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Exogenous Glutathione-Mediated Abiotic Stress Tolerance in Plants

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Glutathione in Plant Growth, Development, and Stress Tolerance

Abstract

Glutathione (GSH), a major non-protein low-molecular-weight thiol tripeptide in plant cells, is involved in a variety of life processes, including cell differentiation, removal of free radicals and hydroperoxides, thiol-disulfide exchange, and the synthesis of phytochelatin. Along with its oxidized form (GSSG), GSH plays key roles in maintaining cellular redox homeostasiss and signaling, as well as in defense reactions. As a component of ascorbate-glutathione (AsA-GSH) and glyoxalase pathways, GSH is involved in the regulation of hydrogen peroxide and methylglyoxal levels, ensuring their signaling functions, which are necessary for normal growth, development, and stress tolerance. In plants, GSH metabolism also plays important functions in determining the degree of expression of defense-related genes during abiotic and biotic stresses. Plants easily uptake exogenously applied GSH, which is transported into cellular compartments inducing a series of physiological and biochemical processes, including the modulation of abiotic stress tolerance. Recent studies have shown the multiple roles of exogenous GSH in improving abiotic stress tolerance through the regulation of multiple stress responsive pathways; however, the precise molecular mechanisms of exogenous GSH-induced abiotic stress tolerance are largely unknown. This chapter provides an overview to highlight the involvement of exogenous GSH in modulating abiotic stress tolerance. We also highlight the possible mechanisms of uptake and transport of the exogenously applied GSH under stressful conditions.

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References

  • Akram S, Siddiqui MN, Hussain BMN, Bari MAA, Mostofa MG, Hossain MA, Tran LSP (2017) Exogenous glutathione modulates salinity tolerance of soybean [Glycine max (L.) Merrill] at reproductive stage. J Plant Growth Regul 36:877–888

    Google Scholar 

  • Almeselmani M, Deshmukh PS, Sairam RK, Kushwaha SR, Singh TP (2006) Protective role of antioxidant enzymes under high temperature stress. Plant Sci 171:382–388

    Article  CAS  PubMed  Google Scholar 

  • Almeselmani M, Deshmukh PS, Sairam RK (2009) High temperature stress tolerance in wheat genotypes: role of antioxidant defence enzymes. Acta Agron Hung 57:1–14

    Article  CAS  Google Scholar 

  • Anjum NA, Hasanuzzaman M, Hossain MA, Thangavel P, Roychoudhury A, Rodrigo M, Adam V, Fujita M, Kizek R, Duarte A, Pereira E, Ahmad I (2014) Jacks of metal/metalloid chelation trade in plants- an overview. Front Plant Sci 6:192

    Google Scholar 

  • Ao PX, Li ZG, Fan DM, Gong M (2013a) Involvement of antioxidant defense system in chill hardening-induced chilling tolerance in Jatropha curcas seedlings. Acta Physiol Plant 35:153–160

    Article  CAS  Google Scholar 

  • Ao PX, Li ZG, Fan DM, Gong M (2013b) Involvement of compatible solutes in chill hardening-induced chilling tolerance in Jatropha curcas seedlings. Acta Physiol Plant 35:3457–3464

    Article  CAS  Google Scholar 

  • Avery SV (2011) Molecular targets of oxidative stress. Biochem J 434:201–210

    Article  CAS  PubMed  Google Scholar 

  • Baxter A, Mittler R, Suzuki N (2014) ROS as key players in plant stress signaling. J Exp Bot 65:1229–1240

    Article  CAS  PubMed  Google Scholar 

  • Biswas MS, Mano J (2015) Lipid peroxide-derived short-chain carbonyls mediate hydrogen peroxide-induced and salt-induced programmed cell death in plants. Plant Physiol 168:885–898

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blum R, Beck A, Korte 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, Wunschmann J, Lendzian KJ, Grill E (2010) Cytosolic action of phytochelatin synthase. Plant Physiol 153:159–169

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bourbouloux A, Shahi P, Chakladar A, Delrot S, Bachhawat AK (2000) Hgt1p, a high affinity glutathione transporter from the yeast Saccharomyces cerevisiae. J Biol Chem 275:13259–13265

    Article  CAS  PubMed  Google Scholar 

  • Cai Y, Lin L, Cheng W, Zhang G, Wu F (2010) Genotypic dependent effect of exogenous glutathione on Cd-induced changes in cadmium and mineral uptake and accumulation in rice seedlings (Oryza sativa). Plant Soil Environ 56:524–533

    Google Scholar 

  • Cai Y, Cao F, Cheng W, Zhang G, Wu F (2011a) Modulation of exogenous glutathione in phytochelatins and photosynthetic performance against Cd stress in the two rice genotypes differing in Cd tolerance. Biol Trace Elem Res 143:1159–1173

