Sulfur assimilation and the role of sulfur in plant metabolism: A survey

Photosynthesis Research

Volumn 79, Issue 3, 2004, Pages 331-348

  Droux, Michel ^a  

^a BAYER AG   (Germany)

Author keywords

Cysteine; Glutathione; Methionine; O acetylserine; Proteins; Redox state; Regulation; Sulfur metabolism

Indexed keywords

EID: 1642308088     PISSN: 01668595     EISSN: None     Source Type: Journal    
DOI: 10.1023/B:PRES.0000017196.95499.11     Document Type: Review

References (154)

1. Amir R, Hacham Y and Galili G (2002) Cystathionine gamma synthase and threonine synthase operate in concert to regulate carbon flow towards methionine in plants. Trends Plant Sci 7: 153-156
2. Bagarinao T (1992) Sulfide as an environmental factor and toxicant: tolerance and adaptation in aquatic organisms. Aquatic Toxicol 24: 21-62
3. Bateman A, Birney E, Cerruti L, Durbin R, Etwiller L, Eddy SR, Griffiths-Jones S, Howe KL, Marshall M and Sonnhammer EL (2002) The Pfam protein families database. Nucleic Acid Res 30: 276-280
4. Beinert H (2000) A tribute to sulfur. Eur J Biochem 267: 5657-5664
5. Berkowitz O, Wirtz M, Wolf A, Kuhlmann J and 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
6. Bick JA and Leustek T (1998) Plant sulfur metabolism: the reduction of sulfate to sulfite. Curr Opin Plant Biol 1: 240-244
7. Bick JA, Aslund F, Chen Y and 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
8. Bittner F, Oreb M and Mendel RR (2001) ABA3 is a molybdenum cofactor sulfurase required for activation of aldehyde oxidase and xanthine dehydrogenase in Arabidopsis thaliana. J Biol Chem 276: 40381-40384
9. Blaszczyk A, Brodzik R and Sirko A (1999) Increased resistance to oxidative stress in transgenic tobacco plants overexpressing bacterial serine acetyltransferase. Plant J 20: 237-243
10. Bork C, Schwenn JD and Hell R (1998) Isolation and characterization of a gene for assimilatory sulfite reductase from Arabidopsis thaliana. Gene 212: 147-153
11. Chiba Y, Ishikawa E, Kijima F, Tyson RH, Kim J, Yamamoto H, Nambara E, Leustek T, Wallsgrove RM and Naito S (1999) Evidence of autoregulation of cystathionine γ-synthase mRNA stability in Arabidopsis. Science 286: 1371-1374
12. Chiba Y, Sakurai R, Yoshino M, Ominato K, Ishikawa M, Onouchi H and Naito S (2003) S-adenosyl-L-methionine is an effector in the posttranscriptional autoregulation of the cystathionine γ-synthase gene in Arabidopsis. Proc Natl Acad Sci USA 100: 10225-10230
13. Cobbett CS and Goldsbrough PB (2002) Phytochelatins and metallothioneins: role in heavy metal detoxification and homeostasis. Annu Rev Plant Biol 53: 159-182
14. Collin V, Issakidis-Bourget E, Marchand C, Hirasawa M, Lancelin JM, Knaff DB and Miginiac-Maslow M (2003) The Arabidopsis plastidial thioredoxins: new functions and new insights into specificity. J Biol Chem 278: 23747-23752
15. Cooper CE, Patel RP, Brookes PS and Darley-Usmar VM (2002) Nanotransducers in cellular redox signaling: modification of thiols by reactive oxygen and nitrogen species. Trends Biochem Sci 27: 489-492
16. Dietz K-J (2003) Plant peroxiredoxins. Annu Rev Plant Biol 54: 93-107
17. Dixon DP, Davis BG and Edwards R (2002a) Functional divergence in the glutathione transferase superfamily in plants. Identification of two classes with putative functions in redox homeostasis in Arabidopsis thaliana. J Biol Chem 277: 30859-30869
18. Dixon DP, Lapthorn A and Edwards R (2002b) Plant glutathione transferase. Genome Biol 3: 1-10
19. Droux M (2003) Plant serine acetyltransferase: new insights for regulation of sulphur metabolism in plant cells. Plant Physiol Biochem 41: 619-627
