Photosynthesis Research

, Volume 86, Issue 3, pp 459–474 | Cite as

Glutathione, photosynthesis and the redox regulation of stress-responsive gene expression

  • Philip M. Mullineaux
  • Thomas Rausch


The ubiquitous antioxidant thiol tripeptide glutathione is present in millimolar concentrations in plant tissues and is regarded as one of the major determinants of cellular redox homeostasis. Recent research has highlighted a regulatory role for glutathione in influencing the expression of many genes important in plants' responses to both abiotic and biotic stress. Therefore, it becomes important to consider how glutathione levels and its redox state are influenced by environmental factors, how glutathione is integrated into primary metabolism and precisely how it can influence the functioning of signal transduction pathways by modulating cellular redox state. This review draws on a number of recent important observations and papers to present a unified view of how the responsiveness of glutathione to changes in photosynthesis may be one means of linking changes in nuclear gene expression to changes in the plant's external environment.


abiotic stress glutathione pathogens photosynthesis redox regulation of gene expression signalling 


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  1. JJ Abbott, J Pei, JL Ford, Y Qi, VN Grishin, LA Pitcher, MA Phillips and NV Grishin, Structure prediction and active site analysis of the metal binding determinants in γ-glutamylcysteine synthetase. J Biol Chem 276 (2001) 42,099-42,107Google Scholar
  2. MR Alfenito, E Souer, CD Goodman, R Buell, J Mol, R Koes and V Walbot, Functional complementation of anthocyanin sequestration in the vacuole by widely divergent glutathione S-transferases. Plant Cell 10 (1998) 1135-1149CrossRefPubMedGoogle Scholar
  3. JF Allen, Control of gene expression by redox potential and the requirement for chloroplast and mitochondrial genomes. J Theor Biol 165 (1993) 603-631CrossRefGoogle Scholar
  4. E Baena-Gonzalez, S Baginsky, P Mulo, H Summer, E-M Aro and G Link, Chloroplast transcription at different light intensities. Glutathione-mediated phosphorylation of the major RNA polymerase involved in redox regulated organellar gene expression. Plant Physiol 127 (2001) 1044-1052CrossRefPubMedGoogle Scholar
  5. M Baier and K-J Dietz, The plant 2-Cys peroxiredoxin BAS1 is a nuclear-encoded chloroplast protein: its expressional regulation, phylogenetic origin, and implications for its specific physiological function in plants. Plant J 12 (1997) 179-190CrossRefPubMedGoogle Scholar
  6. L Ball, GP Accotto, U Bechtold, G Creissen, D Funck, A Jimenez, B Kular, N Leyland, J Mejia-Carranza, H Reynolds, S Karpinski and PM Mullineaux, Evidence for a direct link between glutathione biosynthesis and stress defense gene expression in Arabidopsis. Plant Cell 16 (2004) 2448-2462CrossRefPubMedGoogle Scholar
  7. D Barnes and SP Mayfield, Redox control of posttranscriptional processes in chloroplasts. Anti-oxid Redox Signal 5 (2003) 89-94CrossRefGoogle Scholar
  8. U Bechtold, DJ Murphy and PM Mullineaux, Arabidopsis peptide methionine sulfoxide reductase2 prevents cellular oxidative damage in long nights. Plant Cell 16 (2004) 908-919CrossRefPubMedGoogle Scholar
  9. S Berger, M Papadopoulos, U Schreiber, W Kaiser and T Roitsch, Complex regulation of gene expression, photosynthesis and sugar levels by pathogen infection in tomato. Physiol Plant 122 (2004) 419-428CrossRefGoogle Scholar
