Skip to main content

Ascorbate-Glutathione Cycle and Abiotic Stress Tolerance in Plants

  • Chapter
  • First Online:

Abstract

Plants confront fluctuating and in some cases intense environmental conditions, such as changes in irradiation, water availability, extreme temperatures, mineral nutrient accessibility, and air pollutants exposition among others. In order to face abiotic stress situations, the redox buffer capacity, mainly represented by ascorbic acid (AsA) and glutathione (GSH) pools, is involved in growth–stress responses crossroad. These compounds are associated in a set of reactions known as AsA-GSH cycle. The main function of the AsA-GSH cycle originally observed was the detoxification of reactive oxygen species (ROS) in different subcellular compartments such as chloroplast, mitochondria, or cytosol. More recently, the crucial participation of the AsA-GSH cycle in the optimization of photosynthesis was established. In addition, these antioxidants are considered essential components of cell signaling pathways triggering adaptive plant responses. The role of AsA-GSH cycle is analyzed regarding the ability of plants to overcome some selected abiotic stress situations.

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

Buying options

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

  • Acosta-Motos J, Ortuño M, Bernal-Vicente A, Diaz-Vivancos P, Sanchez-Blanco M, Hernandez JA (2017) Plant responses to salt stress: adaptive mechanisms. Agronomy 7:18

    Article  Google Scholar 

  • Ames BN, Shigenaga MK, Hagen TM (1993) Oxidants, antioxidants, and the degenerative diseases of aging. Proc Natl Acad Sci U S A 90:7915–7922

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aono M, Kubo A, Saji H, Tanaka K, Kondo N (1993) Enhanced tolerance to photooxidative stress of transgenic Nicotiana tabacum with high chloroplast glutathione reductase activity. Plant Cell Physiol 34:129–135

    CAS  Google Scholar 

  • Aono M, Saji H, Sakamoto A, Tanaka K, Kondo N, Tanaka K (1995) Paraquat tolerance of transgenic Nicotiana tabacum with enhanced activities of glutathione reductase and superoxide dismutase. Plant Cell Physiol 36:1687–1691

    Google Scholar 

  • Asada K, Takahashi M (1987) Production and scavenging of active oxygen species in photosynthesis. In: Kyle DJ, Osmond CB, Arntzen CJ (eds) Photoinhibition. Elsevier Science Publishers, Amsterdam, pp 227–287

    Google Scholar 

  • Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol 141:391–396

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Asard H, Kapila J, Verelst W, Bérczi A (2001) Higher-plant plasma membrane cytochrome b561: a protein in search of a function. Protoplasma 217:77–93

    Article  CAS  PubMed  Google Scholar 

  • Baldet P, Bres C, Okabe Y, Mauxion JP, Just D, Bournonville C, Ferrand C, Mori K, Ezure H, Rothan C (2013) Investigating the role of vitamin C in tomato through TILLING identification of ascorbate-deficient tomato mutants. Plant Biotechnol 30:308–314

    Article  CAS  Google Scholar 

  • Bartoli CG, Gómez F, Martínez DE, Guiamet JJ (2004) Mitochondria are the main target for oxidative damage in leaves of wheat (Triticum aestivum L.) J Exp Bot 55:1663–1669

    Article  CAS  PubMed  Google Scholar 

  • Bartoli CG, Tambussi EA, Fanello DD, Foyer CH (2009) Control of ascorbic acid synthesis and accumulation by the incident light red/far red ratio in Phaseolus vulgaris leaves. FEBS Lett 583:118–122

    Article  CAS  PubMed  Google Scholar 

  • Ben Rejeb K, Benzarti M, Debez A, Bailly C, Savouré A, Abdelly C (2015) NADPH oxidase-dependent H2O2 production is required for salt-induced antioxidant defense in Arabidopsis thaliana. J Plant Physiol 174:5–15

    Article  CAS  PubMed  Google Scholar 

  • Bhattachrjee S (2005) Reactive oxygen species and oxidative burst: roles in stress, senescence and signal transducation in plants. Curr Sci 89:1113–1121

    Google Scholar 

  • Boyer JS (1982) Plant productivity and environment. Science 218:443–448

    Article  CAS  PubMed  Google Scholar 

  • Bratt CE, Arvidsson P-O, Carlsson M, Akerlund H-E (1995) Regulation of violaxanthin de-epoxidase activity by pH and ascorbate concentration. Photosynth Res 45:169–175

