-F, Curie C, Gaymard F (2007) Iron utilization and metabolism in plants: physiology and metabolism. Curr Opin Plant Biol 10:276–282 Broadley MR, White PJ, Hammond JP, Zelko I, Lux A (2007) Zinc in plants. New Phytol 173:677–702 Brune A, Urbach W, Dietz KJ (1995) Differential toxicity of heavy-metals is partly related to a loss of preferential extraplasmic compartmentation – a comparison of Cd-stress, Mo-stress, Ni-stress and Zn-stress. New Phytol 129:403–409 Cakmak I (2000) Possible roles of zinc in protecting plant cells from damage by reactive oxygen species. New Phytol 146:185–205 Cakmak I (2008) Enrichment of cereal grains with zinc: agronomic or genetic biofortification? Plant Soil 302:1–17 Callahan DL, Baker AJ, Kolev SD, Wedd AG (2006) Metal ion ligands in hyperaccumulating plants. J Biol Inorg Chem 11:2–12 Campanella JJ, Larko D, Smalley J (2003) A molecular phylogenomic analysis of the ILR1-like family of IAA amidohydrolase genes. Comp Funct Genomics 4:584–600 Clemens S (2006) Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie 88:1707–1719 Clemens S, Bloss T, Vess C, Neumann D, Nies D, Zur Nieden U (2002a) A transporter in the endoplasmic reticulum of Schizosaccharomyces pombe cells mediates zinc storage and differentially affects transition metal tolerance. J Biol Chem 277:18215–18221 Clemens S, Kim EJ, Neumann D, Schroeder JI (1999) Tolerance to toxic metals by a gene family of phytochelatin synthases from plants and yeast. EMBO J 18:3325–3333