    Article  CAS  PubMed  Google Scholar 

  • Cai Y, Cao F, Wei K, Zhang G, Wu F (2011b) Genotypic dependent effect of exogenous glutathione on Cd-induced changes in proteins, ultrastructure and antioxidant defense enzymes in rice seedlings. J Hazard Mater 192:1056–1066

    Article  CAS  PubMed  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 

  • Cao F, Liu L, Ibrahim W, Cai Y, Wu FB (2013a) Alleviating effects of exogenous glutathione, glycinebetain, brassinosteroids and salicylic acid on cadmium toxicity in rice seedlings (Oryza Sativa). Agrotechnol 2:1

    Google Scholar 

  • Cao F, Wang N, Zhang M, Dai H, Dawood M, Zhang G, Wu F (2013b) Comparative study of alleviating effects of GSH, Se and Zn under combined contamination of cadmium and chromium in rice (Oryza sativa). Biometals 26:297–308

    Article  PubMed  CAS  Google Scholar 

  • Cao F, Chen F, Sun H, Zhang G, Chen ZH, Wu F (2014) Genome-wide transcriptome and functional analysis of two contrasting genotypes reveals key genes for cadmium tolerance in barley. BMC Genomics 15:611

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cao F, Cai Y, Liu L, Zhang M, He X, Zhang G, Wu F (2015) Differences in photosynthesis, yield and grain cadmium accumulation as affected by exogenous cadmium and glutathione in the two rice genotypes. Plant Growth Regul 75:715–723

    Article  CAS  Google Scholar 

  • Cervilla LM, Blasco B, Ríos JJ, Romero L, Ruiz JM (2007) Oxidative stress and antioxidants in tomato (Solanum lycopersicum) plants subjected to boron toxicity. Ann Bot 100:747–756

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chaurasia N, Mishra Y, Chatterjee A, Rai R, Yadav S, Rai LC (2016) Overexpression of phytochelatin synthase (PCS) enhances abiotic stress tolerance by altering the proteome of transformed Anabaena sp. PCC 7120. Protoplasma 254:1715. https://doi.org/10.1007/s00709-016-1059-7

    Article  PubMed  CAS  Google Scholar 

  • Chen Z, Gallie DR (2008) Dehydroascorbate reductase affects nonphotochemical quenching and photosynthetic performance. J Biol Chem 283:21347–21361

    Article  CAS  PubMed  Google Scholar 

  • Chen S, Vaghchhipawala Z, Li W, Asard H, Dickman MB (2004) Tomato phospholipid hydroperoxide glutathione peroxidase inhibits cell death induced by Bax and oxidative stresses in yeast and plants. Plant Physiol 135:1630–1641

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen F, Wang F, Wu F, Mao W, Zhang G, Zhou M (2010) Modulation of exogenous glutathione in antioxidant defense system against Cd stress in the two barley genotypes differing in Cd tolerance. Plant Physiol Biochem 48:663–672

    Article  CAS  PubMed  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

    Google Scholar 

  • Cheng MC, Ko K, Chang WL, Kuo WC, Chen GH, Lin TP (2015) Increased glutathione contributes to stress tolerance and global translational changes in Arabidopsis. Plant J 83:926–939

    Article  CAS  PubMed  Google Scholar 

  • Chia JC, Yang CC, Sui YT, Lin SY, Juang RH (2013) Tentative identification of the second substrate binding site in Arabidopsis phytochelatin synthase. PLoS One 8:e82675

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Choe YH, Kim YS, Kim IS, Bae MJ, Lee EJ, Kim YH, Park HM, Yoon HS (2013) Homologous expression of gamma-glutamylcysteine synthetase increases grain yield and tolerance of transgenic rice plants to environmental stresses. J Plant Physiol 170:610–618

    Article  CAS  PubMed  Google Scholar 

  • Clemens S, Ma JF (2016) Toxic heavy metal and metalloid accumulation in crop plants and foods. Annu Rev Plant Biol 67:489–512

    Article  CAS  PubMed  Google Scholar 

  • Cobbett C, Goldsbrough P (2002) Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Annu Rev Plant Biol 53:159–182

    Article  CAS  PubMed  Google Scholar 

  • Cruz de Carvalho MH (2008) Drought stress and reactive oxygen species: production, scavenging and signaling. Plant Signal Behav 3:156–165

    Article  PubMed  PubMed Central  Google Scholar 

  • Daud MK, Mei L, Azizullah A, Dawood M, Ali I, Mahmood Q, Ullah W, Jamil M, Zhu SJ (2016) Leaf-based physiological, metabolic, and ultrastructural changes in cultivated cotton cultivars under cadmium stress mediated by glutathione. Environ Sci Pollut Res 23:15551–15564