    Article  CAS  PubMed  Google Scholar 

  • Britsch L, Grisebach H (1986) Purification and characterization of (2S)-flavanone-3-hydroxylase from Petunia hybrida. Eur J Biochem 156:569–577

    Article  CAS  PubMed  Google Scholar 

  • Britsch L, Heller W, Grisebach H (1981) Conversion of flavanone to flavone, dihydroflavonol and flavonol with an enzyme system from cell cultures of parsley. Z Naturforsch 36:742–750

    Google Scholar 

  • Britsch L (1990) Purification and characterization of flavone synthase I, a 2-oxoglutarate-dependent desaturase. Arch Biochem Biophys 282:152–160

    Article  CAS  PubMed  Google Scholar 

  • Buchner P, Takahashi H, Hawkesford MJ (2004) Plant sulphate transporters: co-ordination of uptake, intracellular and long-distance transport. J Exp Bot 55:1765–1773

    Article  CAS  PubMed  Google Scholar 

  • Buet A, Simontacchi M (2015) Nitric oxide and plant iron homeostasis. Ann N Y Acad Sci 1340:39–46

    Article  CAS  PubMed  Google Scholar 

  • Buettner G, Schafer F (2006) Albert Szent-Györgyi: vitamin C identification. Biochemist 28:31–33

    CAS  Google Scholar 

  • Bulley SM, Rassam M, Hoser D, Otto W, Schünemann N, Wright M, MacRae E, Gleave A, Laing W (2009) Gene expression studies in kiwifruit and gene over-expression in Arabidopsis indicates that GDP-L-galactoseguanyltransferase is a major control point of vitamin C biosynthesis. J Exp Bot 60:765–778

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen Z, Young TE, Ling J, Chang SC, Gallie DR (2003) Increasing vitamin C content of plants through enhanced ascorbate recycling. Proc Natl Acad Sci U S A 100:3525–3530

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen Z, Gallie DR (2005) Increasing tolerance to ozone by elevating foliar ascorbic acid confers greater protection against ozone than increasing avoidance. Plant Physiol 138:1673–1689

    Article  CAS  PubMed  PubMed Central  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 

  • Cisneros-Zevallos L (2003) The use of controlled postharvest abiotic stress as a tool for enhancing the nutraceutical content and adding-value of fresh fruits and vegetables. J Food Sci 68:1560–1565

    Article  CAS  Google Scholar 

  • Costa L, Vicente AR, Civello PM, Chaves AR, Martínez GA (2006) UV-C treatment delays postharvest senescence in broccoli florets. Postharvest Biol Technol 39:204–210

    Article  CAS  Google Scholar 

  • Cushman JC, Bohnert HJ (2000) Genomic approaches to plant stress tolerance. Curr Opin Plant Biol 3:117–124

    Article  CAS  PubMed  Google Scholar 

  • Dat JF, Foyer CH, Scott IM (1998a) Changes in salicylic acid and antioxidants during induced thermotolerance in mustard seedlings. Plant Physiol 118:1455–1461

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dat JF, Lopez-Delgado H, Foyer CH, Scott IM (1998b) Parallel changes in H2O2 and catalase during thermotolerance induced by salicylic acid or heat acclimation in mustard seedlings. Plant Physiol 116:1351–1357

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • De Simone A, Hubbard R, Viñegra de la Torre N, Velappan Y, Wilson M, Considine MJ, WJJ S, Foyer CH (2017) Redox changes during the cell cycle in the embryonic root meristem of Arabidopsis Thaliana. Antioxid Redox Signal 27(18):1505–1519. https://doi.org/10.1089/ars.2016.6959

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • De Tullio MC, Paciolla C, DallaVecchia F, Rascio N, D’Emerico S, De Gara L, Liso R, Arrigoni O (1999) Changes in onion root development induced by the inhibition of peptidyl-prolyl hydroxylase and influence of the ascorbate system on cell division and elongation. Planta 209:424–434

    Article  PubMed  Google Scholar 

  • Demmig-Adams B, Adams WW (1996) The role of xanthophyll cycle carotenoids in the protection of photosynthesis. Trends Plant Sci 1:21–26

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Diaz-Vivancos P, Dong Y, Ziegler K, Markovic J, Pallardó FV, Pellny TK, Verrier PJ, Foyer CH (2010) 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 

