Skip to main content
Log in

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

  • Review
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • 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) 42,099-42,107

    CAS  Google Scholar 

  • 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) 1135-1149

    Article  PubMed  CAS  Google Scholar 

  • JF Allen, Control of gene expression by redox potential and the requirement for chloroplast and mitochondrial genomes. J Theor Biol 165 (1993) 603-631

    Article  Google Scholar 

  • 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) 1044-1052

    Article  PubMed  CAS  Google Scholar 

  • 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) 179-190

    Article  PubMed  CAS  Google Scholar 

  • 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) 2448-2462

    Article  PubMed  CAS  Google Scholar 

  • D Barnes and SP Mayfield, Redox control of posttranscriptional processes in chloroplasts. Anti-oxid Redox Signal 5 (2003) 89-94

    Article  CAS  Google Scholar 

  • U Bechtold, DJ Murphy and PM Mullineaux, Arabidopsis peptide methionine sulfoxide reductase2 prevents cellular oxidative damage in long nights. Plant Cell 16 (2004) 908-919

    Article  PubMed  CAS  Google Scholar 

  • 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) 419-428

    Article  CAS  Google Scholar 

  • 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) 1024-1030

    Article  PubMed  CAS  Google Scholar 

  • 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) 26,317-26,322

    CAS  Google Scholar 

  • 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) 247-255

    Article  CAS  Google Scholar 

  • 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) 499-511

    Article  PubMed  CAS  Google Scholar 

  • WJ Chen and T Zhu, Networks of transcription factors with roles in environmental stress responses. TIPS 9 (2004) 591-596

    CAS  Google Scholar 

  • 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) 3525-3530

    Article  PubMed  CAS  Google Scholar 

  • 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) 73-78

    Article  PubMed  CAS  Google Scholar 

  • 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) 489-492

    PubMed  CAS  Google Scholar 

  • SD Copley and JK Dhillon, Lateral gene transfer and parallel evolution in the history of glutathione biosynthesis genes. Genome Bio 3 (2002) 1-16

    Article  Google Scholar 

  • 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) 1277-1292

    Article  PubMed  CAS  Google Scholar 

  • JF Dat, CH Foyer and IM Scott, Changes in salicylic acid and antioxidants during induced thermotolerance in mustard seedlings. Plant Physiol 118 (1998) 1455-1461

    Article  PubMed  CAS  Google Scholar 

  • 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) 853-858

    PubMed  Google Scholar 

  • 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) 2181-2191

    Article  PubMed  CAS  Google Scholar 

  • XN Dong, NPR1, all things considered. Curr Opin Plant Biol 7 (2004) 547-552

    Article  PubMed  CAS  Google Scholar 

  • WE Durrant and X Dong, Systemic acquired resistance. Annu Rev Phytopathol 42 (2004) 185-209

    Article  PubMed  CAS  Google Scholar 

  • 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) 1443-1451

    PubMed  CAS  Google Scholar 

  • 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) 605-613

    Article  PubMed  CAS  Google Scholar 

  • CH Foyer and B Halliwell, Presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133 (1976) 21-25

    Article  Google Scholar 

  • 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) 1047-1057

    Article  PubMed  CAS  Google Scholar 

  • 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) 2176-2191

    Article  PubMed  CAS  Google Scholar 

  • 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) 691-705

    Article  PubMed  CAS  Google Scholar 

  • 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) 1662-1671

    Article  CAS  Google Scholar 

  • LD Gomez, G Noctor, MR Knight and CH Foyer, Regulation of calcium signalling and gene expression by glutathione. J Exp Bot 55 (2004b) 1851-1859

    Article  CAS  Google Scholar 

  • 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) 11,108-11,113

    CAS  Google Scholar 

  • 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) 1827-1835

    Article  CAS  Google Scholar 

  • TN Hartmann, MD Fricker, H Rennenberg and AJ Meyer, Cell-specific measurement of cytosolic glutathione in poplar leaves. Plant Cell Environ 26 (2003) 965-975

    Article  PubMed  CAS  Google Scholar 

  • 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) 837-845

    Article  PubMed  CAS  Google Scholar 

  • R Hell and L Bergmann, γ-glutamylcysteine synthetase in higher plants: catalytic properties and subcellular localization. Planta 180 (1990) 603-612

    CAS  Google Scholar 

  • 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) 853-862

    Article  CAS  Google Scholar 

  • 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) 3018-3112

    Google Scholar 

  • 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) 461-473

    Article  PubMed  CAS  Google Scholar 

  • 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) 15,052-15,057

    CAS  Google Scholar 

  • 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) 651-663

    Article  PubMed  CAS  Google Scholar 

  • 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) 2464-2468

    PubMed  CAS  Google Scholar 

  • 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) 655-660

    Article  PubMed  CAS  Google Scholar 

  • 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) 173-181

    Article  Google Scholar 

  • A Jamai, R Tommasini, E Martinoia and S Delrot, Characterization of glutathione uptake in broadbean leaf protoplasts. Plant Physiol 111 (1996) 1145-1152