    Article  CAS  Google Scholar 

  • Dazy M, Masfaraud JF, Ferard JF (2009) Induction of oxidative stress biomarkers associated with heavy metal stress in Fontinalis antipyretica Hedw. Chemosphere 75:297–302

    Article  CAS  PubMed  Google Scholar 

  • Del Río LA (2015) ROS and RNS in plant physiology: an overview. J Exp Bot 66:2827–2837

    Article  PubMed  CAS  Google Scholar 

  • Diao Y, Xu H, Li G, Yu A, Yu X, Hu W, Zheng X, Li S, Wang Y, Hu Z (2014) Cloning a glutathione peroxidase gene from Nelumbo nucifera and enhanced salt tolerance by overexpressing in rice. Mol Biol Rep 41:4919–4927

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Diaz-Vivancos P, de Simone A, Kiddle G, Foyer CH (2015) Glutathione-linking cell proliferation to oxidative stress. Free Radic Biol Med 89:1154–1164

    Article  CAS  PubMed  Google Scholar 

  • Ding SH, Lu QT, Zhang Y, Yang ZP, Wen XG, Zhang LX, Lu CM (2009) Enhanced sensitivity to oxidative stress in transgenic tobacco plants with decreased glutathione reductase activity leads to a decrease in ascorbate pool and ascorbate redox state. Plant Mol Biol 69:577–592

    Article  CAS  PubMed  Google Scholar 

  • Ding S, Wang L, Yang Z, Lu Q, Wen X, Lu C (2016a) Decreased glutathione reductase2 leads to early leaf senescence in Arabidopsis. J Inter Plant Biol 58:29–47

    Google Scholar 

  • Ding X, Jiang Y, He L, Zhou Q, Yu J, Hui D, Huang D (2016b) Exogenous glutathione improves high root-zone temperature tolerance by modulating photosynthesis, antioxidant and osmolytes systems in cucumber seedlings. Sci Rep 6:35424

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dixon DP, Edwards R (2010) Glutathione S-transferases. The Arabidopsis Book 8:e0131

    Article  PubMed  PubMed Central  Google Scholar 

  • Edwards EA, Rawsthorne S, Mullineaux PM (1990) Subcellular distribution of multiple forms of glutathione reductase in leaves of pea (Pisum sativum L.) Planta 180:278–284

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • El-Shabrawi H, Kumar B, Kaul T, Reddy MK, Singla-Pareek SL, Sopory SK (2010) Redox homeostasis, antioxidant defense, and methylglyoxal detoxification as markers for salt tolerance in Pokkali rice. Protoplasma 245:85–96

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Fu JY (2014) Cloning of a new glutathione peroxidase gene from tea plant (Camellia sinensis) and expression analysis under biotic and abiotic stresses. Bot Stud 55:7

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gaber A, Ogata T, Maruta T, Yoshimura K, Tamoi M, Shigeoka S (2012) The involvement of Arabidopsis glutathione peroxidase 8 in the suppression of oxidative damage in the nucleus and cytosol. Plant Cell Physiol 53:1596–1606

    Article  CAS  PubMed  Google Scholar 

  • Gallie DR (2013) The role of L-ascorbic acid recycling in responding to environmental stress and in promoting plant growth. J Exp Bot 64:433–443

    Article  CAS  PubMed  Google Scholar 

  • Garg B, Jaiswal JP, Misra S, Tripathi BN, Prasad M (2012) A comprehensive study on dehydration-induced antioxidative responses during germination of Indian bread wheat (Triticum aestivum L. em Thell) cultivars collected from different agroclimatic zones. Physiol Mol Biol Plant 18:217–228

    Article  CAS  Google Scholar 

  • Ghosh A, Kushwaha HR, Hasan MR, Pareek A, Sopory SK, Singla-Pareek SL (2016) Presence of unique glyoxalase III proteins in plants indicates the existence of shorter route for methylglyoxal detoxification. Sci Rep 6:18358

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gietler M, Nykiel M, Zagdańska BM (2016) Changes in the reduction state of ascorbate and glutathione, protein oxidation and hydrolysis leading to the development of dehydration intolerance in Triticum aestivum L. seedlings. Plant Growth Regul 79:287

    Article  CAS  Google Scholar 

  • Gill SS, Anjum NA, Hasanuzzaman M, Gill R, Trivedi DK, Ahmad I, Pereira E, Tuteja N (2013) Glutathione and glutathione reductase: a boon in disguise for plant abiotic stress defense operations. Plant Physiol Biochem 70:204–212

