Sulfur assimilation and glutathione metabolism under cadmium stress in yeast, protists and plants

FEMS Microbiology Reviews

Volumn 29, Issue 4, 2005, Pages 653-671

  Mendoza Cózatl, David ^a   Loza Tavera, Herminia ^b   Hernández Navarro, Andrea ^b   Moreno Sánchez, Rafael ^a  

^a INSTITUTO NACIONAL DE CARDIOLOGÍA IGNACIO CHÁVEZ   (Mexico)

^b Universidad Nacional Autonoma de Mexico Facultad de Quimica   (Mexico)

Author keywords

Glutamylcysteine synthetase; Cadmium accumulation; Cadmium resistance; Glutathione synthetase; Phytochelatin synthase; Phytochelatins; Sulfur assimilation pathway

Indexed keywords

ADENOSINE TRIPHOSPHATE; ADENYLYLSULFATE KINASE; AMINO ACID DERIVATIVE; CADMIUM; CYSTATHIONINE BETA SYNTHASE; CYSTATHIONINE GAMMA LYASE; CYSTEINE; CYSTEINE SYNTHASE; GLUTAMATE CYSTEINE LIGASE; GLUTATHIONE; GLUTATHIONE SYNTHASE; HEAVY METAL; OXIDOREDUCTASE; PHYTOCHELATIN; PHYTOCHELATIN SYNTHASE; REACTIVE OXYGEN METABOLITE; SERINE ACETYLTRANSFERASE; SULFATE; SULFATE ADENYLYLTRANSFERASE; SULFIDE; SULFITE REDUCTASE; SULFUR; XENOBIOTIC AGENT;

BIOSYNTHESIS; CELL COMPARTMENTALIZATION; CELL FUNCTION; CHELATION; CHLOROPLAST; COMPLEX FORMATION; CYTOSOL; ENZYME ACTIVATION; ENZYME LOCALIZATION; ENZYME MECHANISM; EUGLENA; EXPOSURE; GENETIC REGULATION; GLUTATHIONE METABOLISM; GREEN ALGA; METABOLIC REGULATION; MOLECULAR GENETICS; MOLECULE; NONHUMAN; OXIDATIVE STRESS; PLANT; REACTION ANALYSIS; REDUCTION KINETICS; REGULATORY MECHANISM; REVIEW; STRESS; YEAST;

ANIMALS; CADMIUM COMPOUNDS; CILIOPHORA; GENE EXPRESSION REGULATION, PLANT; GLUTATHIONE; PLANT LEAVES; PLANT ROOTS; PLANTS; SULFATES; SULFUR; THIOREDOXIN; YEASTS;

PROTISTA;

EID: 23744506272     PISSN: 01686445     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.femsre.2004.09.004     Document Type: Review

References (203)

