Skip to main content
SpringerLink
Log in
Book cover

Ascorbic Acid in Plant Growth, Development and Stress Tolerance pp 201–231Cite as

Ascorbate-Glutathione Cycle and Biotic Stress Tolerance in Plants

  • Chapter
  • First Online:

Abstract

The ascorbate-glutathione cycle (AsA-GSH cycle) is a central pathway of the plant cells linking the H2O2-scavenging activity to redox signalling. Here, we summarize the most recent advances in our understanding of the role of AsA-GSH cycle in plant–pathogen interactions. Special attention is paid to the regulatory functions of the AsA-GSH cycle components in plant defence against pathogens, their cross talk with other stress signalling pathways and the functional differences between the cellular compartments in relation to the ascorbate and glutathione-dependent protective systems. As under field conditions, different stresses are likely to occur simultaneously, the involvement of AsA-GSH cycle in the signalling network that regulates the response of plants to a combination of pathogen infection and abiotic stress is also addressed.

This is a preview of subscription content, log in via an institution.

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • AbdElgawad H, Zinta G, Hegab MM, Pandey R, Asard H, Abuelsoud W (2016) High salinity induces different oxidative stress and antioxidant responses in maize seedlings organs. Front Plant Sci 7:1–11

    Google Scholar 

  • Acharya B, Assmann S (2009) Hormone interactions in stomatal function. Plant Mol Biol 69:451–462

    Article  CAS  PubMed  Google Scholar 

  • Aranega-Bou P, de la O Leyva M, Finiti I, García-Agustín P, González-Bosch C (2014) Priming of plant resistance by natural compounds. Hexanoic acid as a model. Front Plant Sci 5:488

    Article  PubMed  PubMed Central  Google Scholar 

  • Arnaud D, Hwang I (2015) A sophisticated network of signalling pathways regulates stomatal defences to bacterial pathogens. Mol Plant 8:566–581

    Article  CAS  PubMed  Google Scholar 

  • Arrigoni O, De Tullio MC (2002) Ascorbic acid: much more than just an antioxidant. Biochim Biophys Acta 1569:1–9

    Article  CAS  PubMed  Google Scholar 

  • Asada K (1999) The water–water cycle in chloroplasts: scavenging of active oxygen and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50:601–639

    Article  CAS  PubMed  Google Scholar 

  • Atkinson NJ, Urwin PE (2012) The interaction of plant biotic and abiotic stresses: from genes to the field. J Exp Bot 63:3523–3544

    Article  CAS  PubMed  Google Scholar 

  • Backhausen JE, Kitzmann C, Horton P, Scheibe R (2000) Electron acceptors in isolated intact spinach chloroplasts act hierarchically to prevent over-reduction and competition for electrons. Photosynth Res 64:1–13

    Article  CAS  PubMed  Google Scholar 

  • Ball L, Accotto G, Bechtold U, Creissen G, Funck G, Jimenez A, Kular B, Leyland N, Mejia-Carranza J, Reynolds H, Karpinski S, Mullineaux PM (2004) Evidence for direct link between glutathione biosynthesis and stress defence gene expression in Arabidopsis. Plant Cell 16:2448–2462

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    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 

  • Bienert GP, Møller AL, Kristiansen KA, Schulz A, Møller IM, Schjoerring JK, Jahn TP (2007) Specific aquaporins facilitate the diffusion of hydrogen peroxide across membranes. J Biol Chem 282:1183–1192

    Article  CAS  PubMed  Google Scholar 

  • Blanch M, Rosales R, Goya L, Sanchez-Ballesta MT, Escribano MI, Merodio C (2013) NADP-malic enzyme and glutathione reductase contribute to glutathione regeneration in Fragaria vesca fruit treated with protective high CO2 concentrations. Postharvest Biol Tec 86:431–436

    Article  CAS  Google Scholar 

  • Blanco NE, Guinea-Díaz M, Whelan J, Strand Å (2014) Interaction between plastid and mitochondrial retrograde signalling pathways during changes to plastid redox status. Philos Trans R Soc Lond Ser B Biol Sci 369:20130231

    Article  CAS  Google Scholar 

  • Bolter C, Brammall RA, Cohen R, Lazarovits G (1993) Glutathione alterations in melon and tomato roots following treatment with chemicals which induce disease resistance to Fusarium wilt. Physiol Mol Plant Pathol 42:321–336

    Article  CAS  Google Scholar 

  • Bolwell PP, Page A, Piślewska M, Wojtaszek P (2001) Pathogenic infection and the oxidative defences in plant apoplast. Protoplasma 217:20–32

    Article  CAS  PubMed  Google Scholar 

  • Bordenave CD, Escaray FJ, Menendez AB, Serna E, Carrasco P, Ruiz OA, Gárriz A (2013) Defence responses in two ecotypes of Lotus japonicus against non-pathogenic Pseudomonas syringae. PLoS One 8:e83199

