Impact of sulfur starvation on cysteine biosynthesis in T-DNA mutants deficient for compartment-specific serine-acetyltransferase

Amino Acids

Volumn 39, Issue 4, 2010, Pages 1029-1042

  Krueger, Stephan ^a,c   Donath, Andrea ^a   Lopez Martin, M Carmen ^b   Hoefgen, Rainer ^a   Gotor, Cecilia ^b   Hesse, Holger ^a  

^a MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

^b UNIVERSITY OF SEVILLE   (Spain)

^c UNIVERSITY OF COLOGNE   (Germany)

Author keywords

CSC complex; Non aqueous fractionation; O acetylserine (thiol) lyase; SAT mutants; Serine acetyltransferase

Indexed keywords

CYSTEINE; CYSTEINE SYNTHASE; GAMMA GLUTAMYLCYSTEINE; GLUTATHIONE; ISOENZYME; MUTANT PROTEIN; SERINE ACETYLTRANSFERASE; SULFATE; SULFIDE; SULFUR; THIOL DERIVATIVE;

AMINO ACID SYNTHESIS; ARABIDOPSIS; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOSOLIC FRACTION; DNA TRANSFER; ENZYME ACTIVITY; ENZYME SPECIFICITY; GENE EXPRESSION REGULATION; GENE INACTIVATION; GENE INSERTION; METABOLIC REGULATION; METABOLITE; NONHUMAN; PLANT LEAF; PLANT METABOLISM; PLANT STRESS; PLASTICITY; PRIORITY JOURNAL; REDUCTION KINETICS; STARVATION; WILD TYPE;

ANION TRANSPORT PROTEINS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BIOLOGICAL TRANSPORT; CARBON-OXYGEN LYASES; CHLOROPLASTS; CYSTEINE; CYSTEINE SYNTHASE; CYTOSOL; DNA, BACTERIAL; GENE EXPRESSION REGULATION, PLANT; GENE KNOCKOUT TECHNIQUES; PLANTS, GENETICALLY MODIFIED; PLASMIDS; PLASTIDS; POLYMERASE CHAIN REACTION; RNA, PLANT; SEEDLING; SERINE; SERINE O-ACETYLTRANSFERASE; SULFATES; SULFHYDRYL COMPOUNDS; SULFUR;

ARABIDOPSIS THALIANA;

EID: 78650007274     PISSN: 09394451     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00726-010-0580-9     Document Type: Article

References (101)

