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Cellular Biology of Sulfur and Its Functions in Plants

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Book cover Cell Biology of Metals and Nutrients

Part of the book series: Plant Cell Monographs ((CELLMONO,volume 17))

Abstract

Sulfur is one of the most versatile elements in life. It functions in fundamental processes such as electron transport, structure, and regulation. In plants, additional roles have developed with respect to photosynthetic oxygen production, abiotic and biotic stress resistance and secondary metabolism. Sulfate uptake, reductive assimilation, and integration into cysteine and methionine are the central processes that direct oxidized and reduced forms of organically-bound sulfur into its various functions. These steps are distributed between several cellular compartments and tightly regulated by supply, demand, and environmental factors in a network with assimilation of carbon and nitrogen. Signaling cues such as sulfate availability and thiol-based redox homeostasis via glutathione and their integrating by sensing systems will be presented in this chapter and analyzed.

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References

  • Adams DO, Yang SF (1977) Methionine metabolism in apple tissue: implication of S-adenosylmethionine as an intermediate in the conversion of methionine to ethylene. Plant Physiol 60:892–896

    CAS  PubMed  Google Scholar 

  • Amir R, Hacham Y, Galili G (2002) Cystathionine γ-synthase and threonine synthase operate in concert to regulate carbon flow towards methionine in plants. Trends Plant Sci 7:153–156

    CAS  PubMed  Google Scholar 

  • Amtmann A, Armengaud P (2009) Effects of N, P, K and S on metabolism: new knowledge gained from multi-level analysis. Curr Opin Plant Biol 12:275–283

    CAS  PubMed  Google Scholar 

  • Amtmann A, Blatt MR (2009) Regulation of macronutrient transport. New Phytol 181:35–52

    CAS  PubMed  Google Scholar 

  • Awazuhara M, Fujiwara T, Hayashi H, Watanabe-Takahashi A, Takahashi H, Saito K (2005) The function of SULTR2;1 sulfate transporter during seed development in Arabidopsis thaliana. Physiol Plant 125:95–105

    CAS  Google Scholar 

  • Balk J, Lobreaux S (2005) Biogenesis of iron-sulfur proteins in plants. Trends Plant Sci 10:324–331

    CAS  PubMed  Google Scholar 

  • Bartlem D, Lambein I, Okamoto T, Itaya A, Uda Y, Kijima F, Tamaki Y, Nambara E, Naito S (2000) Mutation in the threonine synthase gene results in an over-accumulation of soluble methionine in Arabidopsis. Plant Physiol 123:101–110

    CAS  PubMed  Google Scholar 

  • Baxter I, Muthukumar B, Park HC, Buchner P, Lahner B, Danku J, Zhao K, Lee J, Hawkesford MJ, Guerinot ML, Salt DE (2008) Variation in molybdenum content across broadly distributed populations of Arabidopsis thaliana is controlled by a mitochondrial molybdenum transporter (MOT1). PLoS Genet 4:e1000004

    PubMed  Google Scholar 

  • Bell CI, Clarkson DT, Cram WJ (1995) Sulphate supply and its regulation of transport in roots of a tropical legume Macroptilium atropurpureum cv. Siratro J Exp Bot 282:65–71

    Google Scholar 

  • Bell CS, Cram WJ, Clarkson DT (1994) Compartmental analysis of 35SO 2−4 exchange kinetics in roots and leaves of a tropical legume Macroptilium atropurpureum cv. Siratro. J Exp Bot 45:879–886

    Google Scholar 

  • Benning C, Garavito RM, Shimojima M (2008) Sulfolipid biosynthesis and function in plants. In: Hell R, Dahl C, Leustek T (eds) Sulfur Metabolism in phototrophicorganisms. Springer, Dordrecht, The Netherlands, pp 185–200

    Google Scholar 

  • Berkowitz O, Wirtz M, Wolf A, Kuhlmann J, Hell R (2002) Use of biomolecular interaction analysis to elucidate the regulatory mechanism of the cysteine synthase complex from Arabidopsis thaliana. J Biol Chem 277:30629–30634

    CAS  PubMed  Google Scholar 

  • Bick JA, Aslund F, Chen Y, Leustek T (1998) Glutaredoxin function for the carboxyl-terminal domain of the plant-type 5′-adenylylsulfate reductase. Proc Natl Acad Sci USA 95:8404–8409

    CAS  PubMed  Google Scholar 

  • Bick JA, Dennis JJ, Zylstra GJ, Nowack J, Leustek T (2000) Identification of a new class of 5′-adenylylsulfate (APS) reductases from sulfate-assimilating bacteria. J Bacteriol 182:135–142

    CAS  PubMed  Google Scholar 

  • Bick JA, Setterdahl AT, Knaff DB, Chen Y, Pitcher LH, Zilinskas BA, Leustek T (2001) Regulation of the plant-type 5′-adenylyl sulfate reductase by oxidative stress. Biochemistry 40:9040–9048

    CAS  PubMed  Google Scholar 

  • Blake-Kalff MM, Harrison KR, Hawkesford MJ, Zhao FJ, McGrath SP (1998) Distribution of sulfur within oilseed rape leaves in response to sulfur deficiency during vegetative growth. Plant Physiol 118:1337–1344

    CAS  PubMed  Google Scholar 

  • Blaszczyk A, Brodzik R, Sirko A (1999) Increased resistance to oxidative stress in transgenic tobacco plants overexpressing bacterial serine acetyltransferase. Plant J 20:237–243

    CAS  PubMed  Google Scholar 

  • Bloem E, Riemenschneider A, Volker J, Papenbrock J, Schmidt A, Salac I, Haneklaus S, Schnug E (2004) Sulphur supply and infection with Pyrenopeziza brassicae influence L-cysteine desulphydrase activity in Brassica napus L. J Exp Bot 55:2305–2312

    CAS  PubMed  Google Scholar 

  • Blum R, Beck A, Korte A, Stengel A, Letzel T, Lendzian K, Grill E (2007) Function of phytochelatin synthase in catabolism of glutathione-conjugates. Plant J 49:740–749

    CAS  PubMed  Google Scholar 

  • Bogdanova N, Hell R (1997) Cysteine synthesis in plants: protein-protein interactions of serine acetyltransferase from Arabidopsis thaliana. Plant J 11:251–262

    CAS  PubMed  Google Scholar 

  • Bolchi A, Petrucco S, Tenca PL, Foroni C, Ottonello S (1999) Coordinate modulation of maize sulfate permease and ATP sulfurylase mRNAs in response to variations in sulfur nutritional status: stereospecific down-regulation by L-cysteine. Plant Mol Biol 39:527–537

    CAS  PubMed  Google Scholar 

  • Bonner ER, Cahoon RE, Knapke SM, Jez JM (2005) Molecular basis of cysteine biosynthesis in plants: structural and functional analysis of O-acetylserine sulfhydrylase from Arabidopsis thaliana. J Biol Chem 280:38803–38813

    CAS  PubMed  Google Scholar 

  • Bourgis F, Roje S, Nuccio ML, Fisher DB, Tarczynski MC, Li C, Herschbach C, Rennenberg H, Pimenta MJ, Shen TL, Gage DA, Hanson AD (1999) S-methylmethionine plays a major role in phloem sulfur transport and is synthesized by a novel type of methyltransferase. Plant Cell 11:1485–1498

    CAS  PubMed  Google Scholar 

  • Brunold C, Suter M (1990) Adenosine-5-phosphosulfate sulfotransferase. In Methods Plant Biochem., P. Lea, ed (London: Academic Press), pp. 339–343

    Google Scholar 

  • Brunold C, Rennenberg H (1997) Regulation of sulfur metabolism in plants: first molecular approaches. Progr Bot 58:164–186

    CAS  Google Scholar 

  • Buchner P, Takahashi H, Hawkesford MJ (2004a) Plant sulphate transporters: co-ordination of uptake, intracellular and long-distance transport. J Exp Bot 55:1765–1773

    CAS  PubMed  Google Scholar 

  • Buchner P, Stuiver CEE, Westerman S, Wirtz M, Hell R, Hawkesford MJ, De Kok LJ (2004b) Regulation of sulfate uptake and expression of sulfate transporter genes in Brassica oleracea as affected by atmospheric H2S and pedospheric sulfate nutrition. Plant Physiol 136:3396–3408

    CAS  PubMed  Google Scholar 

  • Burgener M, Suter M, Jones S, Brunold C (1998) Cyst(e)ine is the transport metabolite of assimilated sulfur from bundle-sheath to mesophyll cells in maize leaves. Plant Physiol 116:1315–1322

    CAS  PubMed  Google Scholar 

  • Burow M, Wittstock U, Gershenzon J (2008) Sulfur-containing secondary metabolites and their role in plant defense. In: Hell R, Dahl C, Leustek T (eds) Sulfur metabolism in phototrophic organisms. Springer, Dordrecht, The Netherlands, pp 205–226