    Article  CAS  PubMed  Google Scholar 

  • Gorantla M, Babu P, Lachagari VBR, Reddy A, Wusirika R, Bennetzen JL, Reddy AR (2007) Identification of stress-responsive genes in an indica rice (Oryza sativa L.) using ESTs generated from drought-stressed seedlings. J Exp Bot 58:253–265

    Article  CAS  PubMed  Google Scholar 

  • Han S, Tang N, Jiang HX, Yang LT, Li Y, Chen LS (2009) CO2 assimilation, photosystem II photochemistry, carbohydrate metabolism and antioxidant system of citrus leaves in response to boron stress. Plant Sci 176:143–153

    Article  CAS  Google Scholar 

  • Hasan MK, Liu C, Wang F, Ahammed GJ, Zhou J, Xu MX, Yu JQ, Xia XJ (2016) Glutathione-mediated regulation of nitric oxide, S-nitrosothiol and redox homeostasis confers cadmium tolerance by inducing transcription factors and stress response genes in tomato. Chemosphere 161:536–545

    Article  CAS  PubMed  Google Scholar 

  • Herbette S, de Labrouhe DT, Drevet JR, Roeckel-Drevet P (2011) Transgenic tomatoes showing higher glutathione peroxydase antioxidant activity are more resistant to an abiotic stress but more susceptible to biotic stresses. Plant Sci 180:548–553

    Article  CAS  PubMed  Google Scholar 

  • Hoque TS, Uraji M, Tuya A, Nakamura Y, Murata Y (2012a) Methylglyoxal inhibits seed germination and root elongation and up-regulates transcription of stress-responsive genes in ABA-dependent pathway in Arabidopsis. Plant Biol 14:854–858

    Article  CAS  PubMed  Google Scholar 

  • Hoque TS, Uraji M, Ye W, Hossain MA, Nakamura Y, Murata Y (2012b) Methylglyoxal-induced stomatal closure accompanied by peroxidase-mediated ROS production in Arabidopsis. J Plant Physiol 169:979–986

    Article  CAS  PubMed  Google Scholar 

  • Hoque TS, Hossain MA, Mostofa MG, Burritt DJ, Fujita M, Tran LSP (2016) Methylglyoxal: an emerging signaling molecule in plant abiotic stress responses and tolerance. Front Plant Sci 7:1341

    Article  PubMed  PubMed Central  Google Scholar 

  • Hossain MA, Fujita M (2009) Purification of glyoxalase I from onion bulbs and molecular cloning of its cDNA. Biosci Biotech Biochem 73:2007–2013

    Article  CAS  Google Scholar 

  • Hossain MA, Hossain MZ, Fujita M (2009) Stress-induced changes of methylglyoxal level and glyoxalase I activity in pumpkin seedlings and cDNA cloning of glyoxalase I gene. Aust J Crop Sci 3(2):53–64

    CAS  Google Scholar 

  • Hossain MA, Hasanuzzaman M, Fujita M (2010) Up-regulation of antioxidant and glyoxalase systems by exogenous glycinebetaine and proline in mung bean confer tolerance to cadmium stress. Physiol Mol Biol Plants 16:259–272

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hossain MA, Teixeira da Silva JA, Fujita M (2011) Glyoxalase system and reactive oxygen species detoxification system in plant abiotic stress response and tolerance: an intimate relationship. In: Shanker A, Venkateswarlu B (eds) Abiotic stress in plants-mechanisms and adaptations. INTECH-Open Access Publisher, Rijeka, pp 235–266

    Google Scholar 

  • Hossain MA, Piyatida P, Teixeira da Silva JA, Fujita M (2012) Molecular mechanism of heavy metal toxicity and tolerance in plants: central role of glutathione in detoxification of reactive oxygen species and methylglyoxal and in heavy metal chelation. J Bot 2012:872875

    Google Scholar 

  • Hossain MA, Mostofa MG, Burritt DJ, Fujita M (2014a) Modulation of reactive oxygen species and methylglyoxal detoxification systems by exogenous glycinebetaine and proline improves drought tolerance in mustard (Brassica juncea L.). Int J Plant Biol Res 2(2):2014

    Google Scholar 

  • Hossain MA, Hoque MA, Burritt DJ, Fujita M (2014b) Proline protects plants against abiotic oxidative stress: biochemical and molecular mechanisms. In: Ahmad P (ed) Oxidative damage to plants. Elsevier, Amsterdam, pp 477–522

    Chapter  Google Scholar 

  • Hossain MA, Bhattacharjee S, Armin SM, Qian P, Xin W, Li H-Y, Burritt DJ, Fujita M, Tran LSP (2015) Hydrogen peroxide-priming modulates abiotic oxidative stress tolerance: insights from ROS detoxification and scavenging. Front Plant Sci 6:420

