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2007 | 54 | 1 | 39-50
Article title

The role of hydrogen peroxide in regulation of plant metabolism and cellular signalling in response to environmental stresses

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Hydrogen peroxide (H2O2) is produced predominantly in plant cells during photosynthesis and photorespiration, and to a lesser extent, in respiration processes. It is the most stable of the so-called reactive oxygen species (ROS), and therefore plays a crucial role as a signalling molecule in various physiological processes. Intra- and intercellular levels of H2O2 increase during environmental stresses. Hydrogen peroxide interacts with thiol-containing proteins and activates different signalling pathways as well as transcription factors, which in turn regulate gene expression and cell-cycle processes. Genetic systems controlling cellular redox homeostasis and H2O2 signalling are discussed. In addition to photosynthetic and respiratory metabolism, the extracellular matrix (ECM) plays an important role in the generation of H2O2, which regulates plant growth, development, acclimatory and defence responses. During various environmental stresses the highest levels of H2O2 are observed in the leaf veins. Most of our knowledge about H2O2 in plants has been obtained from obligate C3 plants. The potential role of H2O2 in the photosynthetic mode of carbon assimilation, such as C4 metabolism and CAM (Crassulacean acid metabolism) is discussed. We speculate that early in the evolution of oxygenic photosynthesis on Earth, H2O2 could have been involved in the evolution of modern photosystem II.

Physical description
  • Institute of Plant Physiology, Polish Academy of Sciences, Kraków, Poland
  • Institute of Plant Physiology, Polish Academy of Sciences, Kraków, Poland
  • Faculty of Life Sciences, University College of Södertörns, Huddinge, Sweden
  • Institute of Plant Physiology, Polish Academy of Sciences, Kraków, Poland
  • Institute of Plant Physiology, Polish Academy of Sciences, Kraków, Poland
  • Alscher RG, Erturk N, Heath LS (2002) Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J Exp Bot 53: 1331-1341.
  • Alvarez ME, Pennell RI, Meijer P-J, 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.
  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55: 373-399.
  • 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.
  • Asada K, Takahashi M (1987) Production and scavenging of active oxygen in photosynthesis. In Photoinhibition. Kyle DJ, Osmond BJ, Arntzen CJ, eds, pp 227-287. Elsevier, Amsterdam.
  • Badger MR, Von Caemmerer S, Ruuska S, Nakano H (2000) Electron flow to oxygen in higher plants and algae: rates and control of direct photoreduction (Mehler reaction) and rubisco oxygenase. Philos Trans R Soc Lond B Biol Sci 355: 1433-1446.
  • Ball L, Accotto GP, Bechtold U, Creissen G, Funck D, Jimenez A, Kular B, Leyland N, Mejia-Carranza J, Reynolds H, Karpinski S, Mullineaux PM (2004) Evidence for a direct link between glutathione biosynthesis and stress defense gene expression in Arabidopsis. Plant Cell 16: 2448-2462.
  • Bartosz G (1997) Oxidative stress in plants. Acta Physiol Plant 19: 47-64.
  • Bechtold U, Karpinski S, Mullineaux PM (2005) The influence of the light environment and photosynthesis on oxidative signalling responses in plant-biotrophic pathogen interactions. Plant Cell Environ 28: 1046-1055.
  • Blankenship RE, Hartman H (1998) The origin and evolution of oxygenic photosynthesis. Trends Biochem Sci 23: 94-97.
  • Bolwell GP, Bindschedler LV, Blee KA, Butt VS, Davies DR, Gardner SL, Gerrish C, Minibayeva F (2002) The apoplastic oxidative burst in response to biotic stress in plants: a three-component system. J Exp Bot 53: 1367-1376.
  • Borda MJ, Elsetinow AR, Schooen AR, Strongin DR (2001) Pyrite-induced hydrogen peroxide formation as a driving force in the evolution of photosynthetic organisms on an early Earth. Astrobiology 1: 283-288.
  • Borland A, Elliot S, Patterson S, Taybi T, Cushman J, Pater B, Barnes J (2006) Are the metabolic components of crassulacean acid metabolism up-regulated in response to an increase in oxidative burden? J Exp Bot 57: 319-328.
  • Brisson LE, Tenhaken R, Lamb C (1994) Function of oxidative cross-linking of cell wall structural proteins in plant disease resistance. Plant Cell 6: 1703-1712.