20. Droux M, Ruffet ML, Douce R and Job D (1998) Interactions between serine acetyltransferase and O-acetylserine(thiol)lyase in higher plants. Structural and kinetics properties of the free and bound enzymes. Eur J Biochem 255: 235-245
21. Eilers T, Schwarz G, Brinkmann H, Witt C, Richter T, Nieder J, Koch B, Hille R, Hänsch R and Mendel RR (2001) Identification and biochemical characterization of Arabidopsis thaliana sulfite oxidase. A new player in plant sulfur metabolism. J Biol Chem 276: 46989-46994
22. +-cotransporters for cellular import of neutral and charged amino-acids. Plant J 29: 717-731
23. Foster MW, McMahon TJ and Stamler JS (2003) S-nitrosylation in health and disease. Trends Mol Med 9: 160-168
24. Foyer CH, Theodoulou FL and Delrot S (2001) The functions of inter-and intracellular glutathione transport systems in plants. Trends Plant Sci 6: 486-492
25. Frazzon J and Dean DR (2003) Formation of iron-sulfur clusters in bacteria: an emerging field in bioinorganic chemistry. Curr Opin Chem Biol 7: 166-173
26. Gakière B, Denis L, Droux M and Job D (2002) Over-expression of cystathionine γ-synthase in Arabidopsis thaliana leads to increased levels of methionine and S-methylmethionine. Plant Phys Biochem 40: 119-126
27. Galili G and Hofgen R (2002) Metabolic engineering of amino-acids and storage proteins in plants. Metab Eng 4: 3-11
28. Gao Y, Schofield OM and Leustek T (2000) Characterization of sulfate assimilation in marine algae focusing on the enzyme 5′-adenylylsulfate reductase. Plant Physiol 123: 1087-1096
29. Georgiou G and Masip L (2003) An overoxidation journey with a return ticket. Science 300: 592-594
30. Gerber J and Lill R (2002) Biogenesis of iron-sulfur proteins in eukaryotes: components, mechanism and pathology. Mitochondrion 2: 71-86
31. Gilbert HF (1990) Molecular and cellular aspects of thiol-disulfide exchange. Adv Enzymol Relat Areas Mol Biol 63: 69-172
32. Giles GI, Tasker KM and Jacob C (2001) Hypothesis: the role of reactive sulfur species in oxidative stress. Free Radic Biol Med 31: 1279-1283
33. Giles NM, Giles GI and Jacob C (2003) Multiple role of cysteine in biocatalysis. Biochem Biophys Res Com 300: 1-4
34. Goto DB, Ogi M, Kijima F, Kumagai T, van Werven F, Onouchi H and 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
35. Gueguen V, Macherel D, Jaquinod M, Douce R and Bouguignon J (2000) Fatty acid and lipoic acid biosynthesis in higher plant mitochondria. J Biol Chem 275: 5016-5025
36. Gustavsson N, Härndahl U, Emanuelsson A, Roepstorff P and Sundby C (1999) Methionine sulfoxidation of the chloroplast small heat shock protein and conformational changes in the oligomer. Protein Sci 8: 2506-2512
37. Gustavsson N, Kokke BP, Anzelius B, Boelens WC and Sundby C (2001) Substitutions of conserved methionine by leucines in chloroplast small heat shock protein results in loss of redox-response but retained chaperone-like activity. Protein Sci 10: 1785-1793
38. Gustavsson N, Kokke BP, Härndahl U, Silow M, Bechtold U, Poghosyan Z, Murphy D, Boelens WC and Sundby C (2002) A peptide methionine sulfoxide reductase highly expressed in photosynthetic tissue in Arabidopsis thaliana can protect the chaperone-like activity of a chloroplast-localized small heat shock protein. Plant J 29: 545-553
39. Gutierrez-Alcala G, Gotor C, Meyer AJ, Fricker M, Vega JM and Romero LC (2000) Glutathione biosynthesis in Arabidopsis trichome cells. Proc Natl Acad Sci USA 97: 11108-11113
40. Gutierrez-Marcos JF, Roberts MA, Campbell EI and 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