Zn – A Versatile Player in Plant Cell Biology

295

Clemens S, Palmgren MG, Kra¨mer U (2002b) A long way ahead: understanding and engineering plant metal accumulation. Trends Plant Sci 7:309–315 Cobbett C, Goldsbrough P (2002) Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Annu Rev Plant Physiol Plant Mol Biol 53:159–182 Colangelo EP, Guerinot ML (2006) Put the metal to the petal: metal uptake and transport throughout plants. Curr Opin Plant Biol 9:322–330 Connolly EL, Fett JP, Guerinot ML (2002) Expression of the IRT1 metal transporter is controlled by metals at the levels of transcript and protein accumulation. Plant Cell 14:1347–1357 Curie C, Panaviene Z, Loulergue C, Dellaporta S, Briat J, Walker E (2001) Maize yellow stripe1 encodes a membrane protein directly involved in Fe(III) uptake. Nature 409:346–349 Delhaize E, Gruber BD, Pittman JK, White RG, Leung H, Miao YS, Jiang LW, Ryan PR, Richardson AE (2007) A role for the AtMTP11 gene of Arabidopsis in manganese transport and tolerance. Plant Journal 51:198–210 Desbrosses-Fonrouge AG, Voigt K, Schro¨der A, Arrivault S, Thomine S, Kra¨mer U (2005) Arabidopsis thaliana MTP1 is a Zn transporter in the vacuolar membrane which mediates Zn detoxification and drives leaf Zn accumulation. FEBS Lett 579:4165–4174 Eide DJ (2006) Zinc transporters and the cellular trafficking of zinc. Biochim Biophys Acta 1763:711–722 Ellis CD, Wang F, MacDiarmid CW, Clark S, Lyons T, Eide DJ (2004) Zinc and the Msc2 zinc transporter protein are required for endoplasmic reticulum function. J Cell Biol 166:325–335 Frausto da Silva JJR, Williams RJP (2001) The biological chemistry of the elements. The inorganic chemistry of life, 2nd edn. Oxford University Press, New York Gamsjaeger R, Liew CK, Loughlin FE, Crossley M, Mackay JP (2007) Sticky fingers: zinc-fingers as protein-recognition motifs. Trends Biochem Sci 32:63–70 Grotz N, Fox T, Connolly E, Park W, Guerinot ML, Eide D (1998) Identification of a family of zinc transporter genes from Arabidopsis that respond to zinc deficiency. Proc Natl Acad Sci USA 95:7220–7224 Grotz N, Guerinot ML (2006) Molecular aspects of Cu, Fe and Zn homeostasis in plants. Biochim Biophys Acta 1763:595–608 Ha SB, Smith AP, Howden R, Dietrich WM, Bugg S, O’Connell MJ, Goldsbrough PB, Cobbett CS (1999) Phytochelatin synthase genes from Arabidopsis and the yeast Schizosaccharomyces pombe. Plant Cell 11:1153–1163 Hacisalihoglu G, Hart JJ, Wang YH, Cakmak I, Kochian LV (2003) Zinc efficiency is correlated with enhanced expression and activity of zinc-requiring enzymes in wheat. Plant Physiol 131:595–602 Hacisalihoglu G, Kochian LV (2003) How do some plants tolerate low levels of soil zinc? Mechanisms of zinc efficiency in crop plants. New Phytol 159:341–350 Hanikenne M, Kra¨mer U, Demoulin V, Baurain D (2005) A comparative inventory of metal transporters in the green alga Chlamydomonas reinhardtii and the red alga Cyanidioschizon merolae. Plant Physiol 137:428–446 Hanikenne M, Talke IN, Haydon MJ, Lanz C, Nolte A, Motte P, Kroymann J, Weigel D, Kra¨mer U (2008) Evolution of metal hyperaccumulation required cis-regulatory changes and triplication of HMA4. Nature 453:391–395 Haydon MJ, Cobbett CS (2007) A novel major facilitator superfamily protein at the tonoplast influences zinc tolerance and accumulation in Arabidopsis. Plant Physiol 143:1705–1719 Hell R, Stephan UW (2003) Iron uptake, trafficking and homeostasis in plants. Planta 216:541–551 Himelblau E, Amasino RM (2001) Nutrients mobilized from leaves of Arabidopsis thaliana during leaf senescence. J Plant Physiol 158:1317–1323 Hotton SK, Callis J (2008) Regulation of cullin ring ligases. Annu Rev Plant Biol 59:467–489 Huffman D, O’Halloran T (2001) Function, structure, and mechanism of intracellular copper trafficking proteins. Annu Rev Biochem 70:677–701