  10. O Borsani, V Valpuesta and MA Botella, Evidence for a role of salicylic acid in the oxidative damage generated by NaCl and osmotic stress in Arabidopsis seedlings. Plant Physiol 126 (2001) 1024-1030CrossRefPubMedGoogle Scholar
  11. DL Brekken and MA Phillips, Trypanosoma brucei γ-glutamylcysteine synthetase characterisation of the kinetic mechanism and the role of Cys-319 in cystamine inactivation. J Biol Chem 273 (1998) 26,317-26,322Google Scholar
  12. P Broadbent, GP Creissen, B Kular, AR Wellburn and PM Mullineaux, oxidative stress responses in transgenic tobacco containing altered levels of glutathione reductase activity. Plant J 8 (1995) 247-255CrossRefGoogle Scholar
  13. CC-C Chang, L Ball, MJ Fryer, NR Baker, S Karpinski and PM Mullineaux, Induction of ASCORBATE PEROXIDASE 2 expression in wounded Arabidopsis leaves does not involve known wound-signalling pathways but is associated with changes in photosynthesis. Plant J 38 (2004) 499-511CrossRefPubMedGoogle Scholar
  14. WJ Chen and T Zhu, Networks of transcription factors with roles in environmental stress responses. TIPS 9 (2004) 591-596Google Scholar
  15. Z Chen, TE Young, J Ling, SC Chang and DR Gallie, Increasing vitamin C content of plants through enhanced ascorbate recycling. Proc Natl Acad Sci USA 100 (2003) 3525-3530CrossRefPubMedGoogle Scholar
  16. CS Cobbett, MJ May, R Howden and B Rolls, The glutathione-deficient, cadmium-sensitive mutant, cad2-1, of Arabidopsis thaliana is deficient in γ-glutamylcysteine synthetase. Plant J 16 (1998) 73-78CrossRefPubMedGoogle Scholar
  17. CE Cooper, RP Patel, PS Brookes and VM Darley-Usmar, Nanotransducers in cellular redox signalling: modification of thiols by reactive oxygen and nitrogen species. TIBS 27 (2002) 489-492PubMedGoogle Scholar
  18. SD Copley and JK Dhillon, Lateral gene transfer and parallel evolution in the history of glutathione biosynthesis genes. Genome Bio 3 (2002) 1-16CrossRefGoogle Scholar
  19. 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) 1277-1292CrossRefPubMedGoogle Scholar
  20. JF Dat, CH Foyer and IM Scott, Changes in salicylic acid and antioxidants during induced thermotolerance in mustard seedlings. Plant Physiol 118 (1998) 1455-1461CrossRefPubMedGoogle Scholar
  21. RHC Vos De, MJ Vonk, R Vooijs and H Schat, Glutathione depletion due to copper-induced phytochelatin synthesis causes oxidative stress in Silene cucubalus. Plant Physiol 98 (1992) 853-858PubMedGoogle Scholar
  22. C Deprès, C Chuback, A Rochon, R Clark, T Bethune, D Desveaux and PR Fobert, The Arabidopsis NPR1 disease resistance protein is a novel co-factor that confers redox regulation of DNA binding activity to the basic domain/leucine zipper transcription factor TGA1. Plant Cell 15 (2003) 2181-2191CrossRefPubMedGoogle Scholar
  23. XN Dong, NPR1, all things considered. Curr Opin Plant Biol 7 (2004) 547-552CrossRefPubMedGoogle Scholar
  24. WE Durrant and X Dong, Systemic acquired resistance. Annu Rev Phytopathol 42 (2004) 185-209CrossRefPubMedGoogle Scholar
  25. J Fodor, G Gullner, AL Adam, B Barna, T Komives and Z Kiraly, Local and systemic responses of antioxidants to tobacco mosaic virus infection and to salicylic acid in tobacco. Plant Physiol 114 (1997) 1443-1451PubMedGoogle Scholar