    PubMed  PubMed Central  Google Scholar 

  • Hung SH, Wang CC, Veselinov SV, Alexieva V, Yu CW (2007) Repetition of hydrogen peroxide treatment induced a chilling tolerance comparable to cold acclimation in mung bean. J Amer Soc Hort Sci 132:770–776

    CAS  Google Scholar 

  • Hussain BMN, Akram S, Raffi SA, Burritt DJ, Hossain MA (2016) Exogenous glutathione improves salinity stress tolerance in rice (Oryza sativa L.). Plant Gene Trait 7:1–17

    Google Scholar 

  • Iannelli MA, Pietrini F, Fiore L, Petrilli L, Massacci A (2002) Antioxidant response to cadmium in Phragmites australis plants. Plant Physiol Bioch 40:977–982

    Article  CAS  Google Scholar 

  • Ibrahim W, Ahmed IM, Chen X, Wu F (2017) Genotype-dependent alleviation effects of exogenous GSH on salinity stress in cotton is related to improvement in chlorophyll content, photosynthetic performance, and leaf/root ultrastructure. Environ Sci Pollut Res 24:9417–9427

    Article  CAS  Google Scholar 

  • Jamai A, Tommasini R, Martinoia E, Delrot S (1996) Characterization of glutathione uptake in broad bean leaf protoplast. Plant Physiol 111:1145–1152

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kataya ARA, Reumann S (2010) Arabidopsis glutathione reductase 1 is dually targeted to peroxisomes and the cytosol. Plant Signal Behav 5:171–175

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaur G, Kumar S, Nayyar H, Upadhyaya HD (2008) Cold stress injury during the pod-filling phase in chickpea (Cicer arietinum L.). Effects on quantitative and qualitative components of seeds. J Agron Crop Sci 194:457–464

    Google Scholar 

  • Kaur C, Ghosh A, Pareek A, Sopory SK, Singla-Pareek SL (2014) Glyoxalases and stress tolerance in plants. Biochem Soc Trans 42:485–490

    Article  CAS  PubMed  Google Scholar 

  • Kim YS, Kim IS, Shin SY, Park TH, Park HM, Kim YH, Lee GS, Kang HG, Lee SH, Yoon HS (2014) Overexpression of dehydroascorbate reductase confers enhanced tolerance to salt stress in rice plants (Oryza sativa L. Japonica). J Agron Crop Sci 200:444–456

    Article  CAS  Google Scholar 

  • Kocsy G, Galiba G, Brunold C (2001) Role of glutathione in adaptation and signalling during chilling and cold acclimation in plants. Physiol Plant 113:158–164

    Article  CAS  PubMed  Google Scholar 

  • Kumar B, Singla-Pareek SL, Sopory SK (2010) Glutathione homeostasis: crucial for abiotic stress tolerance in plants. In: Pareek A, Sopory SK, Bohnert HJ (eds) Abiotic stress adaptation in plants. Springer, Dordrecht, pp 263–282

    Google Scholar 

  • Kumar S, Asif MH, Chakrabarty D, Tripathi RD, Dubey RS, Trivedi PK (2013) Expression of a rice Lambda class of glutathione S-transferase, OsGSTL2, in Arabidopsis provides tolerance to heavy metal and other abiotic stresses. J Hazard Mater 248–249:228–237

    Google Scholar 

  • Lee BD, Hwang S (2015) Tobacco phytochelatin synthase (NtPCS1) plays important roles in cadmium and arsenic tolerance and in early plant development in tobacco. Plant Biotechnol Rep 9:107–114

    Article  Google Scholar 

  • Li ZG, Yuan LX, Wang QL, Ding ZL, Dong CY (2013) Combined action of antioxidant defense system and osmolytes in chilling shock-induced chilling tolerance in Jatropha curcas seedlings. Acta Physiol Plant 35:2127–2136

    Article  CAS  Google Scholar 

  • Li ZG, Duan XQ, Min X, Zhou ZH (2017) Methylglyoxal as a novel signal molecule induces the salt tolerance of wheat by regulating the glyoxalase system, the antioxidant system, and osmolytes. Protoplasma. https://doi.org/10.1007/s00709-017-1094-z

  • Liedschulte V, Wachter A, Zhigang A, Rausch T (2010) Exploiting plants for glutathione (GSH) production: uncoupling GSH synthesis from cellular controls results in unprecedented GSH accumulation. J Plant Biotechnol 8:807–820

    Article  CAS  Google Scholar 

  • Lo Cicero L, Madesis P, Tsaftaris A, Lo Piero AR (2015) Tobacco plants over-expressing the sweet orange tau glutathione transferases (CsGSTUs) acquire tolerance to the diphenyl ether herbicide fluorodifen and to salt and drought stresses. Phytochemistry 116:69–77