    PubMed  CAS  Google Scholar 

  • 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) 33,463-33,470

    CAS  Google Scholar 

  • K Kampfenkel, M Montagu Van and D Inze, Effects of iron excess on Nicotiana plumbaginifolia plants. Plant Physiol 107 (1995) 725-735

    PubMed  CAS  Google Scholar 

  • 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) 63-73

    Article  PubMed  CAS  Google Scholar 

  • 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) 627-640

    Article  PubMed  CAS  Google Scholar 

  • 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) 654-657

    PubMed  CAS  Google Scholar 

  • P Klatt and S Lamas, Regulation of protein function by S-glutathiolation in response to oxidative and nitrosative stress. Eur J Biochem 267 (2000) 4928-4944

    Article  PubMed  CAS  Google Scholar 

  • 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) 123-131

    CAS  Google Scholar 

  • 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) 707-715

    Article  CAS  Google Scholar 

  • S Kopriva and H Rennenberg, Control of sulphate assimilation and glutathione synthesis: interaction with N and C metabolism. J Exp Bot 55 (2004) 1831-1842

    Article  PubMed  CAS  Google Scholar 

  • 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)

  • 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) 177-183

    PubMed  CAS  Google Scholar 

  • G Link, Redox regulation of chloroplast transcription. Anti-oxid Redox Signal 5 (2003) 79-87

    Article  CAS  Google Scholar 

  • 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) 1939-1950

    Article  PubMed  CAS  Google Scholar 

  • K Marrs, The functions and regulation of glutathione S-transferases in plants. Annu Rev Plant Physiol, Plant Mol Biol 47 (1996) 127-158

    CAS  Google Scholar 

  • 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) 499-507

    Article  CAS  Google Scholar 

  • 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) 1039-1046

    PubMed  CAS  Google Scholar 

  • 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) 649-667

    Article  CAS  Google Scholar 

  • 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) 10,059-10,063

    CAS  Google Scholar 

  • 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) 12,049-12,054

    CAS  Google Scholar 

  • 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) 775-782

    Article  PubMed  CAS  Google Scholar 

  • 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) 174-181

    Article  CAS  Google Scholar 

  • AJ Meyer, MJ May and M Fricker, Quantitative in vivo measurement of glutathione in Arabidopsis cells. Plant J 27 (2001) 67-78

    Article  PubMed  CAS  Google Scholar 

  • AJ Meyer and MD Fricker, Control of demand-driven biosynthesis of glutathione in green Arabidopsis suspension culture cells. Plant Physiol 130 (2002) 1927-1937

    Article  PubMed  CAS  Google Scholar 

  • Y Meyer, L Verdoucq and F Vignois, Plant thioredoxins and glutaredoxins: identity and putative roles. Trends Plant Sci 4 (1999) 388-390

    Article  PubMed  Google Scholar 

  • 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) 845-856

    Article  PubMed  CAS  Google Scholar 

  • 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) 1381-1392

    Article  PubMed  CAS  Google Scholar 

  • Z Mou, W Fan and X Dong, Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113 (2003) 935-944

    Article  PubMed  CAS  Google Scholar 

  • 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) 748-760

    Article  PubMed  CAS  Google Scholar 

  • 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) 1163-1172

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • P Mullineaux and S Karpinski, Signal transduction in response to excess light: getting out of the chloroplast. Curr Opin Plant Biol 5 (2002) 43-48

    Article  PubMed  CAS  Google Scholar 

  • 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) 633-650

    Article  PubMed  CAS  Google Scholar 

  • 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) 623-647

    Article  CAS  Google Scholar 

  • G Noctor, AC Arisi, L Jouanin and CH Foyer, Manipulation of glutathione and amino acid biosynthesis in the chloroplast. Plant Physiol 118 (1998b) 471-482

    Article  CAS  Google Scholar 

  • 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) 1157-1167

    Article  CAS  Google Scholar 

  • G Noctor and CH Foyer, Ascorbate and Glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49 (1998) 249-279

    Article  PubMed  CAS  Google Scholar 

  • 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) 1283-1304

    Article  PubMed  CAS  Google Scholar 

  • 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) 1-8

    Article  PubMed  CAS  Google Scholar 

  • DR Ort and NR Baker, A photoprotective role for O2 as an alternative electron sink in photosynthesis. Curr Opin Plant Biol 5 (2002) 193-198