41. Hacham Y, Avraham T and Amir R (2002) The N-terminal region of Arabidopsis cystathionine gamma-synthase plays an important regulatory role in methionine metabolism. Plant Physiol 128: 454-462
42. Hacham Y, Gophna U and Amir R (2003) In vivo analysis of various substrates utilized by cystathionine gamma-synthase and O-acetylhomoserine sulfhydrylase in methionine biosynthesis. Mol Biol Evol 20: 1513-1520
43. Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53: 1-11
44. Harms K, von Ballmoos P, Brunold C, Höfgen R and 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
45. Hatzfeld Y, Lee S, Lee M, Leustek T and Saito K (2000a) Functional characterization of a gene encoding a fourth ATP sulfurylase isoform from Arabidopsis thaliana. Gene 248: 51-58
46. Hatzfeld Y, Maruyama A, Schmidt A, Noji M, Ishizawa K and Saito K (2000b) Beta-cyanoalanine synthase is a mitochondrial cysteine synthase-like protein in spinach and Arabidopsis. Plant Physiol 123: 1163-1171
47. Hawkesford MJ (2000) Plant responses to sulphur deficiency and the genetic manipulation of sulphate transporters to improve S-utilization efficiency. J Exp Bot 51: 131-138
48. Hell R and Bergmann L (1990) γ-glutamylcysteine synthetase in higher plants: catalytic properties and subcellular localization. Planta 180: 303-312
49. Hell R, Jost R, Berkowitz O and Wirtz M (2002) Molecular and biochemical analysis of the enzymes of cysteine biosynthesis in the plant Arabidopsis thaliana. Amino Acids 22: 245-257
50. Hesse H and Hoefgen R (2003) Molecular aspects of methionine biosynthesis. Trends Plant Sci 8: 259-262
51. Hirai MY, Fujiwara T, Awazuhara M, Kimura T, Noji M and 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
52. Hoshi T and Heinemann S (2001) Regulation of cell function by methionine oxidation and reduction. J Physiol 531: 1-11
53. Howarth JR, Dominguez-Solis JR, Gutierrez-Alcala G, Wray JL, Romero LC and Gotor C (2003) The serine acetyltransferase gene family in Arabidopsis thaliana and the regulation of its expression by cadmium. Plant Mol Biol 51: 589-598
54. Huang KP and Huang FL (2002) Glutathionylation of proteins by glutathione disulfide S-dioxide. Biochem Pharmacol 64: 1049-1056
55. Jacquot JP, Gelhaye E, Rouhier N, Corbier C, Didierjean C and Aubry A (2002) Thioredoxins and related proteins in photosynthetic organisms: molecular basis for thiol dependent regulation. Biochem Pharmacol 64: 1065-1069
56. Jones PR, Manabe T, Awazuhara M and Saito K (2003) A new member of plant CS-lyases. A cystine lyase from Arabidopsis thaliana. J Biol Chem 278: 10291-10296
57. Jost R, Berkowitz O, Wirtz M, Hopkins L, Hawkesford MJ and Hell R (2000) Genomic and functional characterization of the oas gene family encoding O-acetylserine (thiol) lyase, enzymes catalyzing the final step in cysteine biosynthesis in Arabidopsis thaliana. Gene 253: 237-247
58. Kim J, Lee M, Chalam R, Martin MN, Leustek T and Boerjan W (2002) Constitutive overexpressionn of cystathionine γ-synthase in Arabidopsis leads to accumulation of soluble methionine and S-methylmethionine. Plant Physiol 128: 95-107
59. Klatt P and Lamas S (2000) Regulation of protein function by S-glutathiolation in response to oxidative and nitrosative stress. Eur J Biochem 267: 4928-4944
60. 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 and Hanson A (2003) Insertional inactivation of the methionine S-methyltransferase gene eliminates the S-methylmethionine cycle and increases the methylation ratio. Plant Physiol 131: 1808-1815
61. Koguchi O and Tamura G (1989) Reduction of S-sulfoglutathione by cyanobacterial ferredoxin-sulfite reductase. Agric Biol Chem 53: 783-788
