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The Regulatory and Signaling Roles of Glutathione in Modulating Abiotic Stress Responses and Tolerance

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Book cover Glutathione in Plant Growth, Development, and Stress Tolerance

Abstract

Glutathione (GSH) plays a key role in the maintenance of tissue antioxidant defence and in the regulation of redox-sensitive signal transduction. The size of the GSH pool and its redox status are strongly correlated with the tolerance of plants. The effect of GSH on plant stress resistance is achieved mainly through the cycle of ascorbate (AsA)-GSH producing dehydroascorbate (DHA) re-reduction, in which GSH is intermediate in the recycling of H2O2 reduction and the recycling of GSH is regulated by the glutathione reductase (GR) enzyme. Under oxidative stress, H2O2 and reactive oxygen species (ROS) can be reduced by GSH, while GSH is oxidized to oxidized glutathione (GSSG). Under normal physiological conditions, GSSG can be reduced to GSH by GR in the presence and with the involvement of NADPH, thus creating the redox cycle. AsA/DHA, GSH/GSSG, NADPH/NADP are the three most important interconnected and coordinated redox pairs in plant cells, and plants can scavenge ROS and strengthen their resistance to abiotic stresses by modulating the status of redox pairs; thus the redox metabolism pathways are initiated by diverse environmental stresses. In addition, GSH can regulate the ROS signal transduction pathway, and ROS levels depend on the redox status of redox pairs in plant cells. GSH can activate the genes involved in phytoalexin biosynthesis to repress the accumulation of plant toxin. H2O2 can strengthen this effect through the up-regulation of GSSG. When H2O2 reaches a higher level, the biosynthesis of GSH is stimulated, while GSH, on the other hand, can mediate the response of the plant to the H2O2 signal.

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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. https://doi.org/10.1007/s00344-017-9691-9

  • Alhdad GM, Seal CE, Al-Azzawi MJ, Flowers TJ (2013) The effect of combined salinity and waterlogging on the halophyte Suaeda maritima: the role of antioxidants. Environ Exp Bot 87:120–125

    Article  CAS  Google Scholar 

  • Bashandy T, Guilleminot J, Vernoux T, Caparros-Ruiz D, Ljung K, Meyer Y, Reichheld JP (2010) Interplay between the NADP-linked thioredoxin and glutathione systems in Arabidopsis auxin signaling. Plant Cell 22:376–391

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Becana M, Matamoros MA, Udvardi M, Dalton DA (2010) Recent insights into antioxidant defenses of legume root nodules. New Phytol 188:960–976

    Article  CAS  PubMed  Google Scholar 

  • Borsani O, Valpuesta V, Botella MA (2001) Evidence for a role of salicylic acid in the oxidative damage generated by NaCl and osmotic stress in Arabidopsis seedlings. Plant Physiol 126:1024–1030

    Article  CAS  PubMed Central  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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chi Y, Cheng Y, Vanitha J, Kumar N, Ramamoorthy R, Ramachandran S, Jiang SY (2011) Expansion mechanisms and functional divergence of the glutathione S-transferase family in sorghum and other higher plants. DNA Res 18:1–16

    Article  CAS  PubMed  Google Scholar 

  • Clark D, Durner J, Navarre DA, Klessig DF (2000) Nitric oxide inhibition of tobacco catalase and ascorbate peroxidase. Mol Plant-Microbe Interact 13:1350–1384

    Article  Google Scholar 

  • Clemente MR, Bustos-Sanmamed P, Loscos J, James EK, Pérez-Rontomé C, Navascués J, Gay M, Becana M (2012) Thiol synthetases of legumes: Immunogold localization and differential gene regulation by phytohormones. J Exp Bot 63:3923–3934

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Copley SD, Dhillon JK (2002) Lateral gene transfer and parallel evolution in the history of glutathione biosynthesis genes. Genome Biol 3:Research 0025. 1

    Article  Google Scholar 

  • Cruz de Carvalho MH, Brunet J, Bazin J, Kranner I, d’ Arcy-Lameta A, Zuily-Fodil Y, Contour-Ansel D (2010) Homoglutathione synthetase and glutathione synthetase in drought-stressed cowpea leaves: expression patterns and accumulation of low-molecular-weight thiols. J Plant Physiol 167:480–487