296

S. Clemens

Hussain D, Haydon MJ, Wang Y, Wong E, Sherson SM, Young J, Camakaris J, Harper JF, Cobbett CS (2004) P-type ATPase heavy metal transporters with roles in essential zinc homeostasis in Arabidopsis. Plant Cell 16:1327–1339 Kirschke CP, Huang LP (2003) Znt7, a novel mammalian zinc transporter, accumulates zinc in the Golgi apparatus. J Biol Chem 278:4096–4102 Kobae Y, Uemura T, Sato MH, Ohnishi M, Mimura T, Nakagawa T, Maeshima M (2004) Zinc transporter of Arabidopsis thaliana AtMTP1 is localized to vacuolar membranes and implicated in zinc homeostasis. Plant Cell Physiol 45:1749–1758 Kra¨mer U, Clemens S (2005) Functions and homeostasis of zinc, copper and nickel in plants. Topics Curr Genet 14:215–271 Kra¨mer U, Talke IN, Hanikenne M (2007) Transition metal transport. FEBS Lett 581:2263–2272 Lanquar V, Lelievre F, Bolte S, Hames C, Alcon C, Neumann D, Vansuyt G, Curie C, Schro¨der A, Kra¨mer U, Barbier-Brygoo H, Thomine S (2005) Mobilization of vacuolar iron by AtNRAMP3 and AtNRAMP4 is essential for seed germination on low iron. EMBO J 24:4041–4051 Le Jean M, Schikora A, Mari S, Briat JF, Curie C (2005) A loss-of-function mutation in AtYSL1 reveals its role in iron and nicotianamine seed loading. Plant J 44:769–782 Li L, Kaplan J (2001) The yeast gene MSC2, a member of the cation diffusion facilitator family, affects the cellular distribution of zinc. J Biol Chem 276:5036–5043 Lin Y-F, Liang H-M, Yang S-Y, Boch A, Clemens S, Chen C-C, Wu J-F, J-Li H, Yeh K-C (2009) Arabidopsis IRT3 is a zinc-regulated and plasma membrane localized zinc/iron transporter. New Phytol 182:392–404 Ling HQ, Koch G, Ba¨umlein H, Ganal MW (1999) Map-based cloning of chloronerva, a gene involved in iron uptake of higher plants encoding nicotianamine synthase. Proc Natl Acad Sci USA 96:7098–7103 Maret W, Sandstead HH (2006) Zinc requirements and the risks and benefits of zinc supplementation. J Trace Elem Med Biol 20:3–18 Marschner H (1995) Mineral nutrition of higher plants (2nd edn). Academic press Amsterdam Matthews JM, Sunde M (2002) Zinc fingers – folds for many occasions. IUBMB Life 54:351–355 Mills RF, Francini A, Ferreira da Rocha PS, Baccarini PJ, Aylett M, Krijger GC, Williams LE (2005) The plant P1B-type ATPase AtHMA4 transports Zn and Cd and plays a role in detoxification of transition metals supplied at elevated levels. FEBS Lett 579:783–791 Natori Y, Nanamiya H, Akanuma G, Kosono S, Kudo T, Ochi K, Kawamura F (2007) A fail-safe system for the ribosome under zinc-limiting conditions in Bacillus subtilis. Mol Microbiol 63:294–307 O’Halloran T, Culotta V (2000) Metallochaperones, an intracellular shuttle service for metal ions. J Biol Chem 275:25057–25060 Outten CE, O’Halloran TV (2001) Femtomolar sensitivity of metalloregulatory proteins controlling zinc homeostasis. Science 292:2488–2492 Palmgren MG, Clemens S, Williams LE, Kra¨mer U, Borg S, Schjorring JK, Sanders D (2008) Zinc biofortification of cereals: problems and solutions. Trends Plant Sci 13:464–473 Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 6:763–775 Peiter E, Montanini B, Gobert A, Pedas P, Husted S, Maathuis FJM, Blaudez D, Chalot M, Sanders D (2007) A secretory pathway-localized cation diffusion facilitator confers plant manganese tolerance. Proc Natl Acad Sci USA 104:8532–8537 Puig S, Andres-Colas N, Garcia-Molina A, Penarrubia L (2007) Copper and iron homeostasis in Arabidopsis: responses to metal deficiencies, interactions and biotechnological applications. Plant Cell Environ 30:271–290 Rauser WE (1999) Structure and function of metal chelators produced by plants. Cell Biochem Biophys 31:19–48