62. Kopriva S, Buchert T, Fritz G, Suter M, Weber M, Benda R, Schaller J, Feller U, Schürmann P, Schunemann V, Trautwein AX, Kroneck PM and Brunold C (2001) Plant adenosine 5′-phophosulfate reductase is a novel iron-sulfur protein. J Biol Chem 276: 42881-42886
63. Kopriva S, Buchert T, Fritz G, Suter M, Benda R, Schunemann V, Koprivova A, Schürmann P, Trautwein AX, Kroneck PM and Brunold C (2002a) The presence of an iron-sulfur cluster in adenosine 5′ phosphosulfate reductase separates organisms utilizing 5′-phosphosulfate and phosphoadenosine 5′-phosphosulfate for sulfate assimilation. J Biol Chem 277: 21786-21791
64. Kopriva S, Suter M, von Ballmoos P, Hesse H, Krähenbühl U, Rennenberg H and Brunold C (2002b) Interaction of sulfate assimilation with carbon and nitrogen metabolism in Lemna minor. Plant Physiol 130: 1406-1413
65. Koprivova A, Suter M, den Camp RO, Brunold C and Kopriva S (2000) Regulation of sulfate assimilation by nitrogen in Arabidopsis. Plant Physiol 122: 737-746
66. Koprivova A, Meyer AJ, Schween G, Herschbach C, Reski R and 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
67. Kredich NM (1996) Biosynthesis of cysteine. In: Neidhardt FC, Curtiss R, Ingraham JL, Lin E, Low KB, Magasanik B, Reznikoff WS, Riley M, Schaechter M and Umbarger HE (eds) Escherichia coli and Salmonella typhimurium. Cellular and Molecular Biology, pp 514-527. ASM Press, Washington, DC
68. Kreft O, Hoefgen R and Hesse H (2003) Functional analysis of cystathionine γ-synthase in genetically engineered potato plants. Plant Physiol 131: 1843-1854
69. Lee S and Leustek T (1998) APS kinase from Arabidopsis thaliana: genomic organization, expression, and kinetic analysis of the recombinant enzyme. Biochem Biophys Res Com 247: 171-175
70. Leimkühler S and Rajagopalan KV (2001) A sulfurtransferase is required in the transfer of cysteine sulfur in the in vitro synthesis of molybdopterin from precursor Z in Escherichia coli. J Biol Chem 276: 22024-22031
71. Leon S, Touraine B, Briat JF and Lobreaux S (2002) The AtNFS2 gene from Arabidopsis thaliana encodes a NifS-like plastidial cysteine desulphurase. Biochem J 366: 557-564
72. Leustek T, Martin MN, Bick JA and 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
73. Levine RL, Berlett BS, Moskovitz J, Mosoni L and Stadtman ER (1999) Methionine residues may protect proteins from critical oxidative damage. Mech Ageing Dev 107: 323-332
74. Levine RL, Moskovitz J and Stadtman ER (2000) Oxidation of methionine in proteins: roles in antioxidant defense and cellular regulation. IUBMB Life 50: 301-307
75. Leyh TS, Vogt TF and Suo Y (1992) The DNA sequence of the sulfate activation locus from Escherichia coli K-12. J Biol Chem 267: 10405-10410
76. Lillig CH, Schiffmann S, Berndt C, Berken A, Tischka R and Schwenn JD (2001) Molecular and catalytic properties of Arabidopsis thaliana adenylyl sulfate (APS)-kinase. Arch Biochem Biophys 392: 303-310
77. Liszewska F, Blaszczyk A and Sirko A (2001) Modification of non-protein thiols contents in transgenic tobacco plants producing bacterial producing bacterial enzymes of cysteine biosynthesis pathway. Acta Biochim Pol 48: 647-656
78. Lu SC (2000) S-adenosylmethionine. Int J Biochem Cell Biol 32: 391-395
79. Lunn JE, Droux M, Martin J and Douce R (1990) Localization of ATP-sulfurylase and O-acetylserine(thiol)lyase in spinach leaves. Plant Physiol 94: 1345-1352
80. Marquet A (2001) Enzymology of carbon-sulfur bond formation. Curr Opin Chem Biol 5: 541-549
