Ascorbate and Glutathione: Keeping Active Oxygen under Control

Annual Review of Plant Biology

Volumn 49, Issue , 1998, Pages 249-279

  Noctor, Graham ^a   Foyer, Christine H ^b  

^a CEMAGREF   (France)

^b ABERYSTWYTH UNIVERSITY   (United Kingdom)

Author keywords

Antioxidative enzymes; Oxidative stress; Photorespiration; Photosynthesis; Signal transduction

Indexed keywords

EID: 0031735647     PISSN: 15435008     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.arplant.49.1.249     Document Type: Article

References (238)

1. Allen RD. 1995. Dissection of oxidative stress tolerance using transgenic plants. Plant Physiol. 107:1049-54
2. Alscher RG. 1989. Biosynthesis and antioxidant function of glutathione in plants. Physiol Plant. 77:457-64
3. Alvarez ME, Lamb C. 1997. Oxidative burst-mediated defense responses in plant disease resistance. See Ref. 185a, pp. 815-39
4. Anderson JV, Chevone BI, Hess JL. 1992. Seasonal variation in the antioxidant system of eastern white pine needles: evidence for thermal dependence. Plant Physiol. 98:501-8
5. Anderson JW, Foyer CH, Walker DA. 1983. Light-dependent reduction of dehydroascorbate and uptake of exogenous ascorbate by spinach chloroplasts. Planta 158:442-50
6. Aono M, Kubo A, Saji H, Tanaka K, Kondo N. 1993. Enhanced tolerance to photooxidative stress of transgenic Nicotiana tabacum with high chloroplastic glutathione reductase activity. Plant Cell Physiol. 34:129-35
7. Aono M, Saji H, Fujiyama K, Sugita M, Kondo N, Tanaka K. 1995. Decrease in activity of glutathione reductase enhances paraquat sensitivity in transgenic Nicotiana tabacum. Plant Physiol. 107:645-48
8. Arisi ACM. 1997. Tolérance au stress de peupliers transformés surexprimant la superoxyde dismutase la Γ-glutamyl cystéine sythétase ou la glutathion synthétase. PhD thesis. Univ. Paris XI, France
9. Arisi ACM, Noctor G, Foyer CH, Jouanin L. 1997. Modification of thiol contents in poplars (Populus tremula x P. alba) overexpressing enzymes involved in glutathione synthesis. Planta. 203:362-72
10. Arrigoni O. 1994. Ascorbate system in plant development. J. Bioenerg. Biomembr. 26:407-19
11. Asada K. 1992. Ascorbate peroxidase - a hydrogen peroxide-scavenging enzyme in plants. Physiol. Plant. 85:235-41
12. 2 scavenging in plants. See Ref. 185a, pp. 715-36
13. Asada K, Takahashi M. 1987. Production and scavenging of active oxygen in photosynthesis. In Photoinhibition, ed. DJ Kyle, CB Osmond, CJ Arntzen, pp. 227-87. Amsterdam: Elsevier
14. Asard H, Horemans N, Caubergs RJ. 1995. Involvement of ascorbic acid and a b-type cytochrome in plant plasma membrane redox reactions. Protoplasma 184: 36-41
15. Baig MM, Kelly S, Loewus F. 1970. L-ascorbic acid biosynthesis in higher plants from L-gulono-l,4-lactone and L-galactono-l,4-lactone. Plant Physiol. 46:277-80
16. Baker CJ, Orlandi EW. 1995. Active oxygen in plant pathogenesis. Annu. Rev. Phytopathol. 33:299-321
17. Beck E, Burkert A, Hofmann M. 1983. Uptake of L-ascorbate by intact chloroplasts. Plant Physiol. 73:41-45
18. Beeor-Tzahar T, Ben-Hayyim G, Holland D, Faltin Z, Eshdat Y. 1995. A stress-associated citrus protein is a distinct plant phospholipid hydroperoxide glutathione peroxidase. FEBS Lett. 366:151-55
19. Bielawski W, Joy KW, 1986. Reduced and oxidised glutathione and glutathione reductase activity in tissues of Pisum sativum. Planta 169:267-72
20. Bowler C, Slooten L, Vandenbranden S, De Rycke R, Botterman J, et al. 1991. Manganese superoxide dismutase can reduce cellular damage mediated by oxygen radicals in transgenic plants. EMBOJ. 10:1723-32
21. Bowler C, Van Montagu M, Inzé D. 1992. Superoxide dismutase and stress tolerance. Annu. Rev. Plant Physiol. Plant Mol. Biol. 43:83-116
22. Bowles DJ. 1990. Defense-related proteins in higher plants. Annu. Rev. Biochem. 59:873-907
23. Bratt CE, Arvidsson P-O, Carlsson M, Akerlund H-E. 1995. Regulation of violaxanthin de-epoxidase activity by pH and ascorbate concentration. Photosynth. Res. 45:169-75
24. Broadbent P, Creissen GP, Kular B, Wellburn AR, Mullineaux P. 1995. Oxidative stress responses in transgenic tobacco containing altered levels of glutathione reductase activity. Plant J. 8:247-55
25. Buettner GR, Jurkiewicz BA. 1996. Chemistry and biochemistry of ascorbic acid. In Handbook of Antioxidants, ed. E Cadenas, L Packer, pp. 91-115. New York: Dekker
26. 4 plants. Intercellular and intracellular location of ATP sulfurylase, cysteine synthase and cystathionine b-lyase in maize leaves. Plant Physiol. 75:873-75
27. Burns JJ. 1957. Missing step in man, monkey and guinea pig required for the biosynthesis of L-ascorbic acid. Nature 180:553