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Borisova MM, Kozuleva MA, Rudenko NN, Naydov IA, Klenina IB, Ivanov BN (2012) Photosynthetic electron flow to oxygen and diffusion of hydrogen peroxide through the chloroplast envelope via aquaporins. Biochim Biophys Acta 1817:1314–1321

    Article  CAS  Google Scholar 

  • Cha JY, Barman DN, Kim MG, Kim WY (2015) Stress defense mechanisms of NADPH-dependent thioredoxin reductases (NTRs) in plants. Plant Signal Behav 10:e1017698

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chen Z, Gallie DR (2004) The ascorbic acid redox state controls guard cell signaling and stomatal movement. Plant Cell 16:1143–1162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chew O, Whelan J, Millar HA (2003) Molecular definition of the ascorbate-glutathione cycle in Arabidopsis mitochondria reveals dual targeting of antioxidant defences in plants. J Biol Chem 278:46869–46877

    Article  CAS  PubMed  Google Scholar 

  • Chojak J, Kuźniak E, Świercz U, Sekulska-Nalewajko J, Gocławski J (2012) Interaction between salt stress and angular leaf spot (Pseudomonas syringae pv lachrymans) in cucumber. Veg Crop Res Bull 77:5–16

    CAS  Google Scholar 

  • Chojak-Koźniewska J (2017) Metabolic and hormonal regulations of cucumber (Cucumis sativus) response to multiple environmental stressors. Dissertation, University of Łódź

    Google Scholar 

  • Chojak-Koźniewska J, Linkiewicz A, Sowa S, Radzioch MA, Kuźniak E (2017) Interactive effects of salt stress and Pseudomonas syringae pv. lachrymans infection in cucumber: involvement of antioxidant enzymes, abscisic acid and salicylic acid. Environ Exp Bot 136:9–20

    Article  CAS  Google Scholar 

  • Conklin PL (2001) Recent advances in the role and biosynthesis of ascorbic acid in plants. Plant Cell Environ 24:383–394

    Article  CAS  Google Scholar 

  • Conrath U, Beckers GJM, Langenbach CJG, Jaskiewicz MR (2015) Priming for enhanced defense. Annu Rev Phytopathol 53:97–119

    Article  CAS  PubMed  Google Scholar 

  • Corpas FJ, Barroso JB, Palma JM, Rodriguez-Ruiz M (2017) Plant peroxisomes: a nitro-oxidative cocktail. Redox Biol 11:535–542

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Davletova S, Rizhsky L, Liang H, Shengqiang Z, Oliver DJ, Coutu J, Shulaev V, Schlauch K, Mittler R (2005) Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen gene network of Arabidopsis. Plant Cell 17:268–281

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • De Gara L, de Pinto MC, Tommasi F (2003) The antioxidant systems vis-à-vis reactive oxygen species during plant-pathogen interaction. Plant Physiol Biochem 41:863–870

    Article  CAS  Google Scholar 

  • de Torres-Zabala M, Truman W, Bennett MH, Lafforgue G, Mansfield JW, Rodriguez Egea P, Bögre L, Grant M (2007) Pseudomonas syringae pv. tomato hijacks the Arabidopsis abscisic acid signalling pathway to cause disease. EMBO J 26:1434–1443

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dempsey DA, Vlot AC, Wildermuth MC, Klessig DF (2011) Salicylic acid biosynthesis and metabolism. Arabidopsis Book 9:e0156

    Article  PubMed  PubMed Central  Google Scholar 

  • Dempsey RW, Merchant A, Tausz M (2012) Differences in ascorbate and glutathione levels as indicators of resistance and susceptibility in Eucalyptus trees infected with Phytophthora cinnamomic. Tree Physiol 32:1148–1160

    Article  CAS  PubMed  Google Scholar 

  • Denancé N, Sánchez-Vallet A, Goffner D, Molina A (2013) Disease resistance or growth: the role of plant hormones in balancing immune responses and fitness costs. Front Plant Sci 4:155

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Dietz K-J, Turkan I, Krieger-Liszkay A (2016) Redox- and reactive oxygen species-dependent signalling into and out of the photosynthesizing chloroplast. Plant Physiol 171:1541–1550

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dixon DP, Skipsey M, Grundy NM, Edwards R (2005) Stress-induced protein S-glutathionylation in Arabidopsis. Plant Physiol 138:2233–2244

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dos Santos CV, Rey P (2006) Plant thioredoxins are key actors in the oxidative stress response. Trends Plant Sci 11:329–334

    Article  CAS  Google Scholar 

  • Doubnerová V, Ryšlavá H (2011) What can enzymes of C4 photosynthesis do for C3 plants under stress? Plant Sci 180:575–583