    Article  CAS  PubMed  Google Scholar 

  • Locato V, de Pinto MC, De Gara L (2009) Different involvement of the mitochondiral, plastidal and cytosolic ascorbate-glutathione redox enzymes in heat shock responses. Phyiol Plant 135:296–306

    Article  CAS  Google Scholar 

  • Lukatkin AS, Anjum NA (2014) Control of cucumber (Cucumis sativus L.) tolerance to chilling stress-evaluating the role of ascorbic acid and glutathione. Front Environ Sci 2:62

    Article  Google Scholar 

  • Marquez-Garcia B, Njo M, Beeckman T, Goormachtig S, Foyer CH (2014) A new role for glutathione in the regulation of root architecture linked to strigolactones. Plant Cell Environ 37:488–498

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Maughan SC, Pasternak M, Cairns N, Kiddle G, Brach T et al (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 

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

    Google Scholar 

  • Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33:453–467

    Article  CAS  PubMed  Google Scholar 

  • Mittova V, Tal M, Volokita M, Guy M (2003a) Up-regulation of the leaf mitochondrial and peroxisomal antioxidative systems in response to salt-induced oxidative stress in the wild salt-tolerant tomato species Lycopersicon pennellii. Plant Cell Environ 26:845–856

    Article  CAS  PubMed  Google Scholar 

  • Mittova V, Theodoulou FL, Kiddle G, Gomez L, Volokita M, Tal M, Foyer CH, Guy M (2003b) 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 

  • Mostofa MG, Seraj ZI, Fujita M (2014a) Exogenous sodium nitroprusside and glutathione alleviate copper toxicity by reducing copper uptake and oxidative damage in rice (Oryza sativa L.) seedlings. Protoplasma 251:1373–1386

    Article  CAS  PubMed  Google Scholar 

  • Mostofa MG, Yoshida N, Fujita M (2014b) Spermidine pretreatment enhances heat tolerance in rice seedlings through modulating antioxidative and glyoxalase systems. Plant Growth Regul 73:31–44

    Article  CAS  Google Scholar 

  • Mostofa MG, Hossain MA, Fujita M (2015a) Trehalose pretreatment induces salt tolerance in rice (Oryza sativa L.) seedlings: oxidative damage and co-induction of antioxidant defense and glyoxalase systems. Protoplasma 252:461–475

    Article  CAS  PubMed  Google Scholar 

  • Mostofa MG, Hossain MA, Fujita M, Tran LS (2015b) Physiological and biochemical mechanisms associated with trehalose-induced copper-stress tolerance in rice. Sci Rep 5:11433

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Müller M, Zechmann B, Zellnig G (2004) Ultrastructural localization of glutathione in Cucurbita pepo plants. Protoplasma 223:213–219

    Article  PubMed  CAS  Google Scholar 

  • Munné-Bosch S, Queval G, Foyer CH (2013) The impact of global change factors on redox signaling underpinning stress tolerance. Plant Physiol 161:5–19

    Article  PubMed  CAS  Google Scholar 

  • Nahar K, Hasanuzzaman M, Alam MM, Fujita M (2015a) Roles of exogenous glutathione in antioxidant defense system and methylglyoxal detoxification during salt stress in mung bean. Biol Plant 59:745–756

    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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nahar K, Hasanuzzaman M, Alam MM, Fujita M (2015c) 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 

  • Navrot N, Collin V, Gualberto J, Gelhaye E, Hirasawa M, Rey P, Knaff DB, Issakidis E, Jacquot JP, Rouhier N (2006) Plant glutathione peroxidases are functional peroxiredoxins distributed in several subcellular compartments and regulated during biotic and abiotic stresses. Plant Physiol 142:1364–1379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Noctor G, Veljovic-Jovanovic S, Foyer CH (2000) Peroxide processing in photosynthesis: antioxidant coupling and redox signalling. Philos Trans R Soc Lond Ser B Biol Sci 355:1465–1475

    Article  CAS  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 

  • 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 

  • Pilon-Smits E (2005) Phytoremediation. Annu Rev Plant Biol 56:15–39

    Article  CAS  PubMed  Google Scholar 

  • Pomponi M, Censi V, Di Girolamo V, De Paolis A, di Toppi LS, Aromolo R, Costantino P, Cardarelli M (2006) Overexpression of Arabidopsis phytochelatin synthase in tobacco plants enhances Cd2+ tolerance and accumulation but not translocation to the shoot. Planta 223:180–190

