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Glutathione homeostasis and redox-regulation by sulfhydryl groups

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Abstract

Continuous control of metabolism and developmental processes is a key feature of live cells. Cysteine thiol residues of proteins are both exceptionally useful in terms of structural and regulatory aspects, but at the same time exceptionally vulnerable to oxidation. Conserved cysteines thus are highly important for the function of metabolic enzymes and for signaling processes underlying responses to environmental factors. The underlying mechanism for the central role of thiol-mediated redox control in cellular metabolism is the ability of the cysteine-thiols to reversibly change their redox state followed by changes of structural, catalytic or regulatory functions. The cellular glutathione/glutathione disulfide redox buffer is present in cells at millimolar concentrations and forms one major basis of redox homeostasis by which protein thiols can maintain their redox state or oxidized protein thiols can be reverted to their reduced state. Besides acting as redox buffer, glutathione also acts as an electron donor for both scavenging of reactive oxygen, e.g. from photosynthesis and respiration, and metabolic reactions such as reduction of hydroperoxides and lipidperoxides or sulfate assimilation. The central role of glutathione is further emphasized by its involvement in signaling processes and the crosstalk of redox signaling processes with other means of signaling including protein glutathionylation and control of transcription factors. The present review aims at highlighting the key functions of glutathione in thiol-mediated redox control and its interplay with other protein-thiol-based redox systems.

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Abbreviations

APR:

adenosine 5'-phosphosulfate reductase

APX:

ascorbate peroxidase

BSO:

buthionine sulfoximine

2CPA:

2-Cys peroxiredoxins A

FBA:

fructose-1,6-bisphosphate aldolase

γ-EC:

γ-glutamylcysteine

GGT:

γ-glutamyl transpeptidase

GPX:

glutathione peroxidase

GR:

glutathione reductase

GRX:

glutaredoxin

GSH:

reduced glutathione

GSSG:

glutathione disulfide

GST:

glutathione S-transferase

MAPK:

mitogen activated protein kinase

MCB:

monochlorobimane

PDI:

protein disulfide isomerase

PMSR:

peptide methionine sulfoxide reductase

PRX:

peroxiredoxins

ROS:

reactive oxygen species

rxYFP:

redox sensitive YFP

TPI:

triose-phosphate isomerase

TRX:

thioredoxin

References

  • K Apel and H Hirt, Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55 (2004) 373-399

    Article  PubMed  CAS  Google Scholar 

  • K Asada, The water–water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50 (1999) 601-639

    Article  PubMed  CAS  Google Scholar 

  • F Aslund, KD Berndt and A Holmgren, Redox potentials of glutaredoxins and other thiol-disulfide oxidoreductases of the thioredoxin superfamily determined by direct protein-protein redox equilibria. J Biol Chem 272 (1997) 30780-30786

    Article  PubMed  CAS  Google Scholar 

  • O Avsian-Kretchmer, Y Eshdat, Y Gueta-Dahan and G Ben-Hayyim, Regulation of stress-induced phospholipid hydroperoxide glutathione peroxidase expression in citrus. Planta 209 (1999) 469-477

    Article  PubMed  CAS  Google Scholar 

  • E Baena-Gonzalez, S Baginsky, P Mulo, H Summer, EM 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 KJ 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) 179-90

    Article  PubMed  CAS  Google Scholar 

  • M Baier, E Stroher and K-J Dietz, The acceptor availability at photosystem I and ABA control nuclear expression of 2-Cys peroxiredoxin-A in Arabidopsis thaliana. Plant Cell Physiol 45 (2004) 997-1006

    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 

  • Y Balmer, A Koller, G Val del, W Manieri, P Schurmann and BB Buchanan, Proteomics gives insight into the regulatory function of chloroplast thioredoxins. Proc Natl Acad Sci USA 100 (2003) 370-375

    Article  PubMed  CAS  Google Scholar 

  • D Bartling, R Radzio, U Steiner and EW Weiler, A glutathione S-transferase with glutathione-peroxidase activity from Arabidopsis thaliana Molecular cloning and functional characterization. Eur J Biochem 216 (1993) 579-586

    Article  PubMed  CAS  Google Scholar 

  • U Baumann and J Juttner, Plant thioredoxins: the multiplicity conundrum. Cell Mol Life Sci 59 (2002) 1042-1057

    Article  PubMed  CAS  Google Scholar 

  • A Baxter-Burrell, R Chang, P Springer and J Bailey-Serres, Gene and enhancer trap transposable elements reveal oxygen deprivation-regulated genes and their complex patterns of expression in Arabidopsis. Ann Bot 91 (2003) 129-141

    Article  PubMed  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 

  • L Bergmann and H Rennenberg De, Glutathione metabolism in plants. In: LJ Kok, I Stulen, H Rennenberg, C Brunold and WE Rauser (eds.) Sulfur Nutrition and Assimilation in Higher Plants. Regulatory, Agricultural and Environmental Aspects. The Netherlands: SPB Academic Publishing, The Hague (1993) pp. 102-123

    Google Scholar 

  • JA Bick, F Aslund, Y Chen and T Leustek, Glutaredoxin function for the carboxyl-terminal domain of the plant-type 5'-adenylylsulfate reductase. Proc Natl Acad Sci USA 95 (1998) 8404-8409

    Article  PubMed  CAS  Google Scholar 

  • JA Bick, AT Setterdahl, DB Knaff, Y Chen, LH Pitcher, BA Zilinskas and T Leustek, Regulation of the plant-type 5'-adenylyl sulfate reductase by oxidative stress. Biochemistry 40 (2001) 9040-9048