    Article  PubMed  CAS  Google Scholar 

  • Dubreuil-Maurizi C, Poinssot B (2012) Role of glutathione in plant signalling 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, defence gene expression, and the hypersensitive response. Plant Physiol 157:2000–2012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Durner J, Klessig DF (1995) Inhibition of ascorbate peroxidase by salicylic acid and 2,6-dichloroisonicotinic acid, two inducers of plant defence responses. Proc Natl Acad Sci U S A 92:11312–11316

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ellouzi H, Hamed KB, Hernández I, Cela J, Müller M, Magné C, Abdelly C, Munné-Bosch S (2014) A comparative study of the early osmotic, ionic, redox and hormonal signalling response in leaves and roots of two halophytes and a glycophyte to salinity. Planta 240:1299–1317

    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 

  • Fedoroff N (2006) Redox regulatory mechanisms in cellular stress responses. Ann Bot 98:289–300

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Finiti I, Leyva MO, Vicedo B, Gómez-Pastor R, López-Cruz J, García-Agustín P, Dolores Real M, González-Bosch C (2014) Hexanoic acid protects tomato plants against Botrytis cinerea by priming defence responses and reducing oxidative stress. Mol Plant Pathol 15:550–562

    Article  CAS  PubMed  Google Scholar 

  • Fotopoulos V, De Tullio MC, Barnes J, Kanellis AK (2008) Altered stomatal dynamics in ascorbate oxidase over-expressing tobacco plants suggest a role for dehydroascorbate signalling. J Exp Bot 59:729–737

    Article  CAS  PubMed  Google Scholar 

  • Foyer CH, Noctor G (2003) Redox sensing and signalling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. Physiol Plant 119:355–364

    Article  CAS  Google Scholar 

  • Foyer CH, Noctor G (2005) Oxidant and antioxidant signalling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. Plant Cell Environ 28:1056–1071

    Article  CAS  Google Scholar 

  • Foyer CH, Noctor G (2009) Redox regulation in photosynthetic organisms: signalling, acclimation, and practical implications. Antioxid Redox Signal 11:861–905

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 

  • Foyer CH, Karpinska B, Krupinska K (2014) The functions of WHIRLY1 and REDOX-RESPONSIVE TRANSCRIPTION FACTOR 1 in cross tolerance responses in plants: a hypothesis. Philos Trans R Soc Lond Ser B Biol Sci 369:20130226

    Article  CAS  Google Scholar 

  • Gabara B, Kuźniak E, Skłodowska M, Surówka E, Miszalski Z (2012) Ultrastructural and metabolic modifications at the plant–pathogen interface in Mesembryanthemum crystallinum leaves infected by Botrytis cinerea. Environ Exp Bot 77:33–43

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ghanta S, Dipto B, Ragini S, Anindita B, Sharmila C (2011) 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 

  • Gillham DJ, Dodge AD (1986) Hydrogen-peroxide-scavenging systems within pea chloroplasts. Planta 167:246–251

    Article  CAS  PubMed  Google Scholar 

  • Gilroy S, Suzuki N, Miller G, Choi W-G, Toyota M, Devireddy AR, Mittler R (2014) A tidal wave of signals: calcium and ROS at the forefront of rapid systemic signalling. Trends Plant Sci 19:623–630

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Govrin EM, Levine A (2000) The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea. Curr Biol 10:751–757

    Article  CAS  PubMed  Google Scholar 

  • Greenberg JT (1997) Programmed cell death in plant–pathogen interactions. Annu Rev Plant Physiol Plant Mol Biol 48:525–545

    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 defence in Arabidopsis against virulent and avirulent Pseudomonas syringae. Phytopathology 102:662–673

    Article  PubMed  CAS  Google Scholar 

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

    Chapter  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heyneke E, Luschin-Ebengreuth N, Krajcer I, Wolkinger V, Müller M, Zechmann B (2013) Dynamic compartment specific changes in glutathione and ascorbate levels in Arabidopsis plants exposed to different light intensities. BMC Plant Biol 13:104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hooijmaijers C, Rhee JY, Kwak KJ, Chung GC, Horie T, Katsuhara M, Kang H (2012) Hydrogen peroxide permeability of plasma membrane aquaporins of Arabidopsis thaliana. J Plant Res 125:147–153

    Article  CAS  PubMed  Google Scholar 

  • Horemans N, Foyer CH, Asard H (2000) Transport and action of ascorbate at the plant plasma membrane. Trends Plant Sci 5:263–267

    Article  CAS  PubMed  Google Scholar 

  • Hu X, Jiang M, Zhang A, Lu J (2005) Abscisic acid-induced apoplastic H2O2 accumulation up-regulates the activities of chloroplastic and cytosolic antioxidant enzymes in maize leaves. Planta 223:57–68

    Article  CAS  PubMed  Google Scholar 

  • Huang C, He W, Guo J, Chang X, Su P, Zhang L (2005) Increased sensitivity to salt stress in an ascorbate-deficient Arabidopsis mutant. J Exp Bot 56(422):3041–3049

