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Glutathione Metabolism and Its Function in Higher Plants Adapting to Stress

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Antioxidants and Antioxidant Enzymes in Higher Plants

Abstract

Glutathione (GSH) is a low molecular weight tripeptide that plays an important role in metabolism and cell function. The cellular glutathione/glutathione disulfide (GSH/GSSG) redox buffer provides homeostasis by maintaining the redox state of other thiol compounds, avoiding their unnecessary oxidation and thus keeping them in the reduced state. Besides its involvement in the ascorbate–glutathione cycle, GSH is also critical for the detoxification of xenobiotics, the sequestration of heavy metals and other processes involved in environmental stress tolerance. Involvement of glutathione in post-translational modifications (PTMs) by the process of S-glutathionylation prevents proteins from becoming oxidized. The reversible formation of a mixed disulfide between GSH and cysteine residue on the target protein brings about conformational changes and alters the activity of several important proteins through a signaling cascade. The precise mechanisms involved in the formation of mixed disulfides in vivo are largely unknown, especially in higher plants. On the other hand, GSH can interact with the free radical nitric oxide (NO) to generate S-nitrosoglutathione (GSNO), which also can mediate other PTMs designated as S-nitrosylation. Environmental stresses affect the redox status of the cell, which in turn triggers signaling cascade pathway(s) leading to the altered physiology of the plants. This chapter highlights the involvement of GSH in redox regulation and its crosstalk with other pathways, particularly under abiotic and biotic stresses in plants.

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References

  • Airaki M, Leterrier M, Mateos RM, Valderrama R, Chaki M, Barroso JB, del Río LA, Palma JM, Corpas FJ (2012) Metabolism of reactive oxygen species and reactive nitrogen species in pepper (Capsicum annuum L.) plants under low temperature stress. Plant Cell Environ 35:281–295

    Google Scholar 

  • Anjum NA, Ahmad I, Mohmood I, Pacheco M, Duarte AC, Pereira E (2012) Modulation of glutathione and its related enzymes in plants’ responses to toxic metals and metalloids-a review. Environ Exp Bot 75:307–324

    CAS  Google Scholar 

  • Astier J, Rasul S, Koen E, Manzoor H, Besson-Bard A, Lamotte O, Jeandroz S, Durner J, Lindermayr C, Wendehenne D (2011) S-nitrosylation: an emerging post-translational protein modification in plants. Plant Sci 181:527–533

    Article  CAS  PubMed  Google Scholar 

  • Atwal PS, Medina CR, Burrage LC, Sutton VR (2016) Ninteen year follow-up of a patient with severe glutathione synthetase deficiency. J Hum Genet 61:669–672

    Article  PubMed  PubMed Central  Google Scholar 

  • Bachhawat AK, Kaur A (2017) Glutathione degradation. Antioxid Redox Sign 27:1200–1216

    Article  CAS  Google Scholar 

  • Ball L, Accotto G, Bechtold U (2004) Evidence for a direct link between glutathione biosynthesis and stress defense gene expression in Arabidopsis. Plant Cell 16:2448–2462

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Begara-Morales JC, Sánchez-Calvo B, Chaki M, Valderrama R, Mata-Pérez C, López-Jaramillo J, Padilla MN, Carreras A, Corpas FJ, Barroso JB (2014a) Dual regulation of cytosolic ascorbate peroxidase (APX) by tyrosine nitration and S-nitrosylation. J Exp Bot 65:527–538

    Article  CAS  PubMed  Google Scholar 

  • Begara-Morales JC, Sánchez-Calvo B, Luque F, Leyva-Pérez MO, Leterrier M, Corpas FJ, Barroso JB (2014b) Differential transcriptomic analysis by RNA-Seq of GSNO-responsive genes between Arabidopsis roots and leaves. Plant Cell Physiol 55:1080–1095

    Article  CAS  PubMed  Google Scholar 

  • Begara-Morales JC, Sánchez-Calvo B, Chaki M, Mata-Pérez C, Valderrama R, Padilla MN, López-Jaramillo J, Luque F, Corpas FJ, Barroso JB (2015) Differential molecular response of monodehydroascorbate reductase and glutathione reductase by nitration and S-nitrosylation. J Exp Bot 66:5983–5996

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bela K, Horváth E, Ágnes Gallé Szabados L, Tari I, Csiszár J (2015) Plant glutathione peroxidases: emerging role of the antioxidant enzymes in plant development and stress responses. J Plant Physiol 176:192–201

    Article  CAS  PubMed  Google Scholar 

  • Bita CE, Tom G (2013) Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stress-tolerant crops. Front Plant Sci 4:273

    Article  PubMed  PubMed Central  Google Scholar 

  • Blum R, Beck A, Korfte A, Stengel A, Letzel T, Lendzian K, Grill E (2007) Function of phytochelatin synthase in catabolism of glutathione-conjugates. Plant J 49:740–749

    Article  CAS  PubMed  Google Scholar 

  • Blum R, Meyer KC, Wünschmann J, Lendzian KJ, Grill E (2010) Cytosolic action of phytochelatin synthase. Plant Physiol 153:159–169

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bobik K, Burchsmith TM (2015) Chloroplast signaling within, between and beyond cells. Front Plant Sci 6:781

    Article  PubMed  PubMed Central  Google Scholar 

  • Bogs J, Bourbouloux A, Cagnac O, Wachter A, Rausch D, Delrot S (2003) Functional chacterization and expression analysis of a glutathione transporter, BjGT1, from Brassica juncea: evidence for regulation by heavy metal exposure. Plant Cell Environ 26:703–1711

    Article  Google Scholar 

  • Böttcher C, Westphal L, Schmotz C, Prade E, Scheel D, Glawischnig E (2009) The multifunctional enzyme CYP71B15 (PHYTOALEXIN DEFICIENT3) converts cysteine-indole-3-acetonitrile to camalexin in the indole-3-acetonitrile metabolic network of Arabidopsis thaliana. Plant Cell 21:1830–1845