    Article  PubMed  CAS  Google Scholar 

  • D Bigelow and T Squier, Redox modulation of cellular signaling and metabolism through reversible oxidation of methionine sensors in calcium regulatory proteins. Biochim Biophys Acta 1703 (2005) 121-134

    PubMed  CAS  Google Scholar 

  • A Blaszczyk, R Brodzik and A Sirko, Increased resistance to oxidative stress in transgenic tobacco plants overexpressing bacterial serine acetyltransferase. Plant J 20 (1999) 237-243

    Article  PubMed  CAS  Google Scholar 

  • C Bréhélin, C Laloi, AT Setterdahl, DB Knaff and Y Meyer, Cytosolic, mitochondrial thioredoxins and thioredoxin reductases in Arabidopsis thaliana. Photosynth Res 79 (2004) 295-304

    Article  PubMed  Google Scholar 

  • M Burgener, M Suter, S Jones and C Brunold, Cyst(e)ine is the transport metabolite of assimilated sulfur from bundle-sheath to mesophyll cells in maize leaves. Plant Physiol 116 (1998) 1315-1322

    Article  PubMed  CAS  Google Scholar 

  • F Buwalda, LJ Kok De, I Stulen and PJC Kuiper, Cysteine, glutamylcysteine and glutathione contents of spinach leaves as affected by darkness and application of excess sulfur. Physiol Plant 74 (1988) 663-668

    CAS  Google Scholar 

  • F Buwalda, I Stulen, LJ Kok De and PJC Kuiper, Cysteine, glutamylcysteine and glutathione contents of spinach leaves as affected by darkness and application of excess sulfur. II. Glutathione accumulation in detached leaves exposed to H2S in the absence of light is stimulated by the supply of glycine to the petiole. Physiol Plant 80 (1990) 196-204

    Article  CAS  Google Scholar 

  • I Carlberg, E Rintamäki, EM Aro and B Andersson, Thylakoid protein phosphorylation and the thiol redox state. Biochemistry 38 (1999) 3197-3204

    Article  PubMed  CAS  Google Scholar 

  • S Casagrande, V Bonetto, M Fratelli, E Gianazza, I Eberini, T Massignan, M Salmona, G Chang, A Holmgren and P Ghezzi, Glutathionylation of human thioredoxin: a possible crosstalk between the glutathione and thioredoxin systems. Proc Natl Acad Sci USA 99 (2002) 9745-9749

    Article  PubMed  CAS  Google Scholar 

  • O Chew, C Rudhe, E Glaser and J Whelan, Characterization of the targeting signal of dual-targeted pea glutathione reductase. Plant Mol Biol 53 (2003a) 341-356

    Article  CAS  Google Scholar 

  • O Chew, J Whelan and AH Millar, Molecular definition of the ascorbate-glutathione cycle in Arabidopsis mitochondria reveals dual targeting of antioxidant defenses in plants. J Biol Chem 278 (2003b) 46869-46877

    CAS  Google Scholar 

  • PT Chivers, MC Laboissiere and RT Raines, The CXXC motif: imperatives for the formation of native disulfide bonds in the cell. EMBO J 15 (1996) 2659-2667

    PubMed  CAS  Google Scholar 

  • MA Ciorba, SH Heinemann, H Weissbach, N Brot and T Hoshi, Modulation of potassium channel function by methionine oxidation and reduction. Proc Natl Acad Sci USA 94 (1997) 9932-9937

    Article  PubMed  CAS  Google Scholar 

  • H Clayton, M Knight, H Knight, M McAinsh and A Hetherington, Dissection of the ozone-induced calcium signature. Plant J 17 (1999) 575-579

    Article  PubMed  CAS  Google Scholar 

  • PL Conklin and RL Last, Differential accumulation of antioxidant mRNAs in Arabidopsis thaliana exposed to ozone. Plant Physiol 109 (1995) 203-212

    Article  PubMed  CAS  Google Scholar 

  • CE Cooper, RP Patel, PS Brookes and VM Darley-Usmar, Nanotransducers in cellular redox signaling: modification of thiols by reactive oxygen and nitrogen species. Trends Biochem Sci 27 (2002) 489-492

    Article  PubMed  CAS  Google Scholar 

  • I Cotgreave and R Gerdes, Recent trends in glutathione biochemistry – glutathione-protein interactions: a molecular link between oxidative stress and cell proliferation?. Biochem Biophys Res Commun 242 (1998) 1-9

    Article  PubMed  CAS  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 

  • G Creissen, H Reynolds, Y Xue and P Mullineaux, Simultaneous targeting of pea glutathione reductase and of a bacterial fusion protein to chloroplasts and mitochondria in transgenic tobacco. Plant J 8 (1995) 167-175

    Article  PubMed  CAS  Google Scholar 

  • I Cummins, DJ Cole and R Edwards, A role for glutathione transferases functioning as glutathione peroxidases in resistance to multiple herbicides in black-grass. Plant J 18 (1999) 285-292

    Article  PubMed  CAS  Google Scholar 

  • JW Cuozzo and CA Kaiser, Competition between glutathione and protein thiols for disulphide-bond formation. Nat Cell Biol 1 (1999) 130-135

    Article  PubMed  CAS  Google Scholar 

  • A Danon, Redox reactions of regulatory proteins: do kinetics promote specificity?. Trends Biochem Sci 27 (2002) 197-203

    Article  PubMed  CAS  Google Scholar 

  • S Davletova, L Rizhsky, H Liang, Z Shengqiang, DJ Oliver, J Coutu, V Shulaev, K Schlauch and R Mittler, Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen gene network of Arabidopsis. Plant Cell 17 (2005) 268-281

