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Cellular Biology of Sulfur and Its Functions in Plants

  • Rüdiger HellEmail author
  • M. Sayyar Khan
  • Markus Wirtz
Chapter
Part of the Plant Cell Monographs book series (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.

Keywords

Sulfate Transporter Sulfate Uptake Sulfate Deficiency Sulfate Starvation Methionine Synthesis 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. 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 60:892–896PubMedGoogle Scholar
  2. 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 7:153–156PubMedGoogle Scholar
  3. 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 12:275–283PubMedGoogle Scholar
  4. Amtmann A, Blatt MR (2009) Regulation of macronutrient transport. New Phytol 181:35–52PubMedGoogle Scholar
  5. 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 125:95–105Google Scholar
  6. Balk J, Lobreaux S (2005) Biogenesis of iron-sulfur proteins in plants. Trends Plant Sci 10:324–331PubMedGoogle Scholar
  7. 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 123:101–110PubMedGoogle Scholar
  8. 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:e1000004PubMedGoogle Scholar
  9. 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 282:65–71Google Scholar
  10. Bell CS, Cram WJ, Clarkson DT (1994) Compartmental analysis of 35SO42− exchange kinetics in roots and leaves of a tropical legume Macroptilium atropurpureum cv. Siratro. J Exp Bot 45:879–886Google Scholar
  11. 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 185–200Google Scholar
  12. 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 277:30629–30634PubMedGoogle Scholar
  13. 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 95:8404–8409PubMedGoogle Scholar
  14. 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 182:135–142PubMedGoogle Scholar
  15. 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 40:9040–9048PubMedGoogle Scholar
  16. 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 118:1337–1344PubMedGoogle Scholar
  17. Blaszczyk A, Brodzik R, Sirko A (1999) Increased resistance to oxidative stress in transgenic tobacco plants overexpressing bacterial serine acetyltransferase. Plant J 20:237–243PubMedGoogle Scholar
  18. 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 55:2305–2312PubMedGoogle Scholar
  19. 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 49:740–749PubMedGoogle Scholar
  20. Bogdanova N, Hell R (1997) Cysteine synthesis in plants: protein-protein interactions of serine acetyltransferase from Arabidopsis thaliana. Plant J 11:251–262PubMedGoogle Scholar
  21. 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 39:527–537PubMedGoogle Scholar
  22. 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 280:38803–38813PubMedGoogle Scholar
  23. 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 11:1485–1498PubMedGoogle Scholar
  24. Brunold C, Suter M (1990) Adenosine-5-phosphosulfate sulfotransferase. In Methods Plant Biochem., P. Lea, ed (London: Academic Press), pp. 339–343Google Scholar
  25. Brunold C, Rennenberg H (1997) Regulation of sulfur metabolism in plants: first molecular approaches. Progr Bot 58:164–186Google Scholar
  26. Buchner P, Takahashi H, Hawkesford MJ (2004a) Plant sulphate transporters: co-ordination of uptake, intracellular and long-distance transport. J Exp Bot 55:1765–1773PubMedGoogle Scholar
  27. 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 136:3396–3408PubMedGoogle Scholar
  28. 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 116:1315–1322PubMedGoogle Scholar
  29. 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 205–226Google Scholar
  30. Burstenbinder K, Rzewuski G, Wirtz M, Hell R, Sauter M (2007) The role of methionine recycling for ethylene synthesis in Arabidopsis. Plant J 49:238–249PubMedGoogle Scholar
  31. Cagnac O, Bourbouloux A, Chakrabarty D, Zhang M-Y, Delrot S (2004) AtOPT6 transports glutathione derivatives and is induced by primisulfuron. Plant Physiol 135:1378–1387PubMedGoogle Scholar
  32. 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 141:446–455PubMedGoogle Scholar
  33. 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 39:835–845PubMedGoogle Scholar
  34. Cantoni GL (1975) Biological methylation: selected aspects. Annu Rev Biochem 44:435–451PubMedGoogle Scholar