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bourgis F, Roje S, Nuccio ML, Fisher DB, Tarczynski MC, Li C, Herschbach C, Rennenberg H, Pimenta MJ, Shen TL, Gage DA, Hanson AD (1999) S-methylmethionine plays a role in phloem sulfur transport and is synthesized by a novel type of methyltransferase. Plant Cell 11:1485–1498

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bouthour D, Kalai T, Chaffei HC, Gouia H, Corpas FJ (2015) Differential response of NADP-dehydrogenases and carbon metabolism in leaves and roots of two durum wheat (Triticum durum Desf.) cultivars (Karim and Azizi) with different sensitivities to salt stress. J Plant Physiol 179:56–63

    Article  CAS  PubMed  Google Scholar 

  • Brandenburg WA (1986) Classification of cultivated plants. Acta Horticult 182:109–116

    Article  Google Scholar 

  • Broniowska KA, Diers AR, Hogg N (2013) S-nitrosoglutathione. Biochim Biophys Acta 1830:3173–3178

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cairns NG, Pasternak M, Wachter A, Cobbett CS, Meyer AJ (2006) Maturation of Arabidopsis seeds is dependent on glutathione biosynthesis within the embryo. Plant Physiol 141:446–455

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carolin CF, Kumar PS, Saravanan A, Joshiba GJ, Naushad M (2017) Efficient techniques for the removal of toxic heavy metals from aquatic environment: a review. J Environ Chem Eng 5:2782–2799

    Article  CAS  Google Scholar 

  • Chen JH, Jiang HW, Hsieh EJ, Chen HY, Chien CT, Hsieh HL, Lin TP (2012) Drought and salt stress tolerance of an arabidopsis glutathione S-transferase U17 knockout mutant are attributed to the combined effect of glutathione and abscisic acid. Plant Physiol 158:340–351

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cohen AC, Bottini R, Pontin M, Berli FJ, Moreno D, Boccanlandro H, Travaglia CN, Piccoli PN (2015) Azospirillum brasilense ameliorates the response of Arabidopsis thaliana to drought mainly via enhancement of aba levels. Physiol Plant 153:79–90

    Article  CAS  PubMed  Google Scholar 

  • Corpas FJ, Alché JD, Barroso JB (2013) Current overview of S-nitrosoglutathione (GSNO) in higher plants. Front Plant Sci 4:126

    PubMed  PubMed Central  Google Scholar 

  • Dalle-Donne I, Rossi R, Giustarini D, Colombo R, Milzani A (2007) S-glutathionylation in protein redox regulation. Free Radical Biol Med 43:883–898

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Diaz-Vivancos P, De SA, Kiddle G, Foyer CH (2015) Glutathione–linking cell proliferation to oxidative stress. Free Rad Bio Med 89:1154–1164

    Article  CAS  Google Scholar 

  • Díaz-Vivancos P, Dong Y, Ziegler K, Markovic J, Pallardo FV, Pellny TK, Verrier PJ, Foyer CH (2010a) Recruitment of glutathione into the nucleus during cell proliferation adjusts whole-cell redox homeo-stasis in Arabidopsis thaliana and lowers the oxidative defence shield. Plant J 64:825–838

    Article  CAS  Google Scholar 

  • Díaz-Vivancos P, Wolff T, Markovic J, Pallardó FV, Foyer CH (2010b) A nuclear glutathione cycle within the cell cycle. Biochem J 431:169–178

    Article  PubMed  CAS  Google Scholar 

  • Dron M, Clouse SD, Dixon RA, Lawton MA, Lamb CJ (1988) Glutathione and fungal elicitor regulation of a plant defense gene promoter in electroporated protoplasts. Proc Natl Acad Sci USA 85:6738–6742

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ferrari S, Plotnikova JM, Lorenzo GD, Ausubel FM (2003) Arabidopsis local resistance to Botrytis cinerea involves salicylic acid and camalexin and requires EDS and PAD2, but not SID2, EDS5 or PAD4. Plant J 35:193–205

    Article  CAS  PubMed  Google Scholar 

  • Foyer CH, Noctor G (2011) Ascorbate and glutathione: the heart of the redox hub. Plant Physiol 155:2–18

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gallego SM, Benavídes MP, Tomaro ML (1996) Effect of heavy metal ion excess on sunflower leaves: evidence for involvement of oxidative stress. Plant Sci 121:151–159

    Article  CAS  Google Scholar 

  • Geuflores F, Nielsen MT, Nafisi M, Møldrup ME, Olsen CE, Motawia MS, Halkier BA (2009) Glucosinolate engineering identifies a gamma-glutamyl peptidase. Nat Chem Biol 5:575–577

    Article  CAS  Google Scholar 

  • Ghezzi P, Romines B, Fratelli M, Eberini I, Gianazza E, Casagrande S, Laragione T, Mengozzi M, Herzenberg LA (2002) Protein glutathionylation: coupling and uncoupling of glutathione to protein thiol groups in lymphocytes under oxidative stress and HIV infection. Mol Immunol 38:773–780

    Article  CAS  PubMed  Google Scholar 

  • Gómez LD, Vanacker H, Buchner P, Noctor G, Foyer CH (2004) Intercellular distribution of glutathione synthesis in maize leaves and its response to short-term chilling. Plant Physiol 134:1662–1671

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Green RM, Graham M, O’Donovan MR, Chipman JK, Hodges NJ (2006) Subcellular compartmentalization of glutathione: correlations with parameters of oxidative stress related to genotoxicity. Mutagenesis 21:383–390