  26. P Fourcroy, G Vansuyt, S Kushnir, D Inze and J-F Briat, Iron-regulated expression of a cytosolic ascorbate peroxidase encoded by the APX1 gene in Arabidopsis seedlings. Plant Physiol 134 (2004) 605-613CrossRefPubMedGoogle Scholar
  27. CH Foyer and B Halliwell, Presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133 (1976) 21-25CrossRefGoogle Scholar
  28. CH Foyer, N Souriau, S Perret, M Lelandais, K-J Kunert, C Pruvost and L Jouanin, Overexpression of glutathione reductase but not glutathione synthetase leads to increases in antioxidant capacity and resistance to photoinhibition in poplar trees. Plant Physiol 109 (1995) 1047-1057CrossRefPubMedGoogle Scholar
  29. JL Freeman, MW Persans, K Nieman, C Albrecht, W Peer, IJ Pickering and DE Salt, Increased glutathione biosynthesis plays a role in nickel tolerance in Thlaspi nickel hyperaccumulators. Plant Cell 16 (2004) 2176-2191CrossRefPubMedGoogle Scholar
  30. MJ Fryer, L Ball, K Oxborough, S Karpinski, PM Mullineaux and NR Baker, Control of Ascorbate Peroxidase 2 expression by hydrogen peroxide and leaf water status during excess light stress reveals a functional organisation of Arabidopsis leaves. Plant J 33 (2003) 691-705CrossRefPubMedGoogle Scholar
  31. LD Gomez, H Vanacker, P Buchner, G Noctor and CH Foyer, Intercellular distribution of glutathione synthesis in maize leaves and its response to short-term chilling. Plant Physiol 134 (2004a) 1662-1671CrossRefGoogle Scholar
  32. LD Gomez, G Noctor, MR Knight and CH Foyer, Regulation of calcium signalling and gene expression by glutathione. J Exp Bot 55 (2004b) 1851-1859CrossRefGoogle Scholar
  33. G Gutierrez-Alcala, C Gotor, AJ Meyer, M Fricker, JM Vega and LC Romero, Glutathione biosynthesis in Arabidopsis trichome cells. Proc Natl Acad Sci USA 97 (2000) 11,108-11,113Google Scholar
  34. A Haag-Kerwer, HJ Schäfer, S Heiss, C Walter and T Rausch, Transpiration but not photosynthesis is affected by cadmium in Brassica juncea L.: temporal coordination of Cd-uptake and phytochelatin synthesis. J Exp Bot 50 (1999) 1827-1835CrossRefGoogle Scholar
  35. TN Hartmann, MD Fricker, H Rennenberg and AJ Meyer, Cell-specific measurement of cytosolic glutathione in poplar leaves. Plant Cell Environ 26 (2003) 965-975CrossRefPubMedGoogle Scholar
  36. T Hartmann, P Honicke, M Wirtz, R Hell, H Rennenberg and S Kopriva, Regulation of sulphate assimilation by glutathione in poplars, (Populus tremula x P. alba) of wild-type and over-expressing γ-glutamylcysteine synthetase in the cytosol. J Exp Bot 55 (2004) 837-845CrossRefPubMedGoogle Scholar
  37. R Hell and L Bergmann, γ-glutamylcysteine synthetase in higher plants: catalytic properties and subcellular localization. Planta 180 (1990) 603-612Google Scholar
  38. JA Hernandez, A Jimenez, P Mullineaux and F Sevilla, Tolerance of pea (Pisum sativum L.) to long-term salt stress is associated with induction of antioxidant defences. Plant Cell Environ 23 (2000) 853-862CrossRefGoogle Scholar
  39. D Herouart, M Montagu Van and D Inze, Redox activated expression of a cytosolic copper/zinc superoxide dismutase gene in Nicotiana. Proc Natl Acad Sci USA 90 (1993) 3018-3112Google Scholar
  40. C Herschbach, E Zalm van der, A Schneider, L Jouanin, LJ Kok De and H Rennenberg, Regulation of sulfur nutrition in wild-type and transgenic poplar over-expressing γ-glutamylcysteine synthetase in the cytosol as affected by atmospheric H2S. Plant Physiol 124 (2000) 461-473CrossRefPubMedGoogle Scholar