  35. Chen S, Petersen BL, Olsen CE, Schulz A, Halkier BA (2001) Long-distance phloem transport of glucosinolates in Arabidopsis. Plant Physiol 127:194–201PubMedGoogle Scholar
  36. 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 278:46869–46877PubMedGoogle Scholar
  37. 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 100:10225–10230PubMedGoogle Scholar
  38. 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 286:1371–1374PubMedGoogle Scholar
  39. Clarkson DT, Smith FW, Vanden Berg PJ (1983) Regulation of sulphate transport in a tropical legume, Macroptilium atropurpureum, cv. Siratro. J Exp Bot 34:1463–1483Google Scholar
  40. Cooper RM, Williams JS (2004) Elemental sulphur as an induced antifungal substance in plant defence. J Exp Bot 55:1947–1953PubMedGoogle Scholar
  41. Crane BR, Siegel LM, Getzoff ED (1995) Sulfite reductase structure at 1.6 Å evolution and catalysis for reduction of inorganic anions. Science 270:59–67PubMedGoogle Scholar
  42. Curien G, Job D, Douce R, Dumas R (1998) Allosteric activation of Arabidopsis threonine synthase by S-adenosylmethionine. Biochemistry 37:13212–13221PubMedGoogle Scholar
  43. 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 280:41178–41183PubMedGoogle Scholar
  44. Curien G, Laurencin M, Robert-Genthon M, Dumas R (2007) Allosteric monofunctional aspartate kinases from Arabidopsis. FEBS J 274:164–176PubMedGoogle Scholar
  45. 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 1–16Google Scholar
  46. 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 60:1207–1218PubMedGoogle Scholar
  47. 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 105:16386–16391PubMedGoogle Scholar
  48. Droux M (2003) Plant serine acetyltransferase: new insights for regulation of sulphur metabolism in plant cells. Plant Physiol Biochem 41:619–627Google Scholar
  49. Droux M (2004) Sulfur assimilation and the role of sulfur in plant metabolism: a survey. Photosynth Res 79:331–348PubMedGoogle Scholar
  50. 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 255:235–245PubMedGoogle Scholar
  51. 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 60:3239–3253PubMedGoogle Scholar
  52. Falkowski PG (2006) Evolution: tracing oxygen's imprint on earth's metabolic evolution. Science 311:1724–1725PubMedGoogle Scholar
  53. Feldman-Salit A, Wirtz M, Hell R, Wade RC (2009) A mechanistic model of the cysteine synthase complex. J Mol Biol 386:37–59PubMedGoogle Scholar
  54. Ferreira RM, Teixeira AR (1992) Sulfur starvation in Lemna leads to degradation of ribulose-bisphosphate carboxylase without plant death. J Biol Chem 267:7253–7257PubMedGoogle Scholar
  55. 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 181:115–126PubMedGoogle Scholar
  56. Fitzpatrick KL, Tyerman SD, Kaiser BN (2008) Molybdate transport through the plant sulfate transporter SHST1. FEBS Lett 582:1508–1513PubMedGoogle Scholar
  57. Foyer CH, Noctor G (2005) Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 17:1866–1875PubMedGoogle Scholar
  58. Foyer CH, Bloom AJ, Queval G, Noctor G (2009a) Photorespiratory metabolism: genes, mutants, energetics, and redox signaling. Annu Rev Plant Biol 60:455–484PubMedGoogle Scholar
  59. Foyer CH, Noctor G, Buchanan B, Dietz KJ, Pfannschmidt T (2009b) Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxid Redox Signal 11:861–905PubMedGoogle Scholar
  60. 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 18:3647–3655PubMedGoogle Scholar
  61. 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 16:2176–2191PubMedGoogle Scholar
  62. Fujiwara T, Nambara E, Yamagishi K, Goto DB, Naito S (2002) Storage proteins. The Arabidopsis Book, 1–12Google Scholar
  63. Fukuda H, Hirakawa Y, Sawa S (2007) Peptide signaling in vascular development. Curr Opin Plant Biol 10:477–482PubMedGoogle Scholar
  64. 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 5:575–577PubMedGoogle Scholar
  65. 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 50:886–901PubMedGoogle Scholar
  66. 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 115:1231–1239PubMedGoogle Scholar
  67. Giordano M, Norici A, Hell R (2005) Sulfur and phytoplankton: acquisition, metabolism and impact on the environment. New Phytol 166:371–382PubMedGoogle Scholar
  68. Glawischnig E (2007) Camalexin. Phytochem 68:401–406Google Scholar
  69. 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 77:89–95PubMedGoogle Scholar