    Article  CAS  PubMed  Google Scholar 

  • Grill ES, Loeffler E, Winnacker L, Zenk MH (1989) Phytochelatins, the heavy-metal-binding peptides of plants, are synthesized from glutathione by a specific γ-glutamylcysteine dipeptide transpeptidase (phytochelatin synthase). Proc Natl Acad Sci U S A 86:6838–6842

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Großkinsky DK, Koffler BE, Roitsch T, Maier R, Zechmann B (2012) Compartment-specific antioxidative defense in Arabidopsis against virulent and a virulent Pseudomonas syringae. Phytopathology 102:662–673

    Article  PubMed  CAS  Google Scholar 

  • Grzam A, Martin MN, Hell R, Meyer AJ (2007) γ-Glutamyl transpeptidase GGT4 initiates vacuolar degradation of glutathione S-conjugates in Arabidopsis. FEBS Lett 581:3131–3138

    Article  CAS  PubMed  Google Scholar 

  • Guaiquil VH, Farber CM, Golde DW, Vera JC (1997) Efficient transport and accumulation of vitamin C in HL-60 cells depleted of glutathione. J Biol Chem 272:9915–9921

    Article  CAS  PubMed  Google Scholar 

  • Gupta DK, Huang HG, Yang XE, Razafindrabe BHN, Inouhe M (2010) The detoxification of lead in Sedum alfredii H. is not related with phytochelatins but the glutathione. J Hazard Mater 177:437–444

    Article  CAS  PubMed  Google Scholar 

  • Gupta DK, Huang HG, Nicoloso FT, Schetinger MRC, Farias JG, Li TQ, Razafindrabe BHN, Aryal N, Inouhe M (2013a) Effect of Hg, As and Pb on biomass production, photosynthetic rate, nutrients uptake and phytochelatin induction in Pfaffia glomerata. Ecotoxicology 22:1403–1412

    Article  CAS  PubMed  Google Scholar 

  • Gupta DK, Inouhe M, Rodríguez-Serrano M, Romero-Puerta MC, Sandalio LM (2013b) Oxidative stress and arsenic toxicity: role of NADPH oxidases. Chemosphere 90:1987–1996

    Article  CAS  PubMed  Google Scholar 

  • Han Y, Chaouch S, Mhamdi A, Queval G, Zechmann B, Noctor G (2013) Functional analysis of Arabidopsis mutants points to novel roles for glutathione in coupling H(2)O(2) to activation of salicylic acid accumulation and signaling. Antioxid Redox Sign 18:2106–2121

    Article  CAS  Google Scholar 

  • Hartung W, Sauter A, Hose E (2002) Abscisic acid in the xylem: where does it come from, where does it go to? J Exp Bot 53:27–32

    Article  CAS  PubMed  Google Scholar 

  • Hatem E, Lagniela G, Jean-Jacques H, Labarre J, Kuras L, Chédin S (2016) Characterization of the oxidative stress response in yeast cells protected by gamma-glutamylcysteine instead of glutathione. J Int Soc Antioxid Nutr Heal 3

    Google Scholar 

  • Hatfield JL, Prueger JH (2015) Temperature extremes: effect on plant growth and development. Weath Clim Extrem 10:4–10

    Article  Google Scholar 

  • He J, Ren Y, Chen X, Chen H (2014) Protective roles of nitric oxide on seed germination and seedling growth of rice (Oryza sativa, L.) under cadmium stress. Ecotox Environ Safe 108:114–119

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Herbinger K, Tausz M, Wonisch A, Soja G, Sorger A, Grill D (2002) Complex interactive effects of drought and ozone stress on the antioxidant defense systems of two wheat cultivars. Plant Physiol Bioch 40:691–696

    Article  CAS  Google Scholar 

  • Ilyas S, Rehman A (2015) Oxidative stress, glutathione level and antioxidant response to heavy metals in multi-resistant pathogen, Candida tropicalis. Environ Monit Assess 187:1–7

    Article  CAS  Google Scholar 

  • Ji W, Zhu Y, Li Y, Yang L, Zhao X, Cai H, Bai X (2010) Over-expression of a glutathione S-transferase gene, GsGST, from wild soybean (Glycine soja) enhances drought and salt tolerance in transgenic tobacco. Biotechnol Lett 32:1173–1179

    Article  CAS  PubMed  Google Scholar 

  • Kalmatskaya OA, Karavaev VA (2015) The fluorescent indices of bean leaves treated with sodium fluoride. Biophysics 60:843–848

    Article  CAS  Google Scholar 

  • Kaymakanova M, Lyubenova L, Schröder P, Stoeva N (2010) Salt stress and glutathione-dependent enzyme activities in bean (Phaseolus Vulgaris L.). Gen Appl Plant Physiol 1–2:55–59

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Klapheck S, Chrost B, Starke J, Zimmermann H (1992) β-glutamylcysteinylserine—a new homologue of glutathione in plants of the family poaceae [Triticum aestivum]. Bot Acta 105:174–179

    Article  CAS  Google Scholar 

  • Koffler BE, Luschinebengreuth N, Zechmann B (2015) Compartment specific changes of the antioxidative status in arabidopsis thaliana during salt stress. J Plant Biol 58:8–16

    Article  CAS  Google Scholar 

  • Koh S, Wiles AM, Sharp JS, Naider FR, Becker JM, Stacey G (2002) An oligopeptide transporter gene family in Arabidopsis. Plant Physiol 128:21–29

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koornneef A, Leon-Reyes A, Ritsema T, Verhage A, Den Otter FC, Van Loon LC, Pieterse CMJ (2008) Kinetics of salicylate-mediated suppression of jasmonate signaling reveal a role for redox modulation. Plant Physiol 147:1358–1368

