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The Signaling Roles of Glutathione in Plant Disease Resistance

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

Abstract

Early studies showed that glutathione (GSH) as an antioxidant has a role in modulating plant tolerance to biotic stresses by suppressing localized necrotic symptoms following virus infections. The role of GSH in reducing severity of pathogen-induced symptoms in plants was confirmed by employing pharmacological and transgenic approaches. However, later studies have shown that GSH also has a key role in restricting pathogen levels. In fact, it seems that GSH is a pivotal factor responsible for signaling processes related to different types of plant disease resistance, including systemic acquired resistance. The signaling role of GSH in these processes is interconnected with reactive oxygen species and salicylic acid. GSH also regulates the function of plant defense-associated transcription factors and the transcriptional coregulator NPR1 by modulating their redox state. Another layer of regulation is provided by the nitric oxide donor S-nitrosoglutathione that promotes S-nitrosylation of defense-related transcription factors and transcriptional coregulators. Importantly, the role of GSH in mediating plant disease resistance-related signaling processes is independent of its antioxidant function. Changes in GSH levels and redox state triggered during plant biotic stress are not simply passive responses to oxidative damage, since GSH status regulates important elements of cellular signaling that leads to activation of defense responses.

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References

  • Abramowski D, Arasimowicz-Jelonek M, Izbiańska K, Billert H, Floryszak-Wieczorek J (2015) Nitric oxide modulates redox-mediated defense in potato challenged with Phytophthora infestans. Eur J Plant Pathol 143:237–260

    Article  CAS  Google Scholar 

  • Akter N, Sobahan MA, Hossain MA, Uraji M, Nakamura Y, Mori IC, Murata Y (2010) The involvement of intracellular glutathione in methyl jasmonate signaling in Arabidopsis guard cells. Biosci Biotechnol Biochem 74:2504–2506

    Article  CAS  PubMed  Google Scholar 

  • Alvarez ME, Pennell RI, Meijer PJ, Ishikawa A, Dixon RA, Lamb C (1998) Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity. Cell 92:773–784

    Article  CAS  PubMed  Google Scholar 

  • Amirsadeghi S, Robson CA, Vanlerberghe GC (2007) The role of the mitochondrion in plant responses to biotic stress. Physiol Plant 129:253–266

    Article  CAS  Google Scholar 

  • Ball L, Accotto GP, Bechtold U, Creissen G, Funck D, Jimenez A, Kular B, Leyland N, Mejia-Carranza J, Reynolds H, Karpinski S, Mullineaux PM (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 

  • Barna B, Ádám A, Király Z (1993) Juvenility and resistance of a superoxide-tolerant plant to diseases and other stresses. Naturwissenschaften 80:420–422

    Article  Google Scholar 

  • Barna B, Fodor J, Harrach B, Pogány M, Király Z (2012) The Janus face of reactive oxygen species in resistance and susceptibility of plants to necrotrophic and biotrophic pathogens. Plant Physiol Biochem 59:37–43

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Begara-Morales JC, Sánchez-Calvo B, Chaki M, Valderrama R, Mata-Pérez C, Padilla MN, Corpas FJ, Barroso JB (2016) Antioxidant systems are regulated by nitric oxide-mediated post-translational modifications (NO-PTMs). Front Plant Sci 7:152

    Article  PubMed  PubMed Central  Google Scholar 

  • Bi YM, Kenton P, Mur L, Darby R, Draper J (1995) Hydrogen peroxide does not function downstream of salicylic acid in the induction of PR protein expression. Plant J 8:235–245

    Article  CAS  PubMed  Google Scholar 

  • Caarls L, Pieterse CMJ, Van Wees SC (2015) How salicylic acid takes transcriptional control over jasmonic acid signaling. Front Plant Sci 6:170

    Article  PubMed  PubMed Central  Google Scholar 

  • Chamnongpol S, Willekens H, Moeder W, Langebartels C, Sandermann H Jr, Van Montagu M, Inzé D, Van Camp W (1998) Defense activation and enhanced pathogen tolerance induced by H2O2 in transgenic tobacco. Proc Natl Acad Sci U S A 95:5818–5823

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen Z, Silva H, Klessig DF (1993) Active oxygen species in the induction of plant systemic acquired resistance by salicylic acid. Science 262:1883–1886