    Article  CAS  PubMed  Google Scholar 

  • Kangasjärvi S, Neukermans J, Li S, Aro EM, Noctor G (2012) Photosynthesis, photorespiration, and light signalling in defence responses. J Exp Bot 63:1619–1636

    Article  PubMed  CAS  Google Scholar 

  • Khan MIR, Fatma M, Per TS, Anjum NA, Khan NA (2015) Salicylic acid-induced abiotic stress tolerance and underlying mechanisms in plants. Front Plant Sci 6:462

    PubMed  PubMed Central  Google Scholar 

  • Kissoudis C, van de Wiel C, Visser RGF, van der Linden G (2014) Enhancing crop resilience to combined abiotic and biotic stress through the dissection of physiological and molecular crosstalk. Front Plant Sci 5:207

    Article  PubMed  PubMed Central  Google Scholar 

  • Koh S, Andre A, Edwards H, Ehrhardt D, Somerville S (2005) Arabidopsis thaliana subcellular responses to compatible Erysiphe cichoracearum infections. Plant J 44:516–529

    Article  CAS  PubMed  Google Scholar 

  • Kombrink E, Schmelzer E (2001) The hypersensitive response and its role in local and systemic disease resistance. Eur J Plant Pathol 107:69–78

    Article  Google Scholar 

  • Kopczewski T, Kuźniak E (2013) Redox signals as a language of interorganellar communication in plant cells. Cent Eur J Biol 8:1153–1163

    CAS  Google Scholar 

  • Kuźniak E (2010) The ascorbate-glutathione cycle and related redox signals in plant-pathogen interactions. In: Anjum N, Umar S, Chan M-T (eds) Ascorbate-glutathione pathway and stress tolerance in plants. Springer, New York, pp 115–136

    Chapter  Google Scholar 

  • Kuźniak E, Skłodowska M (1999) The effect of Botrytis cinerea infection on ascorbate-glutathione cycle in tomato leaves. Plant Sci 148:69–76

    Article  Google Scholar 

  • Kuźniak E, Skłodowska M (2001) Ascorbate, glutathione and related enzymes in chloroplasts of tomato leaves infected by Botrytis cinerea. Plant Sci 160:723–731

    Article  PubMed  Google Scholar 

  • Kuźniak E, Skłodowska M (2004a) The effect of Botrytis cinerea infection on the antioxidant profile of mitochondria from tomato leaves. J Exp Bot 55:605–612

    Article  PubMed  Google Scholar 

  • Kuźniak E, Skłodowska M (2004b) 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 

  • Kuźniak E, Kornaś A, Gabara B, Ullrich C, Skłodowska M, Miszalski Z (2010) Interaction of Botrytis cinerea with the intermediate C3-CAM plant Mesembryanthemum crystallinum. Environ Exp Bot 69:137–147

    Article  CAS  Google Scholar 

  • Kuźniak E, Chojak J, Kopczewski T (2016) The interactions between abiotic and biotic stress responses: from cells to a whole plant. In: Book of Abstracts of 10th International Conference on Plant Functioning under Environmental Stress, Cracow, 16–19 September 2015. Acta Physiol Plant 38:17

    Google Scholar 

  • Laloi C, Mestres-Ortega D, Marco Y, Meyer Y, Reichheld J-P (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 

  • Lanubile A, Bernardi J, Marocco A, Logrieco A, Paciolla C (2012) Differential activation of defence genes and enzymes in maize genotypes with contrasting levels of resistance to Fusarium verticillioides. Environ Exp Bot 78:39–46

    Article  CAS  Google Scholar 

  • Leterrier M, Barroso JB, Palma JM, Corpas FJ (2012) Cytosolic NADP-isocitrate dehydrogenase in Arabidopsis leaves and roots. Biol Plant 56:705–710

    Article  CAS  Google Scholar 

  • Li J, Cao L, Staiger CJ (2017) Capping protein modulates actin remodeling in response to reactive oxygen species during plant innate immunity. Plant Physiol 173:1125–1136

    Article  CAS  PubMed  Google Scholar 

  • Luck J, Spackman M, Freeman A, Trębicki P, Griffiths W, Finlay K, Chakraborty S (2011) Climate change and diseases of crop foods. Plant Pathol 60:113–121

    Article  Google Scholar 

  • Luschin-Ebengreuth N, Zechmann B (2016) Compartment-specific investigations of antioxidants and hydrogen peroxide in leaves of Arabidopsis thaliana during dark-induced senescence. Acta Physiol Plant 38:133

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mateo A, Mühlenbock P, Rusterucci C, Chang CC-C, Miszalski Z, Karpinska B, Parker JE, Mullineaux PM, Karpinski S (2004) LESION SIMULATING DISEASE 1 is required for acclimation to conditions that promote excess excitation energy. Plant Physiol 136:2818–2830