1. Abdel-Ghany SE, Ye H, Garifullina GF, Zhang L, Pilon-Smits EAH, Pilon M (2005) Arabidopsis S-sulfocysteine synthase activity is essential for chloroplast function and long-day light-dependent redox control. Plant Physiol 138:161-172
2. Arnon DI, Hoagland DR (1939) A comparison of water culture and soil as media for crop production. Science 89:512-514
3. Beinert H (2000) A tribute to sulfur. FEBS J 267:5657-5664
4. Berkowitz O, Wirtz M, Wolf A, Kuhlmann J, Hell R (2002) Use of biomolecular interaction analysis to elucidate the regulatory mechanism of the cysteine synthase complex from Arabidopsis thaliana. J Biol Chem 277:30629-30634
5. Bogdanova N, Hell R (1997) Cysteine synthesis in plants: protein-protein interactions of serine acetyltransferase from Arabidopsis thaliana. Plant J 11:251-262
6. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254
7. Brunold C, Suter M (1982) Intracellular localization of serine acetyltransferase in spinach leaves. Planta 155:321-327
8. Buchner P, Stuiver C, Westerman S, Wirtz M, Hell R, Mj Hawkesford, De Kok LJ (2004) Regulation of sulfate uptake and expression of sulfate transporter genes in Brassica oleracea as affected by atmospheric H2S and pedospheric sulfate nutrition. Plant Physiol 136:3396-3408
9. Cobbett CS, Mj May, Howden R, Rolls B (1998) The glutathionedeficient, cadmium-sensitive mutant, cad2-1, of Arabidopsis thaliana is deficient in gamma-glutamylcysteine synthetase. Plant Physiol 16:73-78
10. Czechowski T, Bari RP, Stitt M, Scheible WR, Udvardi MK (2004) Real-time RT-PCR profiling of over 1400 Arabidopsis transcription factors: unprecedented sensitivity reveals novel rootand shoot-specific genes. Plant J 38:366-379
11. Droux M, Ruffet M-L, 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. FEBS J 255:235-245
12. Durenkamp M, De Kok L, Kopriva S (2007) Adenosine 50-phosphosulphate reductase is regulated differently in Allium cepa L. and Brassica oleracea L. upon exposure to H2S. J Exp Bot 58:1571-1579
13. Farré E, Tiessen A, Roessner U, Geigenberger P, Trethewey R, Willmitzer L (2001) Analysis of the compartmentation of glycolytic intermediates, nucleotides, sugars, organic acids, amino acids, and sugar alcohols in potato tubers using a nonaqueous fractionation method. Plant Physiol 127:685-700
14. Fettke J, Eckermann N, Tiessen A, Geigenberger P, Steup M (2005) Identification, subcellular localization and biochemical characterization of water-soluble heteroglycans (SHG) in leaves of Arabidopsis thaliana L.: distinct SHG reside in the cytosol and in the apoplast. Plant J 43:568-585
15. Gaitonde M (1967) A spectrophotometric method for the direct determination of cysteine in the presence of other naturally occurring amino acids. Biochem J 104:627-633
16. Geigenberger P, Stitt M (1993) Sucrose synthase catalyses a readily reversible reaction in vivo in developing potato tubers and other plant tissues. Planta 189:329-339
17. Gerhardt R, Heldt HW (1984) Measurement of subcellular metabolite levels in leaves by fractionation of freeze-stopped material in nonaqueous media. Plant Physiol 75:542-547
18. Haas FH, Heeg C, Queiroz R, Bauer A, Wirtz M, Hell R (2008) Mitochondrial serine acetyltransferase functions as pacemaker of cysteine synthesis in plant cells. Plant Physiol 148:1055-1067
19. Hawkesford M, De Kok L (2006) Managing sulphur metabolism in plants. Plant Cell Environ 29:382-395
20. Hawkesford M, Davidian J-C, Grignon C (1993) Sulphate/proton cotransport in plasma-membrane vesicles isolated from roots of Brassica napus L.: increased transport in membranes isolated from sulphur-starved plants. Planta 190:297-304
21. Heeg C, Kruse C, Jost R, Gutensohn M, Ruppert T, Wirtz M, Hell R (2008) Analysis of the Arabidopsis O-acetylserine(thiol)lyase gene family demonstrates compartment-specific differences in the regulation of cysteine synthesis. Plant Cell 20:168-185