    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 YP, Xing LP, Wu GJ, Wang HZ, Wang XE, Cao AZ, Chen PD (2007) Plastidial glutathione reductase from Haynaldia villosa is an enhancer of powdery mildew resistance in wheat (Triticum aestivum). Plant Cell Physiol 48:1702–1712

    Article  CAS  PubMed  Google Scholar 

  • Chen I-H, Chiu M-H, Cheng S-F, Hsu Y-H, Tsai CH (2013) The glutathione transferase of Nicotiana benthamiana NbGSTU4 plays a role in regulating the early replication of Bamboo mosaic virus. New Phytol 199:749–757

    Article  CAS  PubMed  PubMed Central  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 

  • Choudhary AD, Kessmann H, Lamb CJ, Dixon RA (1990) Stress responses in alfalfa (Medicago sativa L.). IV. Expression of defense gene constructs in electroporated suspension cell protoplasts. Plant Cell Rep 9:42–46

    Article  CAS  PubMed  Google Scholar 

  • Clemente-Moreno MJ, Diaz Vivancos P, Barba-Espín G, Hernández JA (2010) Benzothiadiazole and L-2-oxothiazolidine-4-carboxylic acid reduce the severity of Sharka symptoms in pea leaves: effect on antioxidative metabolism at the subcellular level. Plant Biol 12:88–97

    Article  CAS  PubMed  Google Scholar 

  • Clemente-Moreno MJ, Diaz Vivancos P, Piqueras A, Hernández JA (2012) Plant growth stimulation in Prunus species plantlets by BTH or OTC treatments under in vitro conditions. J Plant Physiol 169:1074–1083

    Article  CAS  PubMed  Google Scholar 

  • Datta R, Chattopadhyay S (2015) Changes in the proteome of pad2-1, a glutathione depleted Arabidopsis mutant, during Pseudomonas syringae infection. J Proteome 126:82–93

    Article  CAS  Google Scholar 

  • Datta R, Kumar D, Sultana A, Hazra S, Bhattacharyya D, Chattopadhyay S (2015) Glutathione regulates 1-aminocyclopropane-1-carboxylate synthase transcription via WRKY33 and 1-aminocyclopropane-1-carboxylate oxidase by modulating messenger RNA stability to induce ethylene synthesis during stress. Plant Physiol 169:2963–2981

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dean JD, Goodwin PH, Hsiang T (2005) Induction of glutathione S-transferase genes of Nicotiana benthamiana following infection by Colletotrichum destructivum and C. orbiculare and involvement of one in resistance. J Exp Bot 56:1525–1533

    Article  CAS  PubMed  Google Scholar 

  • Després C, Chubak C, Rochon A, Clark R, Bethune T, Desveaux D, Fobert PR (2003) The Arabidopsis NPR1 disease resistance protein is a novel cofactor that confers redox regulation of DNA binding activity to the basic domain/leucine zipper transcription factor TGA1. Plant Cell 15:2181–2191

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Diaz 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 homeostasis in Arabidopsis thaliana and lowers the oxidative defence shield. Plant J 64:825–838

    Article  CAS  Google Scholar 

  • Diaz 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  CAS  PubMed  Google Scholar 

  • Dixon DP, Edwards R (2009) Selective binding of glutathione conjugates of fatty acid derivatives by plant glutathione transferases. J Biol Chem 284:21249–21256

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dixon DP, Hawkins T, Hussey PJ, Edwards R (2009) Enzyme activities and subcellular localization of members of the Arabidopsis glutathione transferase superfamily. J Exp Bot 60:1207–1218

    Google Scholar 

  • Dixon DP, Sellars JD, Edwards R (2011) The Arabidopsis phi class glutathione transferase AtGSTF2: binding and regulation by biologically active heterocyclic ligands. Biochem J 438:63–70

    Article  CAS  PubMed  Google Scholar 

  • Dong X (2004) NPR1, all things considered. Curr Opin Plant Biol 7:547–552

    Article  CAS  PubMed  Google Scholar 

  • Dröge-Laser W, Kaiser A, Lindsay WP, Halkier BA, Loake GJ, Doerner P, Dixon RA, Lamb C (1997) Rapid stimulation of a soybean protein-serine kinase that phosphorylates a novel bZIP DNA-binding protein, G/HBF-1, during the induction of early transcription-dependent defenses. EMBO J 16:726–738