1. J.H.R. Kägi, and A. Schäffer Biochemistry of metallothioneins Biochemistry 27 1988 8509 8515
2. N. Grotz, T. Fox, E. Connolly, W. Park, M.L. Guerinot, and D. Eide Identification of a family of zinc transporter genes from Arabidopsis that respond to zinc deficiency Proc. Natl. Acad. Sci. USA 95 1998 7220 7224
3. T. Clarkson Health effects of metals: a role for evolution Environ. Health Perspect. 103 1995 9 12
4. L.T. Paulsen, and M.H. Saier A novel family of ubiquitous heavy metal ion transport family J. Membr. Biol. 156 1997 99 103
5. S. Thomine, R. Wang, J.M. Ward, N.M. Crawford, and J.I. Schroeder Cadmium and iron transport by members of a plant metal transporter family in Arabidopsis with homology to Nramp genes Proc. Natl. Acad. Sci. USA 97 2000 4991 4996
6. E.E. Rogers, D.J. Eide, and M.L. Guerinot Altered selectivity in an Arabidopsis metal transporter Proc. Natl. Acad. Sci. USA 97 2000 12356 12360
7. E. Nieboer, and D.H.S. Richardson The replacement of the non descript term "heavy metal" by biologically and chemically significant classification of metal ions Environ. Pollut. 1 1980 3 8
8. B.L. Valle, and D.D. Ulmer Biochemical effects of mercury, cadmium, and lead Annu. Rev. Biochem. 41 1972 91 128
9. - exchange in liposomes and rabbit renal brush border membranes J. Biol. Chem. 267 1992 12218 12250
10. R.H. Reed, and G.M. Gadd Metal Tolerance in Eukaryotic and Prokaryotic Algae A.J. Shaw Heavy Metal Tolerance in Plants: Evolutionary Aspects 1990 CRC Press Boca Raton, FL 105 118 (Chapter 8)
11. D. Kaplan, Y.M. Heimer, A. Abelovich, and P.B. Goldsbrough Cadmium toxicity and resistance in Chlorella sp Plant Sci. 109 1995 129 137
12. M.H. Zenk Heavy detoxification in higher plants - a review Gene 179 1996 21 30
13. S.M. Macfie, and P.M. Welburn The cell wall as barrier to uptake of metals ions in the unicellular green alga Chlamydomonas reinhardtii (Chlorophyceae) Arch. Environ. Contam. Toxicol. 39 2000 413 419
14. C.S. Cobbett Phytochelatins and their roles in heavy metal detoxification Plant Physiol. 123 2000 825 832
15. J.L. Hall Cellular mechanisms for heavy metal detoxification and tolerance J. Exp. Bot. 53 2002 1 11
16. H. Mutoh, and Y. Hayashi Isolation of mutants of Schizosaccharomyces pombe unable to synthesize cadystins, small cadmium-binding peptides Biochem. Biophys. Res. Commun. 151 1988 32 39
17. R.K. Mehra, E.B. Tarbet, W.R. Gray, and D.R. Winge Metal-specific synthesis of two metallothioneins and γ-glutamyl peptides in Candida glabrata Proc. Natl. Acad. Sci. USA 85 1988 8815 8819
18. R.K. Mehra, P. Mulchandani, and T.C. Hunter Role of CdS quantum crystallites in cadmium resistance in Candida glabrata Biochem. Biophys. Res. Commun. 200 1994 1193 1200
19. W. Gekeler, E. Grill, E.L. Winnacker, and M.H. Zenk Algae sequester heavy metals via synthesis of phytochelatin complexes Arch. Microbiol. 150 1988 197 202
20. D. Mendoza-Cózatl, S. Devars, H. Loza-Tavera, and R. Moreno-Sánchez Cadmium accumulation in the chloroplast of Euglena gracilis Physiol. Plant. 115 2002 276 283
21. E. Grill, E.L. Winnacker, and M.H. Zenk Phytochelatins: the principal heavy-metal complexing peptides of higher plants Science 230 1985 674 676
22. S. Clemens Molecular mechanisms of plant metal tolerance and homeostasis Planta 212 2001 475 486
23. P.A. Rea, Z.S. Li, Y.P. Lu, and Y.M. Drozdowicz From vacuolar GS-X pumps to multispecific ABC transporters Annu. Rev. Plant Physiol. Plant Mol. Biol. 49 1998 727 760
24. D.F. Ortiz, R. Ruscitti, K.F. McCue, and D.W. Ow Transport of metal-binding peptides by HMT1, a fission yeast ABC-type vacuolar membrane protein J. Biol. Chem. 270 1995 4721 4728
25. D.E. Salt, and W.E. Rauser MgATP-dependent transport of phytochelatins across the tonoplast of oat roots Plant Physiol. 107 1995 1293 1301
26. E. Grill, E.L. Winnacker, and M.H. Zenk Phytochelatins, a class of heavy-metal-binding peptides from plants are functionally analogous to metallothioneins Proc. Natl. Acad. Sci. USA 84 1987 439 443
27. J. Thumann, E. Grill, E.L. Winnacker, and M.H. Zenk Reactivation of metal-requiring apoenzymes by phytochelatin-metal complexes FEBS Lett. 284 1991 66 69
28. A. Meister Glutathione metabolism Methods Enzymol. 251 1995 3 13
29. G. Noctor, and C. Foyer Ascorbate and glutathione: keeping active oxygen under control Annu. Rev. Plant Physiol. Plant Mol. Biol. 49 1998 249 279
30. C. Xiang, and D. Oliver Glutathione metabolic genes coordinately respond to heavy metals and jasmonic acid in Arabidopsis Plant Cell 10 1998 1539 1550
31. J.R. Domínguez-Solís, G. Gutiérrez-Alcalá, L.C. Romero, and C. Gotor The cytosolic O-acetylserine(thiol)lyase gene is regulated by heavy metals and can function in cadmium tolerance J. Biol. Chem. 276 2001 9297 9302
32. A. Koprivova, M. Suter, R.O. den Camp, C. Brunold, and S. Kopriva Regulation of sulfate assimilation by nitrogen in Arabidopsis Plant Physiol. 122 2000 737 746
33. E. Harada, Y. Yamaguchi, N. Koizumi, and H. Sano Cadmium stress induces production of thiol compounds and transcripts for enzymes involved in sulfur assimilation pathways in Arabidopsis J. Plant Physiol. 159 2002 445 448
34. D. Thomas, and Y. Surdin-Kerjan Metabolism of sulphur amino acids in Saccharomyces cerevisiae Microbiol. Mol. Biol. Rev. 61 1997 503 532