22. Hell R, Bergmann L (1990) c-Glutamylcysteine synthetase in higher plants: catalytic properties and subcellular localization. Planta 180:603-612
23. Herschbach C, Rennenberg H (1991) Influence of glutathione (GSH) on sulphate influx, xylem loading and exudation in excised tobacco roots. J Exp Bot 42:1021-1029
24. Hesse H, Höfgen R (2003) Molecular aspects of methionine biosynthesis. Trends Plant Sci 8:259-262
25. Hesse H, Lipke J, Altmann T, Höfgen R (1999) Molecular cloning and expression analyses of mitochondrial and plastidic isoforms of cysteine synthase (O-acetylserine(thiol)lyase) from Arabidopsis thaliana. Amino Acids 16:113-131
26. Hirai M, Fujiwara T, Awazuhara M, Kimura T, Noji M, Saito K (2003) Global expression profiling of sulfur-starved Arabidopsis by DNA macroarray reveals the role of O-acetyl-L-serine as a general regulator of gene expression in response to sulfur nutrition. Plant J 33:651-663
27. Hirai M, Klein M, Fujikawa Y, Yano M, Goodenowe D, Yamazaki Y, Kanaya S, Nakamura Y, Kitayama M, Suzuki H, Sakurai N, Shibata D, Tokuhisa J, Reichelt M, Gershenzon J, Papenbrock J, Saito K (2005) Elucidation of gene-to-gene and metabolite-to-gene networks in Arabidopsis by integration of metabolomics and transcriptomics. J Biol Chem 280:25590-25595
28. Hopkins L, Parmar S, Blaszczyk A, Hesse H, Höfgen R, Hawkesford M (2005) O-Acetylserine and the regulation of expression of genes encoding components for sulfate uptake and assimilation in potato. Plant Physiol 138:433-440
29. Hothorn M, Wachter A, Gromes R, Stuwe T, Rausch T, Scheffzek K (2006) Structural basis for the redox control of plant glutamate cysteine ligase. J Biol Chem 281:27557-27565
30. Howarth JR, Domínguez-Solís JR, Gutiérrez- Alcalá G, Wray Jl, Romero LC, 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
31. Jez J, Cahoon R (2004) Kinetic mechanism of glutathione synthetase from Arabidopsis thaliana. J Biol Chem 279:42726-42731
32. Kataoka T, Watanabe-Takahashi A, Hayashi N, Ohnishi M, Mimura T, Buchner P, Mj Hawkesford, Yamaya T, Takahashi H (2004) Vacuolar sulfate transporters are essential determinants controlling internal distribution of sulfate in Arabidopsis. Plant Cell 16:2693-2704
33. Kawashima CG, Berkowitz O, Hell R, Noji M, Saito K (2005) Characterization and expression analysis of a serine acetyltransferase gene family involved in a key step of the sulfur assimilation pathway in Arabidopsis. Plant Physiol 137:220-230
34. Kim H, Awazuhara M, Hayashi H, Chino M, Fujiwara T (1997) Analysis of O-acetyl-L-serine in in vitro cultured soybean cotyledons. In: Cram J, De Kok LJD, Stulen I, Brunold C, Rennenberg H (eds) Sulphur metabolism in higher plants. Backhuys Publishers, Leiden, pp 307-309
35. Kopriva S, Mugford SG, Matthewman CA, Koprivova A (2009) Plant sulfate assimilation genes: redundancy vs. specialization. Plant Cell Rep 28:1769-1780
36. Koprivova A, Suter M, Den Camp R, Brunold C, Kopriva S (2000) Regulation of sulfate assimilation by nitrogen in Arabidopsis. Plant Physiol 122:737-746
37. Kredich N (1992) The molecular basis for positive regulation of cys promoters in Salmonella typhimurium and Escherichia coli. Mol Microbiol 6:2747-2753
38. Kredich N, Tomkins G (1966) The enzymatic synthesis of L-cysteine in Escherichia coli and Salmonella typhimurium. J Biol Chem 241:4955-4965
39. Kredich N, Becker M, Tomkins G (1969) Purification and characterization of cysteine synthetase, a bifunctional protein complex, from Salmonella typhimurium. J Biol Chem 244:2428-2439
40. Krueger S, Niehl A, Lopez-Martin MC, Steinhauser D, Donath A, Hildebrandt T, Romero LC, Hoefgen R, Gotor C, Hesse H (2009) Sub-cellular analysis of Arabidopsis serine acetyltransferase mutants: implications of compartmentation for cysteine biosynthesis. Plant Cell Environ 32:349-367