  • Broetto F, Lüttge U, Ratajczak R (2002) Influence of light intensity and salt-treatment on mode of photosynthesis and enzymes of the antioxidative response system of Mesembryanthemum crystallinum. Funct Plant Biol 29: 13-23.
  • Buchanan BB, Balmer Y (2005) Redox regulation: a broadening horizon. Annu Rev Plant Biol 56: 187-220.
  • Chang CCC, Ball L, Fryer MJ, Baker NR, Karpinski S, Mullineaux PM (2004) Induction of ascorbate peroxidase 2 expression in wounded Arabidopsis leaves does not involve known wound-signalling pathways but is associated with changes in photosynthesis. Plant J 38: 499-511.
  • Cornic G, Fresneau C (2002) Photosynthetic carbon reduction and carbon oxidation cycles are the main electron sinks for photosystem II activity during a mild drought. Ann Bot 89: 887-894.
  • Creissen G, Firmin J, Fryer M, Kular B, Leyland N, Reynolds H, Pastori G, Wellburn F, Baker N, Wellburn A, Mullineaux P (1999) Elevated glutathione biosynthetic capacity in the chloroplasts of transgenic tobacco plants paradoxically causes increased oxidative stress. Plant Cell 11: 1277-1292.
  • Cui K, Xing G, Liu X, Wang Y (1999) Effect of hydrogen peroxide on somatic embryogenesis of Lycium barbarum L. Plant Sci 146: 9-16.
  • Dat J, Vandenabeele S, Vranová E, Van Montagu M, Inzé D, Breusegem F (2000) Dual action of the active oxygen species during plant stress responses. Cell Mol Life Sci 57: 779-795.
  • Demmig-Adams B, Adams III WW (1996) The role of xanthophyll cycle carotenoids in the protection of photosynthesis. Trends Plant Sci 1: 21-26.
  • Desikan R, Mackerness A-H S, Hancock JT, Neill SJ (2001) Regulation of the Arabidopsis transcriptome by oxidative stress. Plant Physiol 127: 159-172.
  • Desikan R, Hancock JT, Neill SJ (2003) Oxidative stress signalling. Top Curr Genet 4: 129-149.
  • Dismukes GC (1996) Manganese enzymes with binuclear active sites. Chem Rev 96: 2909-2926.
  • Dixon RA, Lamb CJ (1990) Molecular communication in interactions between plants and microbial pathogens. Annu Rev Plant Physiol Plant Mol Biol 41: 339-367.
  • Dixon DP, Lapthorn A, Edwards R (2002) Plant glutathione transferases. Genome Biol 3: 3004-3008.
  • Edwards EA, Enard C, Creissen GP, Mullineaux PM (1994) Synthesis and properties of glutathione reductase in stressed peas. Planta 192: 137-143.
  • Encina A, Fry SC (2005) Oxidative coupling of feruloyl-arabinoxylan trisaccharide (FAXX) in the walls of living maize cells requires endogenous hydrogen peroxide and is controlled by a low-Mr apoplastic inhibitor. Planta 223: 77-89.
  • Encrenaz Th, Bézard B, Greathouse TK, Richter MJ, Lacy JH, Atreya SK, Wong AS, Lebonnois S, Lefèvre F, Forget F (2004) Hydrogen peroxide on Mars: evidence for spatial and seasonal variations. Icarus 170: 424-429.
  • Feierabend J, Schaan C, Hertwig B (1992) Photoinactivation of catalase occurs under both high- and low-temperature stress conditions and accompanies photoinhibition of photosystem II. Plant Physiol 100: 1554-1561.
  • Fine PL, Frasch WD (1992) The oxygen-evolving complex requires chloride to prevent hydrogen peroxide formation. Biochemistry 31: 12204-12210.
  • Foyer Ch, Noctor G (2000) Oxygen processing in photosynthesis: regulation and signalling. New Phytol 146: 359-388.
  • Foyer Ch, Noctor G (2003) Redox sensing and signalling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. Physiol Plant 119: 355-364.
  • Frugoli JA, Zhong HH, Nuccio ML, McCourt P, McPeek MA, Thomas TL, McClung CR (1996) Catalase is encoded by multigene family in Arabidopsis thaliana (L.) Heynh. Plant Physiol 112: 327-336.