81. Marsolais F and Varin L (1998) Recent developments in the study of the structure-function relationship of flavonol sulfotransferases. Chem Biol Interact 109: 117-122
82. Marzluf GA (1997) Molecular genetics of sulfur assimilation in filamentous fungi and yeast. Annu Rev Microbiol 51: 73-96
83. May MJ, Vernoux T, Sänchez-Fernändez R, Van Montagu M and Inzé D (1998) Evidence for post-transcriptional activation of γ-glutamylcysteine synthetase during plant stress responses. Proc Natl Acad Sci USA 95: 12049-12054
84. Mendel RR and Hänsch R (2002) Molybdoenzymes and molybdenum cofactor in plants. J Exp Bot 53: 1689-1698
85. Mihara H and Esaki N (2002) Bacterial cysteine desulfurases: their function and mechanisms. Appl Microbiol Biotechnol 60: 12-23
86. Mikkelsen MD, Petersen BL, Olsen CE and Halkier BA (2002) Biosynthesis and metabolic engineering of glucosinolates. Amino Acids 22: 279-295
87. Miranda M, Borisjuk L, Tewes A, Heim U, Sauer N, Wobus U and Weber H (2001) Amino acid permeases in developing seeds of Vicia faba L.: expression precedes storage protein synthesis and is regulated by amino-acid supply. Plant J 28: 61-71
88. Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7: 405-410
89. Moran JF, Iturbe-Ormaetxe I, Matamoros MA, Rubio MC, Clemente MR, Brewin NJ and Becana M (2000) Glutathione and homoglutathione synthetases of legumes nodules. Cloning, expression, and subcellular localization. Plant Physiol 124: 1381-1392
90. Murillo M, Foglia R, Diller A, Lee S and Leustek T (1995) Serine acetyltransferase from Arabidopsis thaliana can functionally complement the cysteine requirement of a cysE mutant strain of Escherichia coli. Cell Mol Biol Res 41: 425-433
91. Nakamura T, Meyer C and Sano H (2002) Molecular cloning and characterization of plant genes encoding novel peroxisomal molybdoenzymes of the sulphite oxidase family. J Exp Bot 53: 1833-1836
92. Nakayama M, Akashi T and Hase T (2000) Plant sulfite reductase: molecular structure, catalytic function and interaction with ferredoxin. J Inorg Biochem 82: 27-32
93. Nikiforova V, Kempa S, Zeh M, Maimann, Kreft O, Casazza AP, Riedel K, Tauberger E, Hoefgen R and Hesse H (2002) Engineering of cysteine and methionine biosynthesis in potato. Amino Acids 22: 259-278
94. Nikiforova V, Freitag J, Kempa S, Adamik M, Hesse H and Hoefgen R (2003) Transcriptome analysis of sulfur depletion in Arabidopsis thaliana: interlacing of biosynthetic pathways provides response specificity. Plant J 33: 633-650
95. Noctor G, Gomez L, Vanacker H and Foyer CH (2002) Interactions between biosynthesis, compartmentation and transport in the control of glutathione homeostasis and signalling. J Exp Bot 53: 1283-1304
96. Noji M and Saito K (2002) Molecular and biochemical analysis of serine acetyltransferase and cysteine synthase towards sulfur metabolic engineering in plants. Amino Acids 22: 231-243
97. Noji M, Inoue K, Kimura N, Gouda A and 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
98. Noji M, Takagi Y, Kimura N, Inoue K, Saito M, Horikoshi M, Saito F, Takahashi H and Saito K (2001) Serine acetyltransferase involved in cysteine biosynthesis from spinach: molecular cloning, characterization and expression analysis of cDNA encoding a plastidic isoform. Plant Cell Physiol 42: 627-634
99. Ominato K, Akita H, Suzuki A, Kijima F, Yoshino T, Yoshino M, Chiba Y, Onouchi H and Naito S (2002) Identification of a short highly conserved amino-acid sequence as the functional region required for posttranscriptional autoregulation of the cystathionine γ-synthase gene in Arabidopsis. J Biol Chem 277: 36380-36386