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar D, Datta R, Hazra S, Sultana A, Mukhopadhyay R, Chattopadhyay S (2015) Transcriptomic profiling of Arabidopsis thaliana mutant pad2.1 in response to combined cold and osmotic stress. PLoS ONE 10:e0122690

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kumar SR, Iyappan G, Jagadeesan H, Ramalingam S (2017) Genomics and genetic engineering in phytoremediation of arsenic. In: Gupta DK, Chatterjee C (eds) Arsenic contamination in the environment. Springer, Berlin, pp 171–186

    Google Scholar 

  • Kuzniak E, Sklodowska A (2005) Fungal pathogen-induced changes in the antioxidant systems of leaf peroxisomes from infected tomato plants. Planta 222:192–200

    Article  CAS  PubMed  Google Scholar 

  • Lee SH, Su YW, Sun MJ (2015) Effects of elevated CO2, and water stress on physiological responses of Perilla frutescens var. japonica, HARA. Plant Growth Regul 75:427–434

    Article  CAS  Google Scholar 

  • Li R, Wang W, Wang W, Li F, Wang Q, Xu Y (2015) Overexpression of a cysteine proteinase inhibitor gene from Jatropha curcas, confers enhanced tolerance to salinity stress. Elect J Biotechn 18:368–375

    Article  CAS  Google Scholar 

  • Li L, Lu X, Ma H, Lyu D (2017) Jasmonic acid regulates the ascorbate–glutathione cycle in Malus baccata Borkh roots under low root-zone temperature. Acta Physiol Plant 39:174

    Article  CAS  Google Scholar 

  • López-Vidal O, Camejo D, Rivera-Cabrera F, Konigsberg M, Villa-Hernández JM, Mendoza-Espinoza JA, Pérez-Flores LJ, Sevilla F, Jiménez A, Díaz de León-Sánchez F (2016) Mitochondrial ascorbate-glutathione cycle and proteomic analysis of carbonylated proteins during tomato (Solanum lycopersicum) fruit ripening. Food Chem 194:1064–1072

    Article  PubMed  CAS  Google Scholar 

  • Lóránt K, András K, Kerstin H, Maria F, Csilla J, Maria M, Gábor G, Bernd Z (2012) Sulfate supply influences compartment specific glutathione metabolism and confers enhanced resistance Totobacco mosaic virus during a hypersensitive response. Plant Physiol Biochem 59:44–54

    Article  CAS  Google Scholar 

  • Lu SC (2009) Regulation of glutathione synthesis. Mol Aspects Med 30:42–59

    Article  CAS  PubMed  Google Scholar 

  • Markovic J, Borrás C, Ortega A, Sastre J, Viña J, Pallardó FV (2007) Glutathione is recruited into the nucleus in early phases of cell proliferation. J Biol Chem 282:20416–20424

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martin MN, Saladores PH, Lambert E, Hudson AO, Leustek T (2007) Localization of members of the γ-glutamyl transpeptidase family identifies sites of glutathione and glutathione S-conjugate hydrolysis. Plant Physiol 144:1715–1732

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maughan SC, Pasternak M, Cairns N (2010) Plant homologs of the Plasmodium falciparum chloroquine resistance transporter, PfCRT, are required for glutathione homeostasis and stress responses. Proc Natl Acad Sci U S A 107:2331–2336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • May MJ, Hammond-Kosack KE, Jones JDG (1996) Involvement of reactive oxygen species, glutathione metabolism and lipid peroxidation in the Cf-gene-dependent defence response of tomato cotyledons induced by race-specific elicitors of Cladosporium fulvum. Plant Physiol 110:1367–1379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mendoza-Cózatl DG, Moreno-Sánchez R (2006) Control of glutathione and phytochelatin synthesis under cadmium stress. Pathway modeling for plants. J Theor Biol 238:919–936

    Article  PubMed  CAS  Google Scholar 

  • Mendoza-Cózatl DG, Butko E, Springer F, Torpey JW, Komives EA, Kehr J, Schroeder JI (2008) Identification of high levels of phytochelatins, glutathione and cadmium in the phloem sap of Brassica napus. A role for thiol-peptides in the long-distance transport of cadmium and the effect of cadmium on iron translocation. Plant J 54:249–259

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Mhamdi A, Hager J, Chaouch S (2010) Arabidopsis GLUTATHIONE REDUCTASE1 plays a crucial role in leaf responses to intracellular hydrogen peroxide and in ensuring appropriate gene expression through both salicylic acid and jasmonic acid signaling pathways. Plant Physiol 153:1144–1160

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mittova V, Theodoulou FL, Kiddle G, Gómez L, Volokita M, Tal M, Foyer CH, Guy M (2003) Coordinate induction of glutathione biosynthesis and glutathione-metabolizing enzymes is correlated with salt tolerance in tomato. FEBS Lett 554:417–421

    Article  CAS  PubMed  Google Scholar 

  • Mohammadi H, Moradi F (2016) Effects of growth regulators on enzymatic and non-enzymatic antioxidants in leaves of two contrasting wheat cultivars under water stress. Braz J Bot 39:1–11

    Article  Google Scholar 

  • Mukherjee SP, Choudhuri MA (1983) Implications of water stress-induced changes in the levels of endogenous ascorbic acid and hydrogen peroxide in Vigna seedlings. Physiol Plant 58:166–170

    Article  CAS  Google Scholar 

  • Mulcahy RT, Gipp JJ (1995) Identification of a putative antioxidant response element in the 5′-flanking region of the human γ-glutamylcysteines synthetase heavy subunit gene. Biochem Biophys Res Commun 209:227–233

    Article  CAS  PubMed  Google Scholar 

  • Mullineaux PM, Rausch T (2005) Glutathione, photosynthesis and the redox regulation of stress-responsive gene expression. Photosynth Res 86:459–474