  • Distéfano AM, Martin MV, Córdoba JP, Bellido AM, D’Ippólito S, Colman SL, Soto D, Roldán JA, Bartoli CG, Zabaleta EJ, Fiol DF, Stockwell BR, Dixon SJ, Pagnussat GC (2017) Heat stress induces ferroptosis-like cell death in plants. J Cell Biol 216:463–476

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dixon DP, Cummins I, Cole DJ, Edwards R (1998) Glutathione-mediated detoxification systems in plants. Curr Opin Plant Biol 1:258–266

    Article  CAS  PubMed  Google Scholar 

  • Duan M, Ma N-N, Li D, Deng Y-S, Kong F-Y, Lv W, Meng Q-W (2012) Antisense-mediated suppression of tomato thylakoidal ascorbate peroxidase influences anti-oxidant network during chilling stress. Plant Physiol Biochem 58:37–45

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Eltelib HA, Fujikawa Y, Esaka M (2012) Overexpression of the acerola (Malpighia glabra) monodehydroascorbatereductase gene in transgenic tobacco plants results in increased ascorbate levels and enhanced tolerance to salt stress. S Afr J Bot 78:295–301

    Article  CAS  Google Scholar 

  • Erkan M, Wang SY, Wang CY (2008) Effect of UV treatment on antioxidant capacity, antioxidant enzyme activity and decay in strawberry fruit. Postharvest Biol Technol 48:163–171

    Article  CAS  Google Scholar 

  • Fankhauser H, Brunold C (1978) Localization of adenosine 5′-phosphosulfate sulfotransferase in spinach leaves. Planta 143:285–289

    Article  CAS  PubMed  Google Scholar 

  • Ferretti M, Destro T, Tosatto SCE, La Rocca N, Rascio N, Masi A (2009) Gamma-glutamyltransferase in the cell wall participates in extracellular glutathione salvage from the root apoplast. New Phytol 181:115–126

    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, Halliwell B (1976) The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133:21–25

    Article  CAS  PubMed  Google Scholar 

  • Foyer CH, Lelandais M, Galap C, Kunert KJ (1991) Effects of elevated cytosolic glutathione reductase activity on the cellular glutathione pool and photosynthesis in leaves under normal and stress conditions. Plant Physiol 97:863–872

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Foyer CH, Lelandais M (1996) A comparison of the relative rates of transport of ascorbate and glucose across the thylakoid, chloroplast and plasmalemma membranes of pea leaf mesophyll cells. J Plant Physiol 148:391–398

    Article  CAS  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, Noctor G (2009) Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxid Redox Signal 11:865–905

    Article  CAS  Google Scholar 

  • Foyer CH, Noctor G (2016) Stress-triggered redox signaling: what’s in pROSpect? Plant Cell Environ 39:951–964

    Article  CAS  PubMed  Google Scholar 

  • Foyer CH, Ruban AV, Noctor G (2017) Viewing oxidative stress through the lens of oxidative signaling rather than damage. Biochem J 474:877–883

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Foyer CH, Souriau N, Perret S, Lelandais M, Kunert KJ, Pruvost C, Jouanin L (1995) Overexpression of glutathione reductase but not glutathione synthetase leads to increases in antioxidant capacity and resistance to photoinhibition in poplar trees. Plant Physiol 109:1047–1057

    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 

  • Franceschi VR, Tarlyn NM (2002) L-Ascorbic acid is accumulated in source leaf phloem and transported to sink tissues in plants. Plant Physiol 130:649–656

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Frendo P, Harrison J, Norman C, Hernandez Jimenez MJ, Van de Sype G, Gilabert A, Puppo A (2005) Glutathione and homoglutathione play a critical role in the nodulation process of Medicago truncatula. Mol Plant-Microbe Interact 18:254–259

    Article  CAS  PubMed  Google Scholar 

  • Gapper NE, McQuinn RP, Giovaninni JJ (2013) Molecular and genetic regulation of fruit ripening. Plant Mol Biol 82:575–591

    Article  CAS  PubMed  Google Scholar 

  • Gergoff Grozeff G, Bartoli CG (2014) Participation of ascorbic acid in the dormancy establishment of poplar lateral branch buds. J Forest Res 19:301–304

    Article  CAS  Google Scholar 

  • Gómez F, Fernández L, Gergoff G, Guiamet JJ, Chaves A, Bartoli CG (2008) Heat shock increases mitochondrial H2O2 production and extends postharvest life of spinach leaves. Postharvest Biol Technol 49:229–234