    Article  PubMed  CAS  Google Scholar 

  • C Despres, C Chubak, A Rochon, R Clark, T Bethune, D Desveaux and PR Fobert, The Arabidopsis NPR1 disease resistance protein is a novel cofactor 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 

  • R Dhindsa, Drought stress, enzymes of glutathione metabolism, oxidation injury and protein synthesis in Tortula ruralis. Plant Physiol 95 (1991) 648-651

    Article  PubMed  CAS  Google Scholar 

  • KJ Dietz, Plant peroxiredoxins. Annu Rev Plant Biol 54 (2003a) 93-107

    Article  CAS  Google Scholar 

  • KJ Dietz, Redox control, redox signaling, and redox homeostasis in plant cells. Int Rev Cytol 228 (2003b) 141-193

    CAS  Google Scholar 

  • K-J Dietz, G Link, EK Pistorius and R Scheibe, Redox regulation in oxigneic photosynthesis. Prog Bot 63 (2002) 207-243

    CAS  Google Scholar 

  • CT Dooley, TM Dore, GT Hanson, WC Jackson, SJ Remington and RY Tsien, Imaging dynamic redox changes in mammalian cells with green fluorescent protein indicators. J Biol Chem 279 (2004) 22284-22293

    Article  PubMed  CAS  Google Scholar 

  • AG Doulis, N Debian, AH Kingston-Smith and CH Foyer, Differential localization of antioxidants in maize leaves. Plant Physiol 114 (1997) 1031-1037

    PubMed  CAS  Google Scholar 

  • R Edwards, D Dixon and V Walbot, Plant glutathione S-transferases: enzymes with multiple functions in sickness and in health. Trends Plant Sci 5 (2000) 193-198

    Article  PubMed  CAS  Google Scholar 

  • N Evans, M McAinsh, A Hetherington and M Knight, ROS perception in Arabidopsis thaliana: the ozone-induced calcium response. Plant J 41 (2005) 615-626

    Article  PubMed  CAS  Google Scholar 

  • RC Fahey and AR Sundquist, Evolution of glutathione metabolism. Adv Enz Rel Areas Mol Biol 64 (1991) 1-53

    CAS  Google Scholar 

  • A Fernandes and A Holmgren, Glutaredoxins: glutathione-dependent redox enzymes with functions far beyond a simple thioredoxin backup system. Antioxid Redox Signal 6 (2004) 63-74

    Article  PubMed  CAS  Google Scholar 

  • V Fey, R Wagner, K Bräutigam, M Wirtz, R Hell, A Dietzmann, D Leister, R Oelmüller and T Pfannschmidt, Retrograde plastid redox signals in the expression of nuclear genes for chloroplast proteins of Arabidopsis thaliana. J Biol Chem 280 (2005) 5318-5328

    Article  PubMed  CAS  Google Scholar 

  • J Foreman, V Demidchik, J Bothwell, P Mylona, H Miedema, M Torres, P Linstead, S Costa, C Brownlee, J Jones, J Davies and L Dolan, Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422 (2003) 442-446

    Article  PubMed  CAS  Google Scholar 

  • CH Foyer and G Noctor, Oxygen processing in photosynthesis: regulation and signalling. New Phytol 146 (2000) 359-388

    Article  CAS  Google Scholar 

  • CH Foyer, FL Theodoulou and S Delrot, The functions of inter- and intracellular glutathione transport systems in plants. Trends Plant Sci 6 (2001) 486-492

    Article  PubMed  CAS  Google Scholar 

  • A Frand, J Cuozzo and C Kaiser, Pathways for protein disulphide bond formation. Trends Cell Biol 10 (2000) 203-210

    Article  PubMed  CAS  Google Scholar 

  • JA Fraser, P Kansagra, C Kotecki, RD Saunders and LI McLellan, The modifier subunit of Drosophila glutamate-cysteine ligase regulates catalytic activity by covalent and noncovalent interactions and influences glutathione homeostasis in vivo. J Biol Chem 278 (2003) 46369-46377

    Article  PubMed  CAS  Google Scholar 

  • MD Fricker, M May, AJ Meyer, N Sheard and NS White, Measurement of glutathione levels in intact roots of Arabidopsis. J Microsc 198 (2000) 162-173

    Article  PubMed  CAS  Google Scholar 

  • C Frova, The plant glutathione transferase gene family: genomic structure, functions, expression and evolution. Physiol Plant 119 (2003) 469-479

    Article  CAS  Google Scholar 

  • J Gao, D Yin, Y Yao, TD Williams and TC Squier, Progressive decline in the ability of calmodulin isolated from aged brain to activate the plasma membrane Ca-ATPase. Biochemistry 37 (1998) 9536-9548

    Article  PubMed  CAS  Google Scholar 

  • E Gelhaye, N Rouhier and J Jacquot, Evidence for a subgroup of thioredoxin h that requires GSH/Grx for its reduction. FEBS Lett 555 (2003) 443-448

    Article  PubMed  CAS  Google Scholar 

  • E Gelhaye, N Rouhier, N Navrot and J Jacquot, The plant thioredoxin system. Cell Mol Life Sci 62 (2005) 24-35

    Article  PubMed  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 (2004) 1851-1859

    Article  PubMed  CAS  Google Scholar 

  • A Goyer, C Haslekas, M Miginiac-Maslow, U Klein, P Le Marechal, J-P Jacquot and P Decottignies, Isolation and characterization of a thioredoxin-dependent peroxidase from Chlamydomonas reinhardtii. Eur J Biochem 269 (2002) 272-282

