Abstract
In plant physiology, low level of oxidative stress produces a favourable effect on the metabolism of a plant. However, when antioxydant defenses are over-passed by the action of oxidative compounds it will produce metabolic alteration that would end in cell death. The increase of oxidative stress is conditioned by different types of abiotic (salinity, drought, heavy metal) and biotic (fungus and insects) stresses. The main objective of this chapter will be to evaluate the role of ascorbate–glutathione cycle in the defense mechanisms and antioxidant capacity in plants under different stress conditions, integrating non enzymatic (ascorbate and glutathione) and enzymatic pathways and its biomolecular regulation. This chapter will describe the integration of both non-enzymatic and enzymatic mechanisms specially those concerning with the regeneration of active compounds. Enzymatic pathway preserves the active form of ascorbate and glutathione. Furthemore, we will also describe the regulation of ascorbate-glutation cycle developed by alterated redox status, which can be produced produced by abiotic and biotic stress.
In addition, in the discussion we will emphasize the agronomic and genomic approaches on how to improve the plant tolerance against the biotic and abiotic stresses, so that a higher antioxidant level can be obtained, which will benefit the healthy quality of vegetable foods.
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References
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
Asada K, Takahashi M (1987) Production and scavenging of active oxygen radicals in photosynthesis. In: Kyle DJ, Osmond CB, Arntzen CJ (eds) Photoinhibition, vol 9. Elsevier, Amsterdam, pp 227–288
Ashraf M (2009) Biotechnological approach of improving salt tolerance using antioxidants as a markers. Biotech Adv 27:84–93
Azevedo Neto AD, Prisco JT, Enéas-Filho J, Braga de Abreu CE, Gomes-Filho E (2006) Effect of salt stress on antioxidative enzymes and lipid peroxidation in leaves and roots of salt-tolerant and salt-sensitive maize genotypes. Environ Exp Bot 56:87–94
Bai Y, Lindhout P (2007) Domestication and breeding of tomatoes: what have we gained and what can we gain in the future? Ann Bot 100:1085–1094
Bartels D, Sunkar R (2005) Drought and salt tolerance in plants. Crit Rev Plant Sci 24:23–58
Borland A, Elliott S, Patterson S (2006) Are the metabolic components of crassulacean acid metabolism up-regulated in responses to an increase in oxidative burden? J Exp Bot 57:319–328
Chang CCC, Slesak I, Jordá L, Sotnikov A, Melzer M, Miszalski Z, Mullineaux PM, Parker JE, Karpinska B, Karpinski S (2009) Arabidopsis chloroplastic glutathine peroxidases play a role in cross talk between photooxidative stress and immune responses. Plant Physiol 150:670–683
Chew O, Whelan J, Millar AH (2003) Molecular definition of the ascorbate-glutathione cycle in Arabidopsis mitochondria reveals dual targeting of antioxidant defenses in plants. J Biol Chem 278:46869–46877
Chookhampaeng S, Pattanagul W, Theerakulpisut P (2008) Effect od salinity on growth, activity of antioxidant enzymes and sucrose content in tomato (Lycopersicon esculentum Mill.) at the reproductive stage. SciAsia 34:69–75
Dalal M, Dani RG, Kumar PA (2006) Current trends in the genetic engineering of vegetable crops. Sci Hort 107:215–225
Dat J, Vandenabeele S, Vranova E, Van Montagu M, Inzé D, Van Breusegem F (2000) Dual action of the active oxygen species during plant stress responses. Cell Mol Life Sci 57:779–795
Dangl JL, Dietrich RA, Richberg MH (1996) Death don’t have no mercy: cell death programs in plant-microbe interactions. Plant Cell 8:1793–1807
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 141:341–345