28. 2S on thiol composition of crop plants. J. Plant Physiol. 142:281-85
29. Buwalda F, De Kok LJ, Stulen I, Kuiper PJC. 1988. Cysteine, γ-glutamylcysteine and glutathione contents of spinach leaves as affected by darkness and application of excess sulfur. Physiol. Plant. 74:663-68
30. 2S in the absence of light is stimulated by the supply of glycine to the petiole. Physiol. Plant. 80: 196-204
31. Chamnongpol S, Willekens H, Langebartels C, Van Montagu M, Inzé D, Van Camp W. 1996. Transgenic tobacco with a reduced catalase activity develops necrotic lesions and induces pathogenesis-related expression under high light. Plant J. 10:491-503
32. Chen JJ, Goldsbrough PB. 1994. Increased activity of γ-glutamylcysteine synthetase in tomato cells selected for cadmium tolerance. Plant Physiol. 106:233-39
33. Chen ZX, Silva H, Klessig DF. 1993. Active oxygen species in the induction of plant systemic acquired resistance by salicylic acid. Science 262:1883-86
34. Conklin PL, Last RL. 1995. Differential accumulation of antioxidant mRNAs in Arabidopsis thaliana exposed to ozone. Plant Physiol. 109:203-12
35. Conklin PL, Pallanca J, Last RL, Smirnoff N. 1997. L-ascorbic acid metabolism in the ascorbate deficient Arabidopsis mutant vtc1. Plant Physiol. 115:1277-85
36. Conklin PL, Williams EH, Last RL. 1996. Environmental stress sensitivity of an ascorbic acid-deficient Arabidopsis mutant. Proc. Natl. Acad. Sci. USA 93:9970-74
37. Cordoba-Pedregosa MC, Gonzalez-Reyes JA, Sanadillas MS, Navas P, Cordoba F. 1996. Role of apoplastic and cell-wall peroxidases on the stimulation of root elongation by ascorbate. Plant Physiol. 112:1119-25
38. Creissen G, Broadbent P, Stevens R, Wellburn AR, Mullineaux P. 1996. Manipulation of glutathione metabolism in transgenic plants. Biochem. Soc. Trans. 24:465-69
39. Criqui MC, Jamet E, Parmentier Y, Marbach J, Durr A, Fleck J. 1992. Isolation and characterization of a plant cDNA showing homology to animal glutathione peroxidases. Plant Mol. Biol. 18:623-27
40. Czaninski Y, Sachot RM, Catesson AM. 1993. Cytochemical localisation of hydrogen peroxide in lignifying cell walls. Ann. Bot. 72:547-50
41. De Gara L, Paciolla C, Tommasi F, Liso R, Arrigoni O. 1994. In vivo inhibition of galactono-γ-lactone conversion to ascorbate by lycorine. J. Plant Physiol. 144:649-53
42. De Kok LJ, Kuiper PJC. 1986. Effect of short-term dark incubation with sulfate, chloride and selenate on the glutathione content of spinach leaf discs. Physiol. Plant. 68:477-82
43. De Kok LJ, Oosterhuis FA. 1983. Effects of frost-hardening and salinity on glutathione and sulfhydryl levels and on glutathione reductase activity in spinach leaves. Physiol. Plant. 58:47-51
44. Dipierro S, Borranccino G. 1991. Dehydroascorbate reductase from potato tubers. Photochemistry 30:427-29
45. Doke N. 1997. The oxidative burst: roles in signal transduction and plant stress. See Ref. 185a, pp. 785-813
46. Doulis AG, Debian N, Kingston-Smith AH, Foyer CH. 1997. Differential localization of antioxidants in maize leaves. Plant Physiol. 114:1031-37
47. Doulis AG, Hausladen A, Mondy B, Alscher RG, Chevone BI, et al. 1993. Antioxidant response and winter hardiness in red spruce (Picea rubens Sarg.). New Phytol 123:365-74
48. Dron M, Clouse SD, Dixon RA, Lawton MA, Lamb CJ. 1988. Glutathione and fungal elicitor regulation of a plant defense promoter in electroporated protoplasts. Proc. Nad. Acad. Sci. USA 85: 6738-42
49. Edwards EA, Rawsthorne S, Mullineaux PM. 1990. Subcellular distribution of multiple forms of glutathione reductase in leaves of pea (Pisum sativum L.). Planta 180:278-84
50. Edwards R, Blount JW, Dixon RA. 1991. Glutathione and elicitation of the phytoalexin response in legume cell cultures. Planta 184:403-9
51. Esterbauer H, Grill D. 1978. Seasonal variation of glutathione and glutathione reductase in needles of Picea abies. Plant Physiol 61:119-21
52. Farago S, Brunold C. 1994. Regulation of thiol contents in maize roots by intermediates and effectors of glutathione synthesis. J. Plant Physiol. 144: 433-37
53. Feierabend J, Dehne S. 1996. Fate of the porphyrin cofactors during the light-dependent turnover of catalase and of the photosystem II reaction centre protein D1 in mature rye leaves. Planta 198:413-22
54. Forti G, Elli G. 1995. The function of ascorbic acid in photosynthetic phosphorylation. Plant Physiol. 109:1207-11
55. Foyer CH. 1997. Oxygen metabolism and electron transport in photosynthesis. See Ref. 185a, pp. 587-22
56. Foyer CH, Furbank RT, Harbinson J, Horton P. 1990. The mechanisms contributing to photosynthetic control of electron transport by carbon assimilation in leaves. Photosynth. Res. 25:83-100