    Article  PubMed  PubMed Central  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 U S A 85:6738–6742

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dubreuil-Maurizi C, Poinssot B (2012) Role of glutathione in plant signaling under biotic stress. Plant Signal Behav 7:210–212

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dubreuil-Maurizi C, Vitecek J, Marty L, Branciard L, Frettinger P, Wendehenne D, Meyer AJ, Mauch F, Poinssot B (2011) Glutathione deficiency of the Arabidopsis mutant pad2-1 affects oxidative stress-related events, defense gene expression, and the hypersensitive response. Plant Physiol 157:2000–2012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Edwards R, Dixon DP (2005) Plant glutathione transferases. Methods Enzymol 401:169–186

    Article  CAS  PubMed  Google Scholar 

  • El-Zahaby HM, Gullner G, Király Z (1995) Effects of powdery mildew infection of barley on the ascorbate-glutathione cycle and other antioxidants in different host-pathogen interactions. Phytopathology 85:1225–1230

    Article  CAS  Google Scholar 

  • Enyedi AJ, Yalpani N, Silverman P, Raskin I (1992) Localization, conjugation, and function of salicylic acid in tobacco during the hypersensitive reaction to tobacco mosaic virus. Proc Natl Acad Sci U S A 89:2480–2484

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Farkas G, Király Z, Solymosi F (1960) Role of oxidative metabolism in the localization of plant viruses. Virology 12:408–421

    Article  CAS  PubMed  Google Scholar 

  • Feechan A, Kwon E, Yun BW, Wang Y, Pallas JA, Loake GJ (2005) A central role for S-nitrosothiols in plant disease resistance. Proc Natl Acad Sci U S A 102:8054–8059

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fobert PR, Després C (2005) Redox control of systemic acquired resistance. Curr Opin Plant Biol 8:378–382

    Article  CAS  PubMed  Google Scholar 

  • Fodor J, Gullner G, Ádám AL, Barna B, Kőmíves T, Király Z (1997) Local and systemic responses of antioxidants to tobacco mosaic virus infection and to salicylic acid in tobacco. Role in systemic acquired resistance. Plant Physiol 114:1443–1451

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Foyer CH, Rennenberg H (2000) Regulation of glutathione synthesis and its role in abiotic and biotic stress defence. In: Brunold C, Rennenberg H, De Kok LJ, Stulen I, Davidian JC (eds) Sulfur nutrition and sulfur assimilation in higher plants. Paul Haupt, Bern, pp 127–153

    Google Scholar 

  • Freeman JL, Garcia D, Kim DG, Hopf A, Salt DE (2005) Constitutively elevated salicylic acid signals glutathione-mediated nickel tolerance in Thlaspi nickel hyperaccumulators. Plant Physiol 137:1082–1091

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Geigenberger P, Thormählen I, Daloso DM, Fernie AR (2017) The unprecedented versatility of the plant thioredoxin system. Trends Plant Sci 22:249–262

    Article  CAS  PubMed  Google Scholar 

  • Ghanta S, Chattopadhyay S (2011) Glutathione as a signaling molecule: another challenge to pathogens. Plant Signal Behav 6:783–788

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ghanta S, Bhattacharyya D, Chattopadhyay S (2011a) Glutathione signaling acts through NPR1-dependent SA-mediated pathway to mitigate biotic stress. Plant Signal Behav 6:607–609

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ghanta S, Bhattacharyya D, Sinha R, Banerjee A, Chattopadhyay S (2011b) Nicotiana tabacum overexpressing γ-ECS exhibits biotic stress tolerance likely through NPR1-dependent salicylic acid-mediated pathway. Planta 233:895–910

    Article  CAS  PubMed  Google Scholar 

  • Ghanta S, Datta R, Bhattacharyya D, Sinha R, Kumar D, Hazra S, Mazumdar AB, Chattopadhyay S (2014) Multistep involvement of glutathione with salicylic acid and ethylene to combat environmental stress. J Plant Physiol 171:940–950