Zn – A Versatile Player in Plant Cell Biology

297

Sarret G, Harada E, Choi YE, Isaure MP, Geoffroy N, Fakra S, Marcus MA, Birschwilks M, Clemens S, Manceau A (2006) Trichomes of tobacco excrete zinc as zinc-substituted calcium carbonate and other zinc-containing compounds. Plant Physiol 141:1021–1034 Sarret G, Saumitou-Laprade P, Bert V, Proux O, Hazemann JL, Traverse AS, Marcus MA, Manceau A (2002) Forms of zinc accumulated in the hyperaccumulator Arabidopsis halleri. Plant Physiol 130:1815–1826 Schaaf G, Ludewig U, Erenoglu BE, Mori S, Kitahara T, von Wiren N (2004) ZmYS1 functions as a proton-coupled symporter for phytosiderophore- and nicotianamine-chelated metals. J Biol Chem 279:9091–9096 Schaaf G, Schikora A, Haberle J, Vert G, Ludewig U, Briat JF, Curie C, von Wiren N (2005) A putative function for the Arabidopsis Fe-phytosiderophore transporter homolog AtYSL2 in Fe and Zn homeostasis. Plant Cell Physiol 46:762–774 Simm C, Lahner B, Salt D, LeFurgey A, Ingram P, Yandell B, Eide DJ (2007) Saccharomyces cerevisiae vacuole in zinc storage and intracellular zinc distribution. Eukaryot Cell 6:1166–1177 Somerville C (2006) Cellulose synthesis in higher plants. Annu Rev Cell Dev Biol 22:53–78 Stephan UW, Schmidke I, Stephan VW, Scholz G (1996) The nicotianamine molecule is made-tomeasure for complexation of metal micronutrients in plants. Biometals 9:84–90 Takahashi M, Terada Y, Nakai I, Nakanishi H, Yoshimura E, Mori S, Nishizawa NK (2003) Role of nicotianamine in the intracellular delivery of metals and plant reproductive development. Plant Cell 15:1263–1280 Talke IN, Hanikenne M, Kra¨mer U (2006) Zinc-dependent global transcriptional control, transcriptional deregulation, and higher gene copy number for genes in metal homeostasis of the hyperaccumulator Arabidopsis halleri. Plant Physiol 142:148–167 Tennstedt P, Peisker D, Bo¨ttcher C, Trampczynska A, Clemens S (2009) Phytochelatin synthesis is essential for the detoxification of excess zinc and contributes significantly to the accumulation of zinc. Plant Physiol 149:938–948 Trampczynska A, Bo¨ttcher C, Clemens S (2006) The transition metal chelator nicotianamine is synthesized by filamentous fungi. FEBS Lett 580:3173–3178 Uauy C, Distelfeld A, Fahima T, Blechl A, Dubcovsky J (2006) A NAC gene regulating senescence improves grain protein, zinc, and iron content in wheat. Science 314:1298–1301 van de Mortel JE, Almar Villanueva L, Schat H, Kwekkeboom J, Coughlan S, Moerland PD, Loren V, van Themaat E, Koornneef M, Aarts MGM (2006) Large expression differences in genes for iron and zinc homeostasis, stress response, and lignin biosynthesis distinguish roots of Arabidopsis thaliana and the related metal hyperaccumulator Thlaspi caerulescens. Plant Physiol 142:1127–1147 Vatamaniuk O, Bucher E, Ward J, Rea P (2001) A new pathway for heavy metal detoxification in animals. Phytochelatin synthase is required for cadmium tolerance in Caenorhabditis elegans. J Biol Chem 276:20817–20820 Verbruggen N, Hermans C, Schat H (2009) Molecular mechanisms of metal hyperaccumulation in plants. New Phytol 181:759–776 Verret F, Gravot A, Auroy P, Leonhardt N, David P, Nussaume L, Vavasseur A, Richaud P (2004) Overexpression of AtHMA4 enhances root-to-shoot translocation of zinc and cadmium and plant metal tolerance. FEBS Lett 576:306–312 Vert G, Grotz N, Dedaldechamp F, Gaymard F, Guerinot M, Briat J, Curie C (2002) IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth. Plant Cell 14:1233–1243 von Wiren N, Klair S, Bansal S, Briat JF, Khodr H, Shioiri T, Leigh RA, Hider RC (1999) Nicotianamine chelates both FeIII and FeII. Implications for metal transport in plants. Plant Physiol 119:1107–1114 von Wiren N, Marschner H, Ro¨mheld V (1996) Roots of iron-efficient maize also absorb phytosiderophore-chelated zinc. Plant Physiol 111:1119–1125

