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
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
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
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
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
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
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
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
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
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
U Baumann and J Juttner, Plant thioredoxins: the multiplicity conundrum. Cell Mol Life Sci 59 (2002) 1042-1057
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
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
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
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
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
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
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
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
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
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
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
I Carlberg, E Rintamäki, EM Aro and B Andersson, Thylakoid protein phosphorylation and the thiol redox state. Biochemistry 38 (1999) 3197-3204
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
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
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
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
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
H Clayton, M Knight, H Knight, M McAinsh and A Hetherington, Dissection of the ozone-induced calcium signature. Plant J 17 (1999) 575-579
PL Conklin and RL Last, Differential accumulation of antioxidant mRNAs in Arabidopsis thaliana exposed to ozone. Plant Physiol 109 (1995) 203-212
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
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
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
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
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
JW Cuozzo and CA Kaiser, Competition between glutathione and protein thiols for disulphide-bond formation. Nat Cell Biol 1 (1999) 130-135
A Danon, Redox reactions of regulatory proteins: do kinetics promote specificity?. Trends Biochem Sci 27 (2002) 197-203
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
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
R Dhindsa, Drought stress, enzymes of glutathione metabolism, oxidation injury and protein synthesis in Tortula ruralis. Plant Physiol 95 (1991) 648-651
KJ Dietz, Plant peroxiredoxins. Annu Rev Plant Biol 54 (2003a) 93-107
KJ Dietz, Redox control, redox signaling, and redox homeostasis in plant cells. Int Rev Cytol 228 (2003b) 141-193
K-J Dietz, G Link, EK Pistorius and R Scheibe, Redox regulation in oxigneic photosynthesis. Prog Bot 63 (2002) 207-243
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
AG Doulis, N Debian, AH Kingston-Smith and CH Foyer, Differential localization of antioxidants in maize leaves. Plant Physiol 114 (1997) 1031-1037
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
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
RC Fahey and AR Sundquist, Evolution of glutathione metabolism. Adv Enz Rel Areas Mol Biol 64 (1991) 1-53
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
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
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
CH Foyer and G Noctor, Oxygen processing in photosynthesis: regulation and signalling. New Phytol 146 (2000) 359-388
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
A Frand, J Cuozzo and C Kaiser, Pathways for protein disulphide bond formation. Trends Cell Biol 10 (2000) 203-210
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
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
C Frova, The plant glutathione transferase gene family: genomic structure, functions, expression and evolution. Physiol Plant 119 (2003) 469-479
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
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
E Gelhaye, N Rouhier, N Navrot and J Jacquot, The plant thioredoxin system. Cell Mol Life Sci 62 (2005) 24-35
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
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
C Grant, Role of the glutathione/glutaredoxin and thioredoxin systems in yeast growth and response to stress conditions. Mol Microbiol 39 (2001) 533-541
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
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
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
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
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
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
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
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
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
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
R Hell and L Bergmann, Glutathione synthetase in tobacco suspension cultures: catalytic properties and localization. Physiol Plant 72 (1988) 70-76
R Hell and L Bergmann, γ-Glutamylcysteine synthetase in higher plants: catalytic properties and subcellular localization. Planta 180 (1990) 603-612
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
A Holmgren, Hydrogen donor system for Escherichia coli ribonucleoside-diphosphate reductase dependent upon glutathione. Proc Natl Acad Sci USA 73 (1976) 2275-2279
A Holmgren, Thioredoxin and glutaredoxin systems. J Biol Chem 264 (1989) 13963-13966
CC Hwang, AJ Sinskey and HF Lodish, Oxidized redox state of glutathione in the endoplasmic reticulum. Science 257 (1992) 1496-1502
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
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
CE Jessop and NJ Bulleid, Glutathione directly reduces an oxidoreductase in the endoplasmic reticulum of mammalian cells. J Biol Chem 279 (2004) 55341-55347
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
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
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
S Klapheck, Homoglutathione: isolation, quantification and occurence in legumes. Physiol Plant 74 (1988) 727-732
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
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
H Knight and MR Knight, Abiotic stress signalling pathways: specificity and cross-talk. Trends Plant Sci 6 (2001) 262-267
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
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
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
L Leichert and U Jakob, Protein thiol modifications visualized in vivo. PLoS Biol 2 (2004) 1723-1737
SD Lemaire, The glutaredoxin family in oxygenic photosynthetic organisms. Photosynth Res 79 (2004) 305-318
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
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
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
SP Long, S Humphries and PG Falkowski, Photoinhibition of photosynthesis in nature. Annu Rev Plant Physiol Plant Mol Biol 45 (1994) 633-662