57. Foyer CH, Halliwell B. 1976. The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133: 21-25
58. Foyer CH, Halliwell B. 1977. Purification and properties of dehydroascorbate reductase from spinach leaves. Phytochemistry 16:1347-50
59. Foyer CH, Harbinson J. 1994. Oxygen metabolism and the regulation of photosynthetic electron transport. In Causes of Photooxidative Stresses and Amelioration of Defense Systems in Plants, ed. CH Foyer, P Mullineaux, pp. 1-42. Boca Raton, FL: CRC Press
60. Foyer CH, Lelandais M. 1996. A comparison of the relative rates of transport of ascorbate and glucose across the thylakoid, chloroplast and plasma membranes of pea leaf mesophyll cells. J. Plant Physiol. 148:391-98
61. Foyer CH, Lelandais M, Galap C, Kunert K-J. 1991. Effects of elevated cytosolic glutathione reductase activity on the cellular glutathione pool and photosynthesis in leaves under normal and stress conditions. Plant Physiol. 97:863-72
62. Foyer CH, Lopez-Delgado H, Dat JF, Scott IM. 1997. Hydrogen peroxide- and glutathione-associated mechanisms of acclimatory stress tolerance and signalling. Physiol. Plant. 100:241-54
63. Foyer CH, Rowell J, Walker D. 1983. Measurements of the ascorbate content of spinach leaf protoplasts and chloroplasts during illumination. Planta 157:239-44
64. Foyer CH, Souriau N, Perret S, Lelandais M, Kunert KJ, et al. 1995. Over-expression of glutathione reductase but not glutathione synthetase leads to increases in antioxidant capacity and resistance to photoinhibition in poplar trees. Plant Physiol. 109:1047-57
65. Frommer WB, Hummel S, Rentsch D. 1994. Cloning of an Arabidopsis transporting protein related to nitrate and peptide transporters. FEBS Lett. 347:185-89
66. 4 photosynthesis plants. Science 209:513-15
67. Gillham DJ, Dodge AD. 1986. Hydrogen peroxide scavenging systems within pea chloroplasts. Planta 167:246-51
68. Gonzalez-Reyes JA, Alcain FJ, Caler JA, Serrano A, Cordoba F, Navas P. 1994. Relationship between apoplastic ascorbate regeneration and the stimulation of root growth in Allium apa L. Plant Sci. 100:23-29
69. Grantz AA, Brummell DA, Bennett AB. 1995. Ascorbate free radical reductase mRNA levels are induced by wounding. Plant Physiol 108:411-18
70. Grill E, Löffler S, Winnacker EL, Zenk MH. 1989. 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 86:6838-42
71. 14C]glucose to L-ascorbic acid in Pelargonium crispum (L.) L' Her. Plant Physiol 70:1233
72. Guo Z-J, Nakagawara S, Sumitani K, Ohta Y. 1993. Effect of intracellular glutathione level on the production of 6-methoxymellein in cultured carrot (Daucus carota) cells. Plant Physiol. 102:45-51
73. Gushima H, Yasuda S, Soeda E, Yokota M, Kondo M, Kimura A. 1984. Complete nucleotide sequence of the E.coli glutathione synthetase gsh-II. Nucleic Acids Res. 12:9299-307
74. Halliwell B, Aeschbach R, Loliger I, Aruoma OI. 1995. The characterization of antioxidants. Food Chem. Toxicol. 333:601-17
75. Hausladen A, Kunert KJ. 1990. Effects of artificially enhanced levels of ascorbate and glutathione on the enzymes monodehydroascorbate reductase, dehydroascorbate reductase, and glutathione reductase in spinach (Spinacia oleracea). Physiol. Plant. 79:384-88
76. Hausladen A, Madamanchi NR, Fellows S, Alscher RG, Amundson RG. 1990. Seasonal changes in antioxidants in red spruce as affected by ozone. New Phytol. 115:447-58
77. Heber U, Krause H. 1980. What is the physiological role of photorespiration? Trends Biochem. Sci. 9:32-34
78. Hell R, Bergmann L. 1988. Glutathione synthetase in tobacco suspension cultures: catalytic properties and localization. Physiol Plant. 72:70-76
79. Hell R, Bergmann L. 1990. γ-Glutamylcysteine synthetase in higher plants: catalytic properties and subcellular localization. Planta 180:603-12
80. Helsper JP, Kagan L, Hilby CL, Maynard TM, Loewus FA. 1982. L-ascorbic acid synthesis in Ochmmonas danica. Plant Physiol. 69:465-68
81. Deleted in proof
82. Herschbach C, Rennenberg H. 1994. Influence of glutathione (GSH) on net uptake of sulphate and sulphate transport in tobacco plants. J. Exp. Bot. 45:1069-76
83. Hertwig B, Streb P, Feirerabend J. 1992. Light dependence of catalase synthesis and degradation in leaves and the influence of interfering stress conditions. Plant Physiol. 100:1547-53
84. Holland D, Ben-Hayyim G, Faltin Z, Camoin L, Strosberg AD, Eshdat Y. 1993. Molecular characterization of a salt-stress associated protein in citrus: protein and cDNA sequence homology to mammalian glutathione peroxidases. Plant Mol. Biol. 21:923-27
85. Horemans N. 1997.Ascorbate-mediated functions at the plasma membrane of higher plants. PhD thesis. Univ. Antwerpen, Belg.