    Article  CAS  PubMed  Google Scholar 

  • Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227

    Article  CAS  PubMed  Google Scholar 

  • Goodman RN, Novacky AJ (1994) The hypersensitive reaction in plants to pathogens. APS Press, St. Paul

    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 

  • Greenberg JT, Yao N (2004) The role and regulation of programmed cell death in plant-pathogen interactions. Cell Microbiol 6:201–211

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Gullner G, Kőmíves T (2001) The role of glutathione and glutathione-related enzymes in plant-pathogen interactions. In: Grill D, Tausz M, De Kok LJ (eds) Significance of glutathione in plant adaptation to the environment. Kluwer Academic Publishers, Dordrecht, pp 207–239

    Chapter  Google Scholar 

  • Gullner G, Kőmíves T (2006) Defense reactions of infected plants: roles of glutathione and glutathione S-transferase enzymes. Acta Phytopathol Entomol Hung 41:3–10

    Article  CAS  Google Scholar 

  • Gullner G, Kőmíves T, Király L (1991) Enhanced inducibility of antioxidant systems in a Nicotiana tabacum L. biotype results in acifluorfen resistance. Z. Naturforsch 46c:875–881

    Google Scholar 

  • Gullner G, Fodor J, Király L (1995) Induction of glutathione-S-transferase activity in tobacco by tobacco necrosis virus infection and by salicylic acid. Pestic Sci 45:290–291

    Article  CAS  Google Scholar 

  • Gullner G, Tóbiás I, Fodor J, Kőmíves T (1999) Elevation of glutathione level and activation of glutathione-related enzymes affect virus infection in tobacco. Free Radic Res 31:S155–S161

    Article  CAS  PubMed  Google Scholar 

  • Hacham Y, Koussevitzky S, Kirma M, Amir R (2014) Glutathione application affects the transcript profile of genes in Arabidopsis seedling. J Plant Physiol 171:1444–1451

    Article  CAS  PubMed  Google Scholar 

  • Han Y, Chaouch S, Mhamdi A, Queval G, Zechmann B, Noctor G (2013a) Functional analysis of Arabidopsis mutants points to novel roles for glutathione in coupling H2O2 to activation of salicylic acid accumulation and signalling. Antioxid Redox Signal 18:2106–2121

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Han Y, Mhamdi A, Chaouch S, Noctor G (2013b) Regulation of basal and oxidative stress-triggered jasmonic acid-related gene expression by glutathione. Plant Cell Environ 36:1135–1146

    Article  CAS  PubMed  Google Scholar 

  • Harrach BD, Fodor J, Pogány M, Preuss J, Barna B (2008) Antioxidant, ethylene and membrane leakage responses to powdery mildew infection of near-isogenic barley lines with various types of resistance. Eur J Plant Pathol 121:21–33

    Article  CAS  Google Scholar 

  • Harrach BD, Baltruschat H, Barna B, Fodor J, Kogel K-H (2013) The mutualistic fungus piriformospora indica protects barley roots from a loss of antioxidant capacity caused by the necrotrophic pathogen Fusarium culmorum. Mol Plant-Microbe Interact 26:599–605

    Article  CAS  PubMed  Google Scholar 

  • Hausladen A, Kunert KJ (1990) Effects of artificially enhanced levels of ascorbate and glutathione on the enzymes monodehydroascorbate reductase, dehydroascorbate reductase, and glutathione reductase in spinach (Spinacia oleracea). Physiol Plant 79:384–388

    Article  CAS  Google Scholar 

  • Herbette S, Lenne C, de Labrouhe DT, Drevet JR, Roeckel-Drevet P (2003) Transcripts of sunflower antioxidant scavengers of the SOD and GPX families accumulate differentially in response to downy mildew infection, phytohormones, reactive oxygen species, nitric oxide, protein kinase and phosphatase inhibitors. Physiol Plant 119:418–428

    Article  CAS  Google Scholar 

  • Hernández I, Chacón O, Rodriguez R, Portieles R, López Y, Pujol M, Borrás-Hidalgo O (2009) Black shank resistant tobacco by silencing of glutathione S-transferase. Biochem Biophys Res Commun 387:300–304