    Article  CAS  PubMed  Google Scholar 

  • De Pinto MC, Paradiso A, Leonetti P, De Gara L (2006) Hydrogen peroxide, nitric oxide and cytosolic ascorbate peroxidase at the crossroad between defence and cell death. Plant J 48:784–795

    Article  PubMed  CAS  Google Scholar 

  • Dhankher OP, Li Y, Rosen BP, Shi J, Salt D, Senecoff JF, Sashti NA, Meagher RB (2002) Engineering tolerance and hyperaccumulation of arsenic in plants by combining arsenate reductase and gamma-glutamylcysteine synthetase expression. Nat Biotechnol 20:1140–1145

    Article  CAS  PubMed  Google Scholar 

  • Diaz Vivancos P, Driscoll SP, Bulman CA, Ying L, Emami K, Treumann A, Mauve C, Noctor G, Foyer CF (2011) Perturbations of amino acid metabolism associated with glyphosate-dependent inhibition of shikimic acid metabolism affect cellular redox homeostasis and alter the abundance of proteins involved in photosynthesis and photorespiration. Plant Physiol 157:256–268

    Article  CAS  Google Scholar 

  • Dietz KJ (2008) Redox signal integration: from stimulus to networks and genes. Physiol Plant 133:459–468

    Article  CAS  PubMed  Google Scholar 

  • Ding S, Lu Q, Zhang Y, Wen X, Zhang L, Lu C (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 Molr Biol 69:577–592

    Article  CAS  Google Scholar 

  • Dixon DP, Lapthorn A, Edwards R (2002) Plant glutathione transferases. Genome Biol 3:Reviews3004. 1

    Article  Google Scholar 

  • El Msehli S, Lambert A, Baldacci-Cresp F, Hopkins J, Boncompagni E, Smiti SA, Hérouart D, Frendo P (2011) Crucial role of (homo)glutathione in nitrogen fixation in Medicago truncatula nodules. New Phytol 192:496–506

    Article  PubMed  CAS  Google Scholar 

  • Eltelib HA, Badejo AA, Fujikawa Y, Esaka M (2011) Gene expression of monodehydroascorbate reductase and dehydroascorbate reductase during fruit ripening and in response to environmental stresses in acerola (Malpighia glabra). J Plant Physiol 168:619–627

    Article  CAS  PubMed  Google Scholar 

  • Estrella-Gómez NE, Sauri-Duch E, Zapata-Pérez O, Santamaría JM (2012) Glutathione plays a role in protecting leaves of Salvinia minima from Pb2+ damage associated with changes in the expression of SmGS genes and increased activity of GS. Environ Exp Bot 75:188–194

    Article  CAS  Google Scholar 

  • Foyer CH, Noctor G (2005) Redox homeostasis and antioxidant signaling: a metabolic link between stress perception and physiological responses. Plant Cell 17:1866–1875

    Article  CAS  PubMed Central  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 Central  PubMed  Google Scholar 

  • Foyer CH, Lopez-Delgado H, Dat JF, Scott IM (1997) Hydrogen peroxide and glutathione-associated mechanisms of acclamatory stress tolerance and signaling. Physiol Plant 100:241–254

    Article  CAS  Google Scholar 

  • Fraser JA, Saunders RDC, McLellan LI (2002) Drosophila melanogaster glutamate-cysteine ligase activity is regulated by a modifier subunit with a mechanism of action similar to that of the mammalian form. J Biol Chem 277:1158–1165

    Article  CAS  PubMed  Google Scholar 

  • Frendo P, Jiménez MJ, Mathieu C, Duret L, Gallesi D, Van de Sype G, Hérouart D, Puppo A (2001) A Medicago truncatula homoglutathione synthetase is derived from glutathione synthetase by gene duplication. Plant Physiol 126:706–715

    Article  Google Scholar 

  • Gadjev I, Vanderauwera S, Gechev TS, Laloi C, Minkov IN, Shulaev V, Apel K, Inze D, Mittler R, van Breusegem F (2006) Transcriptomic footprints disclose specificity of reactive oxygen species signaling in Arabidopsis. Plant Physiol 141:436–445