    Article  CAS  Google Scholar 

  • Griesen D, Su D, Bérczi A, Asard H (2004) Localization of an ascorbate-reducible cytochrome b561 in the plant tonoplast. Plant Physiol 134:726–734

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Groden D, Beck E (1979) H2O2 destruction by ascorbate-dependent systems from chloroplasts. Biochim Biophys Acta 546:426–435

    Article  CAS  PubMed  Google Scholar 

  • Gutierrez-Alcala G, Gotor C, Meyer AJ, Fricker M, Vega JM, Romero LC (2000) Glutathione biosynthesis in Arabidopsis trichome cells. Proc Natl Acad Sci U S A 97:11108–11113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hagen SF, Borge GIA, Bengtsson GB, Bilger W, Berge A, Haffner K, Solhaug KA (2007) Phenolic contents and other health and sensory related properties of apple fruit (Borkh., cv. Aroma): effect of postharvest UV-B irradiation. Postharvest Biol Technol 45:1–10

    Article  CAS  Google Scholar 

  • Hager A, Holocher K (1994) Localization of the xanthophyll-cycle enzyme violaxanthin de-epoxidase within the thylakoid lumen and abolition of its mobility by a (light-dependent) pH decrease. Planta 192:581–589

    Article  CAS  Google Scholar 

  • Hancock RD, McRae D, Haupt S, Viola R (2003) Synthesis of L-ascorbic acid in the phloem. BMC Plant Biol 3:7

    Article  PubMed  PubMed Central  Google Scholar 

  • Horemans N, Asard H, Caubergs RJ (1998) Carrier mediated uptake of dehydroascorbate into higher plant plasma membrane vesicles shows trans-stimulation. FEBS Lett 421:41–44

    Article  CAS  PubMed  Google Scholar 

  • Horemans N, Asard H, Caubergs RJ (1997) The ascorbate carrier of higher plant plasma membranes preferentially translocates the fully oxidized (dehydroascorbate) molecule. Plant Physiol 114:1247–1253

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Horemans N, Asard H, Caubergs RJ (1994) The role of ascorbate free radical as an electron acceptor to cytochrome b-mediated trans-plasma membrane electron transport in higher plants. Plant Physiol 104:1455–1458

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hunter G, Eagles BA (1926) Glutathione. A critical study. J Biol Chem 72:147

    Google Scholar 

  • Jagadeesh SL, Charles MT, Gariépy Y, Goyette B, Raghavan VGS, Vigneault C (2011) Influence of postharvest UV-C hormesis on the bioactive components of tomato during post-treatment handling. Food Bioprocess Technol 4:1463–1472

    Article  CAS  Google Scholar 

  • Jahns P, Holzwarth AR (2012) The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II. Biochim Biophys Acta 2012:182–193

    Article  CAS  Google Scholar 

  • Jiménez A, Hernández JA, del Río LA, Sevilla F (1997) Evidence for the presence of the ascorbate-glutathione cycle in mitochondria and peroxisomes of pea leaves. Plant Physiol 114:275–284

    Article  PubMed  PubMed Central  Google Scholar 

  • Jocelyn PC (1972) Biochemistry of the thiol group. Academic Press, New York

    Google Scholar 

  • Jones MA, Raymong MJ, Yang Z, Smirnoff N (2007) NADPH oxidase-dependent reactive oxygen species formation required for root hair growth depends onROP GTPase. J Exp Bot 58:1261–1270

    Article  CAS  PubMed  Google Scholar 

  • Jubany-Mari T, Alegre-Batlle L, Jiang K, Feldman LJ (2010) Use of a redox-sensing GFP (c-roGFP1) for real-time monitoring of cytosol redox status in Arabidopsis thaliana water-stressed plants. FEBS Lett 584:889–897

    Article  CAS  PubMed  Google Scholar 

  • Kangasjärvi S, Lepistö A, Hännikäinen K, Piippo M, Luomala E-M, Aro E-M, Rintamäki E (2008) Diverse roles for chloroplast stromal and thylakoid-bound ascorbate peroxidases in plant stress responses. Biochem J 412:275–285

    Article  PubMed  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. Biochemie 10:1321–1329