    Google Scholar 

  • Burstenbinder K, Rzewuski G, Wirtz M, Hell R, Sauter M (2007) The role of methionine recycling for ethylene synthesis in Arabidopsis. Plant J 49:238–249

    PubMed  Google Scholar 

  • Cagnac O, Bourbouloux A, Chakrabarty D, Zhang M-Y, Delrot S (2004) AtOPT6 transports glutathione derivatives and is induced by primisulfuron. Plant Physiol 135:1378–1387

    CAS  PubMed  Google Scholar 

  • Cairns NG, Pasternak M, Wachter A, Cobbett CS, Meyer AJ (2006) Maturation of Arabidopsis seeds is dependent on glutathione biosynthesis within the embryo. Plant Physiol 141:446–455

    CAS  PubMed  Google Scholar 

  • Cannon G, Ward L, Case C, Heinhorst S (1999) The 68 kDa DNA compacting nucleoid protein from soybean chloroplasts inhibits DNA synthesis in vitro. Plant Mol Biol 39:835–845

    CAS  PubMed  Google Scholar 

  • Cantoni GL (1975) Biological methylation: selected aspects. Annu Rev Biochem 44:435–451

    CAS  PubMed  Google Scholar 

  • Chen S, Petersen BL, Olsen CE, Schulz A, Halkier BA (2001) Long-distance phloem transport of glucosinolates in Arabidopsis. Plant Physiol 127:194–201

    CAS  PubMed  Google Scholar 

  • Chew O, Whelan J, Millar AH (2003) Molecular definition of the ascorbate-glutathione cycle in Arabidopsis mitochondria reveals dual targeting of antioxidant defenses in plants. J Biol Chem 278:46869–46877

    CAS  PubMed  Google Scholar 

  • Chiba Y, Sakurai R, Yoshino M, Ominato K, Ishikawa M, Onouchi H, Naito S (2003) S-adenosyl-L-methionine is an effector in the posttranscriptional autoregulation of the cystathionine gamma-synthase gene in Arabidopsis. Proc Natl Acad Sci USA 100:10225–10230

    CAS  PubMed  Google Scholar 

  • Chiba Y, Ishikawa M, Kijima F, Tyson RH, Kim J, Yamamoto A, Nambara E, Leustek T, Wallsgrove RM, Naito S (1999) Evidence for autoregulation of cystathionine γ-synthase mRNA stability in Arabidopsis. Science 286:1371–1374

    CAS  PubMed  Google Scholar 

  • Clarkson DT, Smith FW, Vanden Berg PJ (1983) Regulation of sulphate transport in a tropical legume, Macroptilium atropurpureum, cv. Siratro. J Exp Bot 34:1463–1483

    CAS  Google Scholar 

  • Cooper RM, Williams JS (2004) Elemental sulphur as an induced antifungal substance in plant defence. J Exp Bot 55:1947–1953

    CAS  PubMed  Google Scholar 

  • Crane BR, Siegel LM, Getzoff ED (1995) Sulfite reductase structure at 1.6 Å evolution and catalysis for reduction of inorganic anions. Science 270:59–67

    CAS  PubMed  Google Scholar 

  • Curien G, Job D, Douce R, Dumas R (1998) Allosteric activation of Arabidopsis threonine synthase by S-adenosylmethionine. Biochemistry 37:13212–13221

    CAS  PubMed  Google Scholar 

  • Curien G, Ravanel S, Robert M, Dumas R (2005) Identification of six novel allosteric effectors of Arabidopsis thaliana aspartate kinase-homoserine dehydrogenase isoforms. Physiological context sets the specificity. J Biol Chem 280:41178–41183

    CAS  PubMed  Google Scholar 

  • Curien G, Laurencin M, Robert-Genthon M, Dumas R (2007) Allosteric monofunctional aspartate kinases from Arabidopsis. FEBS J 274:164–176

    CAS  PubMed  Google Scholar 

  • Dahl C, Hell R, Leustek T, Knaff D (2008) Introduction to sulfur metabolism in phototrophic organisms. In: Hell R, Dahl C, Leustek T (eds) Sulfur metabolism in phototrophic organisms. Springer, Dordrecht, The Netherlands, pp 1–16

    Google Scholar 

  • Dixon DP, Hawkins T, Hussey PJ, Edwards R (2009) Enzyme activities and subcellular localization of members of the Arabidopsis glutathione transferase superfamily. J Exp Bot 60:1207–1218

    CAS  PubMed  Google Scholar 

  • Dominguez-Solis JR, He Z, Lima A, Ting J, Buchanan BB, Luan S (2008) A cyclophilin links redox and light signals to cysteine biosynthesis and stress responses in chloroplasts. Proc Natl Acad Sci USA 105:16386–16391

    CAS  PubMed  Google Scholar 

  • Droux M (2003) Plant serine acetyltransferase: new insights for regulation of sulphur metabolism in plant cells. Plant Physiol Biochem 41:619–627

    CAS  Google Scholar 

  • Droux M (2004) Sulfur assimilation and the role of sulfur in plant metabolism: a survey. Photosynth Res 79:331–348

    CAS  PubMed  Google Scholar 

  • Droux M, Ruffet ML, Douce R, Job D (1998) Interactions between serine acetyltransferase and O-acetylserine (thiol) lyase in higher plants-structural and kinetic properties of the free and bound enzymes. Eur J Biochem 255:235–245

    CAS  PubMed  Google Scholar 

  • Dubousset L, Abdallah M, Desfeux AS, Etienne P, Meuriot F, Hawkesford MJ, Gombert J, Segura R, Bataille MP, Reze S, Bonnefoy J, Ameline AF, Ourry A, Le Dily F, Avice JC (2009) Remobilization of leaf S compounds and senescence in response to restricted sulphate supply during the vegetative stage of oilseed rape are affected by mineral N availability. J Exp Bot 60:3239–3253

    CAS  PubMed  Google Scholar 

  • Falkowski PG (2006) Evolution: tracing oxygen's imprint on earth's metabolic evolution. Science 311:1724–1725

    CAS  PubMed  Google Scholar 

  • Feldman-Salit A, Wirtz M, Hell R, Wade RC (2009) A mechanistic model of the cysteine synthase complex. J Mol Biol 386:37–59

    CAS  PubMed  Google Scholar 

  • Ferreira RM, Teixeira AR (1992) Sulfur starvation in Lemna leads to degradation of ribulose-bisphosphate carboxylase without plant death. J Biol Chem 267:7253–7257

    CAS  PubMed  Google Scholar 

  • Ferretti M, Destro T, Tosatto SCE, La Rocca L, Rascio N, Masi A (2009) γ-glutamyl transferase in the cell wall participates in extracellular glutathione salvage from the root apoplast. New Phytol 181:115–126

    CAS  PubMed  Google Scholar 

  • Fitzpatrick KL, Tyerman SD, Kaiser BN (2008) Molybdate transport through the plant sulfate transporter SHST1. FEBS Lett 582:1508–1513

    CAS  PubMed  Google Scholar 

  • Foyer CH, Noctor G (2005) Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 17:1866–1875

    CAS  PubMed  Google Scholar 

  • Foyer CH, Bloom AJ, Queval G, Noctor G (2009a) Photorespiratory metabolism: genes, mutants, energetics, and redox signaling. Annu Rev Plant Biol 60:455–484

    CAS  PubMed  Google Scholar 

  • Foyer CH, Noctor G, Buchanan B, Dietz KJ, Pfannschmidt T (2009b) Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxid Redox Signal 11:861–905

    CAS  PubMed  Google Scholar 

  • Francois JA, Kumaran S, Jez JM (2006) Structural basis for interaction of O-acetylserine sulfhydrylase and serine acetyltransferase in the Arabidopsis cysteine synthase complex. Plant Cell 18:3647–3655

    CAS  PubMed  Google Scholar 

  • Freeman JL, Persans MW, Nieman K, Albrecht C, Peer W, Pickering IJ, Salt DE (2004) Increased glutathione biosynthesis plays a role in nickel tolerance in Thlaspi nickel hyperaccumulators. Plant Cell 16:2176–2191

    CAS  PubMed  Google Scholar 

  • Fujiwara T, Nambara E, Yamagishi K, Goto DB, Naito S (2002) Storage proteins. The Arabidopsis Book, 1–12

    Google Scholar 

  • Fukuda H, Hirakawa Y, Sawa S (2007) Peptide signaling in vascular development. Curr Opin Plant Biol 10:477–482

    CAS  PubMed  Google Scholar 

  • Geu-Flores F, Nielsen MT, Nafisi M, Moldrup ME, Olsen CE, Motawia MS, Halkier BA (2009) Glucosinolate engineering identifies a γ-glutamyl peptidase. Nat Chem Biol 5:575–577