100. Papenbrock J and Schmidt A (2000) Characterization of two sulfurtransferase isozymes from Arabidopsis thaliana. Eur J Biochem 267: 5571-5579
101. 2+-sensitive 3′(2′),5′-diphosphonucleoside 3′(2′)-phosphohydrolase and complements yeast met22 and Escherichia coli cysQ mutations. J Biol Chem 270: 29105-29110
102. Picciocchi A, Douce R and Alban C (2003) The plant biotin synthase reaction. Identification and characterization of essential mitochondrial accessory protein components. J Biol Chem 278: 24966-24975
103. Pilon-Smits EA, Garifullina GF, Abdel-Ghany S, Kato S, Mihara H, Hale KL, Burkhead JL, Esaki N, Kurihara T and Pilon M (2002) Characterization of a NifS-like chloroplast protein from Arabidopsis. Implication for its role in sulfur and selenium metabolism. Plant Physiol 130: 1309-1318
104. Quintero FJ, Garciadeblás B and Rodriguez-Navarro A (1996) The SAL1 gene of Arabidopsis, encoding an enzyme with 3′(2′),5′- biphosphate nucleotidase and inositol polyphosphate 1-phosphatase activities, increases salt tolerance in yeast. Plant Cell 8: 529-537
105. Ranocha P, McNeil SD, Ziemak MJ, Li C, Tarczynski MC and Hanson AD (2001) The S-methylmethionine cycle in angiosperms: ubiquity, antiquity and activity. Plant J 25: 575-584
106. Ravanel S, Gakière B, Job D and Douce R (1998) The specific features of methionine biosynthesis and metabolism in plants. Proc Natl Acad Sci USA 95: 7805-7812
107. Ravanel S, Cherest H, Jabrin S, Grunwald D, Surdin-Kerjan Y, Douce R and Rébeillé F (2001) Tetrahydrofolate biosynthesis in plants: molecular and functional characterization of dihydrofolate synthetase and three isoforms of folylpolyglutamate synthetase in Arabidopsis thaliana. Proc Natl Acad Sci USA 98: 15360-15365
108. Renosto F, Patel HC, Martin RL, Thomassian C, Zimmerman G and Segel IH (1993) ATP sulfurylase from higher plants: kinetic and structural characterization of the chloroplast and cytosol enzymes from spinach leaf. Arch Biochem Biophys 307: 272-285
109. Rotte C and 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
110. Rouhier N and Jacquot JP (2002) Plant peroxiredoxins: alternative hydroperoxide scavenging enzymes. Photosynth Res 74: 259-268
111. Rudhe C, Clifton R, Whelan J and Glaser E (2002) N-terminal domain of the dual-targeted pea glutathione reductase signal peptide controls organellar targeting efficiency. J Mol Biol 324: 577-585
112. Ruffet ML, Lebrun M, Droux M and Douce R (1995) Sub-cellular distribution of serine acetyltransferase from Pixum sativum and characterization of an Arabidopsis thaliana putative cytosolic isoform. Eur J Biochem 277: 500-509
113. Sadanandom A, Poghosyan Z, Fairbairn DJ and Murphy DJ (2000) Differential regulation of plastidial and cytosolic isoforms of peptide methionine sulfoxide reductase in Arabidopsis. Plant Physiol 123: 255-264
114. Saito K (2000) Regulation of sulfate transport and synthesis of sulfur-containing amino-acids. Curr Opin Plant Biol 3: 188-195
115. Sakamoto A, Tsukamoto S, Yamamoto H, Ueda-Hashimoto M, Takahashi M, Suzuki H and Morikawa H (2003) Functional complementation in yeast reveals a protective role of chloroplast 2-Cys peroxiredoxin against reactive nitrogen species. Plant J 33: 841-851
116. Sanda S, Leustek T, Theisen MJ, Garavito RM and Benning C (2001) Recombinant Arabidopsis SQD1 converts UDP-glucose and sulfite to the sulfolipid head group precursor UDP-sulfoquinovose in vitro. J Biol Chem 276: 3941-3946
117. Scandalios JG (2002) The rise of ROS. Trends Biochem Sci 27: 483-486
118. Schafer FQ and Buettner GR (2001) Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple. Free Radic Biol Med 30: 1191-1212