    Article  CAS  Google Scholar 

  • Kerchev PI, Pellny TK, Vivancos PD, Kiddle G, Hedden P, Driscoll S, Vanacker H, Verrier PJ, Hancock RD, Foyer CH (2011) The transcription factor ABI-4 is required for the ascorbic acid- dependent regulation of growth and regulation of jasmonate-dependent defense signaling pathways in Arabidopsis. Plant Cell 23:3319–3334

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krueger S, Donath A, Lopez-Martin MC, Hoefgen R, Gotor C, Hesse H (2010) Impact of sulphur starvation on cysteine biosynthesis in T-DNA mutants deficient for compartment-specific serine-acetyltransferase. Amino Acids 39:1029–1042

    Article  CAS  PubMed  Google Scholar 

  • Kuźniak E, Kaźmierczak A, Wielanek M, Głowacki R, Kornas A (2013) Involvement of salicylic acid, glutathione and protein S-thiolation in plant cell death-mediated defence response of Mesembryanthemum crystallinum against Botrytis cinerea. Plant Physiol Biochem 63:30–38

    Article  PubMed  CAS  Google Scholar 

  • Kwak JM, Mori I, Pei Z-M, Leonhardt N, Torres MA, Dangl JL, Bloom RE, Bodde S, Jones JDG, Schroeder JI (2003) NADPH oxidase AtrbohD and AtrbohF genesfunction in ROS-dependent ABA signaling. EMBO J 22:2623–2633

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kwon SY, Choi SM, Ahn YO, Lee HS, Lee HB, Park YM, Kwak SS (2003) Enhanced stress-tolerance of transgenic tobacco plants expressing a human dehydroascorbatereductase gene. J Plant Physiol 160:347–353

    Article  CAS  PubMed  Google Scholar 

  • Labrou NE, Karavangeli M, Tsaftaris A, Clonis YD (2005) Kinetic analysis of maize glutathione S-transferase I catalysing the detoxification from chloroacetanilide herbicides. Planta 222:91–97

    Article  CAS  PubMed  Google Scholar 

  • Lange T (1994) Purification and partial amino-acid sequence of gibberellin 20-oxidase from Cucurbita maxima L. endosperm. Planta 195:108–115

    Google Scholar 

  • Larkindale J, Knight MR (2002) Protection against heat stress-induced oxidative damage in Arabidopsis involves calcium, abscisic acid, ethylene, and salicylic acid. Plant Physiol 128:682–695

    Article  CAS  PubMed  PubMed Central  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 

  • Lim B, Paternak M, Meyer AJ, Cobbett CS (2014) Restricting glutamycysteinesynthetase activity to the cytosol or glutathione biosynthesis to the plastids is sufficient for normal plant development and stress tolerance. Plant Biol 16:58–67

    Article  CAS  PubMed  Google Scholar 

  • Liu W, An H-M, Yang M (2013) Overexpression of Rosa roxburghii l-galactono-1,4-lactone dehydrogenase in tobacco plant enhances ascorbate accumulation and abiotic stress tolerance. Acta Physiol Plant 35:1617–1624

    Article  CAS  Google Scholar 

  • Lorence A, Nessler CL (2007) Chapter 8: Pathway engineering of the plant vitamin C metabolic network. In: Verpoorte R, Alfermann AW, Johnson TS (eds) Applications of plant metabolic engineering. Springer, The Netherlands, pp 197–217

    Chapter  Google Scholar 

  • Lyndermayr C, Saalbach G, Durner J (2005) Proteomic identification of S-nitrosylated proteins in Arabidopsis. Plant Physiol 137:921–930

    Article  CAS  Google Scholar 

  • Ma L, Zhang H, Sun L, Jiao Y, Zhang G, Miao C, Hao F (2012) NADPH oxidase AtrbohD and AtrbohF function in ROS-dependent regulation of Na+/K+ homeostasis in Arabidopsis under salt stress. J Exp Bot 63:305–317

    Article  CAS  PubMed  Google Scholar 

  • Marschner P (2012) Chapter 3: Marschner’s mineral nutrition of higher plants, 3rd edn. Elsevier, San Diego, pp 49–70

    Google Scholar 

  • Maughan S, Foyer CH (2006) Engineering and genetic approaches to modulating the glutathione network in plants. Physiol Plant 126:382–397

    Article  CAS  Google Scholar 

  • Mendoza-Cózatl DG, Jobe TO, Hauser F, Schroeder JI (2011) Long-distance transport, vacuolar sequestration and transcriptional responses induced by cadmium and arsenic. Curr Opin Plant Biol 14:554–562