    CAS  PubMed  Google Scholar 

  • Gigolashvili T, Berger B, Mock HP, Muller C, Weisshaar B, Flugge UI (2007) The transcription factor HIG1/MYB51 regulates indolic glucosinolate biosynthesis in Arabidopsis thaliana. Plant J 50:886–901

    CAS  PubMed  Google Scholar 

  • Gilbert SM, Clarkson DT, Cambridge M, Lambers H, Hawkesford MJ (1997) SO42-deprivation has an early effect on the content of ribulose-1, 5-bisphosphate carboxylase/oxygenase and photosynthesis in young leaves of wheat. Plant Physiol 115:1231–1239

    CAS  PubMed  Google Scholar 

  • Giordano M, Norici A, Hell R (2005) Sulfur and phytoplankton: acquisition, metabolism and impact on the environment. New Phytol 166:371–382

    CAS  PubMed  Google Scholar 

  • Glawischnig E (2007) Camalexin. Phytochem 68:401–406

    CAS  Google Scholar 

  • Goto DB, Ogi M, Kijima F, Kumagai T, van Werven F, Onouchi H, Naito S (2002) A single-nucleotide mutation in a gene encoding S-adenosylmethionine synthetase is associated with methionine over-accumulation phenotype in Arabidopsis thaliana. Genes Genet Syst 77:89–95

    CAS  PubMed  Google Scholar 

  • Goyer A, Collakova E, Shachar-Hill Y, Hanson AD (2007) Functional characterization of a methionine γ-lyase in Arabidopsis and its implication in an alternative to the reverse trans-sulfuration pathway. Plant Cell Physiol 48:232–242

    CAS  PubMed  Google Scholar 

  • Grill E, Winnacker EL, Zenk MH (1985) Phytochelatins: the princial heavy-metal complexing peptides of higher plants. Science 230:674–676

    CAS  PubMed  Google Scholar 

  • Gromes R, Hothorn M, Lenherr ED, Rybin V, Scheffzek K, Rausch, T (2008) The redox switch of γ-glutamylcysteine ligase via a reversible monomer-dimer transition is a mechanism unique to plants. Plant J

    Google Scholar 

  • Gross A, Brückner G, Heldt HW, Flügge U-I (1990) Comparison of the kinetic properties, inhibition and labelling of the phosphate translocators from maize and spinach mesophyll chloroplasts. Planta 180:262–271

    CAS  Google Scholar 

  • Grzam A, Martin M, Hell R, Meyer A (2007) γ-Glutamyl transpeptidase GGT4 initiates vacuolar degradation of glutathione S-conjugates in Arabidopsis. FEBS Lett 581:3131–3138

    CAS  PubMed  Google Scholar 

  • Grzam A, Tennstedt P, Clemens S, Hell R, Meyer AJ (2006) Vacuolar sequestration of glutathione S-conjugates outcompetes a possible degradation of the glutathione moiety by phytochelatin synthase. FEBS Lett 580:6384–6390

    CAS  PubMed  Google Scholar 

  • Gutierrez-Marcos JF, Roberts MA, Campbell EI, Wray JL (1996) Three members of a novel small gene-family from Arabidopsis thaliana able to complement functionally an Escherichia coli mutant defective in PAPS reductase activity encode proteins with a thioredoxin-like domain and “APS reductase” activity. Proc Natl Acad Sci USA 93:13377–13382

    CAS  PubMed  Google Scholar 

  • Haas FH, Heeg C, Queiroz R, Bauer A, Wirtz M, Hell R (2008) Mitochondrial serine acetyltransferase functions as a pacemaker of cysteine synthesis in plant cells. Plant Physiol 148:1055–1067

    CAS  PubMed  Google Scholar 

  • Hacham Y, Avraham T, Amir R (2002) The N-terminal region of Arabidopsis cystathionine γ-synthase plays an important regulatory role in methionine metabolism. Plant Physiol 128:454–462

    CAS  PubMed  Google Scholar 

  • Hacham Y, Schuster G, Amir R (2006) An in vivo internal deletion in the N-terminus region of Arabidopsis cystathionine γ-synthase results in CGS expression that is insensitive to methionine. Plant J 45:955–967

    CAS  PubMed  Google Scholar 

  • Hacham Y, Song L, Schuster G, Amir R (2007) Lysine enhances methionine content by modulating the expression of S-adenosylmethionine synthase. Plant J 51:850–861

    CAS  PubMed  Google Scholar 

  • Halkier B, Gershenzon J (2006) Biology and biochemistry of glucosinolates. Annu Rev Plant Biol 57:303–333

    CAS  PubMed  Google Scholar 

  • Harms K, von Ballmoos P, Brunold C, Hofgen R, Hesse H (2000) Expression of a bacterial serine acetyltransferase in transgenic potato plants leads to increased levels of cysteine and glutathione. Plant J 22:335–343

    CAS  PubMed  Google Scholar 

  • Hatzfeld Y, Cathala N, Grignon C, Davidian J-C (1998) Effect of ATP sulfurylase overexpression in bright yellow 2 tobacco cells. Regulation of ATP sulfurylase and SO42-transport activities. Plant Physiol 116:1307–1313

    CAS  PubMed  Google Scholar 

  • Hawkesford MJ (2003) Transporter gene families in plants: the sulphate transporter gene family redundancy or specialization? Physiol Plant 117:155–163

    CAS  Google Scholar 

  • Hawkesford MJ (2008) Uptake, distribution and subcellular transport of sulfate. In: Hell R, Dahl C, Leustek T (eds) Sulfur Metabolism in Phototrophic Organisms. Springer, Dordrecht, The Netherlands, pp 17–32

    Google Scholar 

  • Hawkesford MJ, De Kok LJ (2006) Managing sulphur metabolism in plants. Plant Cell Environ 29:382–395

    CAS  PubMed  Google Scholar 

  • Heeg C, Kruse C, Jost R, Gutensohn M, Ruppert T, Wirtz M, Hell R (2008) Analysis of the Arabidopsis O-acetylserine(thiol)lyase gene family demonstrates compartment-specific differences in the regulation of cysteine synthesis. Plant Cell 20:168–185

    CAS  PubMed  Google Scholar 

  • Hell R (1997) Molecular physiology of plant sulfur metabolism. Planta 202:138–148

    CAS  PubMed  Google Scholar 

  • Hell R, Bergmann L (1988) Glutathione synthetase in tobacco suspension cultures: catalytic properties and localization. Physiol Plant 72:70–76

    CAS  Google Scholar 

  • Hell R, Bergmann L (1990) γ-Glutamylcysteine synthetase in higher plants: catalytic properties and subcellular localization. Planta 180:603–612

    CAS  Google Scholar 

  • Hell R, Hillebrand H (2001) Plant concepts for mineral acquisition and allocation. Curr Opin Biotechnol 12:161–168

    CAS  PubMed  Google Scholar 

  • Hell R, Jost R, Berkowitz O, Wirtz M (2002) Molecular and biochemical analysis of the enzymes of cysteine biosynthesis in the plant Arabidopsis thaliana. Amino Acids 22:245–257

    CAS  PubMed  Google Scholar 

  • Hernández-Sebastià C, Varin L, Marsolais F (2008) Sulfotransferases from plants, algae and phototrophic bacteria. In: Hell R, Dahl C, Leustek T (eds) Sulfur metabolism in phototrophic organisms. Springer, Dordrecht, The Netherlands, pp 111–130

    Google Scholar 

  • Herschbach C, van Der Zalm E, Schneider A, Jouanin L, De Kok LJ, Rennenberg H (2000) Regulation of sulfur nutrition in wild-type and transgenic poplar over-expressing γ-glutamylcysteine synthetase in the cytosol as affected by atmospheric H2S. Plant Physiol 124:461–473

    CAS  PubMed  Google Scholar 

  • Hesse H, Kreft O, Maimann S, Zeh M, Hoefgen R (2004) Current understanding of the regulation of methionine biosynthesis in plants. J Exp Bot 55:1799–1808

    CAS  PubMed  Google Scholar 

  • Higashi Y, Hirai MY, Fujiwara T, Naito S, Noji M, Saito K (2006) Proteomic and transcriptomic analysis of Arabidopsis seeds: molecular evidence for successive processing of seed proteins and its implication in the stress response to sulfur nutrition. Plant J 48:557–571

    CAS  PubMed  Google Scholar 

  • Hirai M, Fujiwara T, Awazuhara M, Kimura T, Noji M, Saito K (2003) Global expression profiling of sulfur-starved Arabidopsis by DNA macroarray reveals the role of O-acetyl-L-serine as a general regulator of gene expression in response to sulfur nutrition. Plant J 33:651–663

    CAS  PubMed  Google Scholar 

  • Hirai MY, Saito K (2008) Analysis of systemic sulfur metabolism in plants using integrated ‘-omics’ strategies. Mol Biosyst 4:967–973