    Article  PubMed  CAS  Google Scholar 

  • C Grant, Role of the glutathione/glutaredoxin and thioredoxin systems in yeast growth and response to stress conditions. Mol Microbiol 39 (2001) 533-541

    Article  PubMed  CAS  Google Scholar 

  • J Grant, B Yun and G Loake, Oxidative burst and cognate redox signalling reported by luciferase imaging: identification of a signal network that functions independently of ethylene, SA, Me-JA but is dependent on MAPKK activity. Plant J 24 (2000) 569-582

    Article  PubMed  CAS  Google Scholar 

  • O Griffith, Mechanism of action, metabolism, and toxicity of buthionine sulfoximine and its higher homologs, potent inhibitors of glutathione synthesis. J Biol Chem 257 (1982) 13704-13712

    PubMed  CAS  Google Scholar 

  • Griffith OW and Mulcahey RT (1999) The enzymes of glutathione synthesis: γ-glutamylcysteine synthetase. In: Purich DL (ed) Advances in Enzymology and Related Areas of Molecular Biology, pp 209–267. John Wiley & Sons, Newyork.

  • L Grimm, M Collison, R Fisher and J Thomas, Protein mixed-disulfides in cardiac cells. S-thiolation of soluble proteins in response to diamide. Biochim Biophys Acta 844 (1985) 50-54

    Article  PubMed  CAS  Google Scholar 

  • G Gutiérrez-Alcalá, C Gotor, AJ Meyer, M Fricker, JM Vega and LC Romero, Glutathione biosynthesis in Arabidopsis trichome cells. Proc Natl Acad Sci USA 97 (2000) 11108-11113

    Article  PubMed  Google Scholar 

  • JF Gutierrez-Marcos, MA Roberts, EI Campbell and JL Wray, Three members of a novel small gene-family from Arabidopsis thaliana able to complement functionally an Escherichia coli mutant defective in PAPS reductase activity encode proteins with a thioredoxin-like domain and `APS reductase' activity. Proc Natl Acad Sci USA 93 (1996) 13377-13382

    Article  PubMed  CAS  Google Scholar 

  • GT Hanson, R Aggeler, D Oglesbee, M Cannon, RA Capaldi, RY Tsien and SJ Remington, Investigating mitochondrial redox potential with redox-sensitive green fluorescent protein indicators. J Biol Chem 279 (2004) 13044-13053

    Article  PubMed  CAS  Google Scholar 

  • K Harms, P Ballmoos von, C Brunold, R Höfgen and H Hesse, Expression of a bacterial serine acetyltransferase in transgenic potato plants leads to increased levels of cysteine and glutathione. Plant J 22 (2000) 335-343

    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 × P. alba) of wild type and overexpressing γ-glutamylcysteine synthetase in the cytosol. J Exp Bot 55 (2004) 837-845

    Article  PubMed  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 

  • GF Heine, JM Hernandez and E Grotewold, Two cysteines in plant R2R3 MYB domains participate in REDOX-dependent DNA Binding. J Biol Chem 279 (2004) 37878-37885

    Article  PubMed  CAS  Google Scholar 

  • R Hell and L Bergmann, Glutathione synthetase in tobacco suspension cultures: catalytic properties and localization. Physiol Plant 72 (1988) 70-76

    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 

  • D Herouart, M Montagu and D Inzé, Redox-activated expression of the cytosolic copper/zinc superoxide dismutase gene in Nicotiana. Proc Natl Acad Sci USA 90 (1993) 3108-3112

    PubMed  CAS  Google Scholar 

  • A Holmgren, Hydrogen donor system for Escherichia coli ribonucleoside-diphosphate reductase dependent upon glutathione. Proc Natl Acad Sci USA 73 (1976) 2275-2279

    PubMed  CAS  Google Scholar 

  • A Holmgren, Thioredoxin and glutaredoxin systems. J Biol Chem 264 (1989) 13963-13966

    PubMed  CAS  Google Scholar 

  • CC Hwang, AJ Sinskey and HF Lodish, Oxidized redox state of glutathione in the endoplasmic reticulum. Science 257 (1992) 1496-1502

    PubMed  CAS  Google Scholar 

  • V Irihimovitch and M Shapira, Glutathione redox potential modulated by reactive oxygen species regulates translation of Rubisco large subunit in the chloroplast. J Biol Chem 275 (2000) 16289-16295

    Article  PubMed  CAS  Google Scholar 

  • H Ito, M Iwabuchi and K Ogawa, The sugar-metabolic enzymes aldolase and triose-phosphate isomerase are targets of glutathionylation in Arabidopsis thaliana: detection using biotinylated glutathione. Plant Cell Physiol 44 (2003) 655-660

    Article  PubMed  CAS  Google Scholar 

  • CE Jessop and NJ Bulleid, Glutathione directly reduces an oxidoreductase in the endoplasmic reticulum of mammalian cells. J Biol Chem 279 (2004) 55341-55347

    Article  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) 33463-33470

    Article  PubMed  CAS  Google Scholar 

  • M Jiang and J Zhang, Involvement of plasma-membrane NADPH oxidase in abscisic acid- and water stress-induced antioxidant defense in leaves of maize seedlings. Planta 215 (2002) 1022-1030

    Article  PubMed  CAS  Google Scholar 

  • J Juttner, D Olde, P Langridge and U Baumann, Cloning and expression of a distinct subclass of plant thioredoxins. Eur J Biochem 267 (2000) 7109-7117

    Article  PubMed  CAS  Google Scholar 

  • S Klapheck, Homoglutathione: isolation, quantification and occurence in legumes. Physiol Plant 74 (1988) 727-732