    Article  CAS  PubMed  Google Scholar 

  • Nahar K, Hasanuzzaman M, Alam MM, Fujita M (2015a) a) Exogenous glutathione confers high temperature stress tolerance in mung bean (Vigna radiata, L.) by modulating antioxidant defense and methylglyoxal detoxification system. Environ Exp Bot 112:44–54

    Article  CAS  Google Scholar 

  • Nahar K, Hasanuzzaman M, Alam MM, Fujita M (2015b) Glutathione-induced drought stress tolerance in mung bean: coordinated roles of the antioxidant defence and methylglyoxal detoxification systems. Aob Plants 7:plv069

    Google Scholar 

  • Ndamukong I, Abdallat AA, Thurow C, Fode B, Zander M, Weigel R, Gatz C (2007) SA-inducible Arabidopsis glutaredoxin interacts with TGA factors and suppresses JA-responsive PDF1.2 transcription. Plant J 50:128–139

    Article  CAS  PubMed  Google Scholar 

  • Noctor G, Gomez L, Vanacker H, Foyer CH (2002) Interactions between biosynthesis, compartmentation and transport in the control of glutathione homeostasis and signalling. J Exp Bot 53:1283–1304

    Article  CAS  PubMed  Google Scholar 

  • Noctor G, Mhamdi A, Chaouch S, Han Y, Neukermans J, Marquez-Garcia B, Queval G, Foyer CH (2012) Glutathione in plants: an integrated overview. Plant Cell Environ 35:454–484

    Article  CAS  PubMed  Google Scholar 

  • Noshi M, Hatanaka R, Tanabe N, Terai Y, Maruta T, Shigeoka S (2016) Redox regulation of ascorbate and glutathione by a chloroplastic dehydroascorbate reductase is required for high-light stress tolerance in Arabidopsis. Biosci Biotechnol Biochem 80:870–877

    Article  CAS  PubMed  Google Scholar 

  • Ogawa K, Hatanoiwasaki A, Yanagida M, Iwabuchi M (2004) 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 45:1–8

    Article  CAS  PubMed  Google Scholar 

  • Ohkama-Ohtsu N, Radwan S, Peterson A, Zhao P, Badr AF, Xiang C, Oliver DJ (2007a) Characterization of the extracellular γ-glutamyl transpeptidases, GGT1 and GGT2, in Arabidopsis. Plant J 49:865–877

    Article  CAS  PubMed  Google Scholar 

  • Ohkama-Ohtsu N, Zhao P, Xiang C, Oliver DJ (2007b) Glutathione conjugates in the vacuole are degraded by γ-glutamyl transpeptidase GGT3 in Arabidopsis. Plant J 49:878–888

    Article  CAS  PubMed  Google Scholar 

  • Ohkama-Ohtsu N, Oikawa A, Zhao P, Xiang C, Saito K, Oliver DJ (2008) A γ-glutamyl transpeptidase-independent pathway of glutathione catabolism to glutamate via 5-oxoproline in Arabidopsis. Plant Physiol 148:1603–1613

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ohkama-Ohtsu N, Sasaki-Sekimoto Y, Oikawa A (2011) 12-oxo-phytodienoic acid-glutathione conjugate is transported into the vacuole in Arabidopsis. Plant Cell Physiol 52:205–209

    Article  CAS  PubMed  Google Scholar 

  • Parisy V, Poinssot B, Owsianowski L, Buchala A, Glazebrook J, Mauch F (2006) Identification of PAD2 as a γ-glutamylcysteine synthetase highlights the importance of glutathione in disease resistance of Arabidopsis. Plant J 49:159–172

    Article  PubMed  CAS  Google Scholar 

  • Parisy V, Poinssot B, Owsianowski L, Buchala A, Glazebrook J, Mauch F (2007) Identification of pad2 as a γ-glutamylcysteine synthetase highlights the importance of glutathione in disease resistance of Arabidopsis. Plant J 49:159–172

    Article  CAS  PubMed  Google Scholar 

  • Pasternak M, Lim B, Wirtz M, Hell R, Cobbett CS, Meyer AJ (2008) Restricting glutathione biosynthesis to the cytosol is sufficient for normal plant development. Plant J 53:999–1012

    Article  CAS  PubMed  Google Scholar 

  • Piasecka A, Jedrzejczakrey N, Bednarek P (2015) Secondary metabolites in plant innate immunity: conserved function of divergent chemicals. New Phytol 206:948–964

    Article  PubMed  Google Scholar 

  • Pinhero RG, Rao MV, Paliyath G, Murr DP, Fletcher RA (1997) Changes in activities of antioxidant enzymes and their relationship to genetic and paclobutrazol-induced chilling tolerance of maize seedlings. Plant Physiol 114:695–704

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Prasad PVV, Djanaguiraman M, Perumal R, Ciampitti IA (2015) Impact of high temperature stress on floret fertility and individual grain weight of grain sorghum: sensitive stages and thresholds for temperature and duration. Front Plant Sci 6:820

    CAS  PubMed  PubMed Central  Google Scholar 

  • Queval G, Thominet D, Vanacker H, Miginiac-Maslow M, Gakière B, Noctor G (2009) H2O2-activated up-regulation of glutathione in Arabidopsis involves induction of genes encoding enzymes involved in cysteine synthesis in the chloroplast. Mol Plant 2:344–356

    Article  CAS  PubMed  Google Scholar 

  • Queval G, Jaillard D, Zechmann B, Noctor G (2011) Increased intracellular H2O2 availability preferentially drives glutathione accumulation in vacuoles and chloroplasts. Plant Cell Environ 34:21–32

    Article  CAS  PubMed  Google Scholar 

  • Rai S, Gupta S, Mittal PC (2015) Dietary intakes and health risk of toxic and essential heavy metals through the food chain in agricultural, industrial, and coal mining areas of northern India. Hum Ecol Risk Assess 21:913–933