  41. T Hibi, H Nii, T Nakatsu, A Kimura, H Kato, J Hiratake and J Oda, Crystal structure of γ-glutamylcysteine synthetase. Insights into the mechanism of catalysis by a key enzyme for glutathione homeostasis. Proc Natl Acad Sci USA 101 (2004) 15,052-15,057Google Scholar
  42. MY Hirai, T Fujiwara, M Awazuhara, T Kimura, M Noji and K Saito, Global expression profiling of sulphur-starved Arabidopsis by DNA macroarray reveals the role of O-acetyl-L-serine as a general regulator of gene expression in response to sulphur nutrition. Plant J 33 (2003) 651-663CrossRefPubMedGoogle Scholar
  43. CS Huang, WR 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) 2464-2468PubMedGoogle Scholar
  44. H Ito, M Iwabuchi and K Ogawa, The sugar-metabolic enzymes aldolase and triosphosphate isomerase are targets of glutathionylation in Arabidopsis thaliana: detection using biotinylated glutathione. Plant Cell Physiol 44 (2003) 655-660CrossRefPubMedGoogle Scholar
  45. I Iturbe-Ormataexe, PR Escuredo, C Arresse-Igor and M Becana, Oxidative damage in pea plants exposed to water deficit or paraquat. Plant Physiol 116 (1998) 173-181CrossRefGoogle Scholar
  46. A Jamai, R Tommasini, E Martinoia and S Delrot, Characterization of glutathione uptake in broadbean leaf protoplasts. Plant Physiol 111 (1996) 1145-1152PubMedGoogle Scholar
  47. JM Jez, RE Cahoon and S Chen, Arabidopsis thaliana glutamate-cysteine ligase: functional properties, kinetic mechanism, and regulation of activity. J Biol Chem 279 (2004) 33,463-33,470Google Scholar
  48. K Kampfenkel, M Montagu Van and D Inze, Effects of iron excess on Nicotiana plumbaginifolia plants. Plant Physiol 107 (1995) 725-735PubMedGoogle Scholar
  49. A Kandlbinder, I Finkemeier, D Wormuth, M Hanitzsch and K-J Deitz, The antioxidant status of photosynthesizing leaves under nutrient deficiency: redox regulation, gene expression and antioxidant activity in Arabidopsis thaliana. Physiol Plant 120 (2004) 63-73CrossRefPubMedGoogle Scholar
  50. S Karpinski, C Escobar, B Karpinska, G Creissen and PM Mullineaux, Photosynthetic electron transport regulates the expression of cytosolic ascorbate peroxidase genes in Arabidopsis during excess light stress. Plant Cell 9 (1997) 627-640CrossRefPubMedGoogle Scholar
  51. S Karpinski, H Reynolds, B Karpinska, G Wingsle, G Creissen and P Mullineaux, Systemic signaling and acclimation in response to excess excitation energy in Arabidopsis. Science 284 (1999) 654-657PubMedGoogle Scholar
  52. P Klatt and S Lamas, Regulation of protein function by S-glutathiolation in response to oxidative and nitrosative stress. Eur J Biochem 267 (2000) 4928-4944CrossRefPubMedGoogle Scholar
  53. S Klapheck, C Latus and L Bergmann, Localization of glutathione synthetase and distribution of glutathione in leaf cells of Pisum sativum L. J Plant Physiol 131 (1987) 123-131Google Scholar
  54. KM Koistinen, HI Kokko, VH Hassinen, AI Tervahauta, S Auriola and SO Karenlampi, Stress-related RNase PR-10c is post-translationally modified by glutathione in birch. Plant Cell Environ 25 (2002) 707-715CrossRefGoogle Scholar
  55. S Kopriva and H Rennenberg, Control of sulphate assimilation and glutathione synthesis: interaction with N and C metabolism. J Exp Bot 55 (2004) 1831-1842CrossRefPubMedGoogle Scholar
  56. Kuzniak E and Sklodowska M (2005) Compartment-specific role of ascorbate-glutathione cycle in the response of tomato leaf cells to Botrytis cinerea infection. J Exp Bot (in press)Google Scholar