    CAS  Google Scholar 

  • S Klapheck, W Fliegner and I Zimmer, Hydroxymethyl-phytochelatins [(gamma-glutamylcysteine)n-serine] are metal-induced peptides of the Poaceae. Plant Physiol 104 (1994) 1325-1332

    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 

  • H Knight and MR Knight, Abiotic stress signalling pathways: specificity and cross-talk. Trends Plant Sci 6 (2001) 262-267

    Article  PubMed  CAS  Google Scholar 

  • S Kopriva, S Jones, A Koprivova, M Suter, P Ballmoos von, K Brander, J Flückiger and C Brunold, Influence of chilling stress on the intercellular distribution of assimilatory sulfate reduction and thiols in Zea mays. Plant Biol 3 (2001) 24-31

    Article  CAS  Google Scholar 

  • S Kopriva and A Koprivova, Sulphate assimilation: A pathway which likes to surprise. In: YP Abrol and A Ahmad (eds.) Sulphur in Plants. Dordrecht, The Netherlands: Kluwer Academic Publishers, Dordrecht, The Netherlands (2003) pp. 87-112

    Google Scholar 

  • Kopriva S and Koprivova A (2005) Sulfate assimilation and glutathione synthesis in C4 plants. Photosynth Res, this issue

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

    Article  PubMed  CAS  Google Scholar 

  • L Leichert and U Jakob, Protein thiol modifications visualized in vivo. PLoS Biol 2 (2004) 1723-1737

    Article  CAS  Google Scholar 

  • SD Lemaire, The glutaredoxin family in oxygenic photosynthetic organisms. Photosynth Res 79 (2004) 305-318

    Article  PubMed  CAS  Google Scholar 

  • SD Lemaire, B Guillon, P Le Marechal, E Keryer, M Miginiac-Maslow and P Decottignies, New thioredoxin targets in the unicellular photosynthetic eukaryote Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 101 (2004) 7475-7480

    Article  PubMed  CAS  Google Scholar 

  • A Levine, R Tenhaken, R Dixon and C Lamb, H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79 (1994) 583-593

    Article  PubMed  CAS  Google Scholar 

  • RL Levine, L Mosoni, BS Berlett and ER Stadtman, Methionine residues as endogenous antioxidants in proteins. Proc Natl Acad Sci USA 93 (1996) 15036-15040

    Article  PubMed  CAS  Google Scholar 

  • SP Long, S Humphries and PG Falkowski, Photoinhibition of photosynthesis in nature. Annu Rev Plant Physiol Plant Mol Biol 45 (1994) 633-662

    Article  CAS  Google Scholar 

  • WT Lowther, N Brot, H Weissbach and BW Matthews, Structure and mechanism of peptide methionine sulfoxide reductase, an `anti-oxidation' enzyme. Biochemistry 39 (2000) 13307-13312

    Article  PubMed  CAS  Google Scholar 

  • K Maeda, C Finnie and B Svensson, Cy5 maleimide labelling for sensitive detection of free thiols in native protein extracts: identification of seed proteins targeted by barley thioredoxin h isoforms. Biochem J 378 (2004) 497-507

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • MN Martin and JP Slovin, Purified γ-glutamyl transpeptidases from tomato exhibit high affinity for glutathione and glutathione S-conjugates. Plant Physiol 122 (2000) 1417-1426

    Article  PubMed  CAS  Google Scholar 

  • Martin MN, Tarczynski MC, Shen B and Leustek T (2005) The role of 5'-adenylylsulfate reductase in controlling sulfate reduction in plants. Photosynth Res, this volume

  • P Martinsuo, S Pursiheimo, E-M Aro and E Rintamäki, Dithiol oxidant and disulfide reductant dynamically regulate the phosphorylation of light-harvesting complex II proteins in thylakoid membranes. Plant Physiol 133 (2003) 37-46

    Article  PubMed  CAS  Google Scholar 

  • M May, T Vernoux, C Leaver, M Montagu Van and D Inzé, Glutathione homeostasis in plants: implications for environmental sensing and plant development. J Exp Bot 49 (1998) 649-667

    Article  CAS  Google Scholar 

  • MJ May and CJ Leaver, Oxidative stimulation of glutathione synthesis in Arabidopsis thaliana suspension cultures. Plant Physiol 103 (1993) 621-627

    PubMed  CAS  Google Scholar 

  • CA McAuliffe and SG Murray, Metal complexes of sulphur containing amino acids. Inorg Chim Acta Rev 6 (1972) 103-121

    Article  CAS  Google Scholar 

  • AH Mehler, Studies on reactivities of illuminated chloroplasts. I. Mechanism of the reduction of oxygen and other Hill reagents. Arch Biochem Biophys 33 (1951) 65-77

    Article  CAS  Google Scholar 

  • A Meister, Glutathione metabolism and its selective modification. J Biol Chem 263 (1988) 17205-17208

    PubMed  CAS  Google Scholar 

  • P Meuwly, P Thibault and WE Rauser, γ-Glutamylcysteinylglutamic acid – a new homologue of glutathione in maize seedlings exposed to cadmium. FEBS Lett 336 (1993) 472-476

    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 Microsc 198 (2000) 174-181

    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 

  • 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 

  • AH Millar, LJ Sweetlove, P Giege and CJ Leaver, Analysis of the Arabidopsis mitochondrial proteome. Plant Physiol 127 (2001) 1711-1727

    Article  PubMed  CAS  Google Scholar 

  • K Motohashi, A Kondoh, MT Stumpp and T Hisabori, Comprehensive survey of proteins targeted by chloroplast thioredoxin. Proc Natl Acad Sci USA 98 (2001) 11224-11229