86. Horemans N, Asard H, Caubergs RJ. 1994. The role of ascorbate free radical as an electron acceptor to cytochrome b-mediated trans-plasma membrane electron transport in higher plants. Plant Physiol. 104:1455-58
87. Horton P, Ruban AV, Walters RG. 1996. Regulation of light harvesting in green plants. Annu. Rev. Plant. Physiol. Plant Mol. Biol. 47:655-84
88. Hossain MA, Asada K. 1984. Purification of dehydroascorbate reductase from spinach and its characterisation as a thiol enzyme. Plant Cell Physiol. 25:85-92
89. Huang CS, Chang LS, Anderson ME, Meister A. 1993. Catalytic and regulatory properties of the heavy subunit of rat kidney γ-glutamylcysteine synthetase. J. Biol. Chem. 268:19675-80
90. Jabs T, Dietrich RA, Dangl JL. 1996. Initiation of runaway cell death in an Arabidopsis mutant by extracellular superoxide. Science 273:1853-55
91. Jakob B, Heber U. 1996. Photoproduction and detoxification of hydroxyl radicals in chloroplasts and leaves in relation to photoinactivation of photosystems I and II. Plant Cell Physiol. 37:629-35
92. Jamaï A, Tommasini R, Martinoia E, Delrot S. 1996. Characterization of glutathione uptake in broad bean leaf protoplasts. Plant Physiol. 111:1145-52
93. Jiménez A, Hernandez JA, del Rio LA, Sevilla F. 1997. Evidence for the presence of the ascorbate-glutathione cycle in mitochondria and peroxisomes of pea leaves. Plant Physiol. 114:275-84
94. Johnson RR, Cranston HJ, Chaverra ME, Dyer WE. 1995. Characterization of cDNA clones for differentially expressed genes in embryos of dormant and nondormant Avena fatua L. cayopses. Plant Mol. Biol 28:113-22
95. Kaiser WM. 1979. Reversible inhibition of the Calvin cycle and activation of oxidative pentose phosphate cycle in isolated intact chloroplasts by hydrogen peroxide. Planta 145:377-82
96. Kaprinski S, Escobar C, Karprinska B, Creissen G, Mullineaux PM. 1997. Photosynthetic electron transport regulates the expression of cytosolic ascorbate peroxidase genes in Arabidopsis during excess light stress. Plant Cell 9:627-40
97. Kato Y, Urano J, Maki Y, Ushimaru T. 1997. Purification and characterisation of dehydroascorbate reductase from rice. Plant Cell Physiol. 38:173-78
98. Kerk NM, Feldman LJ. 1995. A biochemical model for initiation and maintenance of the quiescent center: implications for organisation of root meristems. Plant Development 121:2825-33
99. Keys AJ. 1980. Prospects for increasing photosynthesis by control of photorespiration. Pestic. Sci. 19:313-16
100. Klapheck S. 1988. Homoglutathione: isolation, quantification and occurrence in legumes. Physiol Plant. 74:727-32
101. Klapheck S, Chrost B, Starke J, Zimmerman H. 1992. γ-Glutamyl-cysteinylserine - a new homologue of glutathione in plants of the family Poaceae. Botanica Acta 105:174-79
102. Klapheck S, Latus C, Bergmann L. 1987. Localization of glutathione synthetase and distribution of glutathione in leaf cells of Pisum sativum L. J. Plant Physiol. 131:123-31
103. Klapheck S, Zopes H, Levels HG, Bergmann L. 1988. Properties and localization of the homoglutathione synthetase from Phaseolus coccineus leaves. Physiol. Plant. 74:733-39
104. Koike S, Patterson BD. 1988. Diurnal variation of glutathione levels in tomato seedlings. Hort. Sci. 23:713-14
105. Kubo A, Saji H, Tanaka K, Kondo N. 1995. Expression of Arabidopsis cytosolic ascorbic peroxidase gene in response to ozone or sulfur dioxide. Plant Mol Biol. 29:479-86
106. Kunert KJ, Foyer C. 1993. Thiol/disulfide exchange in plants. In Sulfur Nutrition and Sulfur Assimilation in Higher Plants, ed. LJ de Kok, I Stulen, H Rennenberg, C Brunold, WE Rauser, pp. 139-51. The Hague: SPB Acad.
107. Kurokawa H, Ishida T, Nishio K, Arioka H, Sata M, et al. 1995. γ-Glutamylcysteine synthetase gene overexpression results in increased activity of the ATP-dependent glutathione S-conjugate export pump and cisplatin resistance. Biochem. Biophys. Res. Commun. 216:258-64
108. Lamoureux GL, Rusness DG. 1993. Glutathione in the metabolism and detoxification of xenobiotics in plants. In Sulfur Nutrition and Assimilation in Higher Plants, ed. LJ de Kok, I Stulen, H Rennenberg, C Brunold, WE Rauser, pp. 221-37. The Hague: SPB Acad.
109. Lappartient AG, Touraine B. 1996. Demand-driven control of root ATP sulfurylase activity and sulphate uptake in intact Canola. Plant Physiol. 111:147-57
110. Lappartient AG, Touraine B. 1997. Glutathione-mediated regulation of ATP sulfurylase activity, sulfate uptake, and oxidative stress response in intact Canola roots. Plant Physiol. 114:177-83
111. Law MY, Charles SA, Halliwell B. 1983. Glutathione and ascorbic acid in spinach (Spinacea oleracea) chloroplasts. Biochem. J. 210:899-903
112. Law MY, Halliwell B. 1986. Purification and properties of glutathione synthetase from spinach (Spinacia oleracea) leaves. Plant Sci. 4:185-91
113. Leegood RC, Lea PJ, Adcock MD, Häusler RE. 1995. The regulation and control of photorespiration. J. Exp. Bot. 46:1397-414
114. 2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79:583-93
115. Liso R, De Gara L, Tommasi F, Arrigoni O. 1985. Ascorbic acid requirement for increased peroxidase activity during potato tuber slice aging. FEBS Lett. 187:141-45
116. Loewus FA. 1988. Ascorbic acid and its metabolic products. In The Biochemistry of Plants, ed. J Priess, 14:85-107. New York: Academic
117. Loewus MW, Bedgar DL, Saito K, Loewus FA. 1990. Conversion of L-sorbosone to L-ascorbic acid by a NADP-dependent dehydrogenase in bean and spinach leaf. Plant Physiol. 94:1492-95