  57. AG Lappartient and B Touraine, Glutathione-mediated regulation of ATP sulfurylase activity, SO 4 2- uptake, and oxidative stress response in intact Canola roots. Plant Physiol 114 (1997) 177-183PubMedGoogle Scholar
  58. G Link, Redox regulation of chloroplast transcription. Anti-oxid Redox Signal 5 (2003) 79-87CrossRefGoogle Scholar
  59. L Loyall, K Uchida, S Braun, M Furuya and H Frohnmeyer, Glutathione and a UV light-induced glutathione-S-transferase are involved in signaling to chalcone synthase in cell cultures. Plant Cell 12 (2000) 1939-1950CrossRefPubMedGoogle Scholar
  60. K Marrs, The functions and regulation of glutathione S-transferases in plants. Annu Rev Plant Physiol, Plant Mol Biol 47 (1996) 127-158Google Scholar
  61. A Masi, R Ghisi and M Ferretti, Measuring low-molecular-weight thiols by detecting the fluorescence of their SBD-derivatives: application to studies of diurnal rythmn and UV-B induced changes in Zea mays L. J Plant Physiol 159 (2002) 499-507CrossRefGoogle Scholar
  62. MA Matamoros, MR Clemente, S Sato, E Asamizu, S Tabata, J Ramos, JF Moran, J Stiller, PM Gresshoff and M Becana, Molecular analysis of the pathway for the synthesis of thiol tripeptides in the model legume Lotus japonicus. Mol Plant Microbe Interact 16 (2003) 1039-1046PubMedGoogle Scholar
  63. M May, T Vernoux, C Leaver, M Montagu Van and D Inze, Glutathione homeostasis in plants: implications for environmental sensing and plant development. J Exp Bot 49 (1998a) 649-667CrossRefGoogle Scholar
  64. MJ May and CJ Leaver, Arabidopsis thaliana γ-glutamylcysteine synthetase is structurally unrelated to mammalian, yeast, and Escherichia coli homologs. Proc Natl Acad Sci USA 91 (1994) 10,059-10,063Google Scholar
  65. MJ May, T Vernoux, R Sanchez-Fernandez, M Montagu Van and D Inze, Evidence for posttranscriptional activation of γ-glutamylcysteine synthetase during plant stress responses. Proc Natl Acad Sci USA 95 (1998b) 12,049-12,054Google Scholar
  66. M Meinhard, PL Rodriguez and E Grill, The sensitivity of ABI2 to hydrogen peroxide links the abscisic acid-response regulator to redox signalling. Planta 214 (2002) 775-782CrossRefPubMedGoogle Scholar
  67. AJ Meyer and MD Fricker, Direct measurement of glutathione in epidermal cells of intact Arabidopsis roots by two-photon laser scanning microscopy. J Microscopy 198 (2000) 174-181CrossRefGoogle Scholar
  68. AJ Meyer, MJ May and M Fricker, Quantitative in vivo measurement of glutathione in Arabidopsis cells. Plant J 27 (2001) 67-78CrossRefPubMedGoogle Scholar
  69. AJ Meyer and MD Fricker, Control of demand-driven biosynthesis of glutathione in green Arabidopsis suspension culture cells. Plant Physiol 130 (2002) 1927-1937CrossRefPubMedGoogle Scholar
  70. Y Meyer, L Verdoucq and F Vignois, Plant thioredoxins and glutaredoxins: identity and putative roles. Trends Plant Sci 4 (1999) 388-390CrossRefPubMedGoogle Scholar
  71. V Mittova, M Tal, M Volokita and M Guy, Up-regulation of the leaf mitochondrial and peroxisomal antioxidative systems in response to salt-induced oxidative stress in the wild salt-tolerant tomato species Lycopersicon pennellii. Plant Cell Environ 26 (2003) 845-856CrossRefPubMedGoogle Scholar
  72. JF Moran, I Iturbe-Ormaetxe, MA Matamoros, MC Rubio, MR Clemente, NJ Brewin and M Becana, Glutathione and homoglutathione synthetases of legume nodules. Cloning, expression, and subcellular localization. Plant Physiol 124 (2000) 1381-1392CrossRefPubMedGoogle Scholar