    CAS  PubMed  Google Scholar 

  • Hirai MY, Yano M, Goodenowe DB, Kanaya S, Kimura T, Awazuhara M, Arita M, Fujiwara T, Saito K (2004) Integration of transcriptomics and metabolomics for understanding of global responses to nutritional stresses in Arabidopsis thaliana. PNAS 101:10205–10210

    CAS  PubMed  Google Scholar 

  • Hirai MY, Sugiyama K, Sawada Y, Tohge T, Obayashi T, Suzuki A, Araki R, Sakurai N, Suzuki H, Aoki K, Goda H, Nishizawa OI, Shibata D, Saito K (2007) Omics-based identification of Arabidopsis Myb transcription factors regulating aliphatic glucosinolate biosynthesis. PNAS 104:6478–6483

    CAS  PubMed  Google Scholar 

  • Hodson RC, Schiff JA (1971) Studies of sulfate utilization by algae: 9. Fractionation of a cell-free system from Chlorella into two activities necessary for the reduction of adenosine 3′-phosphate 5′-phosphosulfate to acid-volatile radioactivity. Plant Physiol 47:300–305

    CAS  PubMed  Google Scholar 

  • Hoefgen R, Nikiforova VJ (2008) Metabolomics integrated with transcriptomics: assessing systems response to sulfur-deficiency stress. Physiol Plant 132:190–198

    CAS  PubMed  Google Scholar 

  • Hopkins L, Parmar S, Blaszczyk A, Hesse H, Hoefgen R, Hawkesford MJ (2005) O-acetylserine and the regulation of expression of genes encoding components for sulfate uptake and assimilation in potato. Plant Physiol 138:433–440

    CAS  PubMed  Google Scholar 

  • Hothorn M, Wachter A, Gromes R, Stuwe T, Rausch T, Scheffzek K (2006) Structural basis for the redox control of plant glutamate cysteine ligase. J Biol Chem 281:27557–27565

    CAS  PubMed  Google Scholar 

  • Howarth J, Parmar S, Barraclough P, Hawkesford M (2009) A sulphur deficiency-induced gene, sdi1, involved in the utilization of stored sulphate pools under sulphur-limiting conditions has potential as a diagnostic indicator of sulphur nutritional status. Plant Biotechnol J 7:200–209

    CAS  PubMed  Google Scholar 

  • Howarth JR, Parmar S, Jones J, Shepherd CE, Corol DI, Galster AM, Hawkins ND, Miller SJ, Baker JM, Verrier PJ, Ward JL, Beale MH, Barraclough PB, Hawkesford MJ (2008) Co-ordinated expression of amino acid metabolism in response to N and S deficiency during wheat grain filling. J Exp Bot 59:3675–3689

    CAS  PubMed  Google Scholar 

  • Inaba K, Fujiwara T, Hayashi H, Chino M, Komeda Y, Naito S (1994) Isolation of an Arabidopsis thaliana mutant, mto1, that overaccumulates soluble methionine. Plant Physiol 104:881–887

    CAS  PubMed  Google Scholar 

  • Jez JM, Cahoon RE, Chen S (2004) Arabidopsis thaliana glutamate-cysteine ligase: functional properties, kinetic mechanism, and regulation of activity. J Biol Chem 279:33463–33470

    CAS  PubMed  Google Scholar 

  • Jones PR, Manabe T, Awazuhara M, Saito K (2003) A new member of plant CS-lyases. A cystine lyase from Arabidopsis thaliana. J Biol Chem 278:10291–10296

    CAS  PubMed  Google Scholar 

  • Kasajima I, Ohkama-Ohtsu N, Ide Y, Hayashi H, Yoneyama T, Suzuki Y, Naito S, Fujiwara T (2007) The BIG gene is involved in regulation of sulfur deficiency-responsive genes in Arabidopsis thaliana. Physiol Plant 129:351–363

    CAS  Google Scholar 

  • Kataoka T, Hayashi N, Yamaya T, Takahashi H (2004a) Root-to-shoot transport of sulfate in Arabidopsis. Evidence for the role of SULTR3;5 as a component of low-affinity sulfate transport system in the root vasculature. Plant Physiol 136:4198–4204

    CAS  PubMed  Google Scholar 

  • Kataoka T, Watanabe-Takahashi A, Hayashi N, Ohnishi M, Mimura T, Buchner P, Hawkesford MJ, Yamaya T, Takahashi H (2004b) Vacuolar sulfate transporters are essential determinants controlling internal distribution of sulfate in Arabidopsis. Plant Cell 16:2693–2704

    CAS  PubMed  Google Scholar 

  • Kawashima CG, Berkowitz O, Hell R, Noji M, Saito K (2005) Characterization and expression analysis of a serine acetyltransferase gene family involved in a key step of the sulfur assimilation pathway in Arabidopsis. Plant Physiol 137:220–230

    CAS  PubMed  Google Scholar 

  • Kawashima CG, Yoshimoto N, Maruyama-Nakashita A, Tsuchiya YN, Saito K, Takahashi H, Dalmay T (2009) Sulphur starvation induces the expression of microRNA-395 and one of its target genes but in different cell types. Plant J 57:313–321

    CAS  PubMed  Google Scholar 

  • Kim H, Hirai MY, Hayashi H, Chino M, Naito S, Fujiwara T (1999) Role of O-acetyl-L-serine in the coordinated regulation of the expression of a soybean seed storage-protein gene by sulfur and nitrogen nutrition. Planta 209:282–289

    CAS  PubMed  Google Scholar 

  • Klapheck S, Latus C, Bergmann L (1987) Localization of glutathione synthetase and distribution of glutathione in leaf cells of Pisum sativum L. J Plant Physiol 131:123–131

    CAS  Google Scholar 

  • Klatte M, Schuler M, Wirtz M, Fink-Straube C, Hell R, Bauer P (2009) The analysis of Arabidopsis nicotianamine synthase mutants reveals functions for nicotianamine in seed iron loading and iron deficiency responses. Plant Physiol 150:257–271

    CAS  PubMed  Google Scholar 

  • Klonus D, Hofgen R, Willmitzer L, Riesmeier JW (1994) Isolation and characterization of two cDNA clones encoding ATP-sulfurylases from potato by complementation of a yeast mutant. Plant J 6:105–112

    CAS  PubMed  Google Scholar 

  • Kocsis MG, Ranocha P, Gage DA, Simon ES, Rhodes D, Peel GJ, Mellema S, Saito K, Awazuhara M, Li C, Meeley RB, Tarczynski MC, Wagner C, Hanson AD (2003) Insertional inactivation of the methionine s-methyltransferase gene eliminates the s-methylmethionine cycle and increases the methylation ratio. Plant Physiol 131:1808–1815

    CAS  PubMed  Google Scholar 

  • Kopriva S (2006) Regulation of sulfate assimilation in Arabidopsis and beyond. Ann Bot 97:479–495

    CAS  PubMed  Google Scholar 

  • Kopriva S, Koprivova A (2004) Plant adenosine 5′-phosphosulphate reductase: the past, the present, and the future. J Exp Bot 55:1775–1783

    CAS  PubMed  Google Scholar 

  • Kopriva S, Koprivova A (2005) Sulfate assimilation and glutathione synthesis in C4 plants. Photosynth Res 86:363–372

    CAS  PubMed  Google Scholar 

  • Kopriva S, Wiedemann G, Reski R (2007a) Sulfate assimilation in basal land plants – what does genomic sequencing tell us? Plant Biol 9:556–564

    CAS  PubMed  Google Scholar 

  • Kopriva S, Fritzemeier K, Wiedemann G, Reski R (2007b) The putative moss 3′-phosphoadenosine-5′-phosphosulfate reductase is a novel form of adenosine-5′-phosphosulfate reductase without an iron-sulfur cluster. J Biol Chem 282:22930–22938

    CAS  PubMed  Google Scholar 

  • Koprivova A, Meyer AJ, Schween G, Herschbach C, Reski R, Kopriva S (2002) Functional knockout of the adenosine 5′-phosphosulfate reductase gene in Physcomitrella patens revives an old route of sulfate assimilation. J Biol Chem 277:32195–32201

    CAS  PubMed  Google Scholar 

  • Kredich NM, Tomkins GM (1966) The enzymic synthesis of L-cysteine in Escherichia coli and Salmonella typhimurium. J Biol Chem 241:4955–4965

    CAS  PubMed  Google Scholar 

  • Kredich NM, Becker MA, Tomkins GM (1969) Purification and characterization of cysteine synthetase, a bifunctional protein complex, from Salmonella typhimurium. J Biol Chem 244:2428–2439

    CAS  PubMed  Google Scholar 

  • Krueger RJ, Siegel LM (1982) Evidence for siroheme-Fe4S4 interaction in spinach ferredoxin-sulfite reductase. Biochemistry 21:2905–2909