118. Lunn JE, Droux M, Martin J, Douce R. 1990. Localization of ATP sulphurylase and O-acetylserine(thiol)lyase in spinach leaves. Plant Physiol. 94:1345-52
119. Luwe M. 1996. Antioxidants in the apoplast and symplast of beech (Fagus sylvatica L.) leaves: seasonal variations and responses to changing ozone concentrations in air. Plant Cell Environ. 19: 321-28
120. Macnicol PK. 1987. Homoglutathione and glutathione synthetases of legume seedlings: partial purification and sub-strate specificity. Plant Sci. 53:229-35
121. Madamanchi NR, Yu X, Doulis A, Alscher RG, Hatzios KK, Cramer CL. 1994. Acquired resistance to herbicides in pea cultivars through pretreatment with sulfur dioxide. Pestic. Biochem. Physiol. 48:31-40
122. Malan C, Greyling MM, Gressel J. 1990. Correlation between CuZn superoxide dismutase and glutathione reductase, and environmental and xenobiotic stress tolerance in maize inbreds. Plant Sci. 69:157-66
123. Mapson LW, Breslow E. 1958. Biological synthesis of ascorbic acid: L-galactono-γ-lactone dehydrogenase. Biochem. J. 68:359-406
124. Mapson LW, Isherwood FA. 1956. Biological synthesis of ascorbic acid: the conversion of derivatives of D-galacturonic acid into L-ascorbic acid by plant extracts. Biochem. J. 64:151-57
125. Marrs K. 1996. The functions and regulation of glutathione S-transferases in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47:127-58
126. May MJ, Hammond-Kosack KE, Jones DG. 1996. Involvement of reactive oxygen species, glutathione metabolism and lipid peroxidation in the Cf-gene-dependent defense response of tomato cotyledons induced by race-specific elicitors of Cladosporium fulvum. Plant Physiol. 110:1367-79
127. May MJ, Leaver CJ. 1993. Oxidative stimulation of glutathione synthesis in Arabidopsis thaliana suspension cultures. Plant Physiol. 103:621-27
128. May MJ, Leaver CJ. 1994. Arabidopsis thaliana γ glutamylcysteine synthetase is structurally unrelated to mammalian, yeast, and Escherichia coli homologs. Proc. Natl. Acad. Sci. USA 91:10059-63
129. McKersie BD, Bowley SR, Harjanto E, Lepreince O. 1996. Water-deficit tolerance and field performance of transgenic alfalfa overexpressing superoxide dismutase. Plant Physiol. 111:1171-81
130. McKersie BD, Chen YR, De Beus M, Bowley SR, Bowler C, et al. 1993. Superoxide dismutase enhances tolerance of freezing stress in transgenic alfalfa (Medicago sativa L.). Plant Physiol. 103:1155-63
131. Mehdy MC. 1994. Active oxygen species in plant defense against pathogens. Plant Physiol. 105:467-42
132. Mehlhorn H, Lelandais M, Korth HG, Foyer CH. 1996. Ascorbate is the natural substrate for plant peroxidases. FEBS Lett. 378:203-6
133. Meister A. 1988. Glutathione metabolism and its selective modification. J. Biol Chem. 263:17205-8
134. Meister A. 1994. Glutathione-ascorbic acid antioxidant system in animals. J. Biol Chem. 269:9397-400
135. Meuwly P, Thibault P.Rauser WE. 1993. γ-Glutamylcysteinylglutamic acid - a new homologue of glutathione in maize seedlings exposed to cadmium. FEBS Lett. 336:472-76
136. Mittler R, Lam E. 1996. Sacrifice in the face of foes: pathogen-induced programmed cell death in higher plants. Trends Microbiol. 4:10-15
137. Mittler R, Zilinskas BA. 1992. Molecular cloning and characterization of a gene encoding pea cytosolic ascorbate peroxidase. J. Biol. Chem. 267:21802-7
138. Mittler R, Zilinskas BA. 1994. Regulation of pea cytosolic ascorbate peroxidase and other antioxidant enzymes during the progression of drought stress and following recovery from drought. Plant J. 5:397-405
139. Miyake C, Asada K. 1992. Thylakoidbound ascorbate peroxidase in spinach chloroplasts and photoregeneration of its primary oxidation product monodehydroascorbate radicals in thylakoids. Plant Cell Physiol. 33:541-53
140. Mulcahy RT, Bailey HH, Gipp JJ. 1994. Up-regulation of γ-glutamylcysteine synthetase activity in melphalan-resistant human multiple myeloma cells expressing increased glutathione levels. Cancer Chemother. Pharmacol. 34:67-71
141. Mulcahy RT, Bailey HH, Gipp JJ. 1995. Transfection of complementary DNAs for the heavy and light subunits of human γ-glutamylcysteine synthetase results in an elevation of intracellular glutathione and resistance to melphalan. Cancer Res. 55:4771-75
142. Mullineaux PM, Creissen G, Broadbent P, Reynolds H, Kular B, Wellburn A. 1994. Elucidation of the role of glutathione reductase using transgenic plants. Biochem. Soc. Trans. 22:931-36
143. Mullineaux PM, Wellburn AR, Baker NR, Creissen GP. 1997. Increased capacity for glutathione biosynthesis in the chloroplast paradoxically promotes oxidative stress in transgenic tobacco. In Sulphur Metabolism in Higher Plants. Molecular, Ecophysiological and Nutritional Aspects, ed. WJ Cram, LJ De Kok, I Stufen, C Brunold, H Rennenberg, pp. 269-70. Leiden: Backhuys
144. Nakagawara S, Nakamura N, Guo Z-J, Sumitani K, Katoh K, Ohta Y. 1993. Enhanced formation of a constitutive sesquiterpenoid in culture cells of liverwort, Calypogeia granulata Inoue during elicitation; effects of vanadate. Plant Cell Physiol. 34:421-29
145. Nakano Y, Asada K. 1987. Purification of ascorbate peroxidase in spinach chloroplasts: its inactivation in ascorbate-depleted medium and reactivation by monodehydroascorbate radical. Plant Cell Physiol. 28:131-40
146. Navas P, Gomez-Diaz C. 1995. Ascorbate free radical and its role in growth control. Protoplasma 184:8-13