  • Fryer MJ, Ball L, Oxborough K, Karpinski S, Mullineaux PM, Baker NR (2003) Control of ascorbate peroxidase 2 expression by hydrogen peroxide and leaf water status during excess light stress reveals a functional organisation of Arabidopsis leaves. Plant J 33: 691-705.
  • Geisler M, Kleczkowski LA, Karpinski S (2006) A universal algorithm for genome-wide in silico identification of biologically significant gene promoter putative cis-regulatory-elements; identification of new elements for reactive oxygen species and sucrose signaling in Arabidopsis. Plant J 45: 384-398.
  • Govrin EM, Levine A (2000) The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea. Curr Biol 10: 751-757.
  • Halliwell B, Gutteridge JMC (1999) The chemistry of free radicals and related 'reactive species'. In Free radicals in biology and medicine. pp 36-104. Oxford University Press, Oxford.
  • Halliwell B (2006) Reactive species and antioxidants. Redox biology is a fundamental theme of aerobic life. Plant Physiol 141: 312-322.
  • Hartman H, McKay CP (1995) Oxygenic photosynthesis and the oxidation state of Mars. Planet Space Sci 43: 123-128.
  • Henzler T, Steudel E (2000) Transport and metabolic degradation of hydrogen peroxide in Chara corallina: model calculations and measurements with the pressure probe suggest transport of H2O2 across water channels. J Exp Bot 51: 2053-2066.
  • Hérouart D, Van Montagu M, Inzé D (1994) Developmental and environmental regulation of the Nicotiana plumbaginifolia cytosolic Cu/Zn-superoxide dismutase promoter in transgenic tobacco. Plant Physiol 104: 873-880.
  • Hertwig B, Streb P, Fieirabend J (1992) Light dependence of catalase synthesis and degradation in leaves and the influence of interfering stress conditions. Plant Physiol 100: 1547-1553.
  • Horling F, König J, Dietz K-J (2002) Type II peroxiredoxin C, a member of the peroxiredoxin family of Arabidopsis thaliana: its expression and activity in comparison with other peroxiredoxins. Plant Physiol Biochem 40: 491-499.
  • Hung S-H, Yu C-W, Lin CH (2005) Hydrogen peroxide function as a stress signal in plants. Bot Bull Acad Sin 46: 1-10.
  • Hurst AC, Grams TEE, Ratajczak R (2004) Effects of salinity, high irradiance, ozone, and ethylene on mode of photosynthesis, oxidative stress and oxidative damage in the C3/CAM intermediate plant Mesembryanthemum crystallinum L. Plant Cell Environ 27: 187- 197.
  • Hückelhoven R, Kogel K-H (2003) Reactive oxygen intermediates in plant-microbe interactions: who is who in powdery mildew resistance? Planta 216: 891-902.
  • Inzé D, Van Montagu M (1995) Oxidative stress in plants. Curr Biol 6: 153-158.
  • Juszczuk IM, Rychter AM (2003) Alternative oxidase in higher plants. Acta Biochim Polon 50: 1257-1271.
  • Kaiser WM (1979) Reversible inhibition of the Calvin cycle and activation of oxidative pentose phosphate cycle in isolated intact chloroplasts by hydrogen peroxide. Planta 145: 377-382.
  • Kacperska A (2004) Sensor types in signal transduction pathways in plant cells responding to abiotic stressors: do they depend on stress intensity? Physiol Plant 122: 159-168.
  • Karpinska B, Wingsle G, Karpinski S (2000) Antagonistic effects of hydrogen peroxide and glutathione on acclimation to excess excitation energy in Arabidopsis. IUBMB Life 50: 21-26.
  • Karpinska B, Karlsson M, Schinkel H, Streller S, Süss K-H, Melzer M, Wingsle G (2001) A novel superoxide dismutase with a high isoelectric point in higher plants. Expression, regulation, and protein localization. Plant Physiol 126: 1668-1677.
  • Karpinski S, Escobar C, Karpinska B, Creissen G, Mullineaux PM (1997) Photosynthetic electron transport regulates the expression of cytosolic ascorbate peroxidase genes in Arabidopsis during excess light stress. Plant Cell 9: 627-640.
  • Karpinski S, Reynolds H, Karpinska B, Wingsle G, Creissen G, Mullineaux P (1999) Systemic signalling and acclimation in response to excess excitation energy in Arabidopsis. Science 284: 654-657.
  • Karpinski S, Gabrys H, Mateo A, Karpinska B, Mullineaux PM (2003) Light perception in plant disease defence signalling. Curr Opin Plant Biol 6: 390-396.