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Galant A, Preuss ML, Cameron JC, Jez JM (2011) Plant glutathione biosynthesis: diversity in biochemical regulation and reaction products. Front Plant Sci 2:45

    Article  PubMed Central  PubMed  Google Scholar 

  • Ganesan V, Thomas G (2001) Salicylic acid response in rice: influence of salicylic acid on H2O2 accumulation and oxidative stress. Plant Sci 160:1095–1106

    Article  CAS  PubMed  Google Scholar 

  • George S, Venkataraman G, Parida A (2010) A chloroplast-localized and auxin-induced glutathione S-transferase from phreatophyte Prosopis juliflora confer drought tolerance on tobacco. J Plant Physiol 167:311–318

    Article  CAS  PubMed  Google Scholar 

  • Ghisla S, Massey V (1989) Mechanisms of flavoprotein-catalyzed reactions. Eur J Biochem 181:1–17

    Article  CAS  PubMed  Google Scholar 

  • Gill SS, Khan NA, Tuteja N (2012) Cadmium at high dose perturbs growth, photosynthesis and nitrogen metabolism while at low dose it up regulates sulfur assimilation and antioxidant machinery in garden cress (Lepidium sativum L.) Plant Sci 182:112–120

    Article  CAS  PubMed  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 Bioch 70:204–212

    Article  CAS  Google Scholar 

  • Gogos A, Shapiro L (2002) Large conformational changes in the catalytic cycle of glutathione synthase. Structure 10:1669–1676

    Article  CAS  PubMed  Google Scholar 

  • Goiris K, Van Colen W, Wilches I, León-Tamariz F, Cooman LD, Muylaert K (2015) Impact of nutrient stress on antioxidant production in three species of microalgae. Algal Res 7:51–57

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Gromes R, Hothorn M, Lenherr ED, Rybin V, Scheffzek K, Rausch T (2008) The redox switch of gamma-glutamylcysteine ligase via a reversible monomer-dimer transition is a mechanism unique to plants. Plant J 54:1063–1075

    Article  CAS  PubMed  Google Scholar 

  • Hasanuzzaman M, Hossain MA, Fujita M (2010) Physiological and biochemical mechanisms of nitric oxide induced abiotic stress tolerance in plants. Am J Plant Physiol 5:295–324

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Hibi T, Nii H, Nakatsu T, Kimura A, Kato H, Hiratake J, Oda J (2004) Crystal structure of g-gluta-mylcysteine synthetase: insights into the mechanism of catalysis by a key enzyme for glutathione homeosta-sis. Proc Natl Acad Sci U S A 101:15052–15057

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hothorn M, Wachter A, Gromes R, Stuwe T, Rausch T, Scheffzek K (2006) Structural basis for the redox control of plant glutamate cysteine ligase. J Biol Chem 281:27557–27565

    Article  CAS  PubMed  Google Scholar 

  • Innocenti G, Pucciariello C, Le Gleuher M, Hopkins J, Stefano M, Delledonne M, Puppo A, Baudouin E, Frendo P (2007) Glutathione synthesis is regulated by nitric oxide in Medicago truncatula roots. Planta 225:1597–1602

    Article  CAS  PubMed  Google Scholar 

  • Janda T, Szalai G, Tari I, Paldi E (1999) Hydroponic treatment with salicylic acid decreases the effects of chilling injury in maize (Zea mays L.) plants. Planta 208:175–180

    Article  CAS  Google Scholar 

  • Jez JM, Cahoon RE (2004) Kinetic mechanism of glutathione synthetase from Arabidopsis thaliana. J Biol Chem 279:42726–42731

    Article  CAS  PubMed  Google Scholar 

  • Jez JM, Cahoon RE, Chen SX (2004) Arabidopsis thaliana glutamate-cysteine ligase: functional properties, kinetic mechanism, and regulation of activity. J Biol Chem 279:33463–33470

    Article  CAS  PubMed  Google Scholar 

  • Jiang M, Zhang J (2003) Cross-talk between calcium and reactive oxygen species originated from NADPH oxidase in abscisic acid-induced antioxidant defence in leaves of maize seedlings. Plant Cell Environ 26:929–939