    CAS  PubMed  Google Scholar 

  • Kruse C, Jost R, Hillebrand H, Hell R (2005) Sulfur-rich proteins and their agrobiotechnological potential for resistance to plant pathogens. FAL Agricult Res 283:73–80

    CAS  Google Scholar 

  • Kruse C, Jost R, Lipschis M, Kopp B, Hartmann M, Hell R (2007) Sulfur-enhanced defence: effects of sulfur metabolism, nitrogen supply, and pathogen lifestyle. Plant Biol 9:608–619

    CAS  PubMed  Google Scholar 

  • Kumaran S, Yi H, Krishnan HB, Jez JM (2009) Assembly of the cysteine synthase complex and the regulatory role of protein-protein interactions. J Biol Chem 284:10268–10275

    CAS  PubMed  Google Scholar 

  • Kushnir S, Babiychuk E, Storozhenko S, Davey MW, Papenbrock J, De Rycke R, Engler G, Stephan UW, Lange H, Kispal G, Lill R, Van Montagu M (2001) A mutation of the mitochondrial ABC transporter Sta1 leads to dwarfism and chlorosis in the Arabidopsis mutant starik. Plant Cell 13:89–100

    CAS  PubMed  Google Scholar 

  • Kuske CR, Hill KK, Guzman E, Jackson PJ (1996) Subcellular location of O-acetylserine sulfhydrylase isoenzymes in cell cultures and plant tissues of Datura innoxia Mill. Plant Physiol 112:659–667

    CAS  PubMed  Google Scholar 

  • Kutz A, Muller A, Hennig P, Kaiser WM, Piotrowski M, Weiler EW (2002) A role for nitrilase 3 in the regulation of root morphology in sulphur-starving Arabidopsis thaliana. Plant J 30:95–106

    CAS  PubMed  Google Scholar 

  • Laber B, Maurer W, Hanke C, Grafe S, Ehlert S, Messerschmidt A, Clausen T (1999) Characterization of recombinant Arabidopsis thaliana threonine synthase. Eur J Biochem 263:212–221

    CAS  PubMed  Google Scholar 

  • Lappartient AG, Touraine B (1996) Demand-driven control of root ATP sulfurylase activity and SO 2-4 uptake in intact Canola. Plant Physiol 111:147–157

    CAS  PubMed  Google Scholar 

  • Lappartient AG, Vidmar JJ, Leustek T, Glass AD, Touraine B (1999) Inter-organ signaling in plants: regulation of ATP sulfurylase and sulfate transporter genes expression in roots mediated by phloem-translocated compound. Plant J 18:89–95

    CAS  PubMed  Google Scholar 

  • Lass B, Ullrich-Eberius CI (1983) Evidence for proton/sulfate cotransport and its kinetics in Lemna gibba G1. Planta 161:53–60

    Google Scholar 

  • Lehmann M, Schwarzlander M, Obata T, Sirikantaramas S, Burow M, Olsen CE, Tohge T, Fricker MD, Moller BL, Fernie AR, Sweetlove LJ, Laxa M (2009) The metabolic response of Arabidopsis roots to oxidative stress is distinct from that of heterotrophic cells in culture and highlights a complex relationship between the levels of transcripts, metabolites, and flux. Mol Plant 2:390–406

    CAS  PubMed  Google Scholar 

  • Leustek T (1996) Molecular genetics of sulfate assimilation in plants. Physiol Plant 97:411–419

    CAS  Google Scholar 

  • Leustek T, Martin MN, Bick J-A, Davies JP (2000) Pathways and regulation of sulfur metabolism revealed through molecular and genetic studies. Ann Rev Plant Physiol Plant Mol Biol 51:141–165

    CAS  Google Scholar 

  • Lewandowska M, Sirko A (2008) Recent advances in understanding plant response to sulfur-deficiency stress. Acta Biochim Pol 55:457–471

    CAS  PubMed  Google Scholar 

  • Li Y, Dankher OP, Carreira L, Smith AP, Meagher RB (2006) The shoot-specific expression of γ-glutamylcysteine synthetase directs the long-distance transport of thiol-peptides to roots conferring tolerance to mercury and arsenic. Plant Physiol 141:288–298

    CAS  PubMed  Google Scholar 

  • Lindermayr C, Saalbach G, Durner J (2005) Proteomic identification of S-nitrosylated proteins in Arabidopsis. Plant Physiol 137:921–930

    CAS  PubMed  Google Scholar 

  • Liu F, Yoo B-C, Lee J-Y, Pan W, Harmon AC (2006) Calcium-regulated phosphorylation of soybean serine acetyltransferase in response to oxidative stress. J Biol Chem 281:27405–27415

    CAS  PubMed  Google Scholar 

  • Logan HM, Cathala N, Grignon C, Davidian JC (1996) Cloning of a cDNA encoded by a member of the Arabidopsis thaliana ATP sulfurylase multigene family. Expression studies in yeast and in relation to plant sulfur nutrition. J Biol Chem 271:12227–12233

    CAS  PubMed  Google Scholar 

  • Loizeau K, Gambonnet B, Zhang GF, Curien G, Jabrin S, Van Der Straeten D, Lambert WE, Rebeille F, Ravanel S (2007) Regulation of one-carbon metabolism in Arabidopsis: the N-terminal regulatory domain of cystathionine γ-synthase is cleaved in response to folate starvation. Plant Physiol 145:491–503

    CAS  PubMed  Google Scholar 

  • Lopez-Martin MC, Becana M, Romero LC, Gotor C (2008) Knocking out cytosolic cysteine synthesis compromises the antioxidant capacity of the cytosol to maintain discrete concentrations of hydrogenperoxide in Arabidopsis. Plant Physiol 147:562–572

    CAS  PubMed  Google Scholar 

  • Loudet O, Saliba-Colombani V, Camilleri C, Calenge F, Gaudon V, Koprivova A, North K, Kopriva S, Daniel-Vedele F (2007) Natural variation for sulfate content in Arabidopsis thaliana is highly controlled by APR2. Nat Genet 39:896–900

    CAS  PubMed  Google Scholar 

  • Lu SC (2000) S-Adenosylmethionine. Int J Biochem Cell Biol 32:391–395

    CAS  PubMed  Google Scholar 

  • Lunn JE, Droux M, Martin J, Douce R (1990) Localization of ATP-sulfurylase and O-acetylserine(thiol)lyase in spinach leaves. Plant Physiol 94:1345–1352

    CAS  PubMed  Google Scholar 

  • Malitsky S, Blum E, Less H, Venger I, Elbaz M, Morin S, Eshed Y, Aharoni A (2008) The transcript and metabolite networks affected by the two clades of Arabidopsis glucosinolate biosynthesis regulators. Plant Physiol 148:2021–2049

    CAS  PubMed  Google Scholar 

  • Martin MN, Tarczynski MC, Shen B, Leustek T (2005) The role of 5′-adenylylsulfate reductase in controlling sulfate reduction in plants. Photosynth Res 86:1–15

    Google Scholar 

  • Martin MN, Saladores PH, Lambert E, Hudson AO, Leustek T (2007) Localization of members of the γ-glutamyl transpeptidase family identifies sites of glutathione and Glutathione S-conjugate hydrolysis. Plant Physiol 144:1715–1732

    CAS  PubMed  Google Scholar 

  • Martin W, Rotte C, Hoffmeister M, Theissen U, Gelius-Dietrich G, Ahr S, Henze K (2003) Early cell evolution, eukaryotes, anoxia, sulfide, oxygen, fungi first (?), and a tree of genomes revisited. IUBMB Life 55:193–204

    CAS  PubMed  Google Scholar 

  • Marty L, Siala W, Schwarzlander M, Fricker MD, Wirtz M, Sweetlove LJ, Meyer Y, Meyer AJ, Reichheld JP, Hell R (2009) The NADPH-dependent thioredoxin system constitutes a functional backup for cytosolic glutathione reductase in Arabidopsis. Proc Natl Acad Sci USA 106:9109–9114

    CAS  PubMed  Google Scholar 

  • Maruyama-Nakashita A, Inoue E, Watanabe-Takahashi A, Yamaya T, Takahashi H (2003) Transcriptome profiling of sulfur-responsive genes in Arabidopsis reveals global effects of sulfur nutrition on multiple metabolic pathways. Plant Physiol 132:597–605

    CAS  PubMed  Google Scholar 

  • Maruyama-Nakashita A, Nakamura Y, Watanabe-Takahashi A, Yamaya T, Takahashi H (2004) Induction of SULTR1;1 sulfate transporter in Arabidopsis roots involves protein phosphorylation/dephosphorylation circuit for transcriptional regulation. Plant Cell Physiol 45:340–345

    CAS  PubMed  Google Scholar 

  • Maruyama-Nakashita A, Nakamura Y, Tohge T, Saito K, Takahashi H (2006) Arabidopsis SLIM1 is a central transcriptional regulator of plant sulfur response and metabolism. Plant Cell 18:3235–3251