35. B. Ono, T. Hazu, S. Yoshida, T. Kawato, S. Shinoda, J. Brzvwczy, and A. Paszewski Cysteine biosynthesis in Saccharomyces cerevisiae: a new outlook on pathway and regulation Yeast 15 1999 1365 1375
36. J. Brzywczy, M. Sienko, A. Kucharska, and A. Paszewski Sulphur amino acid synthesis in Schizosaccharomyces pombe represents a specific variant of sulphur metabolism in fungi Yeast 19 2002 29 35
37. G.A. Marzluf Molecular genetics of sulfur assimilation in filamentous fungi and yeast Annu. Rev. Microbiol. 51 1997 73 96
38. T. Leustek, and K. Saito Sulfate transport and assimilation in plants Plant Physiol. 120 1999 637 643
39. T. Leustek, M.N. Martin, J.A. Bick, and J.P. Davies Pathways and regulation of sulfur metabolism revealed through molecular and genetic studies Annu. Rev. Plant Physiol. Plant Mol. Biol. 51 2000 141 165
40. A. Grossman, and H. Takahashi Macronutrient utilization by photosynthetic eukaryotes and the fabric of interactions Annu. Rev. Plant Physiol. Plant Mol. Biol. 52 2001 163 210
41. B. Lass, and C.I. Ulrich-Eberius Evidence for proton/sulfate cotransport and its kinetics in Lemna gibba G1 Planta 161 1984 53 60
42. A. Breton, and Y. Surdin-Kerjan Sulfate uptake in Saccharomyces cerevisiae: biochemical and genetic study J. Bacteriol. 132 1977 224 232
43. H. Cherest, H.C. Davidian, D. Thomas, V. Benes, W. Ansorge, and Y. Surdin-Kerjan Molecular characterization of two high affinity sulfate transporters in Saccharomyces cerevisiae Genetics 145 1997 627 635
44. H. Bussey, R.K. Storms, A. Ahmed, K. Albermann, E. Allen, W. Ansorge, R. Araujo, A. Aparicio, B. Barrell, K. Badcock, V. Benes, D. Botstein, S. Bowman, M. Bruckner, J. Carpenter, J.M. Cherry, E. Chung, C. Churcher, F. Coster, K. Davis, R.W. Davis, F.S. Dietrich, H. Delius, T. DiPaolo, and J. Hani The nucleotide sequence of Saccharomyces cerevisiae chromosome XVI Nature 387 1997 103 105
45. H. Takahashi, A. Watanabe-Takahashi, F.W. Wmith, M. Blake-Klaff, M.J. Hawkesford, and K. Saito The roles of three different functional sulphate transporters involved in uptake and translocation of sulphate in Arabidopsis thaliana Plant J. 23 2000 171 182
46. N. Yoshimoto, H. Takahashi, F. Smith, T. Yamaya, and K. Saito Two distinct high-affinity sulfate transporters with different inducibilities mediate uptake of sulfate in Arabidopsis roots Plant J. 29 2002 465 473
47. N. Yoshimoto, E. Inoue, K. Saito, T. Yamaya, and H. Takahashi Phloem-localizing sulfate transporter, Sultr1;3, mediates re-distribution of sulfur from source to sink organs in Arabidopsis Plant Physiol. 131 2003 1511 1517
48. H. Takahashi, M. Yamazaki, N. Sasakura, A. Watanabe, T. Leustek, J. de A. Engler, G. Engler, M. Van Mongagu, and K. Saito 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 94 1997 11102 11107
49. J.J. Vidmar, J.K. Schjoerring, B. Touraine, and A.D.M. Glass Regulation of the hvst1 gene encoding a high-affinity sulfate transporter from Hordeum vulgare Plant Mol. Biol. 40 1999 883 892
50. J.J. Vidmar, A. Tagmount, N. Cathala, B. Touraine, and J.C. Davidian Cloning and characterization of a root specific high-affinity sulfate transporter from Arabidopsis thaliana FEBS Lett. 475 2000 65 69
51. F.H. Yildiz, J.P. Davies, and A.R. Grossman Characterization of sulfate transport in Chlamydomonas reinhardtii during sulfur-limited and sulfur-sufficient growth Plant Physiol. 104 1994 981 987
52. F.H. Yildiz, J.P. Davies, and A.R. Grossman Sulfur availabilty and the SAC1 gene control adenosine triphosphate sulfurylase gene expression in Chlamydomonas reinhardtii Plant Physiol. 112 1996 669 675
53. T. Sahida, A. Stern, D. Lee, and J.A. Schiff Localization of a sulphate-activating system within Euglena mitochondria Biochem. J. 232 1985 357 365
54. H.-Ch. Chen, K. Yokthongwattana, A.J. Newton, and A. Melis SulP, a nuclear gene encoding a putative chloroplast-targeted sulfate permease in Chlamydomonas reinhardtii Planta 218 2003 98 106
55. N. Ohta, M. Matsuzaki, O. Misumi, S. Miyagishima, H. Nozaki, K. Tanaka, T. Shin-i, Y. Kohara, and T. Kuroiwa Complete sequence and analysis of the plastid genome of the unicellular red alga Cyanidioschyzon merolae DNA Res. 10 2003 67 77
56. H. Takahashi, W. Asanuma, and K. Saito Cloning of an Arabidopsis cDNA encoding a chloroplast localizing sulphate transporter isoform J. Exp. Bot. 50 1999 1713 1714
57. S. Lee, and T. Leustek APS kinase from Arabidopsis thaliana: genomic organization, expression, and kinetic analysis of the recombinant enzyme Biochem. Biophys. Res. Commun. 247 1998 171 175
58. R. Hell Molecular physiology of plant sulfur metabolism Planta 202 1997 138 148
59. T. Osslund, C. Chandler, and I. Segel ATP sulfurylase from higher plants Plant Physiol. 70 1982 39 45
60. A. Cornish-Bowden, and M.L. Cardenas Information transfer in metabolic pathways Eur. J. Biochem. 268 2001 6616 6624
61. T.C. Ullrich, M. Blaesse, and R. Huber Crystal structure of ATP sulfurylase from Saccharomyces cerevisiae, a key enzyme in sulfate activation EMBO J. 20 2001 316 329
62. I.J. MacRae, I.H. Segel, and A.J. Fisher Crystal structure of ATP sulfurylase from Penicillium chrysogenum: insights into the allosteric regulation of sulfate assimilation Biochemistry 40 2001 6795 6804
63. F. Renosto, R.L. Martin, L.M. Wailes, L.A. Daley, and I.H. Segel Regulation of inorganic sulfate activation in filamentous fungi. Allosteric inhibition of ATP sulfurylase by 3′-phosphoadenosine-5′- phosphosulfate J. Biol. Chem. 265 1990 10300 10308