  70. 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 48:232–242PubMedGoogle Scholar
  71. Grill E, Winnacker EL, Zenk MH (1985) Phytochelatins: the princial heavy-metal complexing peptides of higher plants. Science 230:674–676PubMedGoogle Scholar
  72. 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 JGoogle Scholar
  73. 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 180:262–271Google Scholar
  74. Grzam A, Martin M, Hell R, Meyer A (2007) γ-Glutamyl transpeptidase GGT4 initiates vacuolar degradation of glutathione S-conjugates in Arabidopsis. FEBS Lett 581:3131–3138PubMedGoogle Scholar
  75. 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 580:6384–6390PubMedGoogle Scholar
  76. 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 93:13377–13382PubMedGoogle Scholar
  77. 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 148:1055–1067PubMedGoogle Scholar
  78. 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 128:454–462PubMedGoogle Scholar
  79. 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 45:955–967PubMedGoogle Scholar
  80. Hacham Y, Song L, Schuster G, Amir R (2007) Lysine enhances methionine content by modulating the expression of S-adenosylmethionine synthase. Plant J 51:850–861PubMedGoogle Scholar
  81. Halkier B, Gershenzon J (2006) Biology and biochemistry of glucosinolates. Annu Rev Plant Biol 57:303–333PubMedGoogle Scholar
  82. 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 22:335–343PubMedGoogle Scholar
  83. 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 116:1307–1313PubMedGoogle Scholar
  84. Hawkesford MJ (2003) Transporter gene families in plants: the sulphate transporter gene family redundancy or specialization? Physiol Plant 117:155–163Google Scholar
  85. 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 17–32Google Scholar
  86. Hawkesford MJ, De Kok LJ (2006) Managing sulphur metabolism in plants. Plant Cell Environ 29:382–395PubMedGoogle Scholar
  87. 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 20:168–185PubMedGoogle Scholar
  88. Hell R (1997) Molecular physiology of plant sulfur metabolism. Planta 202:138–148PubMedGoogle Scholar
  89. Hell R, Bergmann L (1988) Glutathione synthetase in tobacco suspension cultures: catalytic properties and localization. Physiol Plant 72:70–76Google Scholar
  90. Hell R, Bergmann L (1990) γ-Glutamylcysteine synthetase in higher plants: catalytic properties and subcellular localization. Planta 180:603–612Google Scholar
  91. Hell R, Hillebrand H (2001) Plant concepts for mineral acquisition and allocation. Curr Opin Biotechnol 12:161–168PubMedGoogle Scholar
  92. 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 22:245–257PubMedGoogle Scholar
  93. 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 111–130Google Scholar
  94. 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 124:461–473PubMedGoogle Scholar
  95. Hesse H, Kreft O, Maimann S, Zeh M, Hoefgen R (2004) Current understanding of the regulation of methionine biosynthesis in plants. J Exp Bot 55:1799–1808PubMedGoogle Scholar
  96. 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 48:557–571PubMedGoogle Scholar
  97. 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 33:651–663PubMedGoogle Scholar
  98. Hirai MY, Saito K (2008) Analysis of systemic sulfur metabolism in plants using integrated ‘-omics’ strategies. Mol Biosyst 4:967–973PubMedGoogle Scholar
  99. 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 101:10205–10210PubMedGoogle Scholar
  100. 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 104:6478–6483PubMedGoogle Scholar
  101. 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 47:300–305PubMedGoogle Scholar
  102. Hoefgen R, Nikiforova VJ (2008) Metabolomics integrated with transcriptomics: assessing systems response to sulfur-deficiency stress. Physiol Plant 132:190–198PubMedGoogle Scholar
  103. 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 138:433–440PubMedGoogle Scholar
  104. 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 281:27557–27565PubMedGoogle Scholar
  105. 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 7:200–209PubMedGoogle Scholar
  106. 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 59:3675–3689PubMedGoogle Scholar
  107. 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 104:881–887PubMedGoogle Scholar