    CAS  PubMed  Google Scholar 

  • Maruyama-Nakashita A, Nakamura Y, Watanabe-Takahashi A, Inoue E, Yamaya T, Takahashi H (2005) Identification of a novel cis-acting element conferring sulfur deficiency response in Arabidopsis roots. Plant J 42:305–314

    CAS  PubMed  Google Scholar 

  • Mas-Droux C, Biou V, Dumas R (2006a) Allosteric threonine synthase. Reorganization of the pyridoxal phosphate site upon asymmetric activation through S-adenosylmethionine binding to a novel site. J Biol Chem 281:5188–5196

    CAS  PubMed  Google Scholar 

  • Mas-Droux C, Curien G, Robert-Genthon M, Laurencin M, Ferrer JL, Dumas R (2006b) A novel organization of ACT domains in allosteric enzymes revealed by the crystal structure of Arabidopsis aspartate kinase. Plant Cell 18:1681–1692

    CAS  PubMed  Google Scholar 

  • May M, Vernoux T, Leaver C, Van Montagu M, Inze D (1998) Glutathione homeostasis in plants: implications for environmental sensing and plant development. J Exp Bot 49:649–667

    CAS  Google Scholar 

  • Meister A (1995) Glutathione biosynthesis and its inhibition. Methods Enzymol 252:26–30

    CAS  PubMed  Google Scholar 

  • Melis A, Chen H-C (2005) Chloroplast sulfate transport in green algae – genes, proteins and effects. Photosynth Res 86:299–307

    CAS  PubMed  Google Scholar 

  • Meyer AJ (2008) The integration of glutathione homeostasis and redox signaling. J Plant Physiol 165:1390–1403

    CAS  PubMed  Google Scholar 

  • Meyer AJ, Fricker MD (2002) Control of demand-driven biosynthesis of glutathione in green Arabidopsis suspension culture cells. Plant Physiol 130:1927–1937

    CAS  PubMed  Google Scholar 

  • Meyer AJ, Hell R (2005) Glutathione homeostasis and redox-regulation by sulfhydryl groups. Photosynth Res 86:435–457

    CAS  PubMed  Google Scholar 

  • Meyer AJ, Rausch T (2008) Biosynthesis, compartmentation and cellular functions of glutathione in plant cells. In: Hell R, Dahl C, Knaff DB, Leustek T (eds) Sulfur metabolism in phototrophic organisms. Springer, Dordrecht, The Netherlands, pp 161–184

    Google Scholar 

  • Meyer AJ, Brach T, Marty L, Kreye S, Rouhier N, Jacquot J-P, Hell R (2007) Redox-sensitive GFP in Arabidopsis thaliana is a quantitative biosensor for the redox potential of the cellular glutathione redox buffer. Plant J 52:973–986

    CAS  PubMed  Google Scholar 

  • Meyer Y, Siala W, Bashandy T, Riondet C, Vignols F, Reichheld JP (2008) Glutaredoxins and thioredoxins in plants. Biochim Biophys Acta 1783:589–600

    CAS  PubMed  Google Scholar 

  • Meyers DM, Ahmad S (1991) Link between L-3-cyanoalanine synthase activity and differential cyanide sensitivity of insects. Biochim Biophys Acta 1075:195–197

    CAS  PubMed  Google Scholar 

  • Miller AJ, Shen Q, Xu G (2009) Freeways in the plant: transporters for N, P and S and their regulation. Curr Opin Plant Biol 12:284–290

    CAS  PubMed  Google Scholar 

  • Mugford SG, Yoshimoto N, Reichelt M, Wirtz M, Hill L, Mugford ST, Nakazato Y, Noji M, Takahashi H, Kramell R, Gigolashvili T, Flugge UI, Wasternack C, Gershenzon J, Hell R, Saito K, Kopriva S (2009) Disruption of adenosine-5′-phosphosulfate kinase in Arabidopsis reduces levels of sulfated secondary metabolites. Plant Cell 21:910–927

    CAS  PubMed  Google Scholar 

  • Müntz K, Christov V, Saalbach G, Saalbach I, Waddell D, Pickardt T, Schieder O, Wustenhagen T (1998) Genetic engineering for high methionine grain legumes. Nahrung 42:125–127

    PubMed  Google Scholar 

  • Nakayama M, Akashi T, Hase T (2000) Plant sulfite reductase: molecular structure, catalytic function and interaction with ferredoxin. J Inorg Biochem 82:27–32

    CAS  PubMed  Google Scholar 

  • Ndamukong I, Abdallat A, Thurow C, Fode B, Zander M, Weigel R, Gatz C (2007) SA-inducible Arabidopsis glutaredoxin interacts with TGA factors and suppresses JA-responsive PDF1.2 transcription. Plant J 50:128–139

    CAS  PubMed  Google Scholar 

  • Nikiforova V, Freitag J, Kempa S, Adamik M, Hesse H, Hoefgen R (2003) Transcriptome analysis of sulfur depletion in Arabidopsis thaliana: interlacing of biosynthetic pathways provides response specificity. Plant J 33:633–650

    CAS  PubMed  Google Scholar 

  • Nikiforova VJ, Gakiere B, Kempa S, Adamik M, Willmitzer L, Hesse H, Hoefgen R (2004) Towards dissecting nutrient metabolism in plants: a systems biology case study on sulphur metabolism. J Exp Bot 55:1861–1870

    CAS  PubMed  Google Scholar 

  • Nikiforova VJ, Kopka J, Tolstikov V, Fiehn O, Hopkins L, Hawkesford MJ, Hesse H, Hoefgen R (2005) Systems rebalancing of metabolism in response to sulfur deprivation, as revealed by metabolome analysis of Arabidopsis plants. Plant Physiol 138:304–318

    CAS  PubMed  Google Scholar 

  • Noji M, Inoue K, Kimura N, Gouda A, Saito K (1998) Isoform-dependent differences in feedback regulation and subcellular localization of serine acetyltransferase involved in cysteine biosynthesis from Arabidopsis thaliana. J Biol Chem 273:32739–32745

    CAS  PubMed  Google Scholar 

  • Ohkama-Ohtsu N, Kasajima I, Fujiwara T, Naito S (2004) Isolation and characterization of an Arabidopsis mutant that overaccumulates O-acetyl-L-Ser. Plant Physiol 136:3209–3222

    CAS  PubMed  Google Scholar 

  • Ohkama-Ohtsu N, Zhao P, Xiang C, Oliver D (2007a) Glutathione conjugates in the vacuole are degraded by γ-glutamyl transpeptidase GGT3 in Arabidopsis. Plant J 49:878–888

    CAS  PubMed  Google Scholar 

  • Ohkama-Ohtsu N, Oikawa A, Zhao P, Xiang C, Saito K, Oliver DJ (2008) A γ-glutamyl transpeptidase-independent pathway of glutathione catabolism to glutamate via 5-oxoproline in Arabidopsis. Plant Physiol 148:1603–1613

    CAS  PubMed  Google Scholar 

  • Ohkama-Ohtsu N, Radwan S, Peterson A, Zhao P, Badr A, Xiang C, Oliver D (2007b) Characterization of the extracellular γ-glutamyl transpeptidases, GGT1 and GGT2, in Arabidopsis. Plant J 49:865–877

    CAS  PubMed  Google Scholar 

  • Palmieri L, Arrigoni R, Blanco E, Carrari F, Zanor MI, Studart-Guimaraes C, Fernie AR, Palmieri F (2006) Molecular identification of an Arabidopsis S-adenosylmethionine transporter. Analysis of organ distribution, bacterial expression, reconstitution into liposomes, and functional characterization. Plant Physiol 142:855–865

    CAS  PubMed  Google Scholar 

  • Pant BD, Musialak-Lange M, Nuc P, May P, Buhtz A, Kehr J, Walther D, Scheible WR (2009) Identification of nutrientresponsive Arabidopsis and rapeseed microRNAs by comprehensive real-time polymerase chain reaction profiling and small RNA sequencing. Plant Physiol 150:1541–1555

    PubMed  Google Scholar 

  • Papenbrock J, Riemenschneider A, Kamp A, Schulz-Vogt HN, Schmidt A (2007) Characterization of cysteine-degrading and H2S-releasing enzymes of higher plants – from the field to the test tube and back. Plant Biol 9:582–588

    CAS  PubMed  Google Scholar 

  • Pasternak M, Lim B, Wirtz M, Hell R, Cobbett CS, Meyer AJ (2008) Restricting glutathione biosynthesis to the cytosol is sufficient for normal plant development. Plant J 53:999–1012

    CAS  PubMed  Google Scholar 

  • Patron NJ, Durnford DG, Kopriva S (2008) Sulfate assimilation in eukaryotes: fusions, relocations and lateral transfers. BMC Evol Biol 8:39