    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 

  • PM Mullineaux, S Karpinski, A Jimenez, SP Cleary, C Robinson and GP Creissen, Identification of cDNAS encoding plastid-targeted glutathione peroxidase. Plant J 13 (1998) 375-379

    Article  PubMed  CAS  Google Scholar 

  • GL Newton and B Javor, γ-Glutamylcysteine and th iosulfate are the major low-molecular-weight thiols in halobacteria. J Bacteriol 161 (1985) 438-441

    PubMed  CAS  Google Scholar 

  • G Noctor, A Arisi, L Jouanin and C 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, 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, A-CM Arisi, L Jouanin, M-H Valadier, Y Roux and CH Foyer, The role of glycine in determining the rate of glutathione synthesis in poplar. Possible implications for glutathione production during stress. Physiol Plant 100 (1997) 255-263

    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 

  • G Noctor, M Strohm, L Jouanin, KJ Kunert, CH Foyer and H Rennenberg, Synthesis of glutathione in leaves of transgenic poplar overexpressing γ-glutamylcysteine synthetase. Plant Physiol 112 (1996) 1071-1078

    PubMed  CAS  Google Scholar 

  • Ogawa Ki, A Ogawa Ki 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  Google Scholar 

  • ML Orozco-Cárdenas, J Narvaez-Vásquez and CA Ryan, Hydrogen peroxide acts as a second messenger for the induction of defense genes in tomato plants in response to wounding, systemin, and methyl jasmonate. Plant Cell 13 (2001) 179-191

    Article  PubMed  Google Scholar 

  • H Ostergaard, A Henriksen, FG Hansen and JR Winther, Shedding light on disulfide bond formation: engineering a redox switch in green fluorescent protein. EMBO J 20 (2001) 5853-5862

    Article  PubMed  CAS  Google Scholar 

  • H Ostergaard, C Tachibana and JR Winther, Monitoring disulfide bond formation in the eukaryotic cytosol. J Cell Biol 166 (2004) 337-345

    Article  PubMed  CAS  Google Scholar 

  • M Paget and M Buttner, Thiol-based regulatory switches. Annu Rev Genet 37 (2003) 91-121

    Article  PubMed  CAS  Google Scholar 

  • S Park and JA Imlay, High levels of intracellular cysteine promote oxidative DNA damage by driving the Fenton reaction. J Bacteriol 185 (2003) 1942-1950

    Article  PubMed  CAS  Google Scholar 

  • GM Pastori, PM Mullineaux and CH Foyer, Post-transcriptional regulation prevents accumulation of glutathione reductase protein and activity in the bundle sheath cells of maize. Plant Physiol 122 (2000) 667-675

    Article  PubMed  CAS  Google Scholar 

  • I Pe'er, C Felder, O Man, I Silman, J Sussman and J Beckmann, Proteomic signatures: amino acid and oligopeptide compositions differentiate among phyla. Proteins 54 (2004) 20-40

    Article  PubMed  CAS  Google Scholar 

  • ZM Pei, Y Murata, G Benning, S Thomine, B Klusener, GJ Allen, E Grill and JI Schroeder, Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature 406 (2000) 731-734

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • T Pfannschmidt, JF Allen and R Oelmüller, Principles of redox control in photosynthesis gene expression. Physiol Plant 112 (2001) 1-9

    Article  CAS  Google Scholar 

  • L Poole, P Karplus and A Claiborne, Protein sulfenic acids in redox signaling. Annu Rev Pharmacol Toxicol 44 (2004) 325-347

    Article  PubMed  CAS  Google Scholar 

  • P Porras, J Pedrajas, E Martinez-Galisteo, C Padilla, C Johansson, A Holmgren and J Barcena, Glutaredoxins catalyze the reduction of glutathione by dihydrolipoamide with high efficiency. Biochem Biophys Res Commun 295 (2002) 1046-1051

    Article  PubMed  CAS  Google Scholar 

  • A Prior, J Uhrig, L Heins, A Wiesmann, C Lillig, C Stoltze, J Soll and J Schwenn, Structural and kinetic properties of adenylyl sulfate reductase from Catharanthus roseus cell cultures. Biochim Biophys Acta 1430 (1999) 25-38

    PubMed  CAS  Google Scholar 

  • M Rao and K Davis, Ozone-induced cell death occurs via two distinct mechanisms in Arabidopsis: the role of salicylic acid. Plant J 17 (1999) 603-614

    Article  PubMed  CAS  Google Scholar 

  • PA Rea, ZS Li, YP Lu, YM Drozdowicz and E Martinoia, From vacuolar GS-X pumps to multispecific ABC transporters. Annu Rev Plant Physiol Plant Mol Biol 49 (1998) 727-760

    Article  PubMed  CAS  Google Scholar 

  • M Rentel, D Lecourieux, F Ouaked, S Usher, L Petersen, H Okamoto, H Knight, S Peck, C Grierson, H Hirt and M Knight, OXI1 kinase is necessary for oxidative burst-mediated signalling in Arabidopsis. Nature 427 (2004) 858-861

    Article  PubMed  CAS  Google Scholar 

  • P Rey, S Cuine, F Eymery, J Garin, M Court, J Jacquot, N Rouhier and M Broin, Analysis of the proteins targeted by CDSP32, a plastidic thioredoxin participating in oxidative stress responses. Plant J 41 (2005) 31-42

    Article  PubMed  CAS  Google Scholar 

  • A Rietsch and J Beckwith, The genetics of disulfide bond metabolism. Annu Rev Genet 32 (1998) 163-184