  • Keller T, Damude HG, Werner D, Doerner P, Dixon RA, Lamb C (1998) A plant homolog of the neutrophil NADPH oxidase gp91-phox subunit gene encodes a plasma membrane protein with Ca2+ binding motifs. Plant Cell 10: 255-266.
  • Kozaki A, Takeba G (1996) Photorespiration protects C3 plants from photooxidation. Nature 384: 557-560.
  • Kuzniak E, Urbanek H (2000) The involvement of hydrogen peroxide in plant responses to stresses. Acta Physiol Plant 22: 195-203.
  • Lane BG (1994) Oxalate, germin, and the extracellular matrix of higher plants. FASEB J 8: 294-301.
  • Lane N (2002) Oxygen. The molecule that made the world. Oxford University Press, Oxford.
  • Levine A, Tenhaken R, Dixon R, Lamb C (1994) H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance. Annu Rev Plant Physiol 121: 245-257.
  • Li J, Zhao X, Matsui S (2001) Hydrogen peroxide contents and activities of antioxidative enzymes among C3, C4 and CAM plants. J Japan Soc Hort Sci 70: 747-752.
  • Libik M, Konieczny R, Pater B, Slesak I, Miszalski Z (2005a) Differences in the activities of some antioxidant enzymes and in H2O2 content during rhizogenesis and somatic embryogenesis in callus cultures of the ice plant. Plant Cell Rep 23: 834-841.
  • Libik M, Konieczny R, Surówka E, Miszalski Z (2005b) Superoxide dismutase activity in organs of Mesembryanthemum crystallinum L. at different stages of CAM development. Acta Biol Cracov Ser Bot 47: 199-204.
  • Logan BA, Kornyeyev D, Hardison J, Holaday AS (2006) The role of antioxidant enzymes in photoprotection. Photosynth Res 88: 119-132.
  • Lüttge U (2002) CO2-concentrating: consequences in crassulacean acid metabolism. J Exp Bot 53: 2131-2142.
  • Lüttge U (2004) Ecophysiology of crassulacean acid metabolism (CAM). Ann Bot 93: 629-652.
  • Mahalingam R, Federoff N (2003) Stress response, cell death and signalling: the many faces of reactive oxygen species. Physiol Plant 119: 56-68.
  • Mateo A, Mühlenbock P, Restérucci C, Chi-Chang C, Miszalski Z, Karpinska B, Parker JE, Mullineaux PM, Karpinski S (2004) LESION SIMULATING DISEASE 1 required for acclimation to conditions that promote excess excitation energy. Plant Physiol 136: 2818-2830.
  • Mateo A, Funck D, Mühlenbock P, Kular B, Mullineaux PM, Karpinski S (2006) Controlled levels of salicylic acid are required for optimal photosynthesis and redox homeostasis. J Exp Bot 57: 1795-1807.
  • Matés JM (2000) Effects of antioxidant enzymes in the molecular control of reactive oxygen species toxicology. Toxicology 153: 83-104.
  • Mehler AH (1951) Studies on reactions of illuminated chloroplasts. II Stimulation and inhibition of the reaction with molecular oxygen. Arch Biochem 34: 339-351.
  • Miszalski Z, Slesak I, Niewiadomska E, Baczek-Kwinta R, Lüttge U, Ratajczak R (1998) Subcellular localization and stress responses of superoxide dismutase isoforms from leaves in the C3-CAM intermediate halophyte Mesembryanthemum crystallinum L. Plant Cell Environ 21: 169-179.
  • Miszalski Z, Niewiadomska E, Slesak I, Lüttge U, Kluge M, Ratajczak R (2001) The effect of irradiation on carboxylating/decarboxylating enzymes and fumarase activities in Mesembryanthemum crystallinum L. exposed to salinity stress. Plant Biol 3: 17-23.
  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7: 405-410.
  • Mittler R (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9: 490-498.
  • Møller IM (2001) Plant mitochondria and oxidative stress: electron transport, NADPH turnover, and metabolism of reactive oxygen species. Annu Rev Plant Physiol Plant Mol Biol 52: 561-591.
  • Mullineaux PM, Karpinski S (2002) Signal transduction in response to excess light: getting out of the chloroplast. Curr Opin Plant Biol 5: 43-48.