    Article  CAS  PubMed  Google Scholar 

  • Jiang YP, Huang LF, Cheng F, Zhou YH, Xia XJ, Mao WH, Shi K, Yu JQ (2013) Brassinosteroids accelerate recovery of photosynthetic apparatus from cold stress by balancing the electron partitioning, carboxylation and redox homeostasis in cucumber. Physiol Plant 148:133–145

    Article  CAS  PubMed  Google Scholar 

  • Kabir MH, Wang MH (2010) Expression pattern of two dehydroascorbate reductase genes from tomato (Solanum lycopersicum L.) in response to stress. J Korean Soc Appl Biol Chem 53:668–676

    Article  CAS  Google Scholar 

  • Kabir MH, Han W, Wang MH (2011) Environmental stress response of a dehydroascorbate reductase gene from tomato, and its protective role in Escherichia coli. Hort Environ Biotech 52:621–628

    Article  CAS  Google Scholar 

  • Kavitha K, George S, Venkataraman G, Parida A (2010) A salt-inducible chloroplastic monodehydroascorbate reductase from halophyte Avicennia marina confers salt stress tolerance on transgenic plants. Biochimie 92:1321–1329

    Article  CAS  PubMed  Google Scholar 

  • Kellos T, Tımar I, Szilagyi V, Szalai G, Galiba G, Kocsy G (2008) Stress hormones and abiotic stresses have different effects on antioxidants in maize lines with different sensitivity. Plant Biol 10:563–572

    Article  CAS  PubMed  Google Scholar 

  • Keunen E, Remans T, Bohler S, Vangronsveld J, Cuypers A (2011) Metal-induced oxidative stress and plant mitochondria. Int J Mol Sci 12:6894–6918

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Klapheck S, Latus C, Bergmann L (1987) Localization of glutathione synthetase and distribution of glutathione in leaf cells of Pisum sativum L. J Plant Physiol 131:123–131

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Klapheck S, Schlunz S, Bergmann L (1995) Synthesis of phytochelatins and homo-phytochelatins in Pisum Sativum L. Plant Physiol 107:515–521

    Google Scholar 

  • Knörzer OC, Lederer B, Durner J, Boger P (1999) Antioxidative defense activation in soybean cells. Physiol Plant 107:294–302

    Article  Google Scholar 

  • Kolbe A, Oliver SN, Fernie AR, Stitt M, van Dongen JT, Geigenberger P (2006) Combined transcript and metabolite profiling of Arabidopsis leaves reveals fundamental effects of the thioldisulphide status on plant metabolism. Plant Physiol 141:412–422

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kumar S, Asif MH, Chakrabarty D, Tripathi RD, Dubey RS, Trivedi PK (2013) Differential expression of rice lambda class GST gene family members during plant growth, development, and in response to stress conditions. Plant Mol Biol Rep 31:569–580

    Article  CAS  Google Scholar 

  • Kusumi K, Yaeno T, Kojo K, Hirayama M, Hirokawa D, Yara A, Iba K (2006) The role of salicylic acid in the glutathione-mediated protection against photooxidative stress in rice. Physiol Plant 128:651–666

    Article  CAS  Google Scholar 

  • Le Martret B, Poage M, Shiel K, Nugent GD, Dix PJ (2011) Tobacco chloroplast transformants expressing genes encoding dehydroascorbate reductase, glutathione reductase, and glutathione-S-transferase, exhibit altered anti-oxidant metabolism and improved abiotic stress tolerance. Plant Biotechnol J 9:661–673

    Article  PubMed  CAS  Google Scholar 

  • LeBlanc MS, Lima A, Montello P, Kim T, Meagher RB, Merkle S (2011) Enhanced arsenic tolerance of transgenic eastern cottonwood plants expressing gamma-glutamylcysteine synthetase. Int J Phytoremediation 13:657–673

    Article  CAS  PubMed  Google Scholar 

  • Leng XP, Jia HF, Sun X, Shangguan LF, Mu Q, Wang BJ, Fang JQ (2015) Comparative transcriptome analysis of grapevine in response to copper stress. Sci Rep 5:17749