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Menon SG, Goswami PC (2007) A redox cycle within the cell cycle: ring in the old with the new. Oncogene 26:1101–1109

    Article  CAS  PubMed  Google Scholar 

  • Meyer AJ, Brach T, Marty L, Kreye S, Rouhier N, Jacquot JP, Hell R (2007) Redox-sensitive GFP in Arabidopsis thaliana is a quantitative biosensor for the redox potential of the cellular glutathione redox buffer. Plant J 52:973–986

    Article  CAS  PubMed  Google Scholar 

  • Mhamdi A, Queval G, Chaouch S, Vanderauwera S, Van Breusegem F, Noctor G (2010) Catalase function in plants: a focus on Arabidopsis mutants as stress-mimic models. J Exp Bot 61:4197–4220

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    Article  CAS  PubMed  Google Scholar 

  • Miyaji T, Kuromori T, Takeuchi Y, Yamaji N, Yokosho K, Shimazawa A, Sugimoto E, Omote H, Ma JF, Shinozaki K, Moriyama Y (2015) AtPHT4;4 is a chloroplast-localized ascorbate transporter in Arabidopsis. Nature 6:5928

    CAS  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 

  • Møller IM, Jensen PE, Hansson A (2007) Oxidative modifications to cellular components in plants. Annu Rev Plant Biol 58:459–481

    Article  PubMed  CAS  Google Scholar 

  • Mozafar A, Oertli JJ (1993) Vitamin C (ascorbic acid): uptake and metabolism by soybean. J Plant Physiol 141:316–321

    Article  CAS  Google Scholar 

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880

    CAS  Google Scholar 

  • Nanasato Y, Akashi K, Yokota A (2005) Co-expression of cytochrome b561 and ascorbate oxidase in leaves of wild watermelon under drought and high light conditions. Plant Cell Physiol 46:1515–1524

    Article  CAS  PubMed  Google Scholar 

  • Nelson DE, Rammesmayer G, Bohnert HJ (1998) Regulation of cell-specific inositol metabolism and transport in plant salinity tolerance. Plant Cell 10:753–764

    CAS  PubMed  PubMed Central  Google Scholar 

  • Noctor G, Mhamdi A, Foyer CH (2016) Oxidative stress and antioxidative systems: recipes for successful data collection and interpretation. Plant Cell Environ 39:1140–1160

    Article  CAS  PubMed  Google Scholar 

  • Noctor G, Mhamdi A, Foyer CH (2014) The roles of reactive oxygen metabolism in drought: not so cut and dried. Plant Physiol 164:1636–1648

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

  • 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 

  • Pastori GM, Kiddle G, Antoniw J, Bernard S, Veljovic-Jovanovic S, Verrier PJ, Noctor G, Foyer CH (2003) Leaf vitamin C contents modulate plant defense transcripts and regulate genes that control development through hormone signaling. Plant Cell 15:939–951

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pedreschi R, Lurie S (2015) Advances and current challenges in understanding postharvest abiotic stresses in perishables. Postharvest Biol Technol 107:77–89

    Article  Google Scholar 

  • Pignocchi C, Fletcher JM, Wilkinson JE, Barnes JD, Foyer CH (2003) The function of ascorbate oxidase in tobacco. Plant Physiol 132:1631–1641

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pignocchi C, Kiddle G, Hernández I, Foster SJ, Asensi A, Taybi T, Barnes J, Foyer CH (2006) Ascorbate oxidase-dependent changes in the redox state of the apoplast modulate gene transcript accumulation leading to modified hormone signaling and orchestration of defense processes in tobacco. Plant Physiol 141:423–435

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Podgórska A, Burian M, Szal B (2017) Extra-cellular but extra-ordinarily important for cells: apoplastic reactive oxygen species metabolism. Front Plant Sci 8:1353

    Article  PubMed  PubMed Central  Google Scholar 

  • Prescott AG, John P (1996) DIOXYGENASES: molecular structure and role in plant metabolism. Annu Rev Plant Physiol Plant Mol Biol 47:245–271

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Ramirez L, Simontacchi M, Murgia I, Zabaleta E, Lamattina L (2011) Nitric oxide, nitrosyl iron complexes, ferritin and frataxin: a well equipped team to preserve plant iron homeostasis. Plant Sci 181:582–592