  108. Jez JM, Cahoon RE, Chen S (2004) Arabidopsis thaliana glutamate-cysteine ligase: functional properties, kinetic mechanism, and regulation of activity. J Biol Chem 279:33463–33470PubMedGoogle Scholar
  109. 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 278:10291–10296PubMedGoogle Scholar
  110. 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 129:351–363Google Scholar
  111. 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 136:4198–4204PubMedGoogle Scholar
  112. 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 16:2693–2704PubMedGoogle Scholar
  113. 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 137:220–230PubMedGoogle Scholar
  114. 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 57:313–321PubMedGoogle Scholar
  115. 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 209:282–289PubMedGoogle Scholar
  116. 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 131:123–131Google Scholar
  117. 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 150:257–271PubMedGoogle Scholar
  118. 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 6:105–112PubMedGoogle Scholar
  119. 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 131:1808–1815PubMedGoogle Scholar
  120. Kopriva S (2006) Regulation of sulfate assimilation in Arabidopsis and beyond. Ann Bot 97:479–495PubMedGoogle Scholar
  121. Kopriva S, Koprivova A (2004) Plant adenosine 5′-phosphosulphate reductase: the past, the present, and the future. J Exp Bot 55:1775–1783PubMedGoogle Scholar
  122. Kopriva S, Koprivova A (2005) Sulfate assimilation and glutathione synthesis in C4 plants. Photosynth Res 86:363–372PubMedGoogle Scholar
  123. Kopriva S, Wiedemann G, Reski R (2007a) Sulfate assimilation in basal land plants – what does genomic sequencing tell us? Plant Biol 9:556–564PubMedGoogle Scholar
  124. 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 282:22930–22938PubMedGoogle Scholar
  125. 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 277:32195–32201PubMedGoogle Scholar
  126. Kredich NM, Tomkins GM (1966) The enzymic synthesis of L-cysteine in Escherichia coli and Salmonella typhimurium. J Biol Chem 241:4955–4965PubMedGoogle Scholar
  127. Kredich NM, Becker MA, Tomkins GM (1969) Purification and characterization of cysteine synthetase, a bifunctional protein complex, from Salmonella typhimurium. J Biol Chem 244:2428–2439PubMedGoogle Scholar
  128. Krueger RJ, Siegel LM (1982) Evidence for siroheme-Fe4S4 interaction in spinach ferredoxin-sulfite reductase. Biochemistry 21:2905–2909PubMedGoogle Scholar
  129. Kruse C, Jost R, Hillebrand H, Hell R (2005) Sulfur-rich proteins and their agrobiotechnological potential for resistance to plant pathogens. FAL Agricult Res 283:73–80Google Scholar
  130. 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 9:608–619PubMedGoogle Scholar
  131. 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 284:10268–10275PubMedGoogle Scholar
  132. 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 13:89–100PubMedGoogle Scholar
  133. 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 112:659–667PubMedGoogle Scholar
  134. 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 30:95–106PubMedGoogle Scholar
  135. 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 263:212–221PubMedGoogle Scholar
  136. Lappartient AG, Touraine B (1996) Demand-driven control of root ATP sulfurylase activity and SO42- uptake in intact Canola. Plant Physiol 111:147–157PubMedGoogle Scholar
  137. 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 18:89–95PubMedGoogle Scholar
  138. Lass B, Ullrich-Eberius CI (1983) Evidence for proton/sulfate cotransport and its kinetics in Lemna gibba G1. Planta 161:53–60Google Scholar
  139. 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 2:390–406PubMedGoogle Scholar
  140. Leustek T (1996) Molecular genetics of sulfate assimilation in plants. Physiol Plant 97:411–419Google Scholar
  141. 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 51:141–165Google Scholar
  142. Lewandowska M, Sirko A (2008) Recent advances in understanding plant response to sulfur-deficiency stress. Acta Biochim Pol 55:457–471PubMedGoogle Scholar
  143. 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 141:288–298PubMedGoogle Scholar
  144. Lindermayr C, Saalbach G, Durner J (2005) Proteomic identification of S-nitrosylated proteins in Arabidopsis. Plant Physiol 137:921–930PubMedGoogle Scholar