64. F. Renosto, H.C. Patel, R.L. Martin, C. Thomassian, G. Zimmerman, and I.H. Segel ATP sulfurylase from higher plants: kinetic and structural characterization of the chloroplast and cytosol enzymes from spinach leaf Arch. Biochem. Biophys. 307 1993 272 285
65. C. Rotte, and T. Leustek 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 2000 715 724
66. J. Li, T. Saidha, and J.A. Schiff Purification and properties of two forms of ATP sulfurylase from Euglena Biochim. Biophys. Acta 1078 1991 68 76
67. H.M. Logan, N. Cathala, C. Grignon, and J.C. Davidian Cloning of a cDNA encoded by a member of the Arabidopsis thaliana ATP sulfurylase multigene family J. Biol. Chem. 271 1996 12227 12233
68. D. Klonus, R. Hofgen, L. Willmitzer, and J.W. Riesmeier Isolation and characterization of two cDNA clones encoding ATP-sulfurylases from potato by complementation of a yeast mutant Plant J. 6 1994 105 112
69. Y. Hatzfeld, N. Cathala, C. Grignon, and J.C. Davidian Effect of ATP sulfurylase overexpression in Bright yellow 2 tobacco cells Plant Physiol 116 1998 1307 1313
70. M. Murillo, and T. Leustek Adenosine-5′-triphosphate-sulfurylase from Arabidopsis thaliana and Escherichia coli are functionally equivalent but structurally and kinetically divergent: nucleotide sequence of two adenosine-5′-triphosphate-sulfurylase cDNAs from Arabidopsis thaliana and analysis of a recombinant enzyme Arch. Biochem. Biophys. 323 1995 195 204
71. T. Nozaki, T. Arase, Y. Shigeta, Y. Asai, T. Leustek, and T. Takeuchi Cloning and bacterial expression of adenosine-5′-triphosphate sulfurylase from the enteric protozoan parasite Entamoeba histolytica Biochim. Biophys. Acta 1429 1998 284 291
72. J.A. Bick, F. Aslund, Y. Chen, and T. Leustek Glutaredoxin function for the carboxyl-terminal domain of the plant-type 5′-adenylylsulfate reductase Proc. Natl. Acad. Sci. USA 95 1998 8404 8409
73. J.F. Gutierrez-Marcos, M.A. Roberts, E.I. Campbell, and J.L. Wray 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 1996 13377 13382
74. C.H. Lillig, S. Schiffmann, C. Berndt, and A. Berken Molecular and catalytic properties of Arabidopsis thaliana adenylyl sulfate (APS)-kinase Arch. Biochem. Biophys. 392 2001 303 310
75. C. Korch, H.A. Mountain, and A.S. Bystrom Cloning, nucleotide sequence, and regulation of MET14, the gene encoding the APS kinase of Saccharomyces cerevisiae Mol. Gen. Genet. 229 1991 96 108
76. D. Thomas, R. Barbey, and Y. Surdin-Kerjan Gene-enzyme relationship in the sulfate assimilation pathway of Saccharomyces cerevisiae. Study of the 3′-phosphoadenylylsulfate reductase structural gene J. Biol. Chem. 265 1990 15518 15524
77. S. Kopriva, T. Buchert, G. Fritz, M. Suter, R. Benda, V. Schunemann, A. Koprivova, P. Schurmann, A.X. Trautwein, P.M. Kroneck, and C. Brunold The presence of an iron-sulfur cluster in adenosine 5′-phosphosulfate reductase separates organisms utilizing adenosine 5′-phosphosulfate and phosphoadenosine 5′-phosphosulfate for sulfate assimilation J. Biol. Chem. 277 2002 21786 21791
78. B.A. Foster, S.M. Thomas, J.A. Mahr, F. Renosto, H.C. Patel, and I.H. Segel Cloning and sequencing of ATP sulfurylase from Penicillium chrysogenum. Identification of a likely allosteric domain J. Biol. Chem. 269 1994 19777 19786
79. A. Koprivova, A.J. Meyer, G. Schween, C. Herschbach, R. Reski, and S. Kopriva Functional knockout of the adenosine 5-phosphosulfate reductase gene in Physcomitrella patens revives an old route of sulfate assimilation J. Biol. Chem. 277 2002 32195 32201
80. Y. Gao, O.M.E. Schofield, and T. Leustek Characterization of sulfate assimilation in marine algae focusing on the enzyme 5′-adenylylsulfate reductase Plant Physiol. 123 2000 1087 1096
81. T. Saidha, S.Q. Na, J. Li, and J.A. Schiff A sulphate metabolizing centre in Euglena mitochondria Biochem. J. 253 1988 533 539
82. M. Nakayama, T. Akashi, and T. Hase Plant sulfite reductase: molecular structure, catalytic function and interaction with ferredoxin J. Inorg. Biochem. 82 2000 27 32
83. K. Kobayashi, and A. Yoshimoto Studies on yeast sulfite reductase IV. Structure and steady state kinetics Biochim. Biophys. Acta 705 1982 348 356
84. K. Yonekura-Sakakibara, T. Ashikari, Y. Tanaka, T. Kusumi, and T. Hase Molecular characterization of tobacco sulfite reductase: enzyme purification, gene cloning, and gene expression analysis J. Biochem. 124 1998 615 621
85. C. Bork, J.D. Schwenn, and R. Hell Isolation and characterization of a gene for assimilatory sulfite reductase from Arabidopsis thaliana Gene 212 1998 147 153
86. A. Brühl, T. Haverkamp, G. Gisselmann, and J.D. Schwenn A cDNA clone from Arabidopsis thaliana encoding plastidic ferredoxin:sulfite reductase Biochim. Biophys. Acta. 1295 1996 119 124
87. R. Hell, R. Jost, O. Berkowitz, and M. Wirtz Molecular and biochemical analysis of the enzymes of cysteine biosynthesis in the plant Arabidopsis thaliana Amino Acids 22 2002 245 257
88. H. Cherest, and Y. Surdin-Kerjan Genetic analysis of a new mutation conferring cysteine auxotrophy in Saccharomyces cerevisiae: updating of the sulfur metabolism pathway Genetics 130 1992 51 58
89. K. Soda Microbial sulfur amino acids: an overview Methods Enzymol. 143 1987 453 459