298

S. Clemens

Vreugdenhil D, Aarts MGM, Koornneef M, Nelissen H, Ernst WHO (2004) Natural variation and QTL analysis for cationic mineral content in seeds of Arabidopsis thaliana. Plant Cell Environ 27:828–839 Waters BM, Chu HH, Didonato RJ, Roberts LA, Eisley RB, Lahner B, Salt DE, Walker EL (2006) Mutations in Arabidopsis yellow stripe-like1 and yellow stripe-like3 reveal their roles in metal ion homeostasis and loading of metal ions in seeds. Plant Physiol 141:1446–1458 Weber M, Harada E, Vess C, von Roepenack-Lahaye E, Clemens S (2004) Comparative microarray analysis of Arabidopsis thaliana and Arabidopsis halleri roots identifies nicotianamine synthase, a ZIP transporter and other genes as potential metal hyperaccumulation factors. Plant J 37:269–281 Welch RM, Graham RD (2004) Breeding for micronutrients in staple food crops from a human nutrition perspective. J Exp Bot 55:353–364 Wintz H, Fox T, Wu YY, Feng V, Chen W, Chang HS, Zhu T, Vulpe C (2003) Expression profiles of Arabidopsis thaliana in mineral deficiencies reveal novel transporters involved in metal homeostasis. J Biol Chem 278:47644–47653 Wong CKE, Cobbett CS (2009) HMA P-type ATPases are the major mechanism for root-to-shoot Cd translocation in Arabidopsis thaliana. New Phytol 181:71–78

Index

A

B

ABA. See Abscisic acid ABC transporter, 136 Abiotic stress, 257 Abscisic acid (ABA), 22–23, 30, 31, 37–38, 131, 135 Acid phosphatase, 178, 182, 186, 188 Adenosine 50 -phosphosulfate (APS), 251–252 AKT1, 39 Aldehyde oxidase (AO), 131–133 Algae, 245 Allosteric regulation, 158 Alternative oxidase (AOX), 57 Amine oxidases, 59 Amino acid, 152, 155 Ammonium, 150–151 assimilation, 153–154 fluxes, 150–151 Apoplast, 8, 284, 286, 289, 290 APS kinase, 253 APS sulfo-transferase, 252 Arabidopsis, 177, 178, 182–185, 187–191 Arabidopsis thaliana, 1, 12–17, 246 Archaea, 283 Ascorbate oxidases, 58 ATPases, 32–33, 39, 176 autoinhibited, 32–33 ER type, 32 Auxin, 186, 189–191

C

Bacteria, 283, 287 B deficiency, 2, 3, 6, 8, 10 B efflux, 9–10 BHLH32, 184, 185 Biofortification, 290, 292 BOR1, 1, 8–11 BOR4, 1, 10 Boric acid B(OH)3, 1–4, 6–8, 11 Boron, 1–11 BORs, 1, 10 BOT1, 10 B-polysaccharide complex, 4 Brassica napus, 249 B toxicity, 3, 10, 11

Cadmium, 289 cADPR. See Cyclic adenosine diphospho ribose Calcineurin-B like proteins (CBL), 25, 35, 37–39 Calcium dependent protein kinases, 32, 35–37, 39 Calcium exchanger, 31–32 Calcium ion coordination number, 20 ionic radius, 20 Calcium nutrition deficiency, 18–19 uptake, 18 Calcium signalling abiotic stimuli, 21 299

300

antiporter, 31–32 biotic factors, 21 channels, 19, 23, 25–30, 33, 37, 39 oscillation, 22–23, 26, 34, 37 pumps, 20, 31, 33 Calmodulin (CaM), 29, 32, 35–36 Calmodulin like (CML), 35–36 CaM. See Calmodulin Camalexin, 244 Catalysis, 284 CAX. See Calcium exchanger CAX transporter, 101–103 CBL. See Calcineurin-B like proteins (CBL) CBL interacting protein kinases (CIPK), 25, 38–39 CCX transporter, 102 CDF transporter, 103 CDPK. See Calcium dependent protein kinases Cell wall, 19, 34, 35 Channel, 1, 6–9, 11 Chelation strategy, 78–80, 82–83 Chlamydomonas reinhardtii, 248 Chloroplasts, 24–25, 27–28, 33, 76, 83, 86–88 Chloroplasts, 76, 83, 86–88 CIPK. See CBL interacting protein kinases (CIPK) Citrate FRD3, 77, 83, 84 CML. See Calmodulin like CNGC. See Cyclic nucleotide gated channels (CNGC) Copper (Cu), 55, 126–127 Copper response regulator (CRR1), 66 COPT-family transporter, 59 Crop productivity, 175, 191 Cu chaperone, 60 Cu deficiency, 66 Cu excess, 62 Cu-proteins, 56 Cu transporters, 56 Cu/Zn superoxide dismutase (Cu/ ZnSOD), 57, 68 Cyanide, 259 Cyclic adenosine diphospho ribose, 23, 30–31