    Article  CAS  Google Scholar 

  • Rea PA, Vatamaniuk OK, Rigden DJ (2004) Weeds, worms, and more. Papain’s long-lost cousin, phytochelatin synthase. Plant Physiol 136:2463–2474

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reniere ML, Whiteley AT, Hamilton KL, John SM, Lauer P, Brennan RG, Portnoy DA (2015) Glutathione activates virulence gene expression of an intracellular pathogen. Nature 517:170–173

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Richman PG, Meister A (1975) Regulation of γ-glutamyl-cysteine synthetase by nonallosteric feedback inhibition by glutathione. J Biol Chem 250:1422–1426

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Ruíz-Torres C, Feriche-Linares R, Rodríguez-Ruíz M, Palma JM, Corpas FJ (2017) Arsenic-induced stress activates sulfur metabolism in different organs of garlic (Allium sativum L.) plants accompanied by a general decline of the NADPH-generating systems in roots. J Plant Physiol 211:27–35

    Article  PubMed  CAS  Google Scholar 

  • Sairam RK, Rao KV, Srivastava GC (2002) Differential response of wheat genotypes to long term salinity stress in relation to oxidative stress, antioxidant activity and osmolyte concentration. Plant Sci 163:1037–1046

    Article  CAS  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  • Schlaeppi K, Bodenhausen N, Buchala A, Mauch F, Reymond P (2008) The glutathione-deficient mutant pad2-1 accumulates lower amounts of glucosinolates and is more susceptible to the insect herbivore Spodoptera littoralis. Plant J 55:774–786

    Article  CAS  PubMed  Google Scholar 

  • Schmidt A, Kunert KJ (1986) Lipid peroxidation in higher plants: the role of glutathione reductase. Plant Physiol 82:700–702

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schnaubelt D, Queval G, Dong Y, Diazvivancos P, Makgopa ME, Howell G (2015) Low glutathione regulates gene expression and the redox potentials of the nucleus and cytosol in Arabidopsis thaliana. Plant Cell Environ 38:266–279

    Article  CAS  PubMed  Google Scholar 

  • Schneider S, Bergmann L (2015) Regulation of glutathione synthesis in suspension cultures of parsley and tobacco. Plant Biol 108:34–40

    Google Scholar 

  • Schröder P, Berkau C (1993) Characterization of cytosolic Glutathione S-transferase in spruce needles: part I: GST-isozymes of healthy trees. Bot Acta Plant Biol 106:301–306

    Article  Google Scholar 

  • Sengupta D, Ramesh G, Mudalkar S, Kumar KRR, Kirti PB, Reddy AR (2012) Molecular cloning and characterization of γ-glutamyl cysteine synthetase (vrγECS) from roots of Vigna radiata (L.) wilczek under progressive drought stress and recovery. Plant Mol Biol Rep 30:894–903

    Article  CAS  Google Scholar 

  • Shereefa LAH, Kumaraswamy M (2016) Reactive oxygen species and ascorbate–glutathione interplay in signaling and stress responses in Sesamum orientale L. against Alternaria sesami (Kawamura) mohanty and behera. J Saudi Soc Agrc Sci 15:48–56

    Google Scholar 

  • Shi J, Sun B, Shi W, Zuo H, Cui D, Ni L, Chen J (2015) Decreasing GSH and increasing ROS in chemo sensitivity gliomas with IDH1 mutation. Tumour Biol 36:655–662

    Article  CAS  PubMed  Google Scholar 

  • Shrivastava P, Kumar R (2015) Soil salinity: A serious environmental issue and plant growth promoting bacteria as one of the tools for its alleviation. Saudi J Biol Sci 22:123–131

    Article  CAS  PubMed  Google Scholar 

  • Simon KU, Polanschütz LM, Koffler BE, Zechmann B (2013) High resolution imaging of temporal and spatial changes of subcellular ascorbate, glutathione and H2O2 distribution during Botrytis cinerea infection in Arabidopsis. PLoS ONE 8:e65811

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Simone AD, Dong Y, Díaz-Vivancos P, Foyer CH (2015) GSH partitioning between the nucleus and cytosol in Arabidopsis thaliana. In: De Kok L, Hawkesford M, Rennenberg H, Saito K, Schnug E (eds) Molecular physiology and ecophysiology of sulfur. Springer, Berlin

    Google Scholar 

  • Singh VP, Singh S, Kumar J, Prasad SM (2015) Hydrogen sulfide alleviates toxic effects of arsenate in pea seedlings through up-regulation of the ascorbate-glutathione cycle: possible involvement of nitric oxide. J Plant Physiol 181:20–29

    Article  CAS  PubMed  Google Scholar 

  • Smirnoff N (1993) The role of active oxygen in the response of plants to water deficit and desiccation. New Phytol 125:27–58

    Article  CAS  Google Scholar 

  • Spadaro D, Yun BW, Spoel SH, Chu C, Wang YQ, Loake GJ (2010) The redox switch: dynamic regulation of protein function by cysteine modifications. Physiol Plant 138:360–371

    Article  CAS  PubMed  Google Scholar 

  • Spoel SH, Koornneef A, Claessens SMC (2003) NPR1 modulates cross-talk between salicylate- and jasmonate dependent defense pathways through a novel function in the cytosol. Plant Cell 15:760–770

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Storozhenko S, Belles-Boix E, Babiychuk E, Hérouart D, Davey MR, Slooten L, Van Montagu M, Inzé D, Kushnir S (2002) γ-Glutamyl transpeptidase in transgenic tobacco plants. Cellular localization, processing, and biochemical properties. Plant Physiol 128:1109–1119

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Su T, Xu J, Li Y, Lei L, Zhao L, Yang H, Feng J, Liu G, Ren D (2011) Glutathione-indole-3-acetonitrile is required for camalexin biosynthesis in Arabidopsis thaliana. Plant Cell 23:364–380