41. 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 15:10268-10275
42. Lappartient A, Vidmar J, Leustek T, Glass A, Touraine B (1999) Inter-organ signaling in plants: regulation of ATP sulfurylase and sulfate transporter genes expression in roots mediated by phloem-translocated compound. Plant J 18:89-95
43. Lass B, Ullrich-Eberius C (1984) Evidence for proton/sulfate cotransport and its kinetics in Lemna gibba G1. Planta 161:53-60
44. Leidreiter K, Kruse A, Heineke D, Robinson D, Heldt H (1995) Subcellular volumes and metabolic concentrations in potato (Solanum tuberosum cv. Désirée) leaves. Bot Acta 108:439-444
45. Leustek T, Martin M, Bick J-A, Davies J (2000) Pathways and regulation of sulphur metabolism revealed through molecular and genetic studies. Ann Rev Plant Physiol Plant Mol Biol 51:141-165
46. Lindroth P, Mopper K (1979) High performance liquid chromatographic determination of subpicomole amounts of amino acids by precolumn fluorescence derivatization with o-phthaldialdehyde. Anal Chem 51:1667-1674
47. Liu F, Yoo B-C, Lee J-Y, Pan W, Harmon A (2006) Calciumregulated phosphorylation of soybean serine acetyltransferase in response to oxidative stress. J Biol Chem 281:27405-27415
48. Lunn J, Droux M, Martin J, Douce R (1990) Localization of ATP sulfurylase and O-acetylserine(thiol)lyase in spinach leaves. Plant Physiol 94:1345-1352
49. Lynch A, Tyrrell R, Smerdon S, Briggs G, Wilkinson A (1994) Characterization of the CysB protein of Klebsiella aerogenes: direct evidence that N-acetylserine rather than O-acetylserine serves as the inducer of the cysteine regulon. Biochem J 299:129-136
50. Marquet A (2001) Enzymology of carbon-sulfur bond formation. Curr Opin Chem Biol 5:541-549
51. Maruyama-Nakashita A, Nakamura Y, Watanabe-Takahashi A, Yamaya T, Takahashi H (2004a) Induction of SULTR1.1 sulfate transporter in Arabidopsis roots involves protein phosphorylation/ dephosphorylation circuit for transcriptional regulation. Plant. Cell Physiol 45:340-345
52. Maruyama-Nakashita A, Nakamura Y, Yamaya T, Takahashi H (2004b) Regulation of high-affinity sulphate transporters in plants: towards systematic analysis of sulphur signalling and regulation. J Exp Bot 55:1843-1849
53. Maruyama-Nakashita A, Nakamura Y, Tohge T, Saito K, Takahashi H (2006) Arabidopsis SLIM1 Is a central transcriptional regulator of plant sulfur response and metabolism. Plant Cell 18:3235-3251
54. May MJ, Vernoux T, Sanchez-Fernandez R, Van Montagu M, Inze D (1998) Evidence for posttranscriptional activation of gammaglutamylcysteine synthetase during plant stress responses. Proc Natl Acad Sci USA 95:12049-12054
55. Mendel R, Hansch R (2002) Molybdoenzymes and molybdenum cofactor in plants. J Exp Bot 53:1689-1698
56. Meyer AJ (2008) The integration of glutathione homeostasis and redox signalling. J Plant Physiol 165:1390-1403
57. Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473-497
58. Neuenschwander U, Suter M, Brunold C (1991) Regulation of sulfate assimilation by light and O-acetyl-L-serine in Lemna minor L. Plant Physiol 97:253-258
59. Nikiforova V, Freitag J, Kempa S, Adamik M, Hesse H, Hoefgen R (2003) Transcriptome analysis of sulfur depletion in Arabidopsis thaliana: interlacing of biosynthetic pathways provides response specificity. Plant J 33:633-650
60. Nikiforova V, Bielecka M, Gakière B, Krüger S, Rinder J, Kempa S, Morcuende R, Scheible W-R, Hesse H, Höfgen R (2006) Effect of sulfur availability on the integrity of amino acid biosynthesis in plants. Amino Acids 30:173-183
61. Noctor G, Foyer C (1998) Ascorbate and glutathione: keeping active oxygen under control. Ann Rev Plant Physiol Plant Mol Biol 49:249-279