Index

Cyclic nucleotide gated channels (CNGC), 23, 29–30 Cysteine, 246 Cysteine desulfurases, 259 Cysteine synthase complex (CSC), 256 Cysteine synthesis, 246 Cytochrome c6, 66 Cytochrome c oxidase (COX), 56 Cytokinin, 189, 190 Cytosol (or cytoplasm), 199, 203, 208

D Defensin, 244 Digalatosyldiacyglycerol (DGDG), 179 DNA, 283, 284

E ECA1, 106 ECA3, 104–106 Ecological aspects, 225, 234–237 Ecosystems, 174, 175, 191 EF hand, 31, 35–38 Endocytosis, 6, 9 Endoplasmic reticulum, 22, 24–28, 30–32, 36 Endosomes, 24–25, 32 Environmental, 173, 175–176, 183, 188–190 Enzyme-activation, 199, 217 ER. See Endoplasmic reticulum Ethylene, 189–191, 262 Ethylene receptors, 57 Evolution, 282, 283, 292

F Fe deficiency, 285, 291 Fenton reaction, 283 Ferredoxin, 253 Ferric reductases, 60, 65 Ferroxidases, 58 Fertilizers, 175, 191 FeSOD regulation, 67 FIT, 80–82 Flavin adenine dinucleotide (FAD), 130, 133

Index

FRO2, 77, 78, 80–82, 86 Fucose, 4–5

G GA. See Giberellic acid Galactolipid, 179

-glutamylcysteine ligase (GSH1), 244 Giberellic acid, 22, 31, 37 GLR. See Glutamate receptors (GLR) Glucosinolates, 244 Glutamate, 20, 23 receptors, 29–30 Glutamate dehydrogenase, 154 Glutamate receptors (GLR), 29, 30 Glutamine synthetase, 153, 154 Glutathione, 246, 284, 288, 291 Golgi, 24–25, 32 Green fluorescent protein, 264 Growth, 174, 175, 181, 182, 184, 186, 189–191 GSH, 244 GSH conjugates, 266 Guard cell, 22, 37 GUT1, 5

H Heavy Metal Associated (HMA) transporter family, 62 Heme, 132 Hormones, 22, 31, 36 Hyperaccumulation, 291, 292

I Indole-3-acetic acid (IAA), 131 Inositol-3-phosphate, 23, 26, 29–31 InsP3. See Inositol-3-phosphate IPS1, 187 Iron, 244 Iron (Fe), 135 Iron-sulfur clusters, 130, 135, 244 IRT1, 77, 78, 80–82, 86, 100 Irving-Williams series, 282

K

K+. See Potassium

301

L Laccases, 58 Lateral root (LR), 181, 182, 186, 189, 190 Ligand gated channels, 25, 29–31 Light, 21, 27–28, 30, 36 Low phosphate root (lpr), 184 Low phosphorus insensitive (lpi), 184 Lsi1, 9 Lsi2, 9

M Macronutrient, 174 Manganese (Mn), 95 Manganese chaperones, 109 Manganese deficiency, 96–101, 103, 105–107, 112 Manganese detoxification, 99–108, 111 Manganese imaging, 101 Manganese regulation, 110 Manganese sequestration, 102, 103 Manganese-superoxide dismutase (MnSOD), 96, 98, 108–110 Manganese toxicity, 99, 101, 105, 106, 111 Manganese uptake, 100, 107 Manganese xylem transport, 107 Mannitol, 24–25, 33–34 Marchantia polmorpha, 248 Metabolism, 174, 178–180, 189 Metallo-chaperones, 56 Metallothionein (MT), 62 Methionine, 249 microRNAs, 66 miR399, 184, 187 miRNAs, 254 Mitochondria, 17, 24–25, 27, 83, 87–88, 132–135, 257 Mitochondrial amidoxime reducing component (mARC), 132 Mn deficiency, 291 Molybdate, 248 Molybdenum (Mo), 120 enzymes, 129–136 insertion, 126–127 uptake, 121 Molybdenum cofactor (Moco), 121–127 binding protein, 128 biosynthesis, 124–127