  73. Z Mou, W Fan and X Dong, Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113 (2003) 935-944CrossRefPubMedGoogle Scholar
  74. P Muller-Moule, M Havaux and KK Niyogi, Zeaxanthin deficiency enhances the high light sensitivity of an ascorbate-deficient mutant of Arabidopsis. Plant Physiol 133 (2003) 748-760CrossRefPubMedGoogle Scholar
  75. P Muller-Moule, T Golan and KK Niyogi, Ascorbate-deficient mutants of Arabidopsis grow in high light despite chronic photooxidative stress. Plant Physiol 134 (2004) 1163-1172CrossRefPubMedGoogle Scholar
  76. PM Mullineaux and GP Creissen, Glutathione reductase: regulation and role in oxidative stress. In: J Scandalios (ed.) Oxidative Stress, Monograph 34. NY: Harbour Press, Cold Spring (1996) pp. Google Scholar
  77. P Mullineaux and S Karpinski, Signal transduction in response to excess light: getting out of the chloroplast. Curr Opin Plant Biol 5 (2002) 43-48CrossRefPubMedGoogle Scholar
  78. V Nikiforova, J Freitag, S Kempa, M Adamik, H Hesse and R Hoefgen, Transcriptome analysis of sulfur depletion in Arabidopsis thaliana: interlacing of biosynthetic pathways provides response specificity. Plant J 33 (2003) 633-650CrossRefPubMedGoogle Scholar
  79. G Noctor, A Arisi, L Jouanin, K Kunert, H Rennenberg and C Foyer, Glutathione: biosynthesis, metabolism and relationship to stress tolerance explored in transformed plants. J Exp Bot 49 (1998a) 623-647CrossRefGoogle Scholar
  80. G Noctor, AC Arisi, L Jouanin and CH Foyer, Manipulation of glutathione and amino acid biosynthesis in the chloroplast. Plant Physiol 118 (1998b) 471-482CrossRefGoogle Scholar
  81. G Noctor, AC Arisi, L Jouanin and CH Foyer, Photorespiratory glycine enhances glutathione accumulation in both the chloroplastic and cytosolic compartments. J Exp Bot 50 (1999) 1157-1167CrossRefGoogle Scholar
  82. G Noctor and CH Foyer, Ascorbate and Glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49 (1998) 249-279CrossRefPubMedGoogle Scholar
  83. G Noctor, L Gomez, H Vanacker and CH Foyer, Interactions between biosynthesis, compartmentation and transport in the control of glutathione homeostasis and signalling. J Exp Bot 53 (2002) 1283-1304CrossRefPubMedGoogle Scholar
  84. K Ogawa, A Hatano-Iwasaki, M Yanagida and M Iwabuchi, Level of glutathione is regulated by ATP-dependent ligation of glutamate and cysteine through photosynthesis in Arabidopsis thaliana: mechanism of strong interaction of light intensity with flowering. Plant Cell Physiol 45 (2004) 1-8CrossRefPubMedGoogle Scholar
  85. DR Ort and NR Baker, A photoprotective role for O2 as an alternative electron sink in photosynthesis. Curr Opin Plant Biol 5 (2002) 193-198CrossRefPubMedGoogle Scholar
  86. II Panchuk, RA Volkov and F Schoffl, Heat stress- and heat shock transcription factor-dependent expression and activity of ascorbate peroxidase in Arabidopsis. Plant Physiol 129 (2002) 838-853CrossRefPubMedGoogle Scholar
  87. CMJ Pieterse and LC Loon Van, NPR1: the spider in the web of induced resistance signalling pathways. Curr Opin Plant Biol 7 (2004) 456-464CrossRefPubMedGoogle Scholar
  88. T Pfannschmidt, Chloroplast redox signals: how photosynthesis controls its own genes. TIPS 8 (2003) 33-41Google Scholar
  89. T Pfannschmidt, A Nilsson and JF Allen, Photosynthetic control of chloroplast gene expression. Nature 397 (1999) 625-628CrossRefGoogle Scholar