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sumption M, Yang Y (2016) Influence of ZnO and Dy2O3 on MgB2 bulks fabricated by high temperature and pressure reaction. APS meeting abstract. Ohio State University, USA

    Google Scholar 

  • Sun J, Zhang Q, Tabassum MA, Ye M, Peng S, Li Y (2017) The inhibition of photosynthesis under water deficit conditions is more severe in flecked than uniform irradiance in rice (Oryza sativa) plants. Funct Plant Biol 44:4

    Google Scholar 

  • Szalai G, Kellős T, Galiba G, Kocsy G (2009) Glutathione as an antioxidant and regulatory molecule in plants under abiotic stress conditions. J Plant Growth Regul 28:66–80

    Article  CAS  Google Scholar 

  • Tausz M, Wonisch A, Peters J, Jimenez MS, Morales D, Grill D (2001) Short-term changes in free-radical scavengers and chloroplast pigments in Pinus canariensis needles as affected by mild drought stress. J Plant Physiol 158:213–219

    Article  CAS  Google Scholar 

  • Tausz M, Šircelj H, Grill D (2004) The glutathione system as a stress marker in plant ecophysiology: is a stress-response concept valid? J Exp Bot 55:1955–1962

    Article  CAS  PubMed  Google Scholar 

  • Tchounwou PB, Yedjou CG, Patlolla AK, Sutton DJ (2012) Molecular, clinical and environmental toxicology. Exp Supp 101:133–164

    Google Scholar 

  • Thangamani S, Eldesouky HE, Mohammad H, Pascuzzi PE, Avramova L, Hazbun TR, Seleem MN (2017) Ebselen exerts antifungal activity by regulating glutathione (GSH) and reactive oxygen species (ROS) production in fungal cells. Biochim Biophy Acta 1861:3002–3010

    Article  CAS  Google Scholar 

  • Tian Q, Wang D, Zhang WL, Duan NB, Qun LI, Yan TJ, Dai S, Ding HF (2016) Effect of artificial aging on soybean seed vigor and ascorbate-glutathione cycle in mitochondria. Plant Physiol J 52:543–550

    Google Scholar 

  • Tolin S, Arrigoni G, Trentin AR, Veljovic-Jovanovic S, Pivato M, Zechmann B (2013) Biochemical and quantitative proteomics investigations in Arabidopsis ggt1 mutant leaves reveal a role for the gamma-glutamyl cycle in plant’s adaptation to environment. Proteomics 13:2031–2045

    Article  CAS  PubMed  Google Scholar 

  • Tsilikochrisos G, Tsaniklidis G, Delis C, Nikoloudakis N, Aivalakis G (2015) Glutamate dehydrogenase is differentially regulated in seeded and parthenocarpic tomato fruits during crop development and postharvest storage. Sci Hortic 181:34–42

    Article  CAS  Google Scholar 

  • Vanacker H, Carver TLW, Foyer CH (1998a) Pathogen-induced changes in the antioxidant status of the apoplast in barley leaves. Plant Physiol 117:1103–1114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vanacker H, Foyer CH, Carver TLW (1998b) Changes in apoplastic antioxidants induced by powdery mildew attack in oat genotypes with race nonspecific resistance. Planta 208:444–452

    Article  Google Scholar 

  • Vanacker H, Harbinson J, Ruisch J, Carver TLW, Foyer CH (1998c) Antioxidant defences of the apoplast. Protoplasma 205:129–140

    Article  CAS  Google Scholar 

  • Vanacker H, Carver TLW, Foyer CH (2000) Early H2O2 accumulation in mesophyll cells leads to induction of glutathione during the hypersensitive response in the barley-powdery mildew interaction. Plant Physiol 123:1289–1300

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vernoux T, Wilson RC, Seeley KA, Reichheld JP, Muroy S, Brown S, Maughan SC, Cobbett CS, Van Montagu M, Inzé D, May MJ, Sung ZR (2000) The root meristemless1/cadmium sensitive 2 gene defines a glutathione-dependent pathway involved in initiation and maintenance of cell division during postembryonic root development. Plant Cell 12:97–110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Voehringer DW, McConkey DJ, McDonnell TJ, Brisbay S, Meyn RE (1998) Bcl-2 expression causes redistribution of glutathione to the nucleus. Proc Natl Acad Sci U S A 95:2956–2960

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wachter A, Wolf S, Steiniger H, Bogs J, Rausch T (2005) Differential targeting of GSH1 and GSH2 is achieved by multiple transcription initiation: implications for the compartmentation of glutathione biosynthesis in the Brassicaceae. Plant J 41:15–30

    Article  CAS  PubMed  Google Scholar 

  • Wang YN, Zhou L, Li YH, Wang Z, Li YC, Zhang YW, Wang Y, Liu G, Shen Y (2015) Protein interacting with C-Kinase 1 deficiency impairs glutathione synthesis and increases oxidative stress via reduction of surface excitatory amino acid carrier 1. J Neurosci 35:6429–6443

    Article  CAS  PubMed  Google Scholar 

  • Wolf AE, Dietz KJ, Schröder P (1996) Degradation of glutathione S-conjugates by a carboxypeptidase in the plant vacuole. FEBS Lett 384:31–34

    Article  CAS  PubMed  Google Scholar 

  • Wu Y, Guo Z, Zhang W, Tan Q, Zhang L, Ge X, Mindong C (2016) Quantitative relationship between cadmium uptake and the kinetics of phytochelatin induction by cadmium in a marine diatom. Sci Rep 6:35935

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yun BW, Skelly MJ, Yin M, Yu M, Mun BG, Lee SU, Hussain A, Spoel SH, Loake GJ (2016) Nitric oxide and S-nitrosoglutathione function additively during plant immunity. New Phytol 211:516–526