del Rio LA, Corpas FJ, Sandalio LM, Palma JM, Gomez M, Barroso JB (2002) Reactive oxygen species, antioxidant systems and nitric oxide in peroxisomes. J Exp Bot 53:1255–1272
Desikan R, Mackerness S, Hancock J, Neill SJ (2001) Regulation of the Arabidopsis transcriptosome by oxidative stress. Plant Physiol 127:159–172
Desikan R, Hancock JT, Bright J, Harrison J, Weir I, Hooley R, Neill SJ (2005) A role for ETR1 in hydrogen peroxide signaling in stomatal guard cells. Plant Physiol 137:831–834
Ding S, Lu Q, Zhan Y, Yang Z, Wen X, Zhang L, Lu C (2009) Enhanced sensitivity to oxidative stress in transgenic tobacco plants with decreased glutathione reductase activity leads to a decrease in ascorbate pool and ascorbate redox state. Plant Mol Bio 69:577–592
Dixon DP, Davis BG, Edwards R (2002) Functional divergence in the glutathione transferase superfamily in plants. Identification of two classes with putative functions in redox homeostasis in Arabidopsis thaliana. J Biol Chem 277:30859–30869
Eastmond PJ (2007) MONODEHYROASCORBATE REDUCTASE4 is required for seed storage oil hydrolysis and postgerminative growth in Arabidopsis. Plant Cell 19:1376–87
Elter A, Hartel A, Sieben C, Hertel B, Fischer-Schliebs E, Lüttge U, Moroni A, Thiel G (2007) A plant homolog of animal chloride intracellular channels (CLICs) generates an ion conductance in heterologous systems. J Biol Chem 282:8786–87892
Eltayeb AE, Kawano N, Badawi GH, Kaminaka H, Sankata T, Shibahara T, Inanaga S, Tanaka K (2007) Overexpression of monodehydroascorbate reductase in transgenic tobacco confers enhanced tolerance to ozone, salt and polyethylene glycol stresses. Planta 225:1255–1264
Flowers TJ, Flowers SA (2005) Why does salinity pose such a difficult problem for plant breeders? Agric Water Manag 78:15–24
Foyer CH, Noctor G (2005a) Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 17:1866–1875
Foyer CH, Noctor G (2005b) Oxidant and antioxidant signaling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. Plant Cell Environ 28:1056–1071
Foyer CH, Noctor G (2003) Redox sensing and signaling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. Physiol Plant 119:355–364
Fraser PD, Bramley PM (2004) The biosynthesis and nutritional uses of carotenoids. Prog Lipid Res 43:228–265
Gapper C, Dolan L (2006) Control of plant development by reactive oxygen species. Plant Physiol 141:341–345
Ghassemi F, Jakeman AJ, Nix HA (1995) Salinisation of land and water resources. human causes, extent management and case studies. University of New South Wales, Sydney, p 526
Gomez M, Arráez D, Segura A, Fernández A (2007) Analytical determination of antioxidants in tomato: typical components of the Mediterranean diet. J Sep Sci 30:452–461
Grant JJ, Loake GJ (2000) Role of reactive oxygen intermediates and cognate redox signaling in disease resistance. Plant Physiol 126:21–29
Gupta R, Luan S (2003) Redox control of protein tyrosine phosphatases and mitogen-activated protein kinases in plants. Plant Physiol 132:1149–1152
Halliwell B, Gutteridge JMC (2000) Free radicals in biology and medicine. Oxford University Press, Oxford, UK
Hammond-Kosack KE, Jones JDG (1996) Resistance gene-dependent plant defense responses. Plant Cell 8:1773–1791
Harinasut P, Poonsopa D, Roengmongkol K, Charoensataporn R (2003) Salinity effects on antioxidant enzymes in Mulberry cultivar. SciAsia 29:109–113
Ishikawa T, Shigeoka S (2008) Recent advances in ascorbate biosynthesis and the physiological significance of ascorbate peroxidase in photosynthesizing organisms. Biosci Biotechnol Biochem 72:1143–1154
Joo JH, Wang S, Chen JG, Jones AM, Fedoroff NV (2005) Differnt signaling and cell death roles of heterotrimeric G protein a and b subunits in the Arabidopsis oxidative stress response to ozone. Plant Cell 17:957–979