    Article  CAS  PubMed  Google Scholar 

  • Rennenberg H, Herschbach C (2014) A detailed view on sulphur metabolism at the cellular and whole-plant level illustrates challenges in metabolite flux analyses. J Exp Bot 65:5711–5724

    Article  CAS  PubMed  Google Scholar 

  • Richardson DR, Lok HC (2008) The nitric oxide-iron interplay in mammalian cells: transport and storage storage of dinitrosyl iron complexes. Biochim Biophys Acta 1780:638–651

    Article  CAS  PubMed  Google Scholar 

  • Saito K, Kobayashi M, Gong Z, Tanaka Y, Yamazaki M (1999) Direct evidence for anthocyanidin synthase as a 2-oxoglutarate-dependent oxygenase: molecular cloning and functional expression of cDNA from a red forma of Perillafrutescens. Plant J 17:181–189

    Article  PubMed  Google Scholar 

  • Sakamoto M, Munemura I, Tomita R, Kobayashi K (2008) Involvement of hydrogen peroxide in leaf abscissionsignaling, revealed by analysis with an in vitro abscissionsystem in Capsicum plants. Plant J 56:13–27

    Article  CAS  PubMed  Google Scholar 

  • Santolini J, André F, Jeandroz S, Wendehenne D (2017) Nitric oxide nitric oxide synthase in plants: where do we stand? Nitric Oxide 63:30–38

    Article  CAS  PubMed  Google Scholar 

  • Schippers JHM, Foyer CH, van Dongen JT (2016) Redox regulation in shoot growth, SAM maintenance and flowering. Curr Opin Plant Biol 29:121–128

    Article  CAS  PubMed  Google Scholar 

  • Schmidt R, Mieulet D, Hubberten H-M, Obata T, Hoefgen R, Fernie AR, Fisahn J, San Segundo B, Guiderdoni E, Schippers JHM, Mueller-Roeber B (2013) Salt-responsive ERF1 regulates reactive oxygen species-dependent signaling during the initial response to salt stress in rice. Plant Cell 25:2115–2131

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Sharma M, Buettner G (1993) Interaction of vitamin C and vitamin E during free radical stress in plasma: an ESR study. Free Radic Biol Med 14:649–653

    Article  CAS  PubMed  Google Scholar 

  • Sheehan D, Meade G, Foley VM, Dowd CA (2001) Structure, function and evolution of glutathione transferases: implications for classification of non-mammalian members of an ancient enzyme superfamily. Biochem J 360(1):16

    Article  Google Scholar 

  • Shu D-F, Wang L-Y, Duan M, Deng Y-S, Meng Q-W (2011) Antisense-mediated depletion of tomato chloroplast glutathione reductase enhances susceptibility to chilling stress. Plant Physiol Biochem 49:1228–1237

    Article  CAS  PubMed  Google Scholar 

  • Smith JJ, Ververidis P, John P (1992) Characterization of the ethylene-forming enzyme partially purified from melon. Phytochemistry 31:1485–1494

    Article  CAS  Google Scholar 

  • Smith VA, Gaskin P, MacMillan J (1990) Partial purification and characterization of the Gibberellin A20 3β-hydroxylase from seeds of Phaseolus vulgaris. Plant Physiol 94:1390–1401

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Chapter  Google Scholar 

  • Tambussi E, Bartoli CG, Guiamet JJ, Beltrano J, Araus JL (2000) Oxidative damage to thylakoid proteins in water-stressed leaves of wheat (Triticum aestivum L.) Physiol Plant 108:398–404

    Google Scholar 

  • Tedone L, Hancock RD, Alberino S, Haupt S, Viola R (2004) Long-distance transport of L-ascorbic acid in potato. BMC Plant Biol 4:16

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • The International Peach Genome Initiative (2013) The high-quality draft genome of peach (Prunus persica) identifies unique patterns of genetic diversity, domestication and genome evolution. Nat Genet 45:487–494

    Google Scholar 

  • The Tomato Genome Consortium (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485:635–641

    Article  CAS  Google Scholar 

  • Toivonen PMA (2003a) Effects of storage conditions and postharvest procedures on oxidative stress in fruits and vegetables. In: Hodges DM (ed) Postharvest oxidative stress in horticultural crops. Food Product Press, New York, pp 69–90

    Google Scholar 

  • Toivonen PMA (2003b) Postharvest treatments to control oxidative stress in fruits and vegetables. In: Hodges DM (ed) Postharvest oxidative stress in horticultural crops. Food Product Press, New York, pp 225–246