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mellersh DG, Foulds IV, Higgins VJ, Heath MC (2002) H2O2 plays different roles in determining penetration failure in three diverse plant-fungal interactions. Plant J 29:257–268

    Article  CAS  PubMed  Google Scholar 

  • Mhamdi A, Mauve C, Gouia H, Saindrenan P, Hodges M, Noctor G (2010) Cytosolic NADP-dependent isocitrate dehydrogenase contributes to redox homeostasis and the regulation of pathogen responses in Arabidopsis leaves. Plant Cell Environ 33:1112–1123

    CAS  PubMed  Google Scholar 

  • Mhamdi A, Han Y, Noctor G (2013) Glutathione dependent phytohormone responses: teasing apart signalling and antioxidant functions. Plant Signal Behav 8:e24181

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mittler R (2006) Abiotic stress, the field environment and stress combination. Trends Plant Sci 11:15–19

    Article  CAS  PubMed  Google Scholar 

  • Mittler R (2017) ROS are good. Trends Plant Sci 22:11–19

    Article  CAS  PubMed  Google Scholar 

  • Mittler R, Feng X, Cohen M (1998) Post-transcriptional suppression of cytosolic ascorbate peroxidase expression during pathogen-induced programmed cell death in tobacco. Plant Cell 10:461–473

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mittler R, Herr EH, Orvar BL, Van Camp W, Willekens H, Inzé D, Ellis BE (1999) Transgenic tobacco plants with reduced capability to detoxify reactive oxygen intermediates are hyperresponsive to pathogen infection. Proc Natl Acad Sci 96:14165–14170

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mittler R, Vanderauwera S, Suzuki N, Miller G, Tognetti VB, Vandepoele K, Gollery M, Shulaev V, Van Breusegem F (2011) ROS signalling: the new wave? Trends Plant Sci 16:300–309

    Article  CAS  PubMed  Google Scholar 

  • Mittova V, Volokita M, Guy M, Tal M (2000) Activities of SOD and the ascorbate-glutathione cycle enzymes in subcellular compartments in leaves and roots of the cultivated tomato and its wild salt tolerant relative Lycopersicon pennellii. Physiol Plant 110:42–51

    Article  CAS  Google Scholar 

  • Miura K, Okamoto H, Okuma E, Shiba H, Kamada H, Hasegawa PM, Murata Y (2013) SIZ1 deficiency causes reduced stomatal aperture and enhanced drought tolerance via controlling salicylic acid-induced ROS accumulation in Arabidopsis. Plant J 73:91–104

    Article  CAS  PubMed  Google Scholar 

  • Miyake C, Asada K (1992) Thylakoid-bound ascorbate peroxidase in spinach chloroplasts and photoreduction of its primary oxidation product monodehydroascorbate radicals in thylakoids. Plant Cell Physiol 33:541–553

    CAS  Google Scholar 

  • Monteiro G, Bruno B, Horta D, Carvalho P, Ohara A, Netto LES (2007) Reduction of 1-Cys peroxiredoxins by ascorbate changes the thiol-specific antioxidant paradigm, revealing another function of vitamin C. Proc Natl Acad Sci U S A 104:4886–4891

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morell S, Follmann H, de Tullio M, Häberlein I (1997) Dehydroascorbate and dehydroascorbate reductase are phantom indicators of oxidative stress in plants. FEBS Lett 414:567–571

    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 

  • Mubarakshina MM, Ivanov BN, Naydov IA, Hillier W, Badger MR, Krieger-Liszkay A (2010) Production and diffusion of chloroplastic H2O2 and its implication to signalling. J Exp Bot 61:3577–3587

    Article  CAS  PubMed  Google Scholar 

  • Muckenschnabel I, Williamson B, Goodman BA, Lyon GD, Stewart D, Deighton N (2001) Markers of oxidative stress associated with soft rots in French beans (Phaseolus vulgaris) infected by Botrytis cinerea. Planta 212:376–381

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Mur LAJ, Brown IR, Darby RM, Bestwick CS, Bi YM, Mansfield JW, Draper J (2000) A loss of resistance to avirulent bacterial pathogens in tobacco is associated with the attenuation of a salicylic acid-potentiated oxidative burst. Plant J 23:609–623

    Article  CAS  PubMed  Google Scholar 

  • Mur LAJ, Kenton P, Draper J (2005) In planta measurements of oxidative bursts elicited by avirulent and virulent bacterial pathogens suggests that H2O2 is insufficient to elicit cell death in tobacco. Plant Cell Environ 28:548–561

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Nenova V, Bogoeva I (2014) Separate and combined effects of excess copper and Fusarium culmorum infection on growth and antioxidative enzymes in wheat (Triticum aestivum L.) plants. J Plant Interact 9:259–266

    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 signalling. Plant Physiol 171:1581–1592