90. K. Saito Regulation of sulfate transport and synthesis of sulfur containing amino acids Curr. Opin. Plant Biol. 3 2000 188 195
91. R. Höfgen, O. Dreft, L. Willmitzer, and H. Hesse Manipulation of thiol contents in plants Amino Acids 20 2001 291 299
92. T. Nozaki, Y. Shigeta, Y. Saito-Nakano, M. Imada, and W.D. Kruger Characterization of transsulfuration and cysteine biosynthetic pathways in the protozoan hemoflagellate, Trypanosoma cruzi. Isolation and molecular characterization of cystathionine β-synthase and serine acetyltransferase from Trypanosoma J. Biol. Chem. 276 2001 6516 6523
93. H. Hesse, J. Lipke, T. Altmann, and R. Hofgen Molecular cloning and expression analyses of mitochondrial and plastidic isoforms of cysteine synthase (O-acetylserine(thiol)lyase) from Arabidopsis thaliana Amino Acids 16 1999 113 131
94. R. Jost, O. Berkowitz, M. Wirtz, L. Hopkins, M.J. Hawkesford, and R. Hell Genomic and functional characterization of the oas gene family encoding O-acetylserine (thiol) lyases, enzymes catalyzing the final step in cysteine biosyntheis in Arabidopsis thaliana Gene 253 2000 237 247
95. G. Noctor, A.C. Arisi, L. Jouanin, and C. Foyer Manipulation of glutathione and amino acid biosynthesis in the chloroplast Plant Physiol. 118 1998 471 482
96. C.H. Foyer, F.L. Theodoulou, and S. Delrot The functions of inter- and intracellular glutathione transport systems in plants Trends Plant Sci. 6 2001 486 492
97. A.J.L. Cooper Biochemistry of sulfur-containing amino acids Annu. Rev. Biochem. 52 1983 187 222
98. J.M. May, and C.J. Leaver Arabidopsis thaliana γ-glutamylcysteine synthetase is structurally unrelated to mammalian, yeast, and Escherichia coli homologs Proc. Natl. Acad. Sci. USA 91 1994 10059 10063
99. S.R. Soltaninassab, K.R. Sekhar, M.J. Meredith, and M.L. Freeman Multi-faceted regulation of γ-glutamylcysteine synthetase J. Cell. Physiol. 182 2000 163 170
100. D.V. Lueder, and M.A. Phillips Characterization of Trypanosoma brucei γ-glutamylcysteine synthetase, an essential enzyme in the biosynthesis of thrypanothione (diglutathionylspermidine) J. Biol. Chem. 271 1996 17485 17490
101. O.W. Griffith Mechanisms of action, metabolism, and toxicity of buthionine sulfoximine and its higher homologs, potent inhibitors of glutathione synthesis J. Biol. Chem. 257 1982 13704 13712
102. C.S. Huang, W.R. Moore, and A. Meister On the active site thiol of γ-glutamylcysteine synthetase: relationships to catalysis, inhibition, and regulation Proc. Natl. Acad. Sci. USA 85 1988 2464 2468
103. B.S. Kelly, W.E. Antholine, and O.W. Griffith Escherichia coli γ-glutamylcysteine synthetase J. Biol. Chem. 277 2001 50 58
104. O.W. Griffith, and R.T. Mulcahy The enzymes of glutathione synthesis: γ-glutamylcysteine synthetase Adv. Enzymol. Relat. Areas Mol. Biol. 73 1999 209 267
105. C.L. Wang, and D.J. Oliver Glutathione synthetase: similarities of the proteins from Schizosaccharomyces pombe and Arabidopsis thaliana Biochem. J. 326 1997 563 566
106. M.R. Rawlins, J.C. Leaver, and M.J. May Characterization of an Arabidopsis thaliana cDNA encoding glutathione synthetase FEBS Lett. 376 1995 81 86
107. S. Meierjohann, R.D. Walter, and S. Muller Glutathione synthetase from Plasmodium falciparum Biochem. J. 363 2002 833 838
108. R. Kneer, T.M. Kutchan, A. Hochberger, and M.H. Zenk Saccharomyces cerevisiae and Neurospora crassa contain heavy metal sequestering phytochelatin Arch. Microbiol. 157 1992 305 310
109. M. Oven, J.E. Page, M.H. Zenk, and T.M. Kutchan Molecular characterization of the homophytochelatin synthase of soybean Gycine max J. Biol. Chem. 277 2002 4747 4754
110. H. Kubota, K. sato, T. Yamada, and T. Maitani Phytochelatin homologs induced in hairy roots of horseradish Phytochemistry 53 2000 239 245
111. C. Avilés, H. Loza-Tavera, N. Terry, and R. Moreno-Sánchez Mercury pretreatment selects an enhanced cadmium accumulating phenotype in Euglena gracilis Arch. Microbiol. 180 2003 1 10
112. M. Berlich, S. Menge, I. Bruns, J. Schimdt, B. Schneider, and G.J. Krauss Coumarins give misleading absorbance with Ellman's reagent suggestive of thiol conjugates Analyst 127 2002 333 336
113. I. Bruns, K. Sutter, S. Menge, D. Neumann, and G.J. Krauss Cadmium let increase the glutathione pool in bryophytes J. Plant Physiol. 158 2001 79 89
114. O.K. Vatamaniuk, S. Mari, Y. Lu, and P.A. Rea Mechanism of heavy metal ion activation of phytochelatin (PC) synthase J. Biol. Chem. 275 2000 31451 31459
115. O.K. Vatamaniuk, S. Mari, A. Lang, S. Chalasani, L.O. Demkiv, and P.A. Rea Phytochelatin synthase, a dipeptidyltransferase that undergoes multisite acylation with γ-glutamylcysteine during catalysis J. Biol. Chem. 279 2004 22449 22460
116. E. Grill, S. Lffler, E.L. Winnacker, and M.H. Zenk Phytochelatins, the heavy-metal-binding peptides of plants, are synthesized from glutathione by a specific γ-glutamylcysteine dipeptidyl transpeptidase (phytochelatin synthase) Proc. Natl. Acad. Sci. USA 86 1989 6838 6842
117. S. Ha, A.P. Smith, R. Howden, W.M. Dietrich, S. Bugg, M.J. O'Connell, P.B. Goldsbrough, and C.S. Cobbett Phytochelatin synthase genes from Arabidopsis and yeast Schizosaccharomyces pombe Plant Cell 11 1999 1153 1163
118. W.E. Rauser Phytochelatins Annu. Rev. Biochem. 59 1990 61 86