147. Nemoto S, Otsuka M, Arakawa N. 1996. Inhibitory effect of ascorbate on cell growth: relation to catalase activity. J. Nutr. Sci. Vitaminol. 43:77-85
148. Nijs D, Kelley PM. 1991. Vitamins C and E donate single hydrogen atoms in vivo. FEBS Lett. 284:147-51
149. Nishikimi M, Yagi K. 1996. Biochemistry and molecular biology of ascorbic acid biosynthesis. In Subcellular Biochemistry Ascorbic Acid: Biochemistry and Biomedical Cell Biology, ed. J Harris, 25:17-39. New York: Plenum
150. Deleted in proof
151. Noctor G, Arisi ACM, Jouanin L, Kunert KJF, Rennenberg H, Foyer CH. 1997. Glutathione biosynthesis and metabolism explored in transformed poplars. J. Exp. Bot. In press
152. Noctor G, Arisi ACM, Jouanin L, Valadier MH, Roux Y, Foyer CH. 1997. Light-dependent modulation of foliar glutathione synthesis and associated amino acid metabolism in transformed poplar. Planta 202:357-69
153. Noctor G, Arisi ACM, Jouanin L, Valadier MH, Roux Y, Foyer CH. 1997. The role of glycine in determining the rate of glutathione synthesis in poplars. Possible implications for glutathione production during stress. Physiol. Plant. 100:255-63
154. Noctor G, Jouanin L, Foyer CH. 1997. The biosynthesis of glutathione explored in transgenic plants. In Regulation of Enzymatic Systems Detoxifying Xenobiotics in Plants, ed. K Hatzios, pp. 109-24. Dordrecht: Kluwer Academic
155. Noctor G, Strohm M, Jouanin L, Kunert KJ, Foyer CH, Rennenberg H. 1996. Synthesis of glutathione in leaves of transgenic poplar (Populus tremula x P. alba) overexpressing y-glutamyl-cysteine synthetase. Plant Physiol 112: 1071-78
156. Nussbaum S, Schmutz D, Brunold C. 1988. Regulation of assimilatory sulfate reduction by cadmium in Zea mays L. Plant Physiol. 88:1407-10
157. Oba K, Fukui M, Imai Y, Iriyama S, Nogami K. 1994. L-galactono-γ-lactone dehydrogenase: partial characterization, induction of activity and role in the synthesis of ascorbic acid in wounded white potato tuber tissue. Plant Cell Physiol. 35:473-78
158. Oba K, Ishikawa S, Nichikawa M, Mizuno H, Yamamoto T. 1995. Purification and properties of L-galactono-γ-lactone dehydrogenase, a key enzyme for ascorbic acid biosynthesis, from sweet potato roots. J. Biochem. 117:120-24
159. Ogren WL. 1984. Photorespiration: pathways, regulation and modification. Annu. Rev. Plant Physiol. 35:415-42
160. Ohtake Y, Kunihiko W, Tezuka H, Ogata T, Yabuuchi S, et al. 1989. Expression of the glutathione synthetase gene of Escherichia coli B in Saccharomyces cervisiae. J. Ferment. Bioeng. 68:390-94
161. Olson PD, Varner JE. 1993. Hydrogen peroxide and lignification. Plant J. 4:887-92
162. Osmond CB, Grace SC. 1995. Perspectives on photoinhibition and photorespiration in the field: quintessential inefficiencies of the light and dark reactions of photosynthesis? J. Exp. Bot. 46:1351-62
163. Padh H. 1990. Cellular functions of ascorbic acid. Biochem. Cell Biol. 68: 1166-73
164. Pitcher LH, Brennan E, Hurley A, Dunsmuir P, Tepperman JM, Zilinskas BA. 1991. Overproduction of petunia copper/zinc superoxide dismutase does not confer ozone tolerance in transgenic tobacco. Plant Physiol. 97:452-55
165. Rolle A, Wieser G, Havranek WM. 1995. Quantification of ozone influx and apoplastic ascorbate content in needles of Norway spruce trees (Picea abies L. Karst.) at high altitudes. Plant Cell Environ. 18:681-88
166. Prasad TK. 1996. Mechanisms of chilling-induced oxidative stress injury and tolerance in developing maize seedlings: changes in antioxidant system, oxidation of proteins and lipids, and protease activities. Plant J. 10:1017-26
167. Prasad TK, Anderson MD, Martin BA, Stewart CR. 1994. Evidence for chilling-induced oxidative stress in maize seedlings and regulatory role of hydrogen peroxide. Plant Cell 6:65-74
168. Ranieri A, D'Urso G, Nali C, Lorenzini G, Soldatini GF. 1996. Ozone stimulates apoplastic antioxidant systems in pumpkin leaves. Physiol. Plant. 97:381-87
169. Rauser WE. 1987. Changes in glutathione content of maize seedlings exposed to cadmium. Plant Sci. 51:171-75
170. Rauser WE, Schupp R, Rennenberg H. 1991. Cysteine, γ-glutamylcysteine and glutathione levels in maize seedlings. Plant Physiol. 97:128-34
171. Rautenkranz AAF, Li J, Machler F, Martinoia E, Oertli JJ. 1994. Transport of ascorbic and dehydroascorbic acids across protoplast and vacuole membranes isolated from barley (Hordeum vulgare L. cv. Gerbel) leaves. Plant Physiol. 106:187-93
172. Rawlins MR, Leaver CJ, May MJ. 1995. Characterisation of an Arabidopsis thaliana cDNA encoding glutathione synthetase. FEBS Lett. 376:81-86
173. Rennenberg H. 1982. Glutathione metabolism and possible biological roles in higher plants. Phytochemistry 21: 2771-81
174. Rennenberg H, Schmilz K, Bergmann L. 1979. Long-distance transport of sulfur in Nicotiana tabucum. Planta 147:57-62
175. Rennenberg H, Steinkamp R, Kesselmeier J. 1981. 5-oxo-prolinase in Nicotiana tabacum: catalytic properties and subcellular localization. Physiol. Plant. 62:211-16
176. Richman PG, Meister A. 1975. Regulation of γ-glutamylcysteine synthetase by nonallosteric feedback inhibition by glutathione. J. Biol. Chem. 250:1422-26
177. Römer S, Harlingue A, Camara B, Schantz R, Kuntz M. 1992. Cysteine synthase from Capsicum annuum chroraoplasts. Characterization and cDNA cloning of an up-regulated enzyme during fruit development. J. Biol. Chem. 267:17966-70
178. Rose RC, Bode AM. 1993. Biology of free radical scavengers: an evaluation of ascorbate. FASEB J. 7:1135-42