    Article  PubMed  CAS  Google Scholar 

  • Hernández JA, Gullner G, Clemente-Moreno MJ, Künstler A, Juhász C, Diaz Vivancos P, Király L (2016) Oxidative stress and antioxidative responses in plant-virus interactions. Physiol Mol Plant Pathol 94:134–148

    Article  CAS  Google Scholar 

  • Herrera-Vásquez A, Salinas P, Holuigue L (2015) Salicylic acid and reactive oxygen species interplay in the transcriptional control of defense genes expression. Front Plant Sci 6:171

    Article  PubMed  PubMed Central  Google Scholar 

  • Höller K, Király L, Künstler A, Müller M, Gullner G, Fattinger M, Zechmann B (2010) Enhanced glutathione metabolism is correlated with sulfur induced resistance in tobacco mosaic virus-infected genetically susceptible Nicotiana tabacum plants. Mol Plant-Microbe Interact 23:1448–1459

    Article  PubMed  CAS  Google Scholar 

  • Juhász C, Gullner G (2014) The monoterpenoid (S)-carvone massively up-regulates several classes of glutathione S-transferase genes in tobacco leaf discs. Acta Phytopathol Entomol Hung 49:163–176

    Article  CAS  Google Scholar 

  • Kauss H, Jeblick W (1995) Pretreatment of parsley suspension cultures with salicylic acid enhances spontaneous and elicited production of H2O2. Plant Physiol 108:1171–1178

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Király Z, Barna B, Kecskés A, Fodor J (2002) Down-regulation of antioxidative capacity in a transgenic tobacco which fails to develop acquired resistance to necrotization caused by tobacco mosaic virus. Free Radic Res 36:981–991

    Article  PubMed  CAS  Google Scholar 

  • Király L, Künstler A, Fattinger M, Höller K, Juhász C, Müller M, Gullner G, Zechmann B (2012) Sulfate supply influences compartment specific glutathione metabolism and confers enhanced resistance to tobacco mosaic virus during a hypersensitive response. Plant Physiol Biochem 59:44–54

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Klement Z (1982) Hypersensitivity. In: Mount MS, Lacy GH (eds) Phytopathogenic prokaryotes II. Academic, New York, pp 149–177

    Chapter  Google Scholar 

  • Koornneef A, Leon-Reyes A, Ritsema T, Verhage A, Den Otter FC, Van Loon LC, Pieterse CM (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 

  • Kovacs I, Durner J, Lindermayr C (2015) Crosstalk between nitric oxide and glutathione is required for NONEXPRESSOR OF PATHOGENESIS-RELATED GENES 1 (NPR1)-dependent defense signaling in Arabidopsis thaliana. New Phytol 208:860–872

    Article  CAS  PubMed  Google Scholar 

  • Kovacs I, Holzmeister C, Wirtz M, Geerlof A, Fröhlich T, Römling G, Kuruthukulangarakoola GT, Linster E, Hell R, Arnold GJ, Durner J, Lindermayr C (2016) ROS-mediated inhibition of S-nitrosoglutathione reductase contributes to the activation of anti-oxidative mechanisms. Front Plant Sci 7:1669

    Article  PubMed  PubMed Central  Google Scholar 

  • Künstler A, Király L, Pogány M, Tóbiás I, Gullner G (2007) Lipoxygenase and glutathione peroxidase activity in tobacco leaves inoculated with tobacco mosaic virus. Acta Phytopathol Entomol Hung 42:197–207

    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 128:651–661

    Article  CAS  Google Scholar 

  • Kuźniak E, Skłodowska M (2004) Differential implication of glutathione, glutathione-metabolizing enzymes and ascorbate in tomato resistance to Pseudomonas syringae. J Phytopathol 152:529–536

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Kuźniak E, Skłodowska M (2005b) Compartment-specific role of the ascorbate-glutathione cycle in the response of tomato leaf cells to Botrytis cinerea infection. J Exp Bot 56:921–933

    Article  PubMed  CAS  Google Scholar 

  • La Camera S, L’Haridon F, Astier J, Zander M, Abou-Mansour E, Page G, Thurow C, Wendehenne D, Gatz C, Métraux JP, Lamotte O (2011) The glutaredoxin ATGRXS13 is required to facilitate Botrytis cinerea infection of Arabidopsis thaliana plants. Plant J 68:507–519