119. S. Clemens, E.J. Kim, D. Neumann, and J. Schroeder Tolerance to toxic metals by a gene family of phytochelatin synthases from plants and yeast EMBO J. 18 1999 3325 3333
120. S. Heiss, A. Wachter, J. Bogs, C. Cobbett, and T. Rausch Phytochelatin synthase (PCS) protein is induced in Brassica juncea leaves after prolonged Cd exposure J. Exp. Bot. 54 2003 1833 1839
121. O.K. Vatamaniuk, E.A. Bucher, J,T. Ward, and P.A. Rea A new pathway for heavy metal detoxification in animals. Phytochelatin synthase is required for cadmium tolerance in Caenorhabditis elegans J. Biol. Chem. 276 2001 20817 20820
122. S. Clemens, J.I. Schroeder, and T. Degenkolb Caenorhabditis elegans expresses a functional phytochelatin synthase Eur. J. Biochem. 268 2001 3640 3643
123. C.S. Cobbett Phytochelatin biosynthesis and function in heavy-metal detoxification Curr. Opin. Plant Biol. 3 2000 211 216
124. R. Ruotolo, A. Peracchi, A. Bolchi, G. Infusini, A. Amoresano, and S. Ottonello Domain organization of phytochelatin synthase J. Biol. Chem. 279 2004 14686 14693
125. R. Howden, P.B. Goldsbrough, C.R. Andersen, and C.S. Cobbett Cadmium-sensitive, cad1 mutants of Arabidopsis thaliana are phytochelatin deficient Plant Physiol. 107 1995 1059 1066
126. T. Maier, C. Yu, G. Kullertz, and S. Clemens Localization and functional characterization of metal-binding sites in phytochelatin synthases Planta 218 2003 300 308
127. Y. Hayashi, C.W. Nakagawa, N. Mutoh, M. Isobe, and T. Goto Two pathways in the biosynthesis of cadystins (gamma EC)nG in the cell-free system of the fission yeast Biochem. Cell Biol. 69 1991 115 121
128. A. Al-Lahham, V. Rohde, P. Heim, R. Leuchter, J. Veeck, C. Wunderlich, K. Wolf, and M. Zimmermann Biosynthesis of phytochelatins in the fission yeast. Phytochelatin synthesis: a second role for the glutathione synthetase gene of Schizosaccharomyces pombe Yeast 15 1999 385 396
129. K. Imai, H. Obata, K. Shimizu, and T. Komiya Conversion of glutathione into cadystins and their analogs catalyzed by carboxypeptidase Y Biosci. Biotechnol. Biochem. 60 1996 1193 1194
130. B. Ono, K. Kijima, N. Ishii, K. Takahiro, A. Matsuda, A. Paszewski, and S. Shinoda Regulation of sulphate assimilation in Saccharomyces cerevisiae Yeast 12 1996 1153 1162
131. H. Takagi, K. Yoshioka, N. Awano, S. Nakamori, and B. Ono Role of Saccharomyces cerevisiae serine O-acetyltransferase in cysteine biosynthesis FEMS Microbiol. Lett. 218 2003 291 297
132. M. Noji, and K. Saito Molecular and biochemical analysis of serine acetyltransferase and cysteine synthase towards sulfur metabolic engineering in plants Amino Acids 22 2002 231 243
133. P.G. Richman, and A. Meister Regulation of γ-glutamylcysteine synthetase by non-allosteric feedback inhibition by glutathione J. Biol. Chem. 250 1975 1422 1426
134. A.C. Arisi, G. Noctor, C.H. Foyer, and L. Jouanin Modification of thiol contents in poplars (Populus tremula × P. alba) overexpressing enzymes involved in glutathione synthesis Planta 203 1997 272 362
135. G. Creissen, J. Firmin, M. Fryer, B. Kular, N. Leyland, H. Reynolds, G. Pastori, F. Wellburn, N. Baker, A. Wellburn, and P. Mullineaux Elevated glutathione biosynthetic capacity in the chloroplasts of transgenic tobacco plants paradoxically causes increased oxidative stress Plant Cell 11 1999 1277 1291
136. R. Hell, and L. Bergmann γ-Glutamylcysteine synthetase in higher plants: catalytic properties and subcellular localization Planta 180 1990 603 612
137. G. Noctor, A.C.M. Arisi, L. Jouanin, M.H. Valadier, Y. Roux, and H. Foyer The role of glycine in determining the rate of glutathione synthesis in poplar. Posible implications for glutathione production during stress Physiol. Plant 100 1997 255 263
138. W.E. Rauser, and P. Meuwly Retention of cadmium in roots of maize seedlings Plant Physiol. 109 1995 195 202
139. Y. Momose, and H. Iwahashi Bioassay of cadmium using a DNA microarray: genome-wide expression patterns of Saccharomyces cerevisiae response to cadmium Environ. Toxicol. Chem. 20 2003 2353 2360
140. M. Fauchon, G. Lagniel, J.C. Aude, L. Lombardia, P. Soularue, C. Petat, G. Marguerie, A. Sentenac, M. Werner, and J. Labarre Sulfur sparing in the yeast proteome in response to sulfur demand Mol. Cell 9 2002 713 723
141. M.Y. Hirai, T. Fujiwara, M. Awazuhara, T. Kimura, M. Noji, and K. Saito 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 2003 651 663
142. F.W. Smith, M.J. Hawkesford, P.M. Ealing, D.T. Clarkson, P.J. Vanden Berg, A.R. Belcher, and A.G. Warrilow Regulation of expression of a cDNA from barley roots encoding a high affinity sulphate transporter Plant J. 12 1997 875 884
143. S. Heiss, H.J. Schäfer, A. Haag-Kerwer, and T. Rausch Cloning sulfur assimilation genes of Brassica juncea L.: cadmium differentially affects the expression of a putative low-affinity sulfate transporter and isoforms of ATP sulfurylase and APS reductase Plant Mol. Biol. 39 1999 847 857
144. F.F. Nocito, L. Pirovano, M. Cocucci, and G.A. Sacchi Cadmium-induced sulfate uptake in maize roots Plant Physiol. 129 2002 1872 1879
145. K. Vido, D. Spector, G. Lagniel, S. Lopez, M. Toledano, and J. Labarre A proteome analysis of the cadmium response in Saccharomyces cerevisiae J. Biol. Chem. 276 2001 8469 8474
146. D.W. Stephen, and D.J. Jamieson Amino acid-dependent regulation of the Saccharomyces cerevisiae GSH1 gene by hydrogen peroxide Mol. Microbiol. 23 1997 203 210