302

cytoskeleton binding, 128 storage, 127–128 Molybdenum cofactor synthesis, 59 Molybdopterin (MPT), 123, 124 Molybdopterin synthase, 125 Monogalatosyldiacyglycerol (MGDG), 179 MTP11, 103 Multi-copper oxidases (MCO), 58 MUR1, 4–5

Index

Nod factor, 25–26, 34 NRAMP transporter, 103, 107 Nucleic acids, 179 Nucleus, 22, 25–26

O O-acetyleserine(thiol)lyase, 256 OPT transporter, 107 Organic acids, 178, 179, 182 Osmoticum (or Osmotica), 200, 201, 203, 217, 218

N NADH oxidase, 130 Na+. See Salt N2 fixation, 2 Nicotianamine (NA), 61, 65, 76, 77, 79, 84–85, 262, 288, 293 NIP5;1, 1, 7, 8, 11 NIP6;1, 1, 7 NIPs, 1, 7 Nitrate, 148–150, 258 channels, 150 efflux, 149 high-affinity, 149 low-affinity, 149 reduction, 153 uptake, 148 vacuole, 149 Nitrate metabolism, 245 Nitrate reductase (NR), 132–133, 153 Nitric oxide (NO), 26, 35, 133, 158 formation, 159–161 targets, 161–163 Nitrite, 148–150 chloroplast, 150 transport, 150 Nitrite reductase, 153, 253 Nitrogen, 145 assimilation, 153–154 deprivation, 155 distribution, 146–148 flux, 148–152 regulation, 154–158 remobilization, 154 Nitrogenase, 123 Nitrosylation, 161 NO. See Nitric oxide (NO)

P PAPS reductase, 252 Passive diffusion, 6 Pathogen, 21, 30, 35, 37 Pathogen defence, 244 Pectic polysaccharide, 1 Peroxisome, 130 Phloem, 247 PHO regulon, 188 Phosphatases, 178, 180, 182, 186, 188 Phosphate transporters (Pht), 180 uptake, 174–178, 181–183, 189, 191 Phosphate 1 (PHO1), 177 Phosphate 2 (PHO2), 177, 184, 186–188 Phosphate deficiency response 2, 184 30 -Phosphoadenosyl-50 -phosphosulfate (PAPS), 252 Phospholipid, 174, 177–179, 190 Phosphorous (P) acquisition, 178, 186, 189, 191 availability, 174–176, 178, 179, 189, 191 homeostasis, 174, 186–188 paradox, 174–176 in soil, 175, 176, 179, 182 translocation, 176–177, 180, 184, 187 Phosphorylation, 157 Photosynthesis, 156, 174, 180 Photosystem II (PSII), 96, 108, 110, 112 Phototrophic, 244 PHR1, 178, 183–191 Physcomitrella patens, 253

Index

Phytochelatins, 62, 288, 289 Phytochelatin synthase, 266 Phytocyanins, 57 Plasmalemma, 246 Plasma membrane, 19, 23–25, 28–29, 36, 38–39, 200, 201, 203–207, 209–211, 215, 216 Plastids, 257 Plastocyanin, 56 PLDZ, 179, 186 Pollen tube, 22, 33, 37 Polyphenol oxidase (PPO), 58 Potassium, 19, 24–25, 29, 31, 39 Potassium-deficiency symptoms, 201–203, 206, 217 Proteome, 281 PSR1, 185 P-type ATPase, 104–106