    Article  PubMed  CAS  Google Scholar 

  • Laloi C, Mestres-Ortega D, Marco Y, Meyer Y, Reichheld JP (2004) The Arabidopsis cytosolic thioredoxin h5 gene induction by oxidative stress and its W-box-mediated response to pathogen elicitor. Plant Physiol 134:1006–1016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • León J, Lawton MA, Raskin I (1995) Hydrogen peroxide stimulates salicylic acid biosynthesis in tobacco. Plant Physiol 108:1673–1678

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Li J, Brader G, Palva ET (2004) The WRKY70 transcription factor: a node of convergence for jasmonate-mediated and salicylate-mediated signals in plant defense. Plant Cell 16:319–331

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li X, Zhang JB, Song B, Li HP, Xu HQ, Qu B, Dang FJ, Liao YC (2010) Resistance to Fusarium head blight and seedling blight in wheat is associated with activation of a cytochrome P450 gene. Phytopathology 100:183–191

    Article  CAS  PubMed  Google Scholar 

  • Mateo A, Funck D, Mühlenbock P, Kular B, Mullineaux PM, Karpinski S (2006) Controlled levels of salicylic acid are required for optimal photosynthesis and redox homeostasis. J Exp Bot 57:1795–1807

    Article  CAS  PubMed  Google Scholar 

  • Matern S, Peskan-Berghoefer T, Gromes R, Kiesel RV, Rausch T (2015) Imposed glutathione-mediated redox switch modulates the tobacco wound-induced protein kinase and salicylic acid-induced protein kinase activation state and impacts on defence against Pseudomonas syringae. J Exp Bot 66:1935–1950

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mauch F, Dudler R (1993) Differential induction of distinct glutathione-S-transferases of wheat by xenobiotics and by pathogen attack. Plant Physiol 102:1193–1201

    Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • May MJ, Parker JE, Daniels MJ, Leaver CJ, Cobbett CS (1996b) An Arabidopsis mutant depleted in glutathione shows unaltered responses to fungal and bacterial pathogens. Mol Plant-Microbe Interact 9:349–356

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Meyer AJ, Hell R (2005) Glutathione homeostasis and redox-regulation by sulfhydryl groups. Photosynth Res 86:435–457

    Article  CAS  PubMed  Google Scholar 

  • Meyer Y, Belin C, Delorme-Hinoux V, Reichheld JP, Riondet C (2012) Thioredoxin and glutaredoxin systems in plants: molecular mechanisms, crosstalks, and functional significance. Antioxid Redox Signal 17:1124–1160

    Article  CAS  PubMed  Google Scholar 

  • Mou Z, Fan W, Dong X (2003) Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113:935–944

    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 

  • 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 

  • 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

    Google Scholar 

  • Neuenschwander U, Vernooij B, Friedrich L, Uknes S, Kessmann H, Ryals J (1995) 1s hydrogen peroxide a second messenger of salicylic acid in systemic acquired resistance? Plant J 8:227–233

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Noctor G, Foyer CH (2016) Intracellular redox compartmentation and ROS-related communication in regulation and signaling. Plant Physiol 171:1581–1592

    Article  CAS  PubMed  PubMed Central  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 

  • 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

    Google Scholar 

  • Perfect ES, Green JR (2001) Infection structures of biotrophic and hemibiotrophic fungal plant pathogens. Mol Plant Pathol 2:101–108

    Article  CAS  PubMed  Google Scholar 

  • Pieterse CM, Leon-Reyes A, Van der Ent S, Van Wees SC (2009) Networking by small-molecule hormones in plant immunity. Nat Chem Biol 5:308–316

    Article  CAS  PubMed  Google Scholar 

  • Rahantaniaina MS, Tuzet A, Mhamdi A, Noctor G (2013) Missing links in understanding redox signaling via thiol/disulfide modulation: how is glutathione oxidized in plants? Front Plant Sci 4:477

    Article  PubMed  PubMed Central  Google Scholar 

  • Rao MV, Paliyath G, Ormrod DP, Murr DP, Watkins CB (1997) Influence of salicylic acid on H2O2 production, oxidative stress, and H2O2-metabolizing enzymes. Salicylic acid-mediated oxidative damage requires H2O2. Plant Physiol 115:137–149