    Article  PubMed  CAS  Google Scholar 

  • E Rintamäki, P Martinsuo, S Pursiheimo and E-M Aro, Cooperative regulation of light-harvesting complex II phosphorylation via the plastoquinol and ferredoxin-thioredoxin system in chloroplasts. Proc Natl Acad Sci USA 97 (2000) 11644-11649

    Article  PubMed  Google Scholar 

  • D Ritz and J Beckwith, Roles of thiol-redox pathways in bacteria. Annu Rev Microbiol 55 (2001) 21-48

    Article  PubMed  CAS  Google Scholar 

  • M Rodriguez Milla, A Maurer, A Rodriguez Huete and J Gustafson, Glutathione peroxidase genes in Arabidopsis are ubiquitous and regulated by abiotic stresses through diverse signaling pathways. Plant J 36 (2003) 602-615

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • N Rouhier, E Gelhaye and JP Jacquot, Glutaredoxin-dependent peroxiredoxin from poplar Protein–protein interaction and catalytic mechanism. J Biol Chem 277 (2002) 13609-13614

    Article  PubMed  CAS  Google Scholar 

  • N Rouhier, E Gelhaye, P-E Sautiere, A Brun, P Laurent, D Tagu, J Gerard, E Fay de, Y Meyer and J-P Jacquot, Isolation and characterization of a new peroxiredoxin from poplar sieve tubes that uses either glutaredoxin or thioredoxin as a proton donor. Plant Physiol 127 (2001) 1299-1309

    Article  PubMed  CAS  Google Scholar 

  • V Roxas, R Smith, E Allen and R Allen, Overexpression of glutathione S-transferase/glutathione peroxidase enhances the growth of transgenic tobacco seedlings during stress. Nat Biotechnol 15 (1997) 988-991

    Article  PubMed  CAS  Google Scholar 

  • VP Roxas, SA Lodhi, DK Garrett, JR Mahan and RD Allen, Stress tolerance in transgenic tobacco seedlings that overexpress glutathione S-transferase/glutathione peroxidase. Plant Cell Physiol 41 (2000) 1229-1234

    Article  PubMed  CAS  Google Scholar 

  • A Sadanandom, Z Poghosyan, DJ Fairbairn and DJ Murphy, Differential regulation of plastidial and cytosolic isoforms of peptide methionine sulfoxide reductase in Arabidopsis. Plant Physiol 123 (2000) 255-264

    Article  PubMed  CAS  Google Scholar 

  • M Samuel, G Miles and B Ellis, Ozone treatment rapidly activates MAP kinase signalling in plants. Plant J 22 (2000) 367-376

    Article  PubMed  CAS  Google Scholar 

  • R Sánchez-Fernández, M Fricker, LB Corben, NS White, N Sheard, CJ Leaver, M Montagu Van, D Inzé and MJ May, Cell proliferation and hair tip growth in the Arabidopsis root are under mechanistically different forms of redox control. Proc Natl Acad Sci USA 94 (1997) 2745-2750

    Article  PubMed  Google Scholar 

  • HJ Sandermann, D Ernst, W Heller and C Langebartels, Ozone: an abiotic elicitor of plant defence reactions. Trends Plant Sci 3 (1998) 47-50

    Article  Google Scholar 

  • FQ Schafer and GR Buettner, Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple. Free Radic Biol Med 30 (2001) 1191-1212

    Article  PubMed  CAS  Google Scholar 

  • R Schupp and H Rennenberg, Diurnal changes in the glutathione content of spruce needles (Picea abies L.). Plant Sci 57 (1988) 113-117

    Article  CAS  Google Scholar 

  • P Schürmann and J-P Jacquot, Plant thioredoxin systems revisited. Annu Rev Plant Physiol Plant Mol Biol 51 (2000) 371-400

    Article  PubMed  Google Scholar 

  • YK Sharma and KR Davis, Ozone-induced expression of stress-related genes in Arabidopsis thaliana. Plant Physiol 105 (1994) 1089-1096

    PubMed  CAS  Google Scholar 

  • H Sies, Glutathione and its role in cellular functions. Free Radic Biol Med 27 (1999) 916-921

    Article  PubMed  CAS  Google Scholar 

  • F Simon-Plas, T Elmayan and J Blein, The plasma membrane oxidase NtrbohD is responsible for AOS production in elicited tobacco cells. Plant J 31 (2002) 137-147

    Article  PubMed  CAS  Google Scholar 

  • DW Starke, PB Chock and JJ Mieyal, Glutathione-thiyl radical scavenging and transferase properties of human glutaredoxin thioltransferase Potential role in redox signal transduction. J Biol Chem 278 (2003) 14607-14613

    Article  PubMed  CAS  Google Scholar 

  • R Steinkamp and H Rennenberg, Degradation of glutathione in plant cells: evidence against the participation of a γ-glutamyltranspeptidase. Z Naturf 40c (1985) 29-33

    CAS  Google Scholar 

  • S Storozhenko, E Belles-Boix, E Babiychuk, D Herouart, MW Davey, L Slooten, M Montagu Van, D Inzé 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, L Jouanin, KJ Kunert, C Pruvost, A Polle, CH Foyer and H Rennenberg, Regulation of glutathione synthesis in leaves of transgenic poplar (Populus tremula × P. alba) overexpressing glutathione synthetase. Plant J 7 (1995) 141-145

    Article  CAS  Google Scholar 

  • C Sundby, U Harndahl, N Gustavsson, E Ahrman and D Murphy, Conserved methionines in chloroplasts. Biochim Biophys Acta 1703 (2005) 191-202