  145. 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 281:27405–27415PubMedGoogle Scholar
  146. 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 271:12227–12233PubMedGoogle Scholar
  147. 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 145:491–503PubMedGoogle Scholar
  148. 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 147:562–572PubMedGoogle Scholar
  149. 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 39:896–900PubMedGoogle Scholar
  150. Lu SC (2000) S-Adenosylmethionine. Int J Biochem Cell Biol 32:391–395PubMedGoogle Scholar
  151. Lunn JE, Droux M, Martin J, Douce R (1990) Localization of ATP-sulfurylase and O-acetylserine(thiol)lyase in spinach leaves. Plant Physiol 94:1345–1352PubMedGoogle Scholar
  152. 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 148:2021–2049PubMedGoogle Scholar
  153. Martin MN, Tarczynski MC, Shen B, Leustek T (2005) The role of 5′-adenylylsulfate reductase in controlling sulfate reduction in plants. Photosynth Res 86:1–15Google Scholar
  154. 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 144:1715–1732PubMedGoogle Scholar
  155. 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 55:193–204PubMedGoogle Scholar
  156. 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 106:9109–9114PubMedGoogle Scholar
  157. 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 132:597–605PubMedGoogle Scholar
  158. 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 45:340–345PubMedGoogle Scholar
  159. 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 18:3235–3251PubMedGoogle Scholar
  160. 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 42:305–314PubMedGoogle Scholar
  161. 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 281:5188–5196PubMedGoogle Scholar
  162. 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 18:1681–1692PubMedGoogle Scholar
  163. 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 49:649–667Google Scholar
  164. Meister A (1995) Glutathione biosynthesis and its inhibition. Methods Enzymol 252:26–30PubMedGoogle Scholar
  165. Melis A, Chen H-C (2005) Chloroplast sulfate transport in green algae – genes, proteins and effects. Photosynth Res 86:299–307PubMedGoogle Scholar
  166. Meyer AJ (2008) The integration of glutathione homeostasis and redox signaling. J Plant Physiol 165:1390–1403PubMedGoogle Scholar
  167. Meyer AJ, Fricker MD (2002) Control of demand-driven biosynthesis of glutathione in green Arabidopsis suspension culture cells. Plant Physiol 130:1927–1937PubMedGoogle Scholar
  168. Meyer AJ, Hell R (2005) Glutathione homeostasis and redox-regulation by sulfhydryl groups. Photosynth Res 86:435–457PubMedGoogle Scholar
  169. 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 161–184Google Scholar
  170. 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 52:973–986PubMedGoogle Scholar
  171. Meyer Y, Siala W, Bashandy T, Riondet C, Vignols F, Reichheld JP (2008) Glutaredoxins and thioredoxins in plants. Biochim Biophys Acta 1783:589–600PubMedGoogle Scholar
  172. Meyers DM, Ahmad S (1991) Link between L-3-cyanoalanine synthase activity and differential cyanide sensitivity of insects. Biochim Biophys Acta 1075:195–197PubMedGoogle Scholar
  173. Miller AJ, Shen Q, Xu G (2009) Freeways in the plant: transporters for N, P and S and their regulation. Curr Opin Plant Biol 12:284–290PubMedGoogle Scholar
  174. 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 21:910–927PubMedGoogle Scholar
  175. 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 42:125–127PubMedGoogle Scholar
  176. Nakayama M, Akashi T, Hase T (2000) Plant sulfite reductase: molecular structure, catalytic function and interaction with ferredoxin. J Inorg Biochem 82:27–32PubMedGoogle Scholar
  177. 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 50:128–139PubMedGoogle Scholar
  178. 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 33:633–650PubMedGoogle Scholar
  179. 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 55:1861–1870PubMedGoogle Scholar
  180. 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 138:304–318PubMedGoogle Scholar
  181. 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 273:32739–32745PubMedGoogle Scholar
  182. 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 136:3209–3222PubMedGoogle Scholar