119. Schafer HJ, Haag-Kerwer A and Rausch T (1998) cDNA cloning and expression analysis of genes encoding GSH synthesis in roots of the heavy-metal accumulator Brassica juncea L.: evidence for Cd-induction of a putative mitochondrial gamma-glutamylcysteine synthetase isoform. Plant Mol Biol 37: 87-97
120. Schürmann P and Jacquot JP (2000) Plant thioredoxin systems revisited. Ann Rev Plant Physiol Plant Mol Biol 51: 371-400
121. Setya A, Murillo M and Leutesk T (1996) Sulfate reduction in higher plants: molecular evidence for a novel 5′-adenylylsulfate reductase. Proc Natl Acad Sci USA 93: 13383-13388
122. Shen B, Li C and Tarczynski MC (2002) High free-methionine and decreased lignin content result from a mutation in Arabidopsis S-adenosyl-L-methionine synthetase 3 gene. Plant J 29: 371-380
123. Shenton D and Grant CM (2003) Protein S-thiolation targets glycolysis and protein synthesis in response to oxidative stress in the yeast Saccharomyces cerevisiae. Biochem J 374: 513-519
124. Shibagaki N, Rose A, McDermott JP, Fujiwara T, Hayashi H, Yoneyama T and 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: 474-486
125. Suter M, von Ballmoos P, Kopriva S, den Camp RO, Schaller J, Kuhlemeier C, Schürmann P and Brunold C (2000) Adenosine 5′-phosphosulfate sulfotransferase and adenosine 5′-phosphosulfate reductase are identical enzymes. J Biol Chem 275: 930-936
126. Tabe L and Higgins TJ (1998) Engineering plant protein composition for improved nutrition. Trends Plant Sci 3: 282-286
127. Takahashi H, Yamazaki M, Sasakura N, Watanabe A, Leustek T, Engler JA, Engler G, Van Montagu M and Saito K (1997) Regulation of sulfur assimilation in higher plants: a sulfate transporter induced in sulfate-starved roots plays a central role in Arabidopsis thaliana. Proc Natl Acad Sci USA 30: 11102-11107
128. Takahashi H, Asanuma W and Saito K (1999) Gene note. Cloning of an Arabidopsis cDNA encoding a chloroplast localizing sulphate transporter isoform. J Exp Bot 50: 1713-1714
129. Takahashi H, Watanebe-Takahashi A, Smith FW, Blake-Kalff M, Hawkesford MJ and Saito K (2000) The role of three functional sulphate transporters involved in uptake and translocation of sulphate in Arabidopsis thaliana. Plant J 23: 171-182
130. Thomas D and Surdin-Kerjan Y (1997) Metabolism of sulfur amino-acids in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 61: 503-532
131. Thomas JA, Poland B and Honzatko R (1995) Protein sulfhydryls and their role in the antioxidant function of protein S-thiolation. Arch Biochem Biophys 319: 1-9
132. Tsakraklides G, Martin M, Chalam R, Tarczynski MC, Schmidt A and Leustek T (2002) Sulfate reduction is increased in transgenic Arabidopsis thaliana expressing 5′-adenylylsulfate reductase from Pseudomonas aeruginosa. Plant J 32: 879-889
133. Varin L, Marsolais F, Richard M and Rouleau M (1997) Sulfation and sulfotransferases 6: biochemistry and molecular biology of plant sulfotransferases. FASEB J 11: 517-525
134. Vauclare P, Kopriva S, Fell D, Suter M, Sticher L, von Ballmoos P, Krahenbuhl U, den Camp RO and Brunold C (2002) Flux control of sulphate assimilation in Arabidopsis thaliana: adenosine 5′-phosphosulfate reductase is more susceptible than ATP sulphurylase to negative control by thiols. Plant J 31: 729-740
135. Vernoux T, Wilson RC, Seeley KA, Reichheld JP, Muroy S, Brown S, Maughan SC, Cobbett CS, Van Montagu M, Inzé D, May MJ and Sung ZR (2000) The ROOT MERISTEMLESS1/CADMIUM SENSITIVE2 gene defines a glutathione-dependent pathway involved in initiation and maintenance of cell division during postembryonic root development. Plant Cell 12: 97-110