179. Rüegsegger A, Brunold C. 1992. Effect of cadmium on γ-glutamylcysteine synthesis in maize seedlings. Plant Physiol. 99:428-33
180. Rüegsegger A, Brunold C. 1993. Localization of γ-glutamylcysteine synthetase and glutathione synthetase activity in maize seedlings. Plant Physiol. 101:561-66
181. Rüegsegger A, Schmutz D, Brunold C. 1990. Regulation of glutathione synthesis by cadmium in Pisum sativum L. Plant Physiol. 93:1579-84
182. Ruffet ML, Lebrun M, Droux M, Douce R. 1995. Subcellullar distribution of serine acetyltransferase from Pisum sativum and characterization of an Arabidopsis thaliana putative cytosolic isoform. Eur. J. Biochem. 227:500-9
183. Saito K, Nick JA, Loewus FA. 1990. D-glucosone and L-sorbosone, putative intermediates of L-ascorbate biosynthesis in detached bean and spinach leaves. Plant Physiol. 94:1496-500
184. 18O into oxalic, L-threonic and L-tartaric acids during cleavage of L-ascorbic and 5-keto-D-gluconic acids in plants. Phytochemistry 44:805-9
185. Sanchez-Fernandez R, Fricker M, Corben LB, White NS, Sheard N, et al. 1997. Cell proliferation and hair tip growth in the Arabidopsis root are under mechanistically different forms of redox control. Proc. Natl. Acad. Sci. USA 94:2745-50
186. 185a. Scandalios J, ed. 1991.Oxidative Stress and the Molecular Biology of Antioxidant Defences. Cold Spring Harbor, NY: Cold Spring Harbor Lab. Press
187. Scheller HV, Huang B, Hatch E, Goldsbrough PB. 1987. Phytochelatin synthesis and glutathione levels in response to heavy metals in tomato cells. Plant Physiol. 85:1031-35
188. Schmidt A, Kunert KJ. 1986. Lipid peroxidation in higher plants: the role of glutathione reductase. Plant Physiol. 82:700-2
189. Schmutz D, Brunold C. 1984. Intercellular localization of assimilatory sulfate reduction in leaves of Zea mays and Triticum aestivum. Plant Physiol. 74:866-70
190. Schneider A, Schatten T, Rennenberg H. 1992. Reduced glutathione (GSH) transport in cultured tobacco cells. Plant Physiol. Biochem. 30:29-38
191. Schneider S, Bergmann L. 1995. Regulation of glutathione synthesis in suspension cultures of parsley and tobacco. Bot. Acta 108:34-40
192. Schupp R, Rennenberg H. 1990. Diurnal changes in the thiol composition of spruce needles. In Sulfur Nutrition and Sulfur Assimilation in Higher Plants, ed. H Rennenberg, CH Brunold, LJ de Kok, I Stulen, pp. 89-96. The Hague: SPB Acad.
193. Sen Gupta A, Alscher RG, McCune D. 1991. Response of photosynthesis and cellular antioxidants to ozone in Populus leaves. Plant Physiol. 96:650-55
194. Sen Gupta A, Meinen JL, Holladay AS, Burke JJ, Allen RD. 1993. Increased resistance to oxidative stress in transgenic plants that overexpress chloroplastic Cu/Zn superoxide dismutase. Proc. Natl. Acad. Sci. USA 90:1629-33
195. Sen Gupta A, Webb RP, Holladay AS, Allen RD. 1993. Overexpression of superoxide dismutase protects plants from oxidative stress. Induction of ascorbate peroxidase in superoxide dismutaseoverexpressing plants. Plant Physiol. 103:1067-73
196. Sharma YK, Davis KR. 1994. Ozone-induced expression of stress-related genes in Arabidopsis thaliana. Plant Physiol. 105:1089-96
197. Shaul O, Mironov V, Burssens S, Van Montagu M, Inzé D. 1996. Two Arabidopsis cyclin promoters mediate distinctive transcriptional oscillation on synchronised tobacco 3Y-2 cells. Proc. Natl. Acad. Sci. USA 93:4868-72
198. Shi MM, Kugelman A, Iwamoto T, Tian L, Forman HJ. 1994. Quinone-induced oxidative stress elevates glutathione and induces γ-glutamylcysteine synthetase activity in rat lung epithelial L2 cells. J.Biol Chem. 42:26512-17
199. Slooten L, Capiau K, Van Camp W, Van Montagu M, Sybesma C, Inzé D. 1995. Factors affecting the enhancement of oxidative stress tolerance in transgenic tobacco overexpressing manganese superoxide dismutase in the chloroplasts. Plant Physiol. 107:737-50
200. Smirnoff N. 1996. The function and metabolism of ascorbic acid in plants. Ann. Bot. 78:661-99
201. Smirnoff N, Colombe SV. 1988. Drought influences the activity of enzymes of the hydrogen peroxide scavenging system. J. Exp. Bot. 39:1097-108
202. Smirnoff N, Cumbes Q. 1989. Hydroxyl radical scavenging activity of compatible solutes. Phytochemistry 28:1957-60
203. Smith IK. 1985. Stimulation of glutathione synthesis in photorespiring plants by catalase inhibitors. Plant Physiol 79:1044-47
204. Smith IK, Kendall AC, Keys AJ, Turner JC, Lea PJ. 1984. Increased levels of glutathione in a catalase-deficient mutant of barley (Hordeum vulgare L.). Plant Sci. Lett. 37:29-33
205. Smith IK, Kendall AC, Keys AJ, Turner JC, Lea PJ. 1985. The regulation of the biosynthesis of glutathione in leaves of barley (Hordeum vulgare L.). Plant Sci. 41:11-17
206. Steinkamp R, Rennenberg H. 1984. γ-Glutamyltranspeptidase in tobacco suspension cultures: catalytic properties and subcellular localization. Physiol. Plant. 61:251-56
207. Steinkamp R, Rennenberg H. 1985. Degradation of glutathione in plant cells: evidence against the participation of a γ-glutamyltranspeptidase. Z. Naturforsch. Teil C 40:29-33
208. Steinkamp R, Schweihofen B, Rennenberg H. 1987. γ-Glutamylcyclo-transferase in tobacco suspension cultures: catalytic properties and subcellular localization. Physiol. Plant. 69:499-503
209. Strohm M. 1996. Biochemische, physiologische und molekulare Grundlagen des Glutathion-Stoffwechs.els in Pappeln (Populus tremula x P. alba). PhD thesis. Univ. Freiburg, Ger.