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Li Y, Dhankher OP, Carreira L, Balish RS, Meagher RB (2005) Arsenic and mercury tolerance and cadmium sensitivity in Arabidopsis plants expressing bacterial γ-glutamylcysteine synthetase. Environ Toxicol Chem 24:1376–1386

    Article  CAS  PubMed  Google Scholar 

  • Lim B, Meyer AJ, Cobbett CS (2011) Development of glutathione-deficient embryos in Arabidopsis is influenced by the maternal level of glutathione. Plant Biol 13:693–697

    Article  CAS  PubMed  Google Scholar 

  • Loscos J, Matamoros MA, Becana M (2008) Ascorbate and homoglutathione metabolism in common bean nodules under stress conditions and during natural senescence. Plant Physiol 146:1282–1292

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lu SY, Li YC, Guo ZF, Li BS, Li MQ (1999) Enhancement of drought resistance of rice seedlings by calcium treatment. Chin J Rice Sci 13:161–164

    Google Scholar 

  • Lueder DV, Phillips MA (1996) Characterization of Trypanosoma bru-cei γ-glutamylcysteine synthetase, an essential enzyme in the biosynthesis of trypanothione. J Biol Chem 271:17485–17490

    Article  CAS  PubMed  Google Scholar 

  • Maher P (2005) The effects of stress and aging on glutathione metabolism. Ageing Res Rev 4:288–314

    Article  CAS  PubMed  Google Scholar 

  • Marty L, Siala W, Schwarzla¨nder M, Fricker MD, Wirtz M, Sweetlove LJ, Meyer Y, Meyer AJ, Reichheld JP, Hell R (2009) The NADPH-dependent thioredoxin system constitutes a functional backup for cytosolic glutathione reductase in Arabidopsis. Proc Natl Acad Sci U S A 106:9109–9114

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Matamoros MA, Moran JF, Iturbe-Ormaetxe I, Rubio MC, Becana M (1999) Glutathione and homoglutathione synthesis in legume root nodules. Plant Physiol 121:879–888

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Meuwly P, Thibault P, Schwan AL, Rauser WE (1995) Three families of thiol peptides are induced by cadmium in maize. Plant J 7:391–400

    Article  CAS  PubMed  Google Scholar 

  • Meyer AJ (2008) The integration of glutathione homeostasis and redox signaling. J Plant Physiol 165:1390–1403

    Article  CAS  PubMed  Google Scholar 

  • Mhamdi A, Hager J, Chaouch S, Queval G, Han Y, Taconnat L, Saindrenan P, Gouia H, Issakidis-Bourguet E, Renou JP, Noctor G (2010a) Arabidopsis GLUTATHIONE REDUCTASE 1 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 Central  PubMed  Google Scholar 

  • Mhamdi A, Queval G, Chaouch S, Vanderauwera S, Van Breusegem F, Noctor G (2010b) Catalase function in plants: a focus on Arabidopsis mutants as stress-mimic models. J Exp Bot 61:41974220

    Article  CAS  Google Scholar 

  • Miao Y, Dong LV, Wang PC, Wang XC, Chen J, Miao C, Song CP (2006) An Arabidopsis glutathione peroxidase functions as both a redox transducer and a scavenger in abscisic acid and drought stress responses. Plant Cell 18:2749–2766

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Miller G, Shulaev V, Mittler R (2008) Reactive oxygen signaling and abiotic stress. Physiol Plant 133:481–489

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Moons A (2005) Regulatory and functional interactions of plant growth regulators and plant glutathione S-transferases (GSTs). Plant Hormones 72:155–202

    Google Scholar 

  • Moran JF, Iturbe-Ormaetxe I, Matamoros MA, Rubio MC, Clemente MR, Brewin NJ, Becana M (2000) Glutathione and homoglutathione synthetases of legume nodules. Cloning, expression, and subcellular localization. Plant Physiol 124:1381–1392

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mur LAJ, Kenton P, Atzorn R, Miersch O, Wasternack C (2006) The outcomes of concentration-specific interactions between salicylate and jasmonate signaling include synergy, antagonism, and oxidative stress leading to cell death. Plant Physiol 140:249–262