62. Noctor G, Gomez L, Vanacker H, Foyer C (2002) Interactions between biosynthesis, compartmentation and transport in the control of glutathione homeostasis and signalling. J Exp Bot 53:1283-1304
63. Noji M, Inoue K,Kimura N, Gouda A, SaitoK(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
64. Ostrowski J, Kredich N (1990) In vitro interactions of CysB protein with the cysJIH promoter of Salmonella typhimurium: inhibitory effects of sulfide. J Bacteriol 172:779-785
65. Ostrowski J, Jagura-Burdzy G, Kredich N (1987) DNA sequences of the cysB regions of Salmonella typhimurium and Escherichia coli. J Biol Chem 262:5999-6005
66. Ostrowski J, Wu J, Rueger D, Miller B, Siegel L, Kredich N (1989) Characterization of the cysJIH regions of Salmonella typhimurium and Escherichia coli B. DNA sequences of cysI and cysH and a model for the siroheme-Fe4S4 active center of sulfite reductase hemoprotein based on amino acid homology with spinach nitrite reductase. J Biol Chem 264:15726-15737
67. Pasternak M, Lim B, Wirtz M, Hell R, Cobbett CS, Meyer AJ (2008) Restricting glutathione biosynthesis to the cytosol is sufficient for normal plant development. Plant J 53:999-1012
68. Ravina C, Chang C-I, Tsakraklides G, Mcdermott J, Vega J, Leustek T, Gotor C, Davies J (2002) The sac mutants of Chlamydomonas reinhardtii reveal transcriptional and posttranscriptional control of cysteine biosynthesis. Plant Physiol 130:2076-2084
69. Rennenberg H (1983) Cysteine desulfhydrase activity in cucurbit plants: stimulation by preincubation with L- or D-cysteine. Phytochemistry 22:1557-1560
70. 2 on metabolite levels, activity of enzymes and expression of genes involved in cysteine metabolism. Plant Physiol Biochem 43:473-483
71. Riens B, Lohaus G, Heineke D, Heldt H (1991) Amino acid and sucrose content determined in the cytosolic, chloroplastic, and vacuolar compartments and in the phloem sap of spinach leaves. Plant Physiol 97:227-233
72. Rouached H, Berthomieu P, El Kassis E, Cathala N, Catherinot V, Labesse G, Davidian J-C, Fourcroy P (2005) Structural and functional analysis of the C-terminal STAS (sulfate transporter and anti-sigma antagonist) domain of the Arabidopsis thaliana sulfate transporter SULTR1.2. J Biol Chem 280:15976-15983
73. Ruffet M, Droux M, Douce R (1994) Purification and kinetic properties of serine acetyltransferase free of O-acetylserine(thiol)lyase from spinach chloroplasts. Plant Physiol 104:597-604
74. Ruffet M-L, Lebrun M, Droux M, Douce R (1995) Subcellular distribution of serine acetyltransferase from Pisum sativum and characterization of an Arabidopsis thaliana putative cytosolic isoform. FEBS J 227:500-509
75. Ruiz J, Blumwald E (2002) Salinity-induced glutathione synthesis in Brassica napus. Planta 214:965-969
76. Saito K (2000) Regulation of sulfate transport and synthesis of sulfurcontaining amino acids. Curr Opin Plant Biol 3:188-195
77. Shibagaki N, Grossman AR (2007) Functions of the STAS domain in the Arabidopsis sulfate transporter Sultr1;2. Bot Plant Biol 2007 (Joint Congress 2007. Abst. 1462 poster P11018)
78. Smith F, Ealing P, Hawkesford M, Clarkson D (1995) Plant members of a family of sulfate transporters reveal functional subtypes. Proc Natl Acad Sci USA 92:9373-9377
79. Stitt M, Wirtz W, Heldt H-W (1983) Regulation of sucrose synthesis by cytoplasmic fructose-bisphosphatase and sucrose phosphate synthase during photosynthesis in varying light and carbon dioxide. Plant Physiol 72:767-774
80. Takahashi H, Saito K (1996) Subcellular localization of spinach cysteine synthase isoforms and regulation of their gene expression by nitrogen and sulfur. Plant Physiol 112:273-280
81. Takahashi H, Yamazaki M, Sasakura N, Watanabe A, Leustek T, Engler J, Engler G, Van Montagu M, 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 94:11102-11107