  90. EA Pilon-Smits, Y Zhu, T Sears and N Terry, Overexpression of glutathione reductase in Brassica juncea: effects on cadmium accumulation and tolerance. Physiol Plant 110 (2000) 455-460CrossRefGoogle Scholar
  91. S Rodermel, Pathways of plastid-to-nucleus signaling. TIPS 6 (2001) 471-474Google Scholar
  92. N Rouhier, E Gelhaye and J-P Jacquot, Plant glutaredoxins: still mysterious reducing systems. Cell Mol Life Sci 61 (2004) 1266-1277CrossRefPubMedGoogle Scholar
  93. A Ruegsegger and C Brunold, Localization of γ-glutamylcysteine synthetase and glutathione synthetase activity in maize seedlings. Plant Physiol 101 (1993) 561-566PubMedGoogle Scholar
  94. JM Ruiz and E Blumwald, Salinity-induced glutathione synthesis in Brassica napus. Planta 214 (2002) 965-969CrossRefPubMedGoogle Scholar
  95. FQ Schaffer and GR Buettner, Redox environment of the cell as viewed through the redox state of the glutathione-disulfide/glutathione couple. Free Rad Biol Med 30 (2001) 1191-1212CrossRefPubMedGoogle Scholar
  96. HJ Schafer, 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) 87-97CrossRefPubMedGoogle Scholar
  97. M Schraudner, W Moeder, C Wiese, W Camp Van, D Inze, C Langebartels and H Sandermann Jr, Ozone-induced oxidative burst in the ozone biomonitor plant, tobacco Bel W3. Plant J 16 (1998) 235-245CrossRefGoogle Scholar
  98. IK Smith, AC Kendall, AJ Keys, JC Turner and PJ Lea, The regulation of the biosynthesis of glutathione in the leaves of barley (Hordeum vulgare L.). Plant Sci 4 (1985) 11-17Google Scholar
  99. A Somanchi, D Barnes and SP Mayfield, A nuclear gene of Chlamydomonas reinhardtii, Tba1, encodes a putative oxidoreductase required for translation of the chloroplast psbA mRNA. Plant J 42 (2005) 341-352CrossRefPubMedGoogle Scholar
  100. B Srivalli, G Sharma and R Khanna-Chopra, Antioxidative defense system in an upland rice cultivar subjected to increasing intensity of water stress followed by recovery. Physiol Plant 119 (2003) 503-512CrossRefGoogle Scholar
  101. R Steinkamp and H Rennenberg, γ-glutamyl transpeptidase in tobacco suspension cultures: catalytic properties and subcellular localisation. Physiol Plant 61 (1984) 251-256Google Scholar
  102. S Storozhenko, E Belles-Boix, E Babiychuk, D Herouart, MW Davey, L Slooten, M Montagu Van, D Inze and S Kushnir, γ-glutamyl transpeptidase in transgenic tobacco plants. Cellular localization, processing, and biochemical properties. Plant Physiol 128 (2002) 1109-1119CrossRefPubMedGoogle Scholar
  103. M Strohm, M Eiblmeier, C Langebartels, L Jouanin, A Polle, H Sandermann and H Rennenberg, Responses of antioxidative systems to acute ozone stress in transgenic poplar (Populus tremulla x P. alba) over-expressing glutathione synthetase or glutathione reductase. Trees-Structure Funct 16 (2002) 262-273Google Scholar
  104. M Surpin, RM Larkin and J Chory, Signal transduction between the chloroplast and the nucleus. Plant Cell Suppl (2002) S327-S338Google Scholar
  105. The Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796-815Google Scholar
  106. T Trebitsh and A Danon, Translation of chloroplast psbA mRNA is regulated by signals initiated by both Photosystems II and I. Proc Natl Acad Sci USA 98 (2001) 12,289-12,294Google Scholar
  107. P Ullmann, L Gondet, S Potier and TJ Bach, Cloning of Arabidopsis thaliana glutathione synthetase (GSH2) by functional complementation of a yeast gsh2 mutant. Eur J Biochem 236 (1996) 662-669CrossRefPubMedGoogle Scholar