147. U.H Dormer, J. Westwater, D.W.S. Stephen, and D.J. Jamieson Oxidant regulation of the Saccharomyces cerevisiae GSH1 gene Biochim. Biophys. Acta 1576 2002 23 29
148. D. Chen, W.M. Toone, J. Mata, R. Lyne, G. Burns, K. Kiviven, A. Brazma, N. Jones, and J. Bähler Global transcriptional responses of fission yeast to enviromental stress Mol. Cell Biol. 14 2003 214 229
149. H. Schäfer, A. Haag-Kerwer, and T. Rausch 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 γ-glutamylcysteine synthetase isoform Plant Mol. Biol. 37 1998 87 97
150. M.J. May, T. Vernoux, R. Sánchez-Fernandez, M.V. Montagu, and D. Ine Evidence for posttranscriptional activation of γ-glutamylcysteine synthetase during plant stress responses Proc. Natl. Acad. Sci. USA 95 1998 12049 12054
151. S. Lee, and S. Korban Transcriptional regulation of Arabidopsis thaliana phytochelatin synthase (AtPCS1) by cadmium during early stages of plant development Planta 215 2002 689 693
152. J. Hansen, and P.F. Johannesen Cysteine is essential for transcriptional regulation of the sulfur assimilation genes in Saccharomyces cerevisiae Mol. Gen. Genet. 263 2000 535 542
153. A. Bolchi, S. Petrucco, P.L. Tenca, C. Foroni, and S. Ottonello 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 1999 527 537
154. A.G. Lappartient, J.J. Vidmar, T. Leustek, A.D. Glass, and B. Touraine Inter-organ signaling in plants: regulation of ATP sulfurylase and sulfate transporter genes expression in roots mediated by phloem-translocated compound Plant J. 18 1999 89 95
155. P. Vauclare, S. Kopriva, D. Fell, M. Suter, L. Sticher, P. von Ballmoos, U. Krahenbuhl, R.O. den Camp, and C. Brunold 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 2002 729 740
156. P.L. Blaiseau, and D. Thomas Multiple transcriptional activation complexes tether the yeast activator Met4 to DNA EMBO J. 17 1998 6327 6336
157. U.H. Dormer, J. Westwater, N.F. McLaren, N.A. Kent, J. Mellor, and D.J. Jamieson Cadmium-inducible expression of the yeast GSH1 gene requires a functional sulfur-amino acid regulatory network J. Biol. Chem. 275 2000 32611 32616
158. L. Kuras, R. Barbey, and D. Thomas Assembly of a bZIP-bHLH transcription activation complex: formation of the yeast Cbf1-Met4-Met28 complex is regulated through Met28 stimulation of Cbf1 DNA binding EMBO J. 16 1997 2441 2451
159. J. Lee, C. Godon, G. Lagniel, D. Spector, J. Garin, J. Labarre, and M.B. Toledano Yap1 and Skn7 control two specialized oxidative stress response regulons in yeast J. Biol. Chem. 274 1997 16040 16046
160. A.L. Wu, and W.S. Moye-Rowley GSH1, which encodes gamma-glutamylcysteine, is a target gene for Yap1 transcriptional regulation Mol. Cell Biol. 14 1994 5832 5839
161. Z.-S. Li, Y.-P. Lu, R.-G. Zhen, M. Szczypka, D.J Thiele, and P.A. Rea A new pathway for vacuolar cadmium sequestration in Saccharomyces cerevisiae: YCF1-catalyzed transport of bis(glutathionato) cadmium Proc. Natl. Acad. Sci. USA 94 1997 42 47
162. D.E. Salt, and G.J. Wagner Cadmium transport across tonoplast of vesicles from oat roots J. Biol. Chem. 17 1993 12297 12302
163. D.M. Speiser, D.F. Ortiz, L. Kreppel, G. Scheel, G. McDonald, and D.W. Ow Purine biosynthetic genes are required for cadmium tolerance in Schizosaccharomyces pombe Mol. Cell Biol. 12 1992 5301 5310
164. R.H. Juang, K.F. McCue, and D.W. Ow Two purine biosynthetic enzymes required for cadmium tolerance in Schizosaccharomyces pombe utilize cysteine sulfinate in vitro Arch. Biochem. Biophys. 304 1993 392 401
165. J.S. Wu, H.Y. Sung, and R.H. Juang Transformation of cadmium-binding complexes during cadmium sequestration in fission yeast Biochem. Mol. Biol. Inter. 36 1995 1169 1175
166. + Mol. Microbiol. 42 2001 29 36
167. D.F. Ortiz, L. Kreppel, D.M. Speiser, G. Scheel, G. McDonald, and D.W. Ow Heavy metal tolerance in the fission yeast requires an ATP-binding cassette-type vacuolar membrane transporter EMBO J. 11 1992 3491 3499
168. Z.S. Li, M. Szczypka, Y.P. Lu, D.J. Thiele, and P.A. Rea The yeast cadmium factor protein (YCF1) is a vacuolar glutathione S-conjugate pump J. Biol. Chem. 271 1996 6509 6517
169. K.G. Sharma, D.L. Mason, G. Liu, P.A. Rea, A.K. Bachhawat, and S. Michaelis Localization, regulation, and substrate transport properties of Bpt1p, a Saccharomyces cerevisiae MRP-type ABC transporter Eukaryot. Cell. 1 2002 391 400
170. R. Sánchez-Fernández, T.G. Davies, J.O. Coleman, and P.A. Rea The Arabidopsis thaliana ABC protein superfamily, a complete inventory J. Biol. Chem. 276 2001 30231 30244
171. C.W. MacDiarmid, M.A. Milanick, and D.J. Eide Biochemical properties of vacuolar zinc transport systems of Saccharomyces cerevisiae J. Biol. Chem. 277 2002 39187 39194
172. L.E. Williams, J.K. Pittman, and J.L. Hall Emerging mechanisms for heavy metal transport in plants Biochim. Biophys. Acta 1465 2000 104 126
173. M.L. Guerinot The ZIP family of metal transporters Biochim. Biophys. Acta 1465 2000 190 198
174. P. Mäser, S. Thomine, J.I. Schroeder, J.M. Ward, K. Hirschi, H. Sze, I.N. Talke, A. Amtmann, J.M. Maathuis, D. Sanders, J. Harper, J. Tchieu, M. Gribskov, M.W. Persans, D. Salt, S.A. Kim, and M.L. Guerinot Phylogenetic relationships within cation transporter families of Arabidopsis Plant Physiol. 126 2001 1646 1667