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Murata Y, Pei Z-M, Mori IC, Schroeder J (2001) Abscisic acid activation of plasma membrane Ca2+ channels in guard cells requires cytosolic NAD(P)H and is differentially disrupted upstream and downstream of reactive oxygen species production in abi1-1 and abi2-1 protein phosphatase 2C mutants. Plant Cell 13:2513–2523

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nazar R, Iqbal N, Masood A, Syeed S, Khan NA (2011) Understanding the significance of sulfur in improving salinity tolerance in plants. Environ Exp Bot 70:80–87

    Article  CAS  Google Scholar 

  • Neill SJ, Desikan R, Clarke A, Hurat RD, Hancock JT (2002) Hydrogen peroxide and nitric oxide as signaling molecules in plants. J Exp Bot 53:1237–1247

    Article  CAS  PubMed  Google Scholar 

  • Noctor G (2006) Metabolic signaling in defence and stress: the central role of soluble redox couples. Plant Cell Environ 29:409–425

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Noctor G, Arisi ACM, Jouanin L, Kunert KJ, Rennenberg H, Foyer CH (1998) Glutathione: biosynthesis, metabolism and relationship to stress tolerance explored in transformed plants. J Exp Bot 49:623–647

    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 signaling. 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 

  • Ohama N, Sato H, Shinozaki K, Yamaguchi-Shinozaki K (2017) Transcriptional regulatory network of plant heat stress response. Trends Plant Sci 22:53–65

    Article  CAS  PubMed  Google Scholar 

  • Parisy V, Poinssot B, Owsianowski L, Buchala A, Glazebrook J, Mauch F (2007) Identification of PAD2 as a c-glutamylcysteine synthetase highlights the importance of glutathione in disease resistance of Arabidopsis. Plant J 49:159–172

    Article  CAS  PubMed  Google Scholar 

  • Pastori GM, Foyer CH (2002) Common components, networks, and pathways of cross-tolerance to stress. The central role of “redox” and abscisic acid-mediated controls. Plant Physiol 129:460–468

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Polekhina G, Board PG, Gali RR, Rossjohn J, Parker MW (1999) Molecular basis of glutathione synthetase deficiency and a rare gene permutation event. EMBO J 18:3204–3213

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Price AH, Taylor A, Ripley SJ, Griffiths A, Trewavas AJ, Knight MR (1994) Oxidative signals in tobacco increase cytosolic calcium. Plant Cell 6:1301–1310

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pyngrope S, Bhoomika K, Dubey RS (2013) Reactive oxygen species, ascorbate-glutathione pool, and enzymes of their metabolism in drought-sensitive and tolerant indica rice (Oryza sativa L.) seedlings subjected to progressing levels of water deficit. Protoplasma 250:585–600

    Article  CAS  PubMed  Google Scholar 

  • Quan LJ, Zhang B, Shi WW, Li HY (2008) Hydrogen peroxide in plants: a versatile molecule of the reactive oxygen species network. J Integr Plant Biol 50:2–16

    Article  CAS  PubMed  Google Scholar 

  • Queval G, Thominet D, Vanacker H, Miginiac-Maslow M, Gakiere 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 

  • Rausch T, Gromes R, Liedschulle V, Mu¨ller I, Bogs J, Galovic V, Wachter A (2007) Novel insight into the regulation of GSH biosynthesis in higher plants. Plant Biol 9:565–572

    Article  CAS  PubMed  Google Scholar 

  • Reichheld JP, Khafif M, Riondet C, Droux M, Bonnard G, Meyer Y (2007) Inactivation of thioredoxin reductases reveals a complex interplay between thioredoxin and glutathione pathways in development. Plant Cell 19(6):1851–1865

    Google Scholar 

  • Rouhier N, Lemaire SD, Jacquot JP (2008) The role of glutathione in photosynthetic organisms: emerging functions for glutaredoxins and glutathionylation. Annu Rev Plant Biol 59:143–166

    Article  CAS  PubMed  Google Scholar 

  • Sasaki-Sekimoto Y, Taki N, Obayashi T, Aono M, Matsumoto F, Sakurai N, Suzuki H, Hirai MY, Noji M, Saito K, Masuda T, Takamiya K, Shibata D, Ohta H (2005) Coordinated activation of metabolic pathways for antioxidants and defence compounds by jasmonates and their roles in stress tolerance in Arabidopsis. Plant J 44:653–668