  • Mullineaux PM, Karpinski S, Jiménez A, Cleary SP, Robinson C, Creissen GP (1998) Identification of cDNAs encoding plastid-targeted glutathione peroxidase. Plant J 13: 375-379.
  • Mullineaux P, Ball L, Escobar C, Karpinska B, Creissen G, Karpinski S (2000) Are diverse signalling pathways integrated in the regulation of Arabidopsis antioxidant defence gene expression in response to excess excitation energy. Philos Trans R Soc Lond B Biol Sci 355: 1531-1540.
  • Mullineaux PM, Karpinski S, Baker NR (2006) Spatial dependence for hydrogen peroxide-directed signalling in light-stressed plants. Plant Physiol 141: 346-350.
  • Neill S, Desikan R, Hancock J (2002a) Hydrogen peroxide signalling. Curr Opin Plant Biol 5: 388-395.
  • Neill S, Desikan R, Clarke A, Hurst RD, Hancock J (2002b) Hydrogen peroxide and nitric oxide as signalling molecules in plants. J Exp Bot 53: 1237-1247.
  • Niewiadomska E, Miszalski Z, Slesak I, Ratajczak R (1999) Catalase activity during C3-CAM transition in Mesembryanthemum crystallinum L. leaves. Free Radic Res 31: S251-256.
  • Niewiadomska E, Pater B, Miszalski Z (2002) Does ozone induce a C3-CAM transition in Mesembryanthemum crystallinum leaves? Phyton (Horn, Austria) 42c: 69-78.
  • Niewiadomska E, Karpinska B, Romanowska E, Slesak I, Karpinski S (2004) A salinity-induced C3-CAM transition increases energy conservation in the halophyte Mesembryanthemum crystallinum L. Plant Cell Physiol 45: 789-794.
  • Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49: 249-279.
  • Noctor G, Arisi ACM, Jouanin L, Foyer CH (1999) Photorespiratory glycine enhances glutathione accumulation in both the chloroplastic and cytosolic compartments. J Exp Bot 50: 1157-1167.
  • Ogawa K, Kanematsu S, Asada K (1997) Generation of superoxide anion and localization of CuZn-superoxide dismutase in vascular tissue of spinach hypocotyls: their association with lignification. Plant Cell Physiol 38: 1118-1126.
  • Olson JM, Blankenship RE (2004) Thinking about the evolution of photosynthesis. Photosynth Res 80: 373-396.
  • Olson PD, Varner JE (1993) Hydrogen peroxide and lignification. Plant Cell 4: 887-892.
  • Orozco-Cárdenas ML, Ryan CA (1999) Hydrogen peroxide is generated systemically in plant leaves by wounding and systemin via the octadecanoid pathway. Proc Natl Acad Sci USA 96: 6553-6557.
  • Pace RJ, Åhrling K (2004) Water oxidation in PSII-H atom abstraction revisited. Biochim Biophys Acta 1655: 172-178.
  • Pastori GM, Foyer CH (2002) Common components, networks, and pathways of cross-tolerance to stress. The central role of 'redox' and abscisic acid-mediated controls. Plant Physiol 129: 460-468.
  • Polle A (2001) Dissecting the superoxide dismutase-ascorbate-glutathione-pathway in chloroplasts by metabolic modelling. Computer simulations as a step toward flux analysis. Plant Physiol 126: 445-462.
  • Potikha TS, Collins CC, Johnson DI, Delmer DP, Levine A (1999) The involvement of hydrogen peroxide in the differentiation of secondary walls in cotton fibers. Plant Physiol 119: 849-858.
  • Prasad TK, Anderson MD, Martin BA, Stewart CR (1994) Evidence for chilling-induced oxidative stress in maize seedlings and regulatory role of hydrogen peroxide. Plant Cell 6: 65-74.
  • Rhoads DM, Umbach AL, Subbaiah CC, Siedow JN (2006) Mitochondrial reactive oxygen species. Contribution to oxidative stress and interorganellar signalling. Plant Physiol 141: 357-366.
  • Roberts MR, Paul ND (2006) Seduced by the dark side: integrating molecular and ecological perspectives on the influence of light on plant defence against pests and pathogens. New Phytol 170: 677-699.
  • Ros Barceló A (1998) Hydrogen peroxide production is a general property of the lignifying xylem from vascular plants. Ann Bot 82: 97-103.