175. X.F. Liu, F. Supek, N. Nelson, and V.C. Culotta Negative control of heavy metal uptake by the Saccharomyces cerevisiae BSD2 gene J. Biol. Chem. 272 1997 11763 11769
176. X.F. Liu, and V.C. Culotta Post-translation control of Nramp metal transport in yeast. Role of metal ions and the BSD2 gene J. Biol. Chem. 274 1999 4863 4868
177. D.S. Conklin, J.A. McMaster, M.R. Culbertson, and C. Kung COT1, a gene involved in cobalt accumulation in Saccharomyces cerevisiae Mol. Cell Biol. 12 1992 3678 3688
178. D.S. Conklin, M.R. Culbertson, and C. Kung Interactions between gene products involved in divalent cation transport in Saccharomyces cerevisiae Mol. Gen. Genet. 244 1994 303 311
179. C.W. MacDiarmid, L.A. Gaither, and D. Eide Zinc transporters that regulate vacuolar zinc storage in Saccharomyces cerevisiae EMBO J. 19 2000 2845 2855
180. C.W. MacDiarmid, M.A. Milanick, and D.J. Eide Induction of the ZRC1 metal tolerance gene in zinc-limited yeast confers resistance to zinc shock J. Biol. Chem. 279 2003 15065 15072
181. T. Bloß, S. Clemens, and D.H. Nies Characterization of the ZAT1p zinc trasnporter from Arabidopsis thaliana in microbial model organisms and reconstituted proteoliposomes Planta 214 2002 783 791
182. K.D. Hirschi, V.D. Korenkov, N.L. Wilganowski, and G.J. Wagner Expression of Arabidopsis CAX2 in tobacco. Altered metal accumulation and increased manganese tolerance Plant Physiol. 124 2000 125 133
183. P. Meuwly, and W.E. Rauser Alteration thiol pools in roots and shoots in maize seedlings exposed to cadmium Plant Physiol. 99 1992 8 15
184. J. Barbas, V. Santhanagopalan, W. Blaszczynski, W.R. Elli, and D.R. Winge Conversion in the peptides coating cadmium:sulfide crystallites in Candida glabrata J. Inorg. Biochem. 48 1992 95 105
185. C.T. Dameron, B.R. Smith, and D.R. Winge Glutathione-coated cadmium-sulfide crystallites in Candida glabrata J. Biol. Chem. 264 1989 17355 17360
186. O. Coppelloti Glutathione, cysteine and acid-soluble thiol levels in Euglena gracilis cells exposed to copper and cadmium Comp. Biochem. Physiol. 94C 1989 35 40
187. K. Nagel, U. Adelmeier, and J. Voigt Subcellular distribution of cadmium in the unicellular green alga Chamydomonas reinhardtii J. Plant Physiol. 149 1996 86 90
188. H.P. Carr, A. Cario, M.S. Yang, and M.H. Wong Characterization of the cadmium-binding capacity of Chlorella vulgaris Bull. Environ. Contam. Toxicol. 60 1998 433 440
189. N. Tsuji, N. Hirayanagi, M. Okada, H. Miyasaka, K. Hirata, M.H. Zenk, and K. Miyamoto Enhancement of tolerance to heavy metals and oxidative stress in Dunaliella tertiolecta by Zn-induced phytochelatin synthesis Biochem. Biophys. Res. Commun. 293 2002 653 659
190. S.K. Mehta, and J.P. Gaur Heavy-metal-induced proline accumulation and its role in ameliorating metal toxicity in Chlorella vulgaris New Phytol. 143 1999 253 259
191. S. Sripornadulsil, S. Traina, D.P.S. Verma, and R.T. Sayre Molecular mechanisms of proline-mediated tolerance to toxic heavy metals in transgenic microalgae Plant Cell 14 2002 2837 2847
192. Alia, P. Mohanty, and J. Matysik Effect of proline on the production of singlet oxygen Amino Acids 21 2001 195 200
193. Y.L. Zhu, E.A.H. Pilon-Smits, A.S. Tarun, S.U. Weber, L. Jouanin, and N. Terry Cadmium tolerance and accumulation in indian mustard is enhanced by overexpressing γ-glutamylcysteine synthetase Plant Physiol. 121 1999 1169 1177
194. Y.L. Zhu, E.A.H. Pilon-Smits, A.S. Tarun, L. Jouanin, and N. Terry Overexpression of glutathione synthetase in indian mustard enhances cadmium accumulation and tolerance Plant Physiol. 119 1999 73 79
195. C.M. Grant, F.H. MacIver, and I.W. Dawes Glutathione synthetase is dispensable for growth under both normal and oxidative stress conditions in the yeast Saccharomyces cerevisiae due to an accumulation of the dipeptide γ-glutamylcysteine Mol. Biol. Cell 8 1997 1699 1707
196. S.J. Kim, Y.H. Shin, E.H. Park, J.H. Sa, and C.J. Lim Regulation of the gene encoding glutathione synthetase from fission yeast J. Biochem. Mol. Biol. 36 2003 326 331
197. S. Lee, J.S. Moon, T.S. Ko, D. Petros, P.B. Goldsbrough, and S.S. Korban Overexpression of Arabidopsis phytochelatin synthase paradoxically leads to hypersensitivity to cadmium stress Plant Physiol. 131 2003 656 663
198. C.S. Hawes, and D.J.D. Nicholas Adenosine 5′-triphosphate sulphurylase from Saccharomyces cerevisiae Biochem. J. 133 1973 541 550
199. U. Schriek, and J.D. Schwenn Properties of the purified APS-kinase from Escherichia coli and Saccharomyces cerevisiae Arch. Microbiol. 145 1986 32 38
200. J.D. Schwenn, F.A. Krone, and K. Husmann Yeast PAPS reductase: properties and requirements of the purified enzyme Arch. Microbiol. 150 1988 313 319
201. B. Ono, K. Kijima, T. Inoue, S. Miyoshi, A. Matsuda, and S. Shinoda Purification and properties of Saccharomyces cerevisiae cystathionine β- synthase Yeast 10 1994 333 339
202. S. Yamagata, R.J. D'Andrea, S. Fujisaki, M. Isaji, and K. Nakamura Cloning and bacterial expression of the CYS3 gene encoding cystathionine γ-lyase of Saccharomyces cerevisiae and the physicochemical and enzymatic properties of the protein J. Bacteriol. 175 1993 4800 4808
203. G. Dennda, and M.R. Kula Purification and evaluation of the glutathione-synthesizing enzymes from Candida boidinni for cell-free synthesis of glutathione J. Biotechnol. 4 1986 143 158