    PubMed  CAS  Google Scholar 

  • A Sundquist and R Fahey, Evolution of antioxidant mechanisms: thiol-dependent peroxidases and thioltransferase among procaryotes. J Mol Evol 29 (1989) 429-435

    PubMed  CAS  Google Scholar 

  • JE Taylor, JF Yan and J-L Wang, The Iron(III)-Catalyzed oxidation of cysteine by molecular oxygen in aqueous phase. An example of a two-thirds-order reaction. J Am Chem Soc 88 (1966) 1663-1667

    Article  PubMed  CAS  Google Scholar 

  • T Trebitsh, E Meiri, O Ostersetzer, Z Adam and A Danon, The protein disulfide isomerase-like RB60 is partitioned between stroma and thylakoids in Chlamydomonas reinhardtii chloroplasts. J Biol Chem 276 (2001) 4564-4569

    Article  PubMed  CAS  Google Scholar 

  • AE Tron, CW Bertoncini, RL Chan and DH Gonzalez, Redox regulation of plant homeodomain transcription factors. J Biol Chem 277 (2002) 34800-34807

    Article  PubMed  CAS  Google Scholar 

  • Z Tu and M Anders, Identification of an important cysteine residue in human glutamate-cysteine ligase catalytic subunit by site-directed mutagenesis. Biochem J 336 (1998) 675-680

    PubMed  CAS  Google Scholar 

  • F Ursini, M Maiorino, R Brigelius-Flohe, K Aumann, A Roveri, D Schomburg and L Flohe, Diversity of glutathione peroxidases. Meth Enzymol 252 (1995) 38-53

    PubMed  CAS  Google Scholar 

  • H Vanacker, TL 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 Inzé, 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, 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 (2000) 515-532

    Article  Google Scholar 

  • M Weber, M Suter, C Brunold and S Kopriva, Sulfate assimilation in higher plants characterization of a stable intermediate in the adenosine 5'-phosphosulfate reductase reaction. Eur J Biochem 267 (2000) 3647-3653

    Article  PubMed  CAS  Google Scholar 

  • G Wheeler and C Grant, Regulation of redox homeostasis in the yeast Saccharomyces cerevisiae. Physiol Plant 120 (2004) 12-20

    Article  PubMed  CAS  Google Scholar 

  • VPM 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 

  • J Wong, Y Balmer, N Cai, C Tanaka, W Vensel, W Hurkman and B Buchanan, Unraveling thioredoxin-linked metabolic processes of cereal starchy endosperm using proteomics. FEBS Lett 547 (2003) 151-156

    Article  PubMed  CAS  Google Scholar 

  • J Wong, N Cai, Y Balmer, C Tanaka, W Vensel, W Hurkman and B Buchanan, Thioredoxin targets of developing wheat seeds identified by complementary proteomic approaches. Phytochemistry 65 (2004) 1629-1640

    Article  PubMed  CAS  Google Scholar 

  • C Xiang and D Bertrand, Glutathione synthesis in Arabidopsis: Multilevel controls coordinate responses to stress. In: C Brunold, H Rennenberg, LJ, Stulen De Kok and IC Davidian (eds.) Sulfur Nutrition and Sulfur Assimilation in Higher Plants. Berne, Switzerland: Paul Haupt Publishers, Berne, Switzerland (2000) pp. 409-412

    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 

  • S Xing, MG Rosso and S Zachgo, ROXY1, a member of the plant glutaredoxin family, is required for petal development in Arabidopsis thaliana. Development 132 (2005) 1555-1565

    Article  PubMed  CAS  Google Scholar 

  • D Yamazaki, K Motohashi, T Kasama, Y Hara and T Hisabori, Target proteins of the cytosolic thioredoxins in Arabidopsis thaliana. Plant Cell Physiol. 45 (2004) 18-27

    Article  PubMed  CAS  Google Scholar 

  • M Yanagida, M Mino, M Iwabuchi and K Ogawa, Reduced glutathione is a novel regulator of vernalization-induced bolting in the rosette plant Eustoma grandiflorum. Plant Cell Physiol 45 (2004) 129-137

    Article  PubMed  CAS  Google Scholar 

  • H Yano, JH Wong, YM Lee, M-J Cho and BB Buchanan, A strategy for the identification of proteins targeted by thioredoxin. Proc Natl Acad Sci USA 98 (2001) 4794-4799

    Article  PubMed  CAS  Google Scholar 

  • K Yap, J Kim, K Truong, M Sherman, T Yuan and M Ikura, Calmodulin target database. J Struct Funct Genomics 1 (2000) 8-14

    Article  PubMed  CAS  Google Scholar 

  • K Yoshimura, K Miyao, A Gaber, T Takeda, H Kanaboshi, H Miyasaka and S Shigeoka, Enhancement of stress tolerance in transgenic tobacco plants overexpressing Chlamydomonas glutathione peroxidase in chloroplasts or cytosol. Plant J 37 (2004) 21-33

    Article  PubMed  CAS  Google Scholar 

  • YL Zhu, EA Pilon-Smits, AS Tarun, SU Weber, L Jouanin and N Terry, Cadmium tolerance and accumulation in Indian mustard is enhanced by over expressing? γ-glutamylcysteine synthetase. Plant Physiol 121 (1999) 1169-1178

    Article  PubMed  CAS  Google Scholar 

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Meyer, A.J., Hell, R. Glutathione homeostasis and redox-regulation by sulfhydryl groups. Photosynth Res 86, 435–457 (2005). https://doi.org/10.1007/s11120-005-8425-1

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