Kaliora AC, Dedoussis GVZ, Schmidt H (2006) Dietary antioxidants in preventing atherogenesis. Atherosclerosis 187:1–17
Kerdnaimongkol KR, Woodson RW (1999) Inhibition of catalase by antisense RNA increases susceptibility to oxidative stress and chilling injury in transgenic tomato plants. J Am Soc Hort Sci 124:330–444
Koussevitzky S, Suzuki N, Huntington S, Armijo L, Sha W, Cortes D, Shulaev V, Mittler R (2008) Ascorbate peroxidase 1 plays a key role in the rsponse of Arabidopsis thaliana to stress combination. J Biol Chem 283:34197–34203
Kovtun Y, Chiu WL, Tena G, Sheen J (2000) Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants. Proc Natl Acad Sci USA 97:2940–2945
Krauss S, Schnitzler WH, Grassmann J, Woitke M (2006) The influence of different electrical conductivity values in a simplified recirculating soil less system on inner and outer fruit quality characteristics of tomato. J Agric Food Chem 54:441–448
Kuzniak E, Sklodowska M (2005) 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
Larkin RM, Alonso JM, Ecker JR, Chory J (2003) GUN4, a regulator of chlorophyll synthesis and intracellular signaling. Science 299:902–906
Lenucci MS, Cadinu D, Taurino M, Piro G, Dalessandro G (2006) Antioxidant composition in cherry and high-pigment tomato cultivars. J Agric Food Chem 54:2606–2613
Li JM, Jin H (2007) Regulation of brassinosteroid signaling. Trends Plant Sci 12:37–41
Lisenbee CS, Lingard MJ, Trelease RN (2005) Arabidopsis peroxisomes possess functionally redundant membrane and matrix isoforms of monodehydroascorbate reductase. Plant J 43:900–91
Ma F, Cheng L (2003) The Sun-exposed peel of apple fruit has higher xanthophyll cycle-dependent thermal dissipation and antioxidants of the ascorbate-glutathione pathway than the shade peel. Plant Sci 165:819–827
Malecka A, Jarmuszkiewicz W, Tomaszewska B (2001) Antioxidative defense to lead stress in subcellular compartments of pea root cells. Acta Biochim Pol 48:687–698
McKersie BD (1994) Oxidative stress. In: McKersie BD, Leshem YY (eds) Stress and stress coping in cultivated plants. Kluwer, Dordrecht, pp 15–55
Miles GP, Samuel MA, Ranish JA, Sperrazzo GM, Ellis BE (2009) Quantitative proteomics identifies oxidant-induced, AtMPK6-dependent changes in Arabidopsis thaliana protein profiles. Plant Signal Behav 4:497–505
Millar AH, Mittova V, Kiddle G (2003) Control of ascorbate synthesis by respiration and its implications for stress responses. Plant Physiol 133:443–447
Miller G, Suzuki N, Rizhsky L, Hegie A, Koussevitzky S, Mittler R (2007) Double mutants deficient in cytosolic and thylakoid ascorbate peroxidase reveal a complex mode of interaction between reactive oxygen species, plant development, and response to abiotic stresses. Plant Physiol 144:1777–1785
Minoggio M, Bramati L, Simonetti P, Gardana C, Lemoli L, Santangelo E, Mauri L, Spigno P, Soressi GP, Pietta PG (2003) Polyphenol pattern and antioxidant activity of different tomato lines and cultivars. Ann Nutr Metab 47:64–69
Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410
Mittler R, Vanderauwera S, Gollery M, Van Breusegem FV (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498
Mittova V, Guy M, Tal M, Volokita M (2002a) Response of the cultavted tomato and its wild salt-tolerant relative Lycopersicon pennelli to salt-dependent oxidative stress: increased activities of antioxidants enzymes in root plastids. Free Radic Res 36:195–202
Mittova V, Tal M, Volokita M, Guy M (2002b) Salt stress induces up-regulation of an efficient chloroplast antioxidant system in the salt-tolerant wild tomato species Lycopersicon pennellii but not in the cultivated species. Physiol Plant 115:393–400