82. Tiessen A, Hendriks JH, Stitt M, Branscheid A, Gibon Y, Farré EM, Geigenberger P (2002) Starch synthesis in potato tubers is regulated by post-translational redox modification of ADPglucose pyrophosphorylase: a novel regulatory mechanism linking starch synthesis to the sucrose supply. Plant Cell 14:2191-2213
83. Tsakraklides G, Martin M, Chalam R, Tarczynski M, Schmidt A, Leustek T (2002) Sulfate reduction is increased in transgenic Arabidopsis thaliana expressing 50-adenylylsulfate reductase from Pseudomonas aeruginosa. Plant J 32:879-889
84. Vauclare P, Kopriva S, Fell D, Suter M, Sticher L, von Ballmoos P, Krahenbuhl U, den Camp R, Brunold C (2002) Flux control of sulphate assimilation in Arabidopsis thaliana: adenosine 50-phosphosulphate reductase is more susceptible than ATP sulphurylase to negative control by thiols. Plant J 31:729-740
85. Vernoux T, Wilson RC, Seeley KA, Reichheld J-P, Muroy S, Brown S, Maughan SC, Cobbett CS, van Montagu M, Inze D, May M, Sung Z (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
86. Vetter RD, Matrai PA, Javor B, O'Brien J (1989) Reduced sulfur compounds in the environment: analysis by HPLC. Symp Ser Am Chem Soc 393:243-261
87. Völkel S, Grieshaber M (1992) Mechanisms of sulfide tolerance in the peanut worm Sipunculus nudus (Sipunculidae) and in the lugworm Arenicola marina (Polychaeta). J Comp Physiol B Biochem Syst Environ Physiol 126:469-477
88. Wachter A, Wolf S, Steininger H, Bogs J, Rausch T (2005) Differential targeting of GSH1 and GSH2 is achieved by multiple transcription initiation: implications for the compartmentation of glutathione biosynthesis in the Brassicaceae. Plant J 41:15-30
89. Warrilow A, Hawkesford M (1998) Separation, subcellular location and influence of sulphur nutrition on isoforms of cysteine synthase in spinach. J Exp Bot 49:1625-1636
90. Watanabe M, Kusano M, Oikawa A, Fukushima A, Noji M, Saito K (2008a) Physiological roles of the b-substituted alanine synthase gene family in Arabidopsis. Plant Physiol 146:310-320
91. Watanabe M, Mochida K, Kato T, Tabata S, Yoshimoto N, Noji M, Saito K (2008b) Comparative genomics and reverse genetics analysis reveal indispensable functions of the serine acetyltransferase gene family in Arabidopsis. Plant Cell 20:2484-2496
92. Winter H, Lohaus G, Heldt HW (1992) Phloem transport of amino acids in relation to their cytosolic levels in barley leaves. Plant Physiol 99:996-1004
93. Winter H, Robinson DG, Heldt HW (1993) Subcellular volumes and metabolite concentrations in barley leaves. Planta 191:180-190
94. Winter H, Robinson D, Heldt H (1994) Subcellular volumes and metabolite concentrations in spinach leaves. Planta 193:530-535
95. Wirtz M, 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
96. Wirtz M, Hell R (2006) Functional analysis of the cysteine synthase protein complex from plants: Structural, biochemical and regulatory properties. J Plant Physiol 163:273-286
97. Wirtz M, Hell R (2007) Dominant-negative modification reveals the regulatory function of the multimeric cysteine synthase protein complex in transgenic tobacco. Plant Cell 19:625-639
98. Wittstock U, Halkier BA (2002) Glucosinolate research in the Arabidopsis era. Trends Plant Sci 7:263-270
99. Wohlgemuth S, Taylor A, Grieshaber M (2000) Ventilatory and metabolic responses to hypoxia and sulphide in the lugworm Arenicola marina (L.). J Exp Biol 203:3177-3188
100. Xiang C, Werner B, Christensen E, Oliver D (2001) The biological functions of glutathione revisited in Arabidopsis transgenic plants with altered glutathione levels. Plant Physiol 126:564-574
101. Zrenner R, Willmitzer L, Sonnewald U (1993) Analysis of the expression of potato uridinediphosphate-glucose pyrophosphorylase and its inhibition by antisense RNA. Planta 190:247-252