    Article  CAS  PubMed  Google Scholar 

  • Qiu B, Zeng F, Cai S, Wu X, Haider SI, Wu F, Zhang G (2013) Alleviation of chromium toxicity in rice seedlings by applying exogenous glutathione. J Plant Physiol 170:772–779

    Article  CAS  PubMed  Google Scholar 

  • Ramírez L, Bartoli CG, Lamattina L (2013) Glutathione and ascorbic acid protect Arabidopsis plants against detrimental effects of iron deficiency. J Exp Bot 64:3169–3178

    Article  PubMed  CAS  Google Scholar 

  • Rapala-Kozik M, Kowalska E, Ostrowska K (2008) Modulation of thiamine metabolism in Zea mays seedlings under conditions of abiotic stress. J Exp Bot 59:4133–4143

    Article  CAS  PubMed  Google Scholar 

  • Ren J, Sun LN, Zhang QY, Song XS (2016) Drought tolerance is correlated with the activity of antioxidant enzymes in Cerasus humilis seedlings. Biomed Res Int 2016:9851095

    PubMed  PubMed Central  Google Scholar 

  • Ruiz JM, Rivero RM, Romero L (2003) Preliminary studies on the involvement of biosynthesis of cysteine and glutathione in the resistance to boron toxicity in sunflower plants. Plant Sci 165:811–817

    Article  CAS  Google Scholar 

  • Saito R, Yamamoto H, Makino A, Sugimoto T, Miyake C (2011) Methylglyoxal functions as Hill oxidant and stimulates the photoreduction of O2 at photosystem I: a symptom of plant diabetes. Plant Cell Environ 34:1454–1464

    Article  CAS  PubMed  Google Scholar 

  • Schnaubelt D, Schulz P, Hannah MA, Yocgo RE, Foyer CH (2013) A phenomics approach to the analysis of the influence of glutathione on leaf area and abiotic stress tolerance in Arabidopsis thaliana. Front Plant Sci 4:416

    Article  PubMed  PubMed Central  Google Scholar 

  • Schneider A, Schatten T, Rennenberg H (1994) Exchange between phloem and xylem during long distance transport of glutathione in spruce trees (Picea abies[Karst.] L). J Exp Bot 45:457–462

    Article  CAS  Google Scholar 

  • Selote DS, Khanna-Chopra R (2004) Drought-induced spikelet sterility is associated with an inefficient antioxidant defence in rice panicles. Physiol Plant 121:462–471

    Article  CAS  Google Scholar 

  • Shanmugam V, Wang YW, Tsednee M, Karunakaran K, Yeh KC (2015) Glutathione plays an essential ro in nitric oxide-mediated iron-deficiency signaling and iron-deficiency tolerance in Arabidopsis. Plant J 84:464–477

    Article  CAS  PubMed  Google Scholar 

  • Singla-Pareek SL, Yadav SK, Pareek A, Reddy MK, Sopory SK (2006) Transgenic tobacco overexpressing glyoxalase pathway enzymes grow and set viable seeds in zinc-spiked soils. Plant Physiol 140:613–623

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Son JA, Narayanankutty DP, Roh KS (2014) Influence of exogenous application of glutathione on rubisco and rubisco activase in heavy metal-stressed tobacco plant grown in vitro. Saudi J Biol Sci 21:89–97

    Article  CAS  PubMed  Google Scholar 

  • Soranzo N, Sari Gorla M, Mizzi L, De Toma G, Frova C (2004) Organisation and structural evolution of the rice glutathione S-transferase gene family. Mol Gen Genomics 271:511–521

    Article  CAS  Google Scholar 

  • Srivalli S, Khanna-Chopra R (2008) Role of glutathione in abiotic stress tolerance. In: Khan NA, Singh S, Umar S (eds) Sulfur assimilation and abiotic stress in plants. Springer, Berlin/Heidelberg, pp 207–225

    Chapter  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, Sircelj 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 

  • Turan Ö, Ekmekçi Y (2011) Activities of photosystem II and antioxidant enzymes in chickpea (Cicer arietinum L.) cultivars exposed to chilling temperatures. Acta Physiol Plant 33:67–78

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Wang F, Chen F, Cai Y, Zhang G, Wu F (2011) Modulation of exogenous glutathione in ultrastructure and photosynthetic performance against Cd stress in the two barley genotypes differing in Cd tolerance. Biol Trace Elem Res 144:1275–1288

    Article  CAS  PubMed  Google Scholar 

  • Wang R, Liu S, Zhou F, Hua C (2014a) Exogenous ascorbic acid and glutathione alleviate oxidative stress induced by salt stress in the chloroplasts of Oryza sativa L. Z Naturforsch C 69:226–236