Moller IM (2001) Plant mitochondria and oxidative stress: electron transport, NADPH turnover, and metabolism of reactive oxygen species. Ann Rev Plant Physiol Plant Mol Bio 52:561–591
Mullineaux P, Karpinski S (2002) Signal transduction in response to excess light: getting out of the chloroplast. Curr Opin Plant Biol 5:43–48
Narendra S, Venkataramani S, Shen G, Wang J, Pasapula V, Lin Y, Kornyeyev D, Holaday AS, Zhang H (2006) The Arabidopsis ascorbate peroxidase 3 is a peroxisomal membrane-bound antioxidant enzyme and is dispensable for Arabidopsis growth and development. J Exp Bot 57:3033–3042
Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Ann Rev Plant Physiol Plant Mol Biol 49:249–279
Orozco-Cardenas M, Ryan CA (1999) Hydrogen peroxide is generated systemically in plant leaves by wounding and systemin via the octadecanoid pathway. PNAS 96:6553–6557
Palma JM, Jiménez A, Sandalio LM, Corpas FJ, Lundqvist M, Gómez M, Sevilla F, Río LA (2006) Antioxidative enzymes from chloroplasts, mitochondria, and peroxisomes during leaf senescence of nodulated pea plants. J Exp Bot 57:1747–1758
Pastori GM, Trippi VS (1992) Oxidative stress induces high rate of glutathione reductase synthesis in a drought-resistant maize strain. Plant Cell Physiol 33:957–961
Pei ZM, Murata Y, Benning G, Thomine S, Klüsener B, Allen GJ, Grill E, Schroeder JI (2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature 406:731–734
Peltier JB, Cai Y, Sun Q, Zabrouskov V, Giacomelli L, Andrea Rudella A, Ytterberg AJ, Rutschow H, van Wijk KJ (2006) The oligomeric stromal proteome of Arabidopsis thaliana chloroplasts. MCP 5:114–133
Polle A (2001) Dissecting the superoxidismutase-ascorbate-glutathione pathway by metabolic modelling: computer analysis as a step towards flux analysis. Plant Physiol 126:445–462
Pourcel L, Routaboul JM, Cheynier V (2007) Flavonoid oxidation in plants: from biochemical properties to physiological functions. Trends Plant Sci 12:29–36
Prasad TK, Anderson MD, Martin BA, Stewart CR (1994) Evidence for chilling-induced oxidative stress in maize seedlings and a regulatory role for hydrogen peroxide. Plant Cell 6:65–74
Raffo A, La Malfa G, Fogliano V, Maiani G, Quaglia G (2006) Seasonal variations in antioxidant components of cherry tomatoes (Lycopersicon esculentum cv. Naomi F1). J Food Compos Anal 19:11–19
Rentel MC, Lecourrieux D, Ouaked F, Usher SL, Peterson L, Okamato H, Knight H, Peck SC, Grierson CS, Hirt H, Knight MR (2004) OXI1 Kinase is necessary for oxidative burst-mediated signal-ling in Arabidopsis. Nature 427:858–861
Rossel JB, Walter PB, Hendrickson L, Chow WS, Poole A, Mullineaux PM, Pogson BJ (2006) A mutation affecting ASCORBATE PEROXIDASE 2 gene expression reveals a link between responses to high Light and drought tolerante. Plant, Cell and Environment 29:269–281
Russo M, Sgherri C, Izzo R, Navari-Izzo F (2008) Brassica napus subjected to copper excess: phospolpases C and D and glutathione system in signalling. Env Exp Bot 62:238–246
Samuel MA, Miles GP, Ellis BE (2000) Ozone treatment rapidly activates MAP kinase signalling in plants. Plant J 22:367–376
Scandalios JG (1997) Molecular genetics of superoxide dismutase in plants. In: Scandalios JG (ed) Oxidative stress and the molecular biology of antioxidant defenses. Cold Spring Harbor Laboratory Press, New York, pp 527–568
Schubert M, Petersson UA, Haas BJ, Funk C, Schröder WP, Kieselbach T (2002). Proteome Map of the Chloroplast Lumen of Arabidopsis thaliana. J Biol Chem 277: 8354–8365
Secenji M, Hideg E, Bebes A, Györgyey (2010) Transcriptional differences in gene families of the ascorbate-glutathione cycle in wheat during mild water deficit. Plant Cell Rep 29:37–50