    Article  CAS  PubMed  Google Scholar 

  • Schafer HJ, Greiner S, Rausch T, Haag-Kerwer A (1997) In seedlings of the heavy metal accumulator Brassica Juncea Cu2+ differentially affects transcript amounts for gamma-glutamylcysteine synthetase (gamma-ECS) and metallothionein (MT2). FEBS Lett 404:216–220

    Article  CAS  PubMed  Google Scholar 

  • Sobrino-Plata J, Ortega-Villasante C, Flores-Cáceres ML, Escobar C, Del Campo FF, Hernández LE (2009) Differential alterations of antioxidant defenses as bioindicators of mercury and cadmium toxicity in alfalfa. Chemosphere 77:946–954

    Article  CAS  PubMed  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 

  • Vázquez S, Goldsbrough P, Carpena RO (2009) Comparative analysis of the contribution of phytochelatins to cadmium and arsenic tolerance in soybean and white lupin. Plant Physiol Bioch 47:63–67

    Article  CAS  Google Scholar 

  • Verslues PE, Agarwal M, Katiyar-Agarwal S, Zhu JH, Zhu JK (2006) Methods and concepts in quantifying resistance to drought, salt and freezing, abiotic stresses that affect plant water status. Plant J 45:523–539

    Article  CAS  PubMed  Google Scholar 

  • Wachter A, Wolf S, Steininger 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

    Google Scholar 

  • Wang Z, Xiao Y, Chen W, Tang K, Zhang L (2010) Increased vitamin C content accompanied by an enhanced recycling pathway confers oxidative stress tolerance in Arabidopsis. J Int Plant Biol 52:400–409

    Article  CAS  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 Central  PubMed  Google Scholar 

  • Xiang C, Werner BL, Christensen EM, Oliver DJ (2001) The biological functions of glutathione revisited in Arabidopsis transgenic plants with altered glutathione levels. Plant Physiol 126:564–574

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yamaguchi H, Kato H, Hata Y, Nishioka T, Kimura A, Oda J, Katsube Y (1993) Three-dimensional structure of the glutathione synthetase from Escherichia coli B at 2.0 Å resolution. J Mol Biol 229:1083–1100

    Article  CAS  PubMed  Google Scholar 

  • Yin L, Wang S, Eltayeb AE, Uddin MI, Yamamoto Y, Tsuji W, Takeuchi Y, Tanaka K (2010) Overexpression of dehydroascorbate reductase, but not monodehydroascorbate reductase, confers tolerance to aluminum stress in transgenic tobacco. Planta 231:609–621

    Article  CAS  PubMed  Google Scholar 

  • Ying J, Clavreul N, Sethuraman M, Adachi T, Cohen RA (2007) Thiol oxidation in signaling and response to stress: detection and quantification of physiological and pathophysiological thiol modifications. Free Radic Bio Med 43:1099–1108

    Article  CAS  Google Scholar 

  • Yousuf PY, Hakeem KUR, Chandna R, Ahmad P (2012) In: Ahmad P, Prasad MNV (eds) Role of glutathione reductase in plant abiotic stress. In abiotic stress responses in plants. Springer, New York, pp 149–158

    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 

  • Zagorchev L, Seal CE, Kranner I, Odjakova M (2012) Redox state of low-molecular-weight thiols and disulphides during somatic embryogenesis of salt-treated suspension cultures of Dactylis glomerata L. Free Radic Res 46:656–664

    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 Central  PubMed  Google Scholar 

  • Zechmann B, Müller M (2010) Subcellular compartmentation of glutathione in dicotyledonous plants. Protoplasma 246:15–24

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zottini M, Costa A, de Michele R, Ruzzene M, Carimi F, Lo Schiavo F (2007) Salicylic acid activates nitric oxide synthesis in Arabidopsis. J Exp Bot 58:1397–1405

    Article  CAS  PubMed  Google Scholar 

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Correspondence to Fang Jinggui .

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Chen, W., Xiangpeng, L., Wenying, Z., Jinggui, F. (2017). The Regulatory and Signaling Roles of Glutathione in Modulating Abiotic Stress Responses and Tolerance. 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_7

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