    CAS  PubMed  Google Scholar 

  • Wang X, Cai J, Liu FL, Dai TB, Cao WX, Wollenweber B, Jiang D (2014b) Multiple heat priming enhances thermo-tolerance to a later high temperature stress via improving subcellular antioxidant activities in wheat seedlings. Plant Physiol Biochem 74:185–192

    Article  CAS  PubMed  Google Scholar 

  • Xu S, Li J, Zhang X, Wei H, Cui L (2006) Effects of heat acclimation pretreatment on changes of membrane lipid peroxidation, antioxidant metabolites, and ultrastructure of chloroplasts in two cool-season turfgrass species under heat stress. Environ Exp Bot 56:274–285

    Article  CAS  Google Scholar 

  • Yadav SK, Singla-Pareek SL, Ray M, Reddy MK, Sopory SK (2005a) Methylglyoxal levels in plants under salinity stress are dependent on glyoxalase I and glutathione. Biochem Biophys Res Commun 337:61–67

    Article  CAS  PubMed  Google Scholar 

  • Yadav SK, Singla-Pareek SL, Ray M, Reddy MK, Sopory SK (2005b) Transgenic tobacco plants overexpressing glyoxalase enzymes resist an increase in methylglyoxal and maintain higher reduced glutathione levels under salinity stress. FEBS Lett 579:6265–6271

    Article  CAS  PubMed  Google Scholar 

  • Yamaguchi T, Blumwald E (2005) Developing salt-tolerant crop plants: challenges and opportunities. Trends Plant Sci 10:615–620

    Article  CAS  PubMed  Google Scholar 

  • Yazici I, Türkan I, Sekmen AH, Demiral T (2007) Salinity tolerance of purslane (Portulaca oleracea L.) is achieved by enhanced antioxidative system, lower level of lipid peroxidation and proline accumulation. Environ Exp Bot 61:49–57

    Article  CAS  Google Scholar 

  • Yin L, Mano J, Tanaka K, Wang S, Zhang M, Deng X, Zhang S (2017) High level of reduced glutathione contributes to detoxification of lipid peroxide-derived reactive carbonyl species in transgenic Arabidopsis overexpressing glutathione reductase under aluminum stress. Physiol Plant DOI. https://doi.org/10.1111/ppl.12583

  • Yu CW, Murphy TM, Sung WW, Lin CH (2002) H2O2 treatment induces glutathione accumulation and chilling tolerance in mung bean. Funct Plant Biol 29:1081–1087

    Article  CAS  Google Scholar 

  • Yu CW, Murphy TM, Lin CH (2003) Hydrogen peroxide-induced chilling tolerance in mung beans mediated through ABA-independent glutathione accumulation. Funct Plant Biol 30:955–963

    Article  CAS  Google Scholar 

  • Zechmann B, Koffler BE, Russell SD (2011) Glutathione synthesis is essential for pollen germination in vitro. BMC Plant Biol 11:54

    Article  CAS  PubMed  PubMed Central  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 in plants. Plant Physiol 134:482–491

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou Q, Guo JJ, He CT, Shen C, Huang YY, Chen JX, Guo JH, Yuan JG, Yang ZY (2016) Comparative transcriptome analysis between low- and high-cadmium-accumulating genotypes of pakchoi (Brassica chinensis L.) in response to cadmium stress. Environ Sci Technol 50:6485–6494

    Article  CAS  PubMed  Google Scholar 

  • Zhou Y, Wen Z, Zhang J, Chen X, Cui J, Xub W, Liu HY (2017) Exogenous glutathione alleviates salt-induced oxidative stress intomato seedlings by regulating glutathione metabolism, redox status, and the antioxidant system. Sci Hort 220:90–101

    Article  CAS  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 γ-glutamylcysteine synthetase. Plant Physiol 121:1169–1177

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (31501233) and the China Postdoctoral Science Foundation funded project (2015M570513, 2016T90542). PDV thanks CSIC and the Spanish Ministry of Economy and Competitiveness for his ‘Ramon & Cajal’ research contract, co-financed by FEDER funds. The last author thankfully acknowledges the postdoctural fellowship from the Japan Society for the Promotion of Science (JSPS).

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Correspondence to Fangbin Cao or Mohammad Anwar Hossain .

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Cao, F., Fu, M., Wang, R., Diaz-Vivancos, P., Hossain, M.A. (2017). Exogenous Glutathione-Mediated Abiotic Stress Tolerance in Plants. In: Hossain, M., Mostofa, M., Diaz-Vivancos, P., Burritt, D., Fujita, M., Tran, LS. (eds) Glutathione in Plant Growth, Development, and Stress Tolerance. Springer, Cham. https://doi.org/10.1007/978-3-319-66682-2_8

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