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
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
KA Marrs, The functions and regulation of glutathione S-transferases in plants. Annu Rev Plant Physiol Plant Mol Biol 47 (1996) 127-158
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
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
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
MJ May and CJ Leaver, Oxidative stimulation of glutathione synthesis in Arabidopsis thaliana suspension cultures. Plant Physiol 103 (1993) 621-627
CA McAuliffe and SG Murray, Metal complexes of sulphur containing amino acids. Inorg Chim Acta Rev 6 (1972) 103-121
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
A Meister, Glutathione metabolism and its selective modification. J Biol Chem 263 (1988) 17205-17208
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
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
AJ Meyer and MD Fricker, Control of demand-driven biosynthesis of glutathione in green Arabidopsis suspension culture cells. Plant Physiol 130 (2002) 1927-1937
AJ Meyer, MJ May and M Fricker, Quantitative in vivo measurement of glutathione in Arabidopsis cells. Plant J 27 (2001) 67-78
AH Millar, LJ Sweetlove, P Giege and CJ Leaver, Analysis of the Arabidopsis mitochondrial proteome. Plant Physiol 127 (2001) 1711-1727
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
Z Mou, W Fan and X Dong, Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113 (2003) 935-944
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
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
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
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
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
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
G Noctor and CH Foyer, Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49 (1998) 249-279
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
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
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
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
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
H Ostergaard, C Tachibana and JR Winther, Monitoring disulfide bond formation in the eukaryotic cytosol. J Cell Biol 166 (2004) 337-345
M Paget and M Buttner, Thiol-based regulatory switches. Annu Rev Genet 37 (2003) 91-121
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
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
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
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
T Pfannschmidt, Chloroplast redox signals: how photosynthesis controls its own genes. Trends Plant Sci 8 (2003) 33-41
T Pfannschmidt, JF Allen and R Oelmüller, Principles of redox control in photosynthesis gene expression. Physiol Plant 112 (2001) 1-9
L Poole, P Karplus and A Claiborne, Protein sulfenic acids in redox signaling. Annu Rev Pharmacol Toxicol 44 (2004) 325-347
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
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
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
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
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
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
A Rietsch and J Beckwith, The genetics of disulfide bond metabolism. Annu Rev Genet 32 (1998) 163-184
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
D Ritz and J Beckwith, Roles of thiol-redox pathways in bacteria. Annu Rev Microbiol 55 (2001) 21-48
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
N Rouhier, E Gelhaye and J Jacquot, Plant glutaredoxins: still mysterious reducing systems. Cell Mol Life Sci 61 (2004) 1266-1277
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
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
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
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
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
M Samuel, G Miles and B Ellis, Ozone treatment rapidly activates MAP kinase signalling in plants. Plant J 22 (2000) 367-376
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
HJ Sandermann, D Ernst, W Heller and C Langebartels, Ozone: an abiotic elicitor of plant defence reactions. Trends Plant Sci 3 (1998) 47-50
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
R Schupp and H Rennenberg, Diurnal changes in the glutathione content of spruce needles (Picea abies L.). Plant Sci 57 (1988) 113-117
P Schürmann and J-P Jacquot, Plant thioredoxin systems revisited. Annu Rev Plant Physiol Plant Mol Biol 51 (2000) 371-400
YK Sharma and KR Davis, Ozone-induced expression of stress-related genes in Arabidopsis thaliana. Plant Physiol 105 (1994) 1089-1096
H Sies, Glutathione and its role in cellular functions. Free Radic Biol Med 27 (1999) 916-921
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
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
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
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
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
C Sundby, U Harndahl, N Gustavsson, E Ahrman and D Murphy, Conserved methionines in chloroplasts. Biochim Biophys Acta 1703 (2005) 191-202
A Sundquist and R Fahey, Evolution of antioxidant mechanisms: thiol-dependent peroxidases and thioltransferase among procaryotes. J Mol Evol 29 (1989) 429-435
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
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
AE Tron, CW Bertoncini, RL Chan and DH Gonzalez, Redox regulation of plant homeodomain transcription factors. J Biol Chem 277 (2002) 34800-34807
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
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
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
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
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
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
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
G Wheeler and C Grant, Regulation of redox homeostasis in the yeast Saccharomyces cerevisiae. Physiol Plant 120 (2004) 12-20
VPM Wingate, MA Lawton and CJ Lamb, Glutathione causes a massive and selective induction of plant defense genes. Plant Physiol 87 (1988) 206-210
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
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
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
C Xiang and DJ Oliver, Glutathione metabolic genes coordinately respond to heavy metals and jasmonic acid in Arabidopsis. Plant Cell 10 (1998) 1539-1550
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
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
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
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
K Yap, J Kim, K Truong, M Sherman, T Yuan and M Ikura, Calmodulin target database. J Struct Funct Genomics 1 (2000) 8-14
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
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
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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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DOI: https://doi.org/10.1007/s11120-005-8425-1