    Google Scholar 

  • Tóth SZ, Puthur JT, Nagy V, Garab G (2009) Experimental evidence for ascorbate-dependent electron transport in leaves with inactive oxygen-evolving complexes. Plant Physiol 149:1568–1578

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tukendorf A, Rauser WE (1990) Changes in glutathione and phytochelatins in roots of maize seedlings exposed to cadmium. Plant Sci 70:155–166

    Article  CAS  Google Scholar 

  • Ueno T, Suzuki Y, Fujii S, Vanin AF, Yoshimura T (1999) In vivo distribution and behavior of paramagnetic dinitrosyldithiolato iron complex in the abdomen of mouse. Free Radic Res 31:525–534

    Article  CAS  PubMed  Google Scholar 

  • Upadhyaya CP, Venkatesh J, Gururani MA, Asnin L, Sharma K, Ajappala H, Park SW (2011) Transgenic potato overproducing L-ascorbic acid resisted an increase in methylglyoxal under salinity stress via maintaining higher reduced glutathione level and glyoxalase enzyme activity. Biotechnol Lett 33:2297–2307

    Article  CAS  PubMed  Google Scholar 

  • Ushimaru T, Nakagawa T, Fujioka Y, Daicho K, Naito M, Yamauchi Y, Nonaka H, Amako K, Yamawaki K, Murata N (2006) Transgenic plants expressing the rice dehydroascorbate reductase gene are resistant to salt stress. J Plant Physiol 163:1179–1184

    Article  CAS  PubMed  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 

  • Vauclare P, Kopriva S, Fell D, Sutter M, Sticher L, von Ballmoos P, Krähenbühl U, Op den Camp R, Brunold C (2002) Flux control of sulphate assimilation in Arabidopsis thaliana: adenosine 5′-phosphosulphate reductase is more susceptible that ATP sulphurylase to negative control by thiols. Plant J 31:729–740

    Google Scholar 

  • Verpoorte R, Memelink J (2002) Engineering secondary metabolite production in plants. Curr Opin Biotechnol 13:181–187

    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 

  • Wang L-Y, Li D, Deng Y-S, Lv W, Meng Q-W (2013) Antisense-mediated depletion of tomato GDP-l-galactosephosphorylase increases susceptibility to chilling stress. J Plant Physiol 170:303–314

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Li J, Wang J, Li Z (2010a) Exogenous H2O2 improves the chilling tolerance of manilagrass and mascarenegrass by activating the antioxidative system. Plant Growth Regul 61:195–204

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Wise RR, Naylor AW (1987) Chilling-enhanced photooxidation. Evidence for the role of singlet oxygen and superoxide in the breakdown of pigments and endogenous antioxidants. Plant Physiol 83:278–282

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang D-Y, Li M, Ma N-N, Yang X-H, Meng Q-W (2017) Tomato SlGGP-LIKE gene participates in plant responses to chilling stress and pathogenic infection. Plant Physiol Biochem 112:218–226

    Article  CAS  PubMed  Google Scholar 

  • Yu C-W, Murphy TM, Lin C-H (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 

  • Zhang L, Wang Z, Xia Y, Kai G, Chen W, Tang K (2007) Metabolic engineering of plant L-ascorbic acid biosynthesis: recent trends and applications. Crit Rev Biotechnol 27:173–182

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Zhang L, Dong F, Gao J, Galbraith DW, Song C-P (2001) Hydrogen peroxide is involved in abscisic acid-induced stomatal closure in Vicia faba. Plant Physiol 126:1438–1448

    Google Scholar 

  • Zhu YL, Pilon-Smits EA, Jouanin L, Terry N (1999) Overexpression of glutathione synthetase in Indian mustard enhances cadmium accumulation and tolerance. Plant Physiol 119:73–80

    Article  CAS  Google Scholar 

Download references

Acknowledgements

Authors are researchers at CONICET and are grateful to CONICET, FONCyT, and Universidad Nacional de La Plata (Argentina) for supporting the work.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Carlos G. Bartoli .

Editor information

Editors and Affiliations

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

Bartoli, C.G., Buet, A., Gergoff Grozeff, G., Galatro, A., Simontacchi, M. (2017). Ascorbate-Glutathione Cycle and Abiotic 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_7

Download citation

Publish with us

Policies and ethics