    Article  CAS  PubMed  PubMed Central  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 

  • Noctor G, Mhamdi A, Queval G, Foyer CH (2013) Regulating the redox gatekeeper: vacuolar sequestration puts glutathione disulfide in its place. Plant Physiol 163:665–671

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Noctor G, Reichheld J-P, Foyer CH (2017) ROS-related redox regulation and signalling in plants. Semin Cell Dev Biol. https://doi.org/10.1016/j.semcdb.2017.07.013

  • Nosek M, Kornaś A, Kuźniak E, Miszalski Z (2015) Plastoquinone redox state modifies plant response to pathogen. Plant Physiol Biochem 96:163–170

    Article  CAS  PubMed  Google Scholar 

  • Nostar O, Ozdemir F, Bor M, Turkan I, Tosun N (2013) Combined effects of salt stress and cucurbit downy mildew (Pseudoperospora cubensis Berk. And Curt. Rostov.) infection on growth, physiological traits and antioxidant activity in cucumber (Cucumis sativus L.) seedlings. Physiol Mol Plant Pathol 83:84–92

    Article  CAS  Google Scholar 

  • Nyathi Y, Baker A (2006) Plant peroxisomes as a source of signalling molecules. Biochim Biophys Acta 1763:1478–1495

    Article  CAS  PubMed  Google Scholar 

  • Paciolla C, Paradiso A, de Pinto MC (2016) Cellular redox homeostasis as central modulator in plant stress response. In: Gupta DK, Palma JM, Corpas FJ (eds) Redox state as a central regulator of plant-cell stress responses. Springer, New York, pp 1–23

    Google Scholar 

  • Page M, Sultana N, Paszkiewicz K, Florance H, Smirnoff S (2012) The influence of ascorbate on anthocyanin accumulation during high light acclimation in Arabidopsis thaliana: further evidence for redox control of anthocyanin synthesis. Plant Cell Environ 35:388–404

    Article  CAS  PubMed  Google Scholar 

  • Pandey P, Ramegowda V, Senthil-Kumar M (2015) Shared and unique responses of plants to multiple individual stresses and stress combinations: physiological and molecular mechanisms. Front Plant Sci 6:723–737

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Pastori GM, Kiddle G, Antoniw J, Bernard S, Veljovic-Jovanovic S, Verrier PJ, Noctor G, Foyer CH (2003) Leaf vitamin C contents modulate plant defence transcripts and regulate genes controlling development through hormone signalling. Plant Cell 15:1212–1226

    Article  CAS  Google Scholar 

  • Pavet V, Olmos E, Kiddle G, Mowla S, Kumar S, Antoniw J, Alvarez ME, Foyer CH (2005) Ascorbic acid deficiency activates cell death and disease resistance responses in Arabidopsis. Plant Physiol 139:1291–1303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Perez IB, Brown PJ (2014) The role of ROS signalling in cross-tolerance:from model to crop. Front Plant Sci 5:754

    Article  PubMed  PubMed Central  Google Scholar 

  • Petrov VD, Van Breusegem F (2012) Hydrogen peroxide—a central hub for information flow in plant cells. AoB Plants 2012. https://doi.org/10.1093/aobpla/pls014

  • Pignocchi C, Foyer CH (2003) Apoplastic ascorbate metabolism and its role in the regulation of cell signalling. Curr Opin Plant Biol 6:379–389

    Article  CAS  PubMed  Google Scholar 

  • Pilon M, Ravet K, Tapken W (2011) The biogenesis and physiological function of chloroplast superoxide dismutases. Biochim Biophys Acta 1807:989–998

    Article  CAS  PubMed  Google Scholar 

  • Pogány M, von Rad U, Grün S, Dongó A, Pintye A, Simoneau P, Bahnweg G, Kiss L, Barna B, Durner J (2009) Dual roles of reactive oxygen species and NADPH oxidase RBOHD in an Arabidopsis-Alternaria pathosystem. Plant Physiol 151:1459–1479

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Polle A (2001) Dissecting the superoxide dismutase-ascorbate-glutathione-pathway in chloroplasts by metabolic modeling. Computer simulations as a step towards flux analysis. Plant Physiol 126:445–462

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qi J, Wang J, Gong Z, Zhou J-M (2017) Apoplastic ROS signalling in plant immunity. Curr Opin Plant Biol 38:92–100

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Ramegowda V, Senthil-Kumar M (2015) The interactive effects of simultaneous biotic and abiotic stresses on plants: mechanistic understanding from drought and pathogen combination. J Plant Physiol 176:47–54

    Article  CAS  PubMed  Google Scholar 

  • Rasmussen S, Barah P, Suarez-Rodriguez MC, Bressendorff S, Friis P, Costantino P, Bones AM, Nielsen HB, Mundy J (2013) Transcriptome responses to combinations of stresses in Arabidopsis. Plant Physiol 161:1783–1794