Seong ES, Cho HS, Choi D, Joung YH, Lim CK, Hur JH, Wang MH (2007) Tomato plants overexpressing CaKR1 enhanced tolerance to salt and oxidative stress. Biochem Biophys Res Commun 363:983–988
Shalata A, Mittova V, Volokita M, Guy M, Tal M (2001) Response of the cultivated tomato and its wild salt-tolerant relative Lycopersicon pennellii to salt-dependent oxidative stress: the root antioxidative system. Physiol Plant 112:487–494
Shao HB, Chu LY, Lu ZH, Kang CM (2008) Primary antioxidant free radical scavenging and redox signaling pathways in higher plant cells. Int J Biol Sci 4:8–14
Shigeoka S, Ishikawa T, Tamoi M, Miyagawa Y, Tkeda T, Yabuta Y, Yoshimura K (2002) Regulation and function of ascorbate peroxidase isoenzymes. J Exp Bot 53:1305–1319
Smirnoff N (2000) Ascorbic acid: metabolism and functions of a multifacetted molecule. Curr Opin Plant Biol 3:229–235
Strand A, Asami T, Alonso J, Ecker JR, Chory J (2003) Chloroplast to nucleus communication triggered by accumulation of Mg-protoporphyrinIX. Nature 421:79–83
Vadassery J, Tripathi S, Prasad R, Varma A, Oelmüller R (2009) Monodehydroascorbate reductase 2 and dehydroascorbate reductase 5 are crucial for a mutualistic interaction between Piriformospora indica and Arabidopsis. J Plant Physiol 166:1263–1274
Vaidyanathan H, Sivakumar P, Chakrabarty R, Thomas G (2003) Sacvenging of reactive oxygen species in NaCl-stressed rice (Oryza sativa L.)- differencial response in salt-tolerant and sensitive varieties. Plant Sci 165:1411–1418
Valero E, González-Sánchez MI, Maciá H, García-Carmona F (2009) Computer simulation of the dynamic behavior of the glutathione-ascorbate redox cycle in chloroplasts. Plant Physiol 149:1958–1969
Verhoeyen ME, Bovy A, Collins G, Muir S, Robinson S, de Vos CHR, Colliver S (2002) Increasing antioxidant levels in tomatoes through modification of the flavonoid biosynthetic pathway. J Exp Bot 53:2099–2106
Wang WB, Kim YH, Lee HS, Kim KY, Deng XP, Kwak SS (2009) Analysis of antioxidant enzyme activity during germination of alfalfa under salt and drought stresses. Plant Physiol Biochem 47:570–577
Wormuth D, Heiber I, Shaikali J, Kandlbinder K, Baier M, Dietz KJ (2007) Redox regulation and antioxidative defence in Arabidopsis leaves viewed from a systems biology perspective. J Biotech 129:229–248
Yabuta Y, Maruta T, Yoshimura K (2004) Two distinct redox signaling pathways for cytosolic APX induction under photooxdidative stress. Plant Cell Physiol 45:1586–594
Yeo A (1998) Predicting the interaction between the effects of salinity and climate change on crop plants. Sci Hort 78:159–174
Yoshida S, Tamaoki M, Shikano T, Nakajima N, Ogawa D, Ioki M, Aono M, Kubo A, Kamada H, Inoue Y, Saji H (2006) Cytosolic dehydroascorbate reductase is important for ozone tolerance in Arabidopsis thaliana. Plant Cell Physiol 47:304–308
Xiang C, Olivier DJ (1998) Glutathione metabolic genes coordinately respond to heavy metals and jasmonic acid in Arabidopsis. Plan Cell 10:1539–1550
Acknowledgements
The authors are grateful to Dr. Mei Lie Tan for stimulating discussions and comments on this manuscript. This work was supported by the FONDECYT (grants project Nº 1090405), National Commision for Scientific and Technological Research (CONICYT), Ministery of Education, Chile.
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Martínez, J.P., Araya, H. (2010). Ascorbate–Glutathione Cycle: Enzymatic and Non-enzymatic Integrated Mechanisms and Its Biomolecular Regulation. In: Anjum, N., Chan, MT., Umar, S. (eds) Ascorbate-Glutathione Pathway and Stress Tolerance in Plants. Springer, Dordrecht. https://doi.org/10.1007/978-90-481-9404-9_11
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