  183. 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 49:878–888PubMedGoogle Scholar
  184. 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 148:1603–1613PubMedGoogle Scholar
  185. 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 49:865–877PubMedGoogle Scholar
  186. 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 142:855–865PubMedGoogle Scholar
  187. 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 150:1541–1555PubMedGoogle Scholar
  188. 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 9:582–588PubMedGoogle Scholar
  189. 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 53:999–1012PubMedGoogle Scholar
  190. Patron NJ, Durnford DG, Kopriva S (2008) Sulfate assimilation in eukaryotes: fusions, relocations and lateral transfers. BMC Evol Biol 8:39PubMedGoogle Scholar
  191. 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 54:20–40PubMedGoogle Scholar
  192. 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 119:123–132PubMedGoogle Scholar
  193. 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 118:431–438PubMedGoogle Scholar
  194. 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 275:15962–15968PubMedGoogle Scholar
  195. Rausch T, Wachter A (2005) Sulfur metabolism: a versatile platform for launching defence operations. Trends Plant Sci 10:503–509PubMedGoogle Scholar
  196. 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 279:22548–22557PubMedGoogle Scholar
  197. Rea P (2007) Plant ATP-binding cassette transporters. Annu Rev Plant Biol 58:347–375PubMedGoogle Scholar
  198. 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 103:15687–15692PubMedGoogle Scholar
  199. Rennenberg H (1976) Glutathione in conditioned media of tobacco suspension cultures. Phytochem 15:1433–1434Google Scholar
  200. Rennenberg H, Schmitz K, Bergmann L (1979) Long distance transport of sulfur in Nicotiana tabacum. Planta 176:68–74Google Scholar
  201. 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 59:3781–3801PubMedGoogle Scholar
  202. Robinson D (1994) The responses of plants to non-uniform supplies of nutrients. New Phytol 127:635–674Google Scholar
  203. Rolland N, Droux M, Douce R (1992) Subcellular distribution of O-acetylserine(thiol)lyase in cauliflower (Brassica oleracea L.) inflorescence. Plant Physiol 98:927–935PubMedGoogle Scholar
  204. 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 124:715–724PubMedGoogle Scholar
  205. 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 280:15976–15983PubMedGoogle Scholar
  206. 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 147:897–911PubMedGoogle Scholar
  207. 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 59:143PubMedGoogle Scholar
  208. 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 104:597–604PubMedGoogle Scholar
  209. 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 227:500–509PubMedGoogle Scholar
  210. Saito K (2004) Sulfur assimilatory metabolism. The long and smelling road. Plant Physiol 136:2443–2450PubMedGoogle Scholar
  211. 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 72:188–192Google Scholar
  212. 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 106:887–895PubMedGoogle Scholar
  213. Schachtman DP, Shin R (2007) Nutrient sensing and signaling: NPKS. Annu Rev Plant Biol 58:47–69PubMedGoogle Scholar
  214. Schiffmann S, Schwenn JD (1994) APS-sulfotransferase activity is identical to higher plant APS-kinase (EC 2.7.1.25). FEBS Lett 355:229–232PubMedGoogle Scholar
  215. 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 93:29–52PubMedGoogle Scholar
  216. Schmidt A (1975) A sulfotransferase from spinach leaves using adenosine-5′-phosphosulfate. Planta 124:267–275Google Scholar
  217. Schmidt A (1976) The adenosine-5′-phosphosulfate sulfotransferase from spinach (Spinacea oleracea L.). Stabilization, partial purification, and properties. Planta 130:257–263Google Scholar
  218. Schmidt A, Jäger K (1992) Open questions about sulfur metabolism in plants. Annu Rev Plant Physiol Plant Mol Biol 43:325–349Google Scholar
  219. 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 47:423–434PubMedGoogle Scholar
  220. Schwenn JD (1989) Sulphate assimilation in higher plants: a thioredoxin-dependent PAPS-reductase from spinach leaves. Z. Naturforsch 44c, 504–508Google Scholar