  108. H Vanacker, TLW Carver and CH Foyer, Early H2O2 accumulation in mesophyll cells leads to induction of glutathione during the hyper-sensitive response in the barley-powdery mildew interaction. Plant Physiol 123 (2000) 1289-1300CrossRefPubMedGoogle Scholar
  109. T Vernoux, RC Wilson, KA Seeley, JP Reichheld, S Muroy, S Brown, SC Maughan, CS Cobbett, M Montagu Van, D Inze, MJ May and ZR Sung, 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 (2000) 97-110CrossRefPubMedGoogle Scholar
  110. A Wachter, Synthesis and compartmentation of glutathione in plants: complex regulatory mechanisms. Heidelberg: Heidelberg University (20047).Google Scholar
  111. Wachter A and Rausch T (2005) Regulation of glutathione (GSH) synthesis in plants: Novel insight from Arabidopsis. FAL Agricultural Research, in pressGoogle Scholar
  112. A Wachter, S Wolf, H Steininger, J Bogs and T Rausch, 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 (2005) 15-30CrossRefPubMedGoogle Scholar
  113. U Wagner, R Edwards, DP Dixon and F Mauch, Probing the diversity of the Arabidopsis glutathione S-transferase gene family. Plant Mol Biol 49 (2002) 515-532CrossRefPubMedGoogle Scholar
  114. MA Walker and BD McKersie, Role of the ascorbate-glutathione antioxidant system in chilling resistance in tomato. J Plant Physiol 141 (1993) 234-239Google Scholar
  115. CL Wang and DJ Oliver, Cloning of the cDNA and genomic clones for glutathione synthetase from Arabidopsis thaliana and complementation of a gsh2 mutant in fission yeast. Plant Mol Biol 31 (1996) 1093-1104CrossRefPubMedGoogle Scholar
  116. VMP Wingate, MA Lawton and CJ Lamb, Glutathione causes a massive and selective induction of plant defense genes. Plant Physiol 87 (1988) 206-210PubMedCrossRefGoogle Scholar
  117. G Wingsle and S Karpinski, Differential redox regulation of glutathione reductase and Cu/Zn superoxide dismutase genes expression in Pinus sylvestris (L.) needles. Planta 198 (1996) 151-157CrossRefPubMedGoogle Scholar
  118. C Xiang and DJ Oliver, Glutathione metabolic genes coordinately respond to heavy metals and jasmonic acid in Arabidopsis. Plant Cell 10 (1998) 1539-1550CrossRefPubMedGoogle Scholar
  119. Xiang C and Bertrand D (2000) Glutathione synthesis in Arabidopsis: multilevel controls coordinate responses to stress. In: Sulfur Nutrition and Sulfur Assimilation in Higher Plants, pp 409-412.Google Scholar
  120. C Xiang, BL Werner, EM Christensen and DJ Oliver, The biological functions of glutathione revisited in Arabidopsis transgenic plants with altered glutathione levels. Plant Physiol 126 (2001) 564-574CrossRefPubMedGoogle Scholar
  121. S Youssefian, M Nakamura, E Orudgev and N Kondo, Increased biosynthesis capacity of transgenic tobacco overexpressing an O-acetylserine(thiol) lyase modifies plant responses to oxidative stress. Plant Physiol 126 (2001) 1001-1011CrossRefPubMedGoogle Scholar
  122. H Zer and I Ohad, Light, redox state, thylakoid-protein phosphorylation and signalling gene expression. TIBS 28 (2003) 467-470PubMedGoogle Scholar

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© Springer 2005

Authors and Affiliations

  1. 1.Department of Biological SciencesUniversity of EssexColchesterUK
  2. 2.Heidelberg Institute of Plant Sciences (HIP)Ruprecht-Karls-UniversityHeidelbergGermany

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