  • Samuilov VD, Timofeev KN, Sinitsyn SV, Bezryadnov DV (2001) H2O2-induced inhibition of photosynthetic O2 evolution by Anabaena variabilis cells. Biochemistry (Moscow) 69: 926-933.
  • Schmidt M, Dehne S, Feierabend J (2002) Post-transcriptional mechanisms control catalase synthesis during its light-induced turnover in rye leaves through the availability of the hemin cofactor and reversible changes of the translation efficiency of mRNA. Plant J 31: 601-613.
  • Shulaev V, Oliver DJ (2006) Metabolic and proteomic markers for oxidative stress. New tools for reactive oxygen species research. Plant Physiol 141: 367-372.
  • Smirnoff N (1996) The function and metabolism of ascorbic acid in plants. Ann Bot 78: 661-669.
  • Srivastava V, Schinkel H, Witzell J, Hertzberg H, Torp M, Srivastava KM, Karpinska B, Melzer M, Wingsle G (2006) Down-regulation of high isoelectric point extracellular superoxide dismutase mediates alterations in reactive oxygen species metabolism and developmental disturbances in hybrid aspen. Plant J 49: 135-148.
  • Surówka E, Karolewski P, Niewiadomska E, Libik M, Miszalski Z (2007) Antioxidative response of Mesembryanthemum crystallinum plants to exogenous SO2 application. Plant Sci 172: 76-84.
  • Svedruzic D, Jónsson S, Toyota CG, Reinhardt LA, Ricagno S, Lindquist Y, Richards NGJ (2005) The enzymes of oxalate metabolism: unexpected structures and mechanisms. Arch Biochem Biophys 433: 176-192.
  • Slesak I, Miszalski Z, Karpinska B, Niewiadomska E, Ratajczak R, Karpinski S (2002) Redox control of oxidative stress responses in the C3-CAM intermediate plant Mesembryanthemum crystallinum. Plant Physiol Biochem 40: 669-677.
  • Slesak I, Karpinska B, Surówka E, Miszalski Z, Karpinski S (2003) Redox changes in the chloroplast and hydrogen peroxide are essential for regulation of C3-CAM transition and photooxidative stress responses in the facultative CAM plant Mesembryanthemum crystallinum L. Plant Cell Physiol 44: 573-581.
  • Talarczyk A, Hennig J (2001) Early defence responses in plants infected with pathogenic organisms. Cell Mol Biol Lett 6: 955-970.
  • Talarczyk A, Krzymowska M, Borucki W, Hennig J (2002) Effect of yeast CTA1 gene expression on response of tobacco plants to tobacco mosaic virus infection. Plant Physiol 129: 1032-1044.
  • Torres MA, Jones JDG, Dangl JL (2006) Reactive oxygen species signalling in response to pathogens. Plant Physiol 141: 373-378.
  • Van Breusegem F, Vranová E, Dat JF, Inzé D (2001) The role of active oxygen species in plant signal transduction. Plant Sci 161: 405-414.
  • Van Lis R, Atteia A (2004) Control of mitochondrial function via photosynthetic redox signals. Photosynth Res 79: 133-148.
  • Veljovic-Jovanovic S, Noctor G, Foyer CH (2002) Are leaf hydrogen peroxide concentrations commonly overestimated? The potential influence of artefactual interference by tissue phenolics and ascorbate. Plant Physiol Biochem 40: 501-507.
  • Vranová E, Inzé D, Van Breusegem F (2002) Signal transduction during oxidative stress. J Exp Bot 53: 1227-1236.
  • Walz C, Juenger M, Schad M, Kehr J (2002) Evidence for the presence and activity of a complete antioxidant defence system in mature sieve tubes. Plant J 31: 189-197.
  • 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 indispensable for stress defence in C3 plants. EMBO J 16: 4806-4816.
  • Wingler A, Lea PJ, Quick WP, Leegood RC (2000) Photorespiration: metabolic pathways and their role in stress protection. Philos Trans R Soc Lond B Biol Sci 355: 1517-1529.
  • Wingsle G, Karpinski S (1996) Differential redox regulation by glutathione of glutathione reductase and CuZn superoxide dismutase genes expression in Pinus sylvestris (L.) needles. Planta 198: 151-157.
  • Wojtaszek P (1997) Oxidative burst: an early plant response to pathogen infection. Biochem J 322: 681-692.
  • Yamasaki H (2005) The NO world for plants: achieving balance in an open system. Plant Cell Environ 28: 78-84.
  • 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.
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