  221. Schwenn JD, Kemena A (1984) Expression of the plant sulphite reductase in cell suspension cultures from Catharanthus roseus L. Planta 160:151–158Google Scholar
  222. Sekine K, Hase T, Sato N (2002) Reversible DNA compaction by sulfite reductase regulates transcriptional activity of chloroplast nucleoids. J Biol Chem 277:24399–24404PubMedGoogle Scholar
  223. 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 93:13383–13388PubMedGoogle Scholar
  224. 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 29:371–380PubMedGoogle Scholar
  225. Shibagaki N, Grossman AR (2004) Probing the function of STAS domains of the Arabidopsis sulfate transporters. J Biol Chem 279:30791–30799PubMedGoogle Scholar
  226. 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 29:475–486PubMedGoogle Scholar
  227. Sirko A, Blaszczyk A, Liszewska F (2004) Overproduction of SAT and/or OASTL in transgenic plants: a survey of effects. J Exp Bot 55:1881–1888PubMedGoogle Scholar
  228. 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 3–11Google Scholar
  229. 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 128:335–343PubMedGoogle Scholar
  230. 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 275:930–936PubMedGoogle Scholar
  231. 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 44:16054–16063Google Scholar
  232. Tabe L, Hagan N, Higgins T (2002) Plasticity of seed protein composition in response to nitrogen and sulfur availability. Curr Opin Plant Biol 5:212–217PubMedGoogle Scholar
  233. 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 321:952–956PubMedGoogle Scholar
  234. Takahashi H, Asanuma W, Saito K (1999) Cloning of an Arabidopsis cDNA encoding a chloroplast localizing sulphate transporter isoform. J Exp Bot 50:1713–1714Google Scholar
  235. 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 23:171–182PubMedGoogle Scholar
  236. 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 104:20126–20130PubMedGoogle Scholar
  237. 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 149:938–948PubMedGoogle Scholar
  238. 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 104:18807–18812PubMedGoogle Scholar
  239. 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 32:879–889PubMedGoogle Scholar
  240. 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 31:729–740PubMedGoogle Scholar
  241. Walker C, Boothe EJ (2003) Sulphur nutrition and oilseed quality. In: Abrol YP, Ahmad A (eds) Sulphur in plants. Kluwer Academic Publishers, Dordrecht, pp 323–340Google Scholar
  242. 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 125:1778–1787PubMedGoogle Scholar
  243. 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 146:310–320PubMedGoogle Scholar
  244. 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 20:2484–2496PubMedGoogle Scholar
  245. 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 56:1575–1590PubMedGoogle Scholar
  246. Wirtz M, Droux M (2005) Synthesis of the sulfur amino acids: cysteine and methionine. Photosynth Res 86:345–362PubMedGoogle Scholar
  247. Wirtz M, Hell R (2006) Functional analysis of the cysteine synthase protein complex from plants: structural, biochemical and regulatory properties. J Plant Physiol 163:273–286PubMedGoogle Scholar
  248. Wirtz M, Hell R (2007) Dominant-negative modification reveals the regulatory function of the multimeric cysteine synthase protein complex in transgenic tobacco. Plant Cell 19:625–639PubMedGoogle Scholar
  249. 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 268:686–693PubMedGoogle Scholar
  250. 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 448:123–132PubMedGoogle Scholar
  251. 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 122:887–894PubMedGoogle Scholar
  252. 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 29:465–473PubMedGoogle Scholar
  253. 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 131:1511–1517PubMedGoogle Scholar
  254. 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 127:792–802PubMedGoogle Scholar
  255. 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 134:482–491PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2010

Authors and Affiliations

  1. 1.Heidelberg Institute for Plant SciencesUniversity of HeidelbergHeidelbergGermany
  2. 2.Department of Plant Breeding and GeneticsNWFP Agricultural UniversityPeshawarPakistan

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