    Article  PubMed  CAS  Google Scholar 

  • 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) 838-853

    Article  PubMed  CAS  Google Scholar 

  • CMJ Pieterse and LC Loon Van, NPR1: the spider in the web of induced resistance signalling pathways. Curr Opin Plant Biol 7 (2004) 456-464

    Article  PubMed  CAS  Google Scholar 

  • T Pfannschmidt, Chloroplast redox signals: how photosynthesis controls its own genes. TIPS 8 (2003) 33-41

    CAS  Google Scholar 

  • T Pfannschmidt, A Nilsson and JF Allen, Photosynthetic control of chloroplast gene expression. Nature 397 (1999) 625-628

    Article  CAS  Google Scholar 

  • 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) 455-460

    Article  CAS  Google Scholar 

  • S Rodermel, Pathways of plastid-to-nucleus signaling. TIPS 6 (2001) 471-474

    CAS  Google Scholar 

  • N Rouhier, E Gelhaye and J-P Jacquot, Plant glutaredoxins: still mysterious reducing systems. Cell Mol Life Sci 61 (2004) 1266-1277

    Article  PubMed  CAS  Google Scholar 

  • A Ruegsegger and C Brunold, Localization of γ-glutamylcysteine synthetase and glutathione synthetase activity in maize seedlings. Plant Physiol 101 (1993) 561-566

    PubMed  CAS  Google Scholar 

  • JM Ruiz and E Blumwald, Salinity-induced glutathione synthesis in Brassica napus. Planta 214 (2002) 965-969

    Article  PubMed  CAS  Google Scholar 

  • 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) 1191-1212

    Article  PubMed  Google Scholar 

  • 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) 87-97

    Article  PubMed  CAS  Google Scholar 

  • 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) 235-245

    Article  CAS  Google Scholar 

  • 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) 11-17

    Google Scholar 

  • 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) 341-352

    Article  PubMed  CAS  Google Scholar 

  • 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) 503-512

    Article  CAS  Google Scholar 

  • R Steinkamp and H Rennenberg, γ-glutamyl transpeptidase in tobacco suspension cultures: catalytic properties and subcellular localisation. Physiol Plant 61 (1984) 251-256

    CAS  Google Scholar 

  • 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) 1109-1119

    Article  PubMed  CAS  Google Scholar 

  • 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) 262-273

    CAS  Google Scholar 

  • M Surpin, RM Larkin and J Chory, Signal transduction between the chloroplast and the nucleus. Plant Cell Suppl (2002) S327-S338

    Google Scholar 

  • The Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796-815

    Google Scholar 

  • 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) 12,289-12,294

    CAS  Google Scholar 

  • 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) 662-669

    Article  PubMed  CAS  Google Scholar 

  • 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) 1289-1300

    Article  PubMed  CAS  Google Scholar 

  • 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) 97-110

    Article  PubMed  CAS  Google Scholar 

  • A Wachter, Synthesis and compartmentation of glutathione in plants: complex regulatory mechanisms. Heidelberg: Heidelberg University (20047).

    Google Scholar 

  • Wachter A and Rausch T (2005) Regulation of glutathione (GSH) synthesis in plants: Novel insight from Arabidopsis. FAL Agricultural Research, in press

  • 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) 15-30

    Article  PubMed  CAS  Google Scholar 

  • 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) 515-532

    Article  PubMed  CAS  Google Scholar 

  • MA Walker and BD McKersie, Role of the ascorbate-glutathione antioxidant system in chilling resistance in tomato. J Plant Physiol 141 (1993) 234-239

    CAS  Google Scholar 

  • 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) 1093-1104

    Article  PubMed  CAS  Google Scholar 

  • VMP Wingate, MA Lawton and CJ Lamb, Glutathione causes a massive and selective induction of plant defense genes. Plant Physiol 87 (1988) 206-210

    Article  PubMed  CAS  Google Scholar 

  • 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) 151-157

    Article  PubMed  CAS  Google Scholar 

  • C Xiang and DJ Oliver, Glutathione metabolic genes coordinately respond to heavy metals and jasmonic acid in Arabidopsis. Plant Cell 10 (1998) 1539-1550

    Article  PubMed  CAS  Google Scholar 

  • 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.

  • 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) 564-574

    Article  PubMed  CAS  Google Scholar 

  • 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) 1001-1011

    Article  PubMed  CAS  Google Scholar 

  • H Zer and I Ohad, Light, redox state, thylakoid-protein phosphorylation and signalling gene expression. TIBS 28 (2003) 467-470

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Philip M. Mullineaux.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mullineaux, P.M., Rausch, T. Glutathione, photosynthesis and the redox regulation of stress-responsive gene expression. Photosynth Res 86, 459–474 (2005). https://doi.org/10.1007/s11120-005-8811-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-005-8811-8

Keywords

Navigation