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rizhsky L, Hallak-Herr E, Van Breusegem F, Rachmilevitch S, Barr JE, Rodermel S, Inzé D, Mittler R (2002) Double antisense plants lacking ascorbate peroxidase and catalase are less sensitive to oxidative stress than single antisense plants lacking ascorbate peroxidase or catalase. Plant J 32:329–342

    Article  CAS  PubMed  Google Scholar 

  • Rouhier N, Lemaire S, Jacquot J-P (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 

  • Sappl PG, Carroll AJ, Clifton R, Lister R, Whelan J, Millar AH, Singh KB (2009) The Arabidopsis glutathione transferase gene family displays complex stress regulation and co-silencing of multiple genes results in altered metabolic sensitivity to oxidative stress. Plant J 58:53–68

    Article  CAS  PubMed  Google Scholar 

  • Satapathy P, Achary VMM, Panda BB (2012) Aluminum induced abiotic stress counteracts Fusarium infection in Cajanus cajan (L.) Millsp. J Plant Interact 7:121–128

    Article  CAS  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 

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

    Article  CAS  PubMed  Google Scholar 

  • Schnaubelt D, Queval G, Dong Y, Diaz-Vivancos P, Eugene Makgopa M, Howell G, De Simone A, Bai J, Hannah MA, Foyer CH (2015) Low glutathione regulates gene expression and the redox potentials of the nucleus and cytosol in Arabidopsis thaliana. Plant Cell Environ 38:266–279

    Article  CAS  PubMed  Google Scholar 

  • Sewelam N, Kazan K, Schenk PM (2016) Global plant stress signalling: reactive oxygen species at the cross-road. Front Plant Sci 7:187–208

    Article  PubMed  PubMed Central  Google Scholar 

  • Shapiguzov A, Vainonen JP, Wrzaczek M, Kangasjärvi J (2012) ROS-talk–how the apoplast, the chloroplast, and the nucleus get the message through. Front Plant Sci 3:292

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sharma P, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage, and antioxidative defence mechanism in plants under stressful conditions. J Bot 217037

    Google Scholar 

  • Shigeoka S, Maruta T (2014) Cellular redox regulation, signalling, and stress response in plants. Biosci Biotechnol Biochem 78:1457–1470

    Article  CAS  PubMed  Google Scholar 

  • Shigeoka S, Ishikawa T, Tamoi M, Miyagawa Y, Takeda T, Yabuta Y, Yoshimura K (2002) Regulation and function of ascorbate peroxidase isoenzymes. J Exp Bot 53:1305–1319

    Article  CAS  PubMed  Google Scholar 

  • Suzuki N (2016) Hormone signalling pathways under stress combinations. Plant Signal Behav 11:e1247139

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Suzuki N, Rivero RM, Shulaev V, Blumwald E, Mittler R (2014) Abiotic and biotic stress combinations. New Phytol 203:32–43

    Article  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(5891):952

    Article  CAS  PubMed  Google Scholar 

  • Takahama U (2004) Oxidation of vacuolar and apoplastic phenolic substrates by peroxidase: physiological significance of the oxidation reactions. Phytochem Rev 3:207–219

    Article  CAS  Google Scholar 

  • Tian S, Wang XB, Li P, Wang H, Ji HT, Xie JY, Qiu QL, Shen D, Dong HS (2016) Plant aquaporin AtPIP1;4 links apoplastic H2O2 induction to disease immunity pathways. Plant Physiol 171:1635–1650

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Torres MA, Jones JD, Dangl JL (2006) Reactive oxygen species signalling in response to pathogens. Plant Physiol 141:373–378

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trotta A, Rahikainen M, Konert G, Finazzi G, Kangasjärvi S (2014) Signalling crosstalk in light stress and immune reactions in plants. Phil Trans R Soc Lond B Biol Sci 369:e20130235

    Article  CAS  Google Scholar 

  • Vanacker H, Carver TL, 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 

  • Wang S-D, Zhu F,·Yuan S,·Yang H,·Xu F, Shang J, Xu M-Y,·Jia S-D,·Zhang Z-W,·Wang J-H,·Xi D-H,·Lin H-H (2011) The roles of ascorbic acid and glutathione in symptom alleviation to SA-deficient plants infected with RNA viruses. Planta 234:171–181

    Article  CAS  PubMed  Google Scholar 

  • Wiese J, Kranz T, Schubert S (2004) Induction of pathogen resistance in barley by abiotic stress. Plant Biol 6:529–536

    Article  CAS  PubMed  Google Scholar 

  • Willekens H, Chamnongpol S, Davey M, Schraudner M, Langebartels C, Van Montagu M, Inzé D, Van Camp W (1997) Catalase is a sink for H2O2 and is indispensable for stress defence in C3 plants. EMBO J 16(16):4806

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wojtaszek P (1997) Oxidative burst: an early plant response to pathogen infection. Biochem J 332:681–692