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Robert-Seilaniantz A, Grant M, Jones JD (2011) Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism. Annu Rev Phytopathol 49:317–343

    Article  CAS  PubMed  Google Scholar 

  • Romero-Puertas MC, Laxa M, Mattè A, Zaninotto F, Finkemeier I, Jones AME, Perazzolli M, Vandelle E, Dietz KJ, Delledonne M (2007) S-nitrosylation of peroxiredoxin IIE promotes peroxynitrite-mediated tyrosine nitration. Plant Cell 19:4120–4130

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Romero-Puertas MC, Campostrini N, Mattè A, Righetti PG, Perazzolli M, Zolla L, Roepstorff P, Delledonne M (2008) Proteomic analysis of S-nitrosylated proteins in Arabidopsis thaliana undergoing hypersensitive response. Proteomics 8:1459–1469

    Article  CAS  PubMed  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 

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

    Article  CAS  PubMed  Google Scholar 

  • Senda K, Ogawa K (2004) Induction of PR-1 accumulation accompanied by runaway cell death in the lsd1 mutant of Arabidopsis is dependent on glutathione levels, but independent of the redox state of glutathione. Plant Cell Physiol 45:1578–1585

    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 

  • Singh K, Foley RC, Oñate-Sánchez L (2002) Transcription factors in plant defense and stress responses. Curr Opin Plant Biol 5:430–436

    Article  CAS  PubMed  Google Scholar 

  • Sinha R, Kumar D, Datta R, Hazra S, Bhattacharyya D, Mazumdar AB, Mukhopadhyay R, Sultana A, Chattopadhyay S (2015) Integrated transcriptomic and proteomic analysis of Arabidopsis thaliana exposed to glutathione unravels its role in plant defense. Plant Cell Tissue Organ Cult 120:975–988

    Article  CAS  Google Scholar 

  • Spanu PD, Panstruga R (2017) Editorial: biotrophic plant-microbe interactions. Front Plant Sci 8:192

    Article  PubMed  PubMed Central  Google Scholar 

  • Spoel SH, Loake GJ (2011) Redox-based protein modifications: the missing link in plant immune signalling. Curr Opin Plant Biol 14:358–364

    Article  CAS  PubMed  Google Scholar 

  • Srivastava MK, Dwivedi UN (1998) Salicylic acid modulates glutathione metabolism in pea seedlings. J Plant Physiol 153:409–414

    Article  CAS  Google Scholar 

  • Sun L, Ren H, Liu R, Li B, Wu T, Sun F, Liu H, Wang X, Dong H (2010) An h-type thioredoxin functions in tobacco defense responses to two species of viruses and an abiotic oxidative stress. Mol Plant-Microbe Interact 23:1470–1485

    Article  CAS  PubMed  Google Scholar 

  • Tada Y, Spoel SH, Pajerowska-Mukhtar K, Mou Z, Song J, Wang C, Zuo J, Dong X (2008) Plant immunity requires conformational changes of NPR1 via S-nitrosylation and thioredoxins. Science 321:952–956

    Article  CAS  PubMed  Google Scholar 

  • Tenhaken R, Levine A, Brisson LF, Dixon RA, Lamb C (1995) Function of the oxidative burst in hypersensitive disease resistance. Proc Natl Acad Sci U S A 92:4158–4163

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thalineau E, Truong H-N, Berger A, Fournier C, Boscari A, Wendehenne D, Jeandroz S (2016) Cross-regulation between N metabolism and nitric oxide (NO) signaling during plant immunity. Front Plant Sci 7:472

    Article  PubMed  PubMed Central  Google Scholar 

  • Van Camp W, Van Montagu M, Inzé D (1998) H2O2 and NO: redox signals in disease resistance. Trends Plant Sci 3:330–334

    Article  Google Scholar 

  • Vanacker H, Carver TLW, Foyer CH (1998) 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, 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 

  • Vianello A, Zancani M, Peresson C, Petrussa E, Casolo V, Krajnakova J, Patui S, Braidot E, Macri F (2007) Plant mitochondrial pathway leading to programmed cell death. Physiol Plant 129:242–252

    Article  CAS  Google Scholar 

  • Vlot AC, Dempsey DA, Klessig DF (2009) Salicylic acid, a multifaceted hormone to combat disease. Annu Rev Phytopathol 47:177–206