    Article  CAS  PubMed  Google Scholar 

  • Zaffagnini M, Bedhomme M, Marchand CH, Morisse S, Trost P, Lemaire SD (2012) Redox regulation in photosynthetic organisms: focus on glutathionylation. Antioxid Redox Signal 16:567–586

    Article  CAS  PubMed  Google Scholar 

  • Zagorchev L, Seal CE, Kranner I, Odjakova M (2013) A central role for thiols in plant tolerance to abiotic stress. Int J Mol Sci 14:7405–7432

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zandalinas SI, Mittler R, Balfagón D, Arbona V, Gómezcadenas A (2018) Plant adaptations to the combination of drought and high temperatures. Physiol Plant 162:2–12

    Google Scholar 

  • Zechmann B (2014) Compartment-specific importance of glutathione during abiotic and biotic stress. Front Plant Sci 5:566

    Article  PubMed  PubMed Central  Google Scholar 

  • Zechmann B, Zellnig G, Müller M (2005) Changes in the subcellular distribution of glutathione during virus infection in Cucurbita pepo (L.). Plant Biol 7:49–57

    Article  CAS  PubMed  Google Scholar 

  • Zechmann B, Zellnig G, Urbanek-Krajnc A, Müller M (2007) Artificial elevation of glutathione affects symptom development in zymv-infected Cucurbita pepo L. plants. Arch Virol 152:747–762

    Article  CAS  PubMed  Google Scholar 

  • Zechmann B, Mauch F, Sticher L, Müller M (2008) Subcellular immunocytochemical analysis detects the highest concentrations of glutathione in mitochondria and not in plastids. J Exp Bot 59:4017–4027

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zelmanov G, Semiat R (2015) The influence of competitive inorganic ions on phosphate removal from water by adsorption on iron (fe+3) oxide/hydroxide nanoparticles-based agglomerates. J Water Proc Eng 5:143–152

    Article  Google Scholar 

  • Zhang MY, Bourbouloux A, Cagnac O, Srikanth CV, Rentsch D, Bachhawat AK, Delrot S (2004) A novel family of transporters mediating the transport of glutathione derivatives inplants. Plant Physiol 134:482–491

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang J, Chen S, Yingli LI, Bao DI, Zhang J, Liu Y (2008) Effect of high temperature and excessive light on glutathione content in apple peel. Front Agric China 2:97–102

    Article  CAS  Google Scholar 

  • Zhang J, Yang S, Huang Y, Zhou S (2015) The tolerance and accumulation of Miscanthus sacchariflorus (maxim.) Benth., an energy plant species, to cadmium. Int J Phytorem 17:538–545

    Article  CAS  Google Scholar 

  • Zhang Z, Lv Z, Wei Z, Li C, Shao Y, Zhang W, Zhao X, Xiong J (2017) Microsomal glutathione transferase 2 modulates LTC4 synthesis and ROS production in Apostichopus japonicus. Mol Immunol 91:114–122

    Article  CAS  PubMed  Google Scholar 

  • Zhao Y, Dan dan MA, Jiang W, Yan SY, Chen MJ (2015) The relative expression of glutathione reductase gene in Volvariella volvacea during low temperature stress. J Biol https://doi.org/10.3969/j.issn.2095-1736.2015.01.044

  • Zhou Y, Liu H, Wang S, Zhang J, Xin B (2016) Effect of exogenous GSH on tomato seedlings growth and physiological indexes of resistance stress under salt stress. Acta Bota Sin 36:515–520

    Google Scholar 

  • Zhu JK (2003) Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol 6:441–445

    Article  CAS  PubMed  Google Scholar 

  • Zhu YL, Pilon-Smits EAH, Tarun AS, Weber SU, Jouanin L, Terry N (1999) Cadmium tolerance and accumulation in Indian mustard is enhanced by overexpressing-glutamylcysteine synthetase. Plant Physiol 121:1169–1177

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zou M, Yuan L, Zhu S, Liu S, Ge J, Wang C (2016) Response of osmotic adjustment and ascorbate-glutathione cycle to heat stress in a heat-sensitive and a heat-tolerant genotype of wucai (Brassica campestris, L.). Sci Hortic 211:87–94

    Article  CAS  Google Scholar 

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Acknowledgements

Authors express their deep gratitude for all the suggestions and comments made by the editors of this book (Gupta D. K., Palma J. M. and Corpas F. J.) regarding the content of this chapter.

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  1. College of Horticulture Science and Engineering, Shandong Agricultural University, Daizong Road No. 61, Tai’an, 271018, Shandong, China

    Biao Gong, Shasha Sun, Yanyan Yan, Xin Jing & Qinghua Shi

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  1. Biao Gong
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  5. Qinghua Shi
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  1. Institut für Radioökologie und Strahlenschutz (IRS), Gottfried Wilhelm Leibniz Universität Hannover, Hannover, Germany

    Dharmendra K. Gupta

  2. Group of Antioxidants, Free Radicals and Nitric Oxide in Biotechnology, Food and Agriculture, Estación Experimental del Zaidín, CSIC, Granada, Spain

    José M. Palma

  3. Group of Antioxidants, Free Radicals and Nitric Oxide in Biotechnology, Food and Agriculture, Estación Experimental del Zaidín, CSIC, Granada, Spain

    Francisco J. Corpas

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Gong, B., Sun, S., Yan, Y., Jing, X., Shi, Q. (2018). Glutathione Metabolism and Its Function in Higher Plants Adapting to Stress. In: Gupta, D., Palma, J., Corpas, F. (eds) Antioxidants and Antioxidant Enzymes in Higher Plants. Springer, Cham. https://doi.org/10.1007/978-3-319-75088-0_9

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