136. Vidmar JJ, Tagmount A, Cathala N, Touraine B and Davidian JE (2000) Cloning and characterization of a root specific high-affinity sulfate transporter from Arabidopsis thaliana. FEBS Lett 475: 65-69
137. Vogt W (1995) Oxidation of methionyl residues in proteins: tools, targets, and reversal. Free Radic Biol Med 18: 93-105
138. Warrilow AG and Hawkesford MJ (2000) Cysteine synthase (O-acetylserine (thiol) lyase) substrate specificities classify the mitochondrial isoform as a cyanoalanine synthase. J Exp Bot 51: 985-993
139. Warrilow AG and Hawkesford MJ (2002) Modulation of cyanoalanine synthase and O-acetylserine (thiol) lyase A and B activity by beta-substituted alanyl and anion inhibitors. J Exp Bot 53: 439-445
140. Weber M, Suter M, Brunold C and Kopriva S (2000) Sulfate assimilation in higher plants characterization of a stable intermediate in the adenosine 5′-phosphosulfate reductase reaction. Eur J Biochem 267: 3647-3653
141. Weissbach H, Etienne F, Hoshi T, Heinemann SH, Lowther WT, Matthews B, St John G, Nathan C and Brot N (2002) Peptide methionine sulfoxide reductase: structure, mechanism of action, and biological function. Arch Biochem Biophys 397: 172-178
142. Wipf D, Ludewig U, Tegeder M, Rentsch D, Koch W and Frommer WB (2002) Conservation of amino-acid transporters in fungi, plants and animals. Trends Biochem Sci 27: 139-147
143. Wirtz M and Hell R (2003) Production of cysteine for bacterial and plant biotechnology: application of cysteine feedback-insensitive isoforms of serine acetyltransferase. Amino Acids 24: 195-203
144. Wirtz M, Berkowitz O, Droux M and 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
145. Wittstock U and Halkier BA (2002) Glucosinolate research in the Arabidopsis era. Trends Plant Sci 7: 263-270
146. Wood ZA, Schröder E, Robin Harris J and Poole LB (2003a) Structure, mechanism and regulation of peroxiredoxins. Trends Biochem Sci 28: 32-40
147. Wood ZA, Pool LB and Karplus PA (2003b) Peroxiredoxin evolution and the regulation of hydrogen peroxide signaling. Science 300: 650-653
148. Wray JL, Campbell EI, Roberts MA and Gutierrez-Marcos JF (1998) Redefining reductive sulfate assimilation in higher plants: a role for APS reductase, a new member of the thioredoxin superfamily? Chem Biol Interact 109: 153-167
149. Xiong L, Ishitani M, Lee H and Zhu JK (2001) The Arabidopsis LOS5/ABA3 locus encodes a molybdenum cofactor sulfurase and modulates cold stress-and osmotic stress-responsive gene expression. Plant Cell 13: 2063-2083
150. Yamaguchi Y, Nakamura T, Kusano T and Sano H (2000) Three Arabidopsis genes encoding proteins with differential activities for cysteine synthase and beta-cyanoalanine synthase. Plant Cell Physiol 41: 465-475
151. Yonekura-Sakakibara K, Onda Y, Ashikari T, Tanaka Y, Kusumi T and 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
152. Yoshimoto N, Takahashi H, Smith FW, Yamaya T and Saito K (2002) Two distinct high-affinity sulfate transporters with different inducibilities mediate uptake of sulfate in Arabidopsis roots. Plant J 29: 465-473
153. Yoshimoto N, Inoue E, Saito K, Yamaya T and Takahashi H (2003) Phloem-localizing sulphate transporter, Sultr1;3, mediates redistribution of sulfur from source to sink organs in Arabidopsis. Plant Physiol 131: 1511-1517
154. Zeh M, Casazza AP, Kreft O, Roessner U, Bieberich K, Willmitzer L, Hoefgen R and Hesse H (2001) Antisense inhibition of threonine synthase leads to high methionine content in transgenic potato plants. Plant Physiol 127: 792-802