    PubMed  Google Scholar 

  • Pe'er I, Felder C, Man O, Silman I, Sussman J, Beckmann J (2004) Proteomic signatures: amino acid and oligopeptide compositions differentiate among phyla. Proteins 54:20–40

    PubMed  Google Scholar 

  • Pilon-Smits EAH, Hwang S, Mel Lytle C, Zhu Y, Tai JC, Bravo RC, Chen Y, Leustek T, Terry N (1999) Overexpression of ATP sulfurylase in Indian mustard leads to increased selenate uptake, reduction, and tolerance. Plant Physiol 119:123–132

    CAS  PubMed  Google Scholar 

  • Pimenta JM, Kaneta T, Larondelle Y, Dohmae N, Kamiya Y (1998) S-Adenosyl-L-methionine:L-methionine S-methyltransferase from germinating barley. Purification and lcalization. Plant Physiol 118:431–438

    CAS  PubMed  Google Scholar 

  • Ranocha P, Bourgis F, Ziemak MJ, Rhodes D, Gage DA, Hanson AD (2000) Characterization and functional expression of cDNAs encoding methionine-sensitive and -insensitive homocysteine S-methyltransferases from Arabidopsis. J Biol Chem 275:15962–15968

    CAS  PubMed  Google Scholar 

  • Rausch T, Wachter A (2005) Sulfur metabolism: a versatile platform for launching defence operations. Trends Plant Sci 10:503–509

    CAS  PubMed  Google Scholar 

  • Ravanel S, Block MA, Rippert P, Jabrin S, Curien G, Rebeille F, Douce R (2004) Methionine metabolism in plants: chloroplasts are autonomous for de novo methionine synthesis and can import S-adenosylmethionine from the cytosol. J Biol Chem 279:22548–22557

    CAS  PubMed  Google Scholar 

  • Rea P (2007) Plant ATP-binding cassette transporters. Annu Rev Plant Biol 58:347–375

    CAS  PubMed  Google Scholar 

  • Rebeille F, Jabrin S, Bligny R, Loizeau K, Gambonnet B, Van Wilder V, Douce R, Ravanel S (2006) Methionine catabolism in Arabidopsis cells is initiated by a γ-cleavage process and leads to S-methylcysteine and isoleucine syntheses. PNAS 103:15687–15692

    CAS  PubMed  Google Scholar 

  • Rennenberg H (1976) Glutathione in conditioned media of tobacco suspension cultures. Phytochem 15:1433–1434

    CAS  Google Scholar 

  • Rennenberg H, Schmitz K, Bergmann L (1979) Long distance transport of sulfur in Nicotiana tabacum. Planta 176:68–74

    Google Scholar 

  • Rinalducci S, Murgiano L, Zolla L (2008) Redox proteomics: basic principles and future perspectives for the detection of protein oxidation in plants. J Exp Bot 59:3781–3801

    CAS  PubMed  Google Scholar 

  • Robinson D (1994) The responses of plants to non-uniform supplies of nutrients. New Phytol 127:635–674

    CAS  Google Scholar 

  • Rolland N, Droux M, Douce R (1992) Subcellular distribution of O-acetylserine(thiol)lyase in cauliflower (Brassica oleracea L.) inflorescence. Plant Physiol 98:927–935

    CAS  PubMed  Google Scholar 

  • Rotte C, Leustek T (2000) Differential subcellular localization and expression of ATP sulfurylase and 5′-adenylylsulfate reductase during ontogenesis of Arabidopsis leaves indicates that cytosolic and plastid forms of ATP sulfurylase may have specialized functions. Plant Physiol 124:715–724

    CAS  PubMed  Google Scholar 

  • Rouached H, Berthomieu P, El Kassis E, Cathala N, Catherinot V, Labesse G, Davidian JC, Fourcroy P (2005) Structural and functional analysis of the C-terminal STAS (sulfate transporter and anti-sigma antagonist) domain of the Arabidopsis thaliana sulfate transporter SULTR1.2. J Biol Chem 280:15976–15983

    CAS  PubMed  Google Scholar 

  • Rouached H, Wirtz M, Alary R, Hell R, Arpat AB, Davidian J-C, Fourcroy P, Berthomieu P (2008) Differential regulation of the expression of two high-affinity sulfate Transporters, SULTR1.1 and SULTR1.2, in Arabidopsis. Plant Physiol 147:897–911

    CAS  PubMed  Google Scholar 

  • Rouhier N, Lemaire SD, Jacquot J-P (2008) The role of glutathione in photosynthetic organisms: emerging functions for glutaredoxins and glutathionylation. Annu Rev Plant Biol 59:143

    CAS  PubMed  Google Scholar 

  • Ruffet ML, Droux M, Douce R (1994) Purification and kinetic properties of serine acetyltransferase free of O-acetylserine(thiol)lyase from spinach chloroplasts. Plant Physiol 104:597–604

    CAS  PubMed  Google Scholar 

  • Ruffet ML, Lebrun M, Droux M, Douce R (1995) Subcellular distribution of serine acetyltransferase from Pisum sativum and characterization of an Arabidopsis thaliana putative cytosolic isoform. Eur J Biochem 227:500–509

    CAS  PubMed  Google Scholar 

  • Saito K (2004) Sulfur assimilatory metabolism. The long and smelling road. Plant Physiol 136:2443–2450

    CAS  PubMed  Google Scholar 

  • Saito K, Kanda R, Kurosawa M, Murakoshi I (1994a) Overexpression of a plant cysteine synthase gene and biosynthesis of a plant specific metabolite, P-(pyrazol-l-yl)-L-alanine, in Escherichia coli. Can J Chem 72:188–192

    CAS  Google Scholar 

  • Saito K, Kurosawa M, Tatsuguchi K, Takagi Y, Murakoshi I (1994b) Modulation of cysteine biosynthesis in chloroplasts of transgenic tobacco overexpressing cysteine synthase [O-acetylserine(thiol)-lyase]. Plant Physiol 106:887–895

    CAS  PubMed  Google Scholar 

  • Schachtman DP, Shin R (2007) Nutrient sensing and signaling: NPKS. Annu Rev Plant Biol 58:47–69

    CAS  PubMed  Google Scholar 

  • Schiffmann S, Schwenn JD (1994) APS-sulfotransferase activity is identical to higher plant APS-kinase (EC 2.7.1.25). FEBS Lett 355:229–232

    CAS  PubMed  Google Scholar 

  • Schmidt A (1973) Sulfate reduction in a cell-free system of Chlorella. The ferredoxin dependent reduction of a protein-bound intermediate by a thiosulfonate reductase. Arch Mikrobiol 93:29–52

    CAS  PubMed  Google Scholar 

  • Schmidt A (1975) A sulfotransferase from spinach leaves using adenosine-5′-phosphosulfate. Planta 124:267–275

    CAS  Google Scholar 

  • Schmidt A (1976) The adenosine-5′-phosphosulfate sulfotransferase from spinach (Spinacea oleracea L.). Stabilization, partial purification, and properties. Planta 130:257–263

    CAS  Google Scholar 

  • Schmidt A, Jäger K (1992) Open questions about sulfur metabolism in plants. Annu Rev Plant Physiol Plant Mol Biol 43:325–349

    CAS  Google Scholar 

  • Schmidt A, Abrams WR, Schiff JA (1974) Reduction of adenosine 5′-phosphosulfate to cysteine in extracts from Chlorella and mutants blocked for sulfate reduction. Eur J Biochem 47:423–434

    CAS  PubMed  Google Scholar 

  • Schwenn JD (1989) Sulphate assimilation in higher plants: a thioredoxin-dependent PAPS-reductase from spinach leaves. Z. Naturforsch 44c, 504–508

    Google Scholar 

  • Schwenn JD, Kemena A (1984) Expression of the plant sulphite reductase in cell suspension cultures from Catharanthus roseus L. Planta 160:151–158

    CAS  Google Scholar 

  • Sekine K, Hase T, Sato N (2002) Reversible DNA compaction by sulfite reductase regulates transcriptional activity of chloroplast nucleoids. J Biol Chem 277:24399–24404

    CAS  PubMed  Google Scholar 

  • Setya A, Murillo M, Leustek T (1996) Sulfate reduction in higher plants: molecular evidence for a novel 5′-adenylylsulfate reductase. Proc Natl Acad Sci USA 93:13383–13388

    CAS  PubMed  Google Scholar 

  • Shen B, Li C, Tarczynski MC (2002) High free-methionine and decreased lignin content result from a mutation in the Arabidopsis S-adenosyl-L-methionine synthetase 3 gene. Plant J 29:371–380

    CAS  PubMed  Google Scholar 

  • Shibagaki N, Grossman AR (2004) Probing the function of STAS domains of the Arabidopsis sulfate transporters. J Biol Chem 279:30791–30799