    Article  Google Scholar 

  • Wrzaczek M, Brosché M, Salojärvi J, Kangasjärvi S, Idänheimo N, Mersmann S, Robatzek S, Karpinski S, Karpinska B, Kangasjärvi J (2010) Transcriptional regulation of the CRK/DUF26 group of receptor-like protein kinases by ozone and plant hormones in Arabidopsis. BMC Plant Biol 10:1–19

    Article  CAS  Google Scholar 

  • Wu Y, Zhang D, Chu JY, Boyle P, Wang Y, Brindle ID, De Luca V, Després C (2012) The Arabidopsis NPR1 protein is a receptor for the plant defence hormone salicylic acid. Cell Rep 1:639–647

    Article  CAS  PubMed  Google Scholar 

  • Xia X-J, Zhou Y-H, Shi K, Zhou J, Foyer CH, J-Q Y (2015) Interplay between reactive oxygen species and hormones in the control of plant development and stress tolerance. J Exp Bot 66:2839–2856

    Article  CAS  PubMed  Google Scholar 

  • Yabuta Y, Maruta T, Nakamura A, Mieda T, Yoshimura K, Ishikawa T, Shigeoka S (2008) Conversion of L-galactono-1,4-lactone to L-ascorbate is regulated by the photosynthetic electron transport chain in Arabidopsis. Biosci Biotechnol Biochem 72:2598–2607

    Article  CAS  PubMed  Google Scholar 

  • You MP, Colmer TD, Barbetti MJ (2011) Salinity drives host reaction in Phaseolus vulgaris (common bean) to Macrophomina phaseolina. Funct Plant Biol 38:984–992

    Article  CAS  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, Urbanek-Krajnc A, Müller M (2007) Artificial elevation of glutathione affects symptom development in ZYMV-infected Cucurbita pepo L. plants. Arch Virol 152:747–762

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zechmann B, Stumpe M, Mauch F (2011) Immunocytochemical determination of the subcellular distribution of ascorbate in plants. Planta 233:1–12

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y (2013) Biological role of ascorbate in plants. In: Ascorbic acid in plants, Springer briefs in plant science. Springer, New York, pp 7–33

    Chapter  Google Scholar 

  • Zhou JM, Trifa Y, Silva H, Pontier D, Lam E, Shah J, Klessig DF (2000) NPR1 differentially interacts with members of the TGA/OBF family of transcription factors that bind an element of the PR-1 gene required for induction by salicylic acid. Mol Plant-Microbe Interact 13:191–202

    Article  CAS  PubMed  Google Scholar 

  • Zurbriggen MD, Carrillo N, Tognetti VB, Melzer M, Peisker M, Hause B, Hajirezaei MR (2009) Chloroplast-generated reactive oxygen species play a major role in localized cell death during the non-host interaction between tobacco and Xanthomonas campestris pv. vesicatoria. Plant J 60:962–973

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by Grants No. 2013/11/N/NZ9/00116 (T. K.) and No. 2012/07/N/NZ9/00041(J. Ch-K.) from the National Science Centre (NCN, Poland).

Author information

Authors and Affiliations

  1. Department of Plant Physiology and Biochemistry, Faculty of Biology and Environmental Protection, University of Lodz, Lodz, Poland

    Elżbieta Kuźniak, Tomasz Kopczewski & Joanna Chojak-Koźniewska

  2. Genetically Modified Organisms Controlling Laboratory, Plant Breeding and Acclimatization Institute – National Research Institute, Błonie, Poland

    Joanna Chojak-Koźniewska

Authors
  1. Elżbieta Kuźniak
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tomasz Kopczewski
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Joanna Chojak-Koźniewska
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Elżbieta Kuźniak .

Editor information

Editors and Affiliations

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

    Mohammad Anwar Hossain

  2. Department of Evolutionary Biology, Ecology and Environmental Sciences, University of Barcelona, Barcelona, Spain

    Sergi Munné-Bosch

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

    David J. Burritt

  4. Department of Plant Biology, University of Murcia, Espinardo, Murcia, Spain

    Pedro Diaz-Vivancos

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

    Masayuki Fujita

  6. Arkansas Biosciences Institute, Arkansas State University, Jonesboro, Arkansas, USA

    Argelia Lorence

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing AG, part of Springer Nature

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Kuźniak, E., Kopczewski, T., Chojak-Koźniewska, J. (2017). Ascorbate-Glutathione Cycle and Biotic Stress Tolerance in Plants. In: Hossain, M., Munné-Bosch, S., Burritt, D., Diaz-Vivancos, P., Fujita, M., Lorence, A. (eds) Ascorbic Acid in Plant Growth, Development and Stress Tolerance. Springer, Cham. https://doi.org/10.1007/978-3-319-74057-7_8

Download citation

Publish with us

Policies and ethics

Search

Navigation