    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

    Article  CAS  PubMed  Google Scholar 

  • Wagner U, Edwards R, Dixon DP, Mauch F (2002) Probing the diversity of the Arabidopsis glutathione S-transferase gene family. Plant Mol Biol 49:515–532

    Article  CAS  PubMed  Google Scholar 

  • Wang Z, Xing S, Birkenbihl RP, Zachgo S (2009) Conserved functions of Arabidopsis and rice CC-type glutaredoxins in flower development and pathogen response. Mol Plant 2:323–335

    Article  CAS  PubMed  Google Scholar 

  • Whitham SA, Quan S, Chang HS, Cooper B, Estes B, Zhu T, Wang X, Hou YM (2003) Diverse RNA viruses elicit the expression of common sets of genes in susceptible Arabidopsis thaliana plants. Plant J 33:271–283

    Article  CAS  PubMed  Google Scholar 

  • Wingate VPM, Lawton MA, Lamb CJ (1988) Glutathione causes a massive and selective induction of plant defense genes. Plant Physiol 87:206–210

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Winterbourn CC (2013) The biological chemistry of hydrogen peroxide. Methods Enzymol 528:3–25

    Article  CAS  PubMed  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 

  • Yang Y, Shah J, Klessig DF (1997) Signal perception and transduction in plant defense responses. Genes Dev 11:1621–1639

    Article  CAS  PubMed  Google Scholar 

  • Yu LM, Lamb CJ, Dixon RA (1993) Purification and biochemical characterization of proteins which bind to the H-box cis-element implicated in transcriptional activation of plant defense genes. Plant J 3:805–816

    Article  CAS  PubMed  Google Scholar 

  • Yun BW, Spoel SH, Loake GJ (2012) Synthesis of and signalling by small, redox active molecules in the plant immune response. Biochim Biophys Acta 1820:770–776

    Article  CAS  PubMed  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 

  • Zander M, La Camera S, Lamotte O, Métraux JP, Gatz C (2010) Arabidopsis thaliana class-II TGA transcription factors are essential activators of jasmonic acid/ethylene-induced defense responses. Plant J 61:200–210

    Google Scholar 

  • Zander M, Chen S, Imkampe J, Thurow C, Gatz C (2012) Repression of the Arabidopsis thaliana jasmonic acid/ethylene-induced defense pathway by TGA-interacting glutaredoxins depends on their C-terminal ALWL motif. Mol Plant 5:831–840

    Article  CAS  PubMed  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 

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Acknowledgments

Research in the laboratory of the authors is supported by grants of the Hungarian National Research, Development and Innovation Office (NKFIH K111995 and PD108455).

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Authors and Affiliations

  1. Plant Protection Institute, Centre for Agricultural Research, Hungarian Academy of Sciences, H-1525, Budapest, P.O. Box 102, Hungary

    Gábor Gullner, András Künstler & Lóránt Király

  2. Center for Microscopy and Imaging, Baylor University, Waco, TX, 76798, USA

    Bernd Zechmann

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  1. Gábor Gullner
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  2. Bernd Zechmann
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  3. András Künstler
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  4. Lóránt Király
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Correspondence to Lóránt Király .

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Editors and Affiliations

  1. Department of Genetics and Plant Breeding, Bangladesh Agricultural University, Mymensingh, Bangladesh

    Mohammad Anwar Hossain

  2. Department of Biochemistry and Molecular Biology, Bangabandhu Sheikh Mujibur Rahman Agricultural University, Gazipur, Bangladesh

    Mohammad Golam Mostofa

  3. Department of Plant Breeding, CEBAS-CSIC, Murcia, Murcia, Spain

    Pedro Diaz-Vivancos

  4. Department of Botany, University of Otago, Dunedin, Otago, New Zealand

    David J Burritt

  5. Department of Applied Biological Science, Kagawa University, Kagawa, Japan

    Masayuki Fujita

  6. RIKEN Center for Sustainable Resource Science, Signaling Pathway Research Unit, Yokohama, Japan

    Lam-Son Phan Tran

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Gullner, G., Zechmann, B., Künstler, A., Király, L. (2017). The Signaling Roles of Glutathione in Plant Disease Resistance. 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_15

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