    CAS  PubMed  Google Scholar 

  • Shibagaki N, Rose A, McDermott JP, Fujiwara T, Hayashi H, Yoneyama T, Davies JP (2002) Selenate-resistant mutants of Arabidopsis thaliana identify Sultr1;2, a sulfate transporter required for efficient transport of sulfate into roots. Plant J 29:475–486

    CAS  PubMed  Google Scholar 

  • Sirko A, Blaszczyk A, Liszewska F (2004) Overproduction of SAT and/or OASTL in transgenic plants: a survey of effects. J Exp Bot 55:1881–1888

    CAS  PubMed  Google Scholar 

  • Smith FW, Diatlof E (2005) Sulfate transport processes in plants. In: Saito K, De Kok LJ, Stulen I, Hawkesford MJ, Schnug E, Sirko A, Rennenberg H (eds) Sulfur transport and assimilation in plants in the post genomic era. Backhuys Publishers, Leiden, pp 3–11

    Google Scholar 

  • Stiller I, Dancs G, Hesse H, Hoefgen R, Banfalvi Z (2007) Improving the nutritive value of tubers: elevation of cysteine and glutathione contents in the potato cultivar White Lady by marker-free transformation. J Biotechnol 128:335–343

    CAS  PubMed  Google Scholar 

  • Suter M, von Ballmoos P, Kopriva S, den Camp RO, Schaller J, Kuhlemeier C, Schurmann P, Brunold C (2000) Adenosine 5′-phosphosulfate sulfotransferase and adenosine 5′-phosphosulfate reductase are identical enzymes. J Biol Chem 275:930–936

    CAS  PubMed  Google Scholar 

  • Swamy U, Wang M, Tripathy J, Kim S, Hirasawa M, Knaff D, Allen J (2005) Structure of spinach nitrite reductase: implications for multi-electron reactions by the iron-sulfur:siroheme cofactor. Biochem 44:16054–16063

    CAS  Google Scholar 

  • Tabe L, Hagan N, Higgins T (2002) Plasticity of seed protein composition in response to nitrogen and sulfur availability. Curr Opin Plant Biol 5:212–217

    CAS  PubMed  Google Scholar 

  • Tada Y, Spoel SH, Pajerowska-Mukhtar K, Mou Z, Song J, Wang C, Zuo J, Dong X (2008) Plant immunity requires conformational charges of NPR1 via S-nitrosylation and thioredoxins. Science 321:952–956

    CAS  PubMed  Google Scholar 

  • Takahashi H, Asanuma W, Saito K (1999) Cloning of an Arabidopsis cDNA encoding a chloroplast localizing sulphate transporter isoform. J Exp Bot 50:1713–1714

    CAS  Google Scholar 

  • Takahashi H, Watanabe-Takahashi A, Smith FW, Blake-Kalff M, Hawkesford MJ, Saito K (2000) The roles of three functional sulphate transporters involved in uptake and translocation of sulphate in Arabidopsis thaliana. Plant J 23:171–182

    CAS  PubMed  Google Scholar 

  • Tejada-Jimenez M, Llamas A, Sanz-Luque E, Galvan A, Fernandez E (2007) A high-affinity molybdate transporter in eukaryotes. Proc Nat Acad Sci USA 104:20126–20130

    CAS  PubMed  Google Scholar 

  • Tennstedt P, Peisker D, Bottcher 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

    CAS  PubMed  Google Scholar 

  • Tomatsu H, Takano J, Takahashi H, Watanabe-Takahashi A, Shibagaki N, Fujiwara T (2007) An Arabidopsis thaliana high-affinity molybdate transporter required for efficient uptake of molybdate from soil. Proc Nat Acad Sci USA 104:18807–18812

    CAS  PubMed  Google Scholar 

  • Tsakraklides G, Martin M, Chalam R, Tarczynski MC, Schmidt A, Leustek T (2002) Sulfate reduction is increased in transgenic Arabidopsis thaliana expressing 5′-adenylylsulfate reductase from Pseudomonas aeruginosa. Plant J 32:879–889

    CAS  PubMed  Google Scholar 

  • Vauclare P, Kopriva S, Fell D, Suter M, Sticher L, von Ballmoos P, Krahenbühl U, den Camp RO, Brunold C (2002) Flux control of sulphate assimilation in Arabidopsis thaliana: adenosine 5′-phosphosulphate reductase is more susceptible than ATP sulphurylase to negative control by thiols. Plant J 31:729–740

    CAS  PubMed  Google Scholar 

  • Walker C, Boothe EJ (2003) Sulphur nutrition and oilseed quality. In: Abrol YP, Ahmad A (eds) Sulphur in plants. Kluwer Academic Publishers, Dordrecht, pp 323–340

    Google Scholar 

  • Wang X, Stumpf DK, Larkins BA (2001) Aspartate kinase 2. A candidate gene of a quantitative trait locus influencing free amino acid content in maize endosperm. Plant Physiol 125:1778–1787

    CAS  PubMed  Google Scholar 

  • Watanabe M, Kusano M, Oikawa A, Fukushima A, Noji M, Saito K (2008a) Physiological roles of the β-substituted alanine synthase gene family in Arabidopsis. Plant Physiol 146:310–320

    CAS  PubMed  Google Scholar 

  • Watanabe M, Mochida K, Kato T, Tabata S, Yoshimoto N, Noji M, Saito K (2008b) Comparative genomics and reverse genetics analysis reveal indispensable functions of the serine acetyltransferase gene family in Arabidopsis. Plant Cell 20:2484–2496

    CAS  PubMed  Google Scholar 

  • Wawrzynska A, Lewandowska M, Hawkesford MJ, Sirko A (2005) Using a suppression subtractive library-based approach to identify tobacco genes regulated in response to short-term sulphur deficit. J Exp Bot 56:1575–1590

    CAS  PubMed  Google Scholar 

  • Wirtz M, Droux M (2005) Synthesis of the sulfur amino acids: cysteine and methionine. Photosynth Res 86:345–362

    CAS  PubMed  Google Scholar 

  • Wirtz M, Hell R (2006) Functional analysis of the cysteine synthase protein complex from plants: structural, biochemical and regulatory properties. J Plant Physiol 163:273–286

    CAS  PubMed  Google Scholar 

  • Wirtz M, Hell R (2007) Dominant-negative modification reveals the regulatory function of the multimeric cysteine synthase protein complex in transgenic tobacco. Plant Cell 19:625–639

    CAS  PubMed  Google Scholar 

  • Wirtz M, Berkowitz O, Droux M, Hell R (2001) The cysteine synthase complex from plants. Mitochondrial serine acetyltransferase from Arabidopsis thaliana carries a bifunctional domain for catalysis and protein-protein interaction. Eur J Biochem 268:686–693

    CAS  PubMed  Google Scholar 

  • Yang Y, Yuan JS, Ross J, Noel JP, Pichersky E, Chen F (2006) An Arabidopsis thaliana methyltransferase capable of methylating farnesoic acid. Arch Biochem Biophys 448:123–132

    CAS  PubMed  Google Scholar 

  • Yonekura-Sakakibara K, Onda Y, Ashikari T, Tanaka Y, Kusumi T, Hase T (2000) Analysis of reductant supply systems for ferredoxin-dependent sulfite reductase in photosynthetic and nonphotosynthetic organs of maize. Plant Physiol 122:887–894

    CAS  PubMed  Google Scholar 

  • Yoshimoto N, Takahashi H, Smith FW, Yamaya T, Saito K (2002) Two distinct high-affinity sulfate transporters with different inducibilities mediate uptake of sulfate in Arabidopsis roots. Plant J 29:465–473

    CAS  PubMed  Google Scholar 

  • Yoshimoto N, Inoue E, Saito K, Yamaya T, Takahashi H (2003) Phloem-localizing sulfate transporter, Sultr1;3, mediates re-distribution of sulfur from source to sink organs in Arabidopsis. Plant Physiol 131:1511–1517

    CAS  PubMed  Google Scholar 

  • Zeh M, Casazza AP, Kreft O, Roessner U, Bieberich K, Willmitzer L, Hoefgen R, Hesse H (2001) Antisense inhibition of threonine synthase leads to high methionine content in transgenic potato plants. Plant Physiol 127:792–802

    CAS  PubMed  Google Scholar 

  • Zhang M-Y, Bourbouloux A, Cagnac O, Srikanth CV, Rentsch D, Bachhawat AK, Delrot S (2004) A novel family of transporters mediating the transport of glutathione derivatives in plants. Plant Physiol 134:482–491

    CAS  PubMed  Google Scholar 

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Hell, R., Khan, M.S., Wirtz, M. (2010). Cellular Biology of Sulfur and Its Functions in Plants. In: Hell, R., Mendel, RR. (eds) Cell Biology of Metals and Nutrients. Plant Cell Monographs, vol 17. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-10613-2_11

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