R Reactive oxygen species (ROS), 130, 133, 244 Redox, 243 Reduction strategy, 77–78, 80–82 Regulation, 154 post-transcriptional, 157 transcriptional, 155 Regulators, 156, 158 Rhamonogalacturonan-II (RG-II), 1, 3–6, 11 Rhizosphere, 178 Ribosomes, 284 roGFP, 264 Root, 247 architecture, 181, 182, 184, 189, 191 hair (HR), 181, 191 meristem, 176, 181, 184

S Saccharomyces cerevisiae, 120, 252 S-adensoylmethionine (SAM), 261 Salt, 19, 21, 25–26, 33–34, 37–39 Secondary sulfur compounds, 251 Second messengers, 23 Secretory pathway, 64 Seed loading, 106–108 Seed storage protein, 246

303

Selenium accumulation, 229–237 metabolism, 225–238 tolerance, 230–233, 236, 237 volatilization, 230–235, 237 Senescence, 285, 290 Serine acetyltransferase, 257 Signaling, 283 SIZ1, 185 Slow vacuolar channel, 30–31 S-methylmethionine (SMM), 249, 262 S-nitrosylation, 262 Sodium. See Salt Soil, 285, 286, 292 SPL7, 67 SPL family, 67 SPX domain, 187, 188 Stomata closure, 22–23, 28, 37 opening, 22 response, 21–22, 37, 39 Stomata (or guard cell), 201, 203, 210, 216, 217 Sucrose, 180, 188, 189 Sulfate, 245 Sulfate deprivation, 245 Sulfate permeases, 248 Sulfate transport, 246 Sulfate transporters, 246 Sulfide, 259 Sulfite oxidase (SO), 132 Sulfite reductase, 252 Sulfolipids, 179, 251 Sulfur, 244 Sulfuration, 134–135 Sulfur-enhanced defence, 244 Sulfur starvation, 247 Sulphoquinovosyldiacylglycerol (SQDG), 179 Sultr, 246 Symbiosis, 286 Symplastic pathway, 176

T Target mimicry, 184, 187 Thionin, 244 Thioredoxin, 252

304

Tonoplast, 200, 205, 206, 215, 217 Trace element, 121 Transcription factor, 184, 185, 188, 254 Transgenic approaches, 230–231 Transnitrosation, 162 Transpiration, 201, 203, 206, 210, 217 Transport, 1–11 Transporter (or Transport protein) CNGC (cyclic nucleotide gated channel), 200, 216 CPA (cation/proton-antiporter), 200, 205–207, 211, 217 GLR (glutamate receptor), 216 HKT/Trk, 216 K+ channel (KIRC, KORC, shaker), 200, 201, 203–205, 207, 208, 210, 211, 216 KEA, 200 K+/H+-antiporter, 205–207 K+/H+-symporter, 200, 205, 207–209, 211, 216 kir-like, 200, 217 KT/KUP/HAK (K+ uptake permease), 211 slowly-activating vacuolar channel (SV channel), 200, 211 TPC1, 200, 217 TPK/KCO (tandem pore K+ channel), 216, 217 VICC (voltage-independent cation channel), 200, 209–211, 216, 217

U Urea, 151–152

Index

V Vacuole, 24–25, 30, 32, 33, 35, 38, 85–86, 200, 201, 205, 207, 208, 211, 217, 284, 288, 290, 291 VIT1 transporter, 98, 108 Voltage dependent channels, 25, 28–31

W WRKY75, 184–186

X Xanthine dehydrogenase (XDH), 130, 133 Xanthine oxidase (XO), 134–135 Xenobiotics, 265 Xylem, 176, 177, 184, 248, 288–290, 292 Xylem loading, 8

Y Yellow stripe like (YSL), 84 Yellow Stripe-Like (YSL) transporters, 65, 107 YNL275w, 11

Z ZAT6, 184–186 ZIP family transporters, 60 ZIP transporter, 98, 100 Zn chemistry, 281 Zn deficiency, 284, 285, 287–292 Zn toxicity, 285, 291, 292