210. Deleted in proof
211. Strohm M, Jouanin L, Kunert KJ, Pruvost C, Polle A, et al. 1995. Regulation of glutathione synthesis in leaves of transgenic poplar (Populus tremula x P. alba) overexpressing glutathione synthetase. Plant J. 7:141-45
212. Sun WM, Huang ZZ, Lu SC. 1996. Regulation of γ-glutamylcysteine synthetase by protein phosphorylation. Biochem. J. 320:321-28
213. Takahama U. 1993. Redox state of ascorbic acid in the apoplast of stems of Kalanchoe daigremontiana. Physiol. Plant. 89:791-98
214. Takahama U, Oniki T. 1994. Effects of ascorbate on the oxidation of derivatives of hydroxycinnamic acid and the mechanism of oxidation of sinapic acid by cell wall-bound peroxidases. Plant Cell Physiol 35:593-600
215. Takahashi H, Saito K. 1996. Subcellular localization of spinach cysteine synthase isoforms and regulation of their gene expression by nitrogen and sulfur. Plant Physiol. 112:273-80
216. 2 decomposing system in chloroplasts. Plant Cell Physiol. 26:1425-31
217. Teppermann JM, Dunsmuir P. 1990. Transformed plants with elevated levels of chloroplastic SOD are not more resistant to superoxide toxicity. Plant Mol. Biol. 14:501-11
218. Thomsen B, Drumm-Herrel H, Mohr H. 1992. Control of the appearance of ascorbate peroxidase (EC 1.11.1.11) in mustard seedling cotyledons by phytochrome and photooxidative treatments. Planta 186:600-8
219. 2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J. 11:1187-94
220. Tommasi FLD, Liso R, Arrigoni O. 1990. The ascorbic acid system in Cuscuta reflexa Roxb. J. Plant Physiol. 135:766-68
221. Trumper S, Follmann H, Haberlein I. 1994. A novel dehydroascorbate reductase from spinach chloroplasts homologous to plant trypsin inhibitor. FEBS Lett. 352:159-62
222. Ullman P, Gondet L, Potier S, Bach TJ. 1996. Cloning of Ambidopsis thaliana glutathione synthetase (GSH2) by functional complementation of a yeast gsh2 mutant. Eur. J. Biochem. 236:662-69
223. Deleted in proof
224. Van Camp W, Capiau K, Van Montagu M, Inzé D, Slooten L. 1996. Enhancement of oxidative stress tolerance in transgenic tobacco plants overproducing Fe superoxide dismutase in chloroplasts. Plant Physiol. 112:1703-14
225. Van Camp W, Willekens H, Bowler C, Van Montagu M, Inzé D, et al. 1994. Elevated levels of superoxide dismutase protect transgenic plants against ozone damage. BioTechnology 12:165-68
226. Walker MA, McKersie BD. 1993. Role of the ascorbate-glutathione antioxidant system in chilling resistance of tomato. J. Plant Physiol. 141:234-39
227. Washko PW, Welch RW, Dhariwal KR, Wang Y, Levine M. 1992. Ascorbic acid and dehydroascorbic acid analysis in biological samples. Anal. Biochem. 204:1-14
228. Watanabe K, Yamano Y, Murata K, Kimura A. 1986. The nucleotide sequence of the gene for γ-glutamylcysteine synthetase of Escherichia coli. Nucleic Acids Res. 14:4393-400
229. Wells WW, Xu DP, Yang Y, Rocque PA. 1990. Mammalian thioltransferase (glutaredoxin) and protein disulfide isomerase have dehydroascorbate reductase activity. J. Bial. Chem. 265:15361-64
230. 3 plants. EMBO J. 14:4806-16
231. Willekens H, Inzé D, Van Montagu M, Van Camp W. 1995. Catalase in plants. Mol. Breed. 1:207-28
232. Willekens H, Van Camp W, Van Montagu M, Inzé D, Langebartels C, Sandermann H. 1994. Ozone, sulfur dioxide, and ultraviolet B have similar effects on mRNA accumulation of antioxidant genes in Nicotiana plumbaginifolia L. Plant Physiol. 106:1007-14
233. Wingate VPM, Lawton MA, Lamb CJ. 1988. Glutathione causes a massive and selective induction of plant defense genes. Plant Physiol. 31:205-11
234. Winter H, Robinson G, Heldt HW. 1993. Subcellular volumes and metabolite concentrations in barley leaves. Planta 191:180-90
235. Winter H, Robinson G, Heldt HW. 1994. Subcellular volumes and metabolite concentrations in spinach leaves. Planta 193:530-35
236. Wise RR, Naylor AW. 1987. Chilling-enhanced photooxidation. Evidence for the role of singlet oxygen and superoxide in the breakdown of pigments and endogenous antioxidants. Plant Physiol. 83:278-82
237. Yamaguchi K, Mori H, Nishimura M. 1995. A novel isozyme of ascorbate peroxidase localized on glyoxysomal and leaf peroxisomal membranes in pumpkin. Plant Cell Physiol. 36:1157-62
238. Torsethaugen G, Pitcher LH, Zilinskas BA, Pell EJ. 1997. Overproduction of ascorbate peroxidase in the tobacco chloroplast does not provide protection against ozone. Plant Physiol. 114:529-37