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The involvement of hydrogen peroxide in plant responses to stresses

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Abstract

The role of reactive oxygen species, especially H2O2, in plant response to stresses has been the focus of much attention. Hydrogen peroxide has been postulated to play multiple functions in plant defence against pathogens. (1) H2O2 may possess direct microbicidal activity at the sites of pathogen invasion. (2) It is used for cell-wall reinforcing processes: lignification and oxidative cross-linking of hydroxyproline-rich proteins and other cell-wall polymers. (3) It was found to be necessary for phytoalexin synthesis. (4) H2O2 may trigger programmed plant cell death during the hypersensitive response that restricts the spread of infection. (5) H2O2 has been suggested to act as a signal in the induction of systemic acquired resistance and (6) it induces defence genes. Recently H2O2 has been proposed to be involved in the signal transduction pathways leading to acclimation and protection from abiotic stresses. The present review discusses new insights into the function of H2O2 in plant responses to biotic and abiotic stresses.

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References

  • Adam, A.L., Bestwick, C.S., Barna, B., Mansfield, J.W. 1995. Enzymes regulating the accumulation of active oxygen species during the hypersensitive reaction of bean to Pseudomonas syringae pv. phaseolicola. Planta 197: 240–249.

    Article  CAS  Google Scholar 

  • Alvarez, M.E., Pennnell, R.I., Meijer, P-J., Ishikawa, A., Dixon, R.A., Lamb, C. 1998. Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity. Cell 92: 773–784.

    Article  PubMed  CAS  Google Scholar 

  • Anderson, M.D., Chen, Z., Klessig, D.F. 1998. Possible involvement of lipid peroxidation in salicylic acidmediated induction of PR-1 gene expression. Phytochemistry 47: 555–566.

    Article  CAS  Google Scholar 

  • Apostol, I., Heinstein, P.F., Low, P.S. 1989. Rapid stimulation of an oxidative burst during elicitation of culture plant cells. Plant Physiol. 90: 109–116.

    PubMed  CAS  Google Scholar 

  • Auh, C-K., Murphy, T.M. 1995. Plasma membrane redox enzyme is involved in the synthesis of O2 − and H2O2 by Phytophthora elicitor-stimulated rose cells. Plant Physiol. 107: 1241–1247.

    PubMed  CAS  Google Scholar 

  • Baker, C.J., Orlandi, E.W., 1995. Active oxygen in plant pathogenesis. Annu. Rev. Phytopathol. 33: 299–321.

    Article  CAS  PubMed  Google Scholar 

  • Bestwick, C.S., Brown, I.R., Bennett, M.H., Mansfield, J.W. 1997. Localization of hydrogen peroxide accumulation during the hypersensitive reaction of lettuce cells to Pseudomonas syringae pv phaseolicola. Plant Cell 9: 209–221.

    Article  PubMed  CAS  Google Scholar 

  • Bolwell, G.P., Butt, V.S., Davies, D.R., Zimmerlin, A. 1995. The origin of the oxidative burst in plants. Free Rad. Res. 23: 517–532.

    CAS  Google Scholar 

  • Bolwell G.P., Davies, D.R., Gerrish, C., Auh, C-K., Murphy, T.M. 1998. Comparative biochemistry of the oxidative burst produced by rose and French bean cells reveals two distinct mechanisms. Plant Physiol. 116: 1379–1385.

    Article  PubMed  CAS  Google Scholar 

  • Bolwell, G.P., Wojtaszek, P. 1997. Mechanisms for the generation of reactive oxygen species in plant defence — a broad perspective. Physiol. Mol. Plant Pathol. 51: 347–366.

    Article  CAS  Google Scholar 

  • Bostock, R.M. 1999. Signal conflicts and synergies in induced resistance to multiple attackers. Physiol. Mol. Plant Pathol. 55: 99–109.

    Article  Google Scholar 

  • Burke, J.J., Gamble, P.E., Hartfield, J.L., Quinsberry, J.E. 1985. Plant morphological and biochemical responses to field water deficit. I. Responses of glutathione reductase activity and paraquat sensitivity. Plant Physiol. 79: 415–419.

    PubMed  CAS  Google Scholar 

  • Chamnongpol, S., Willekens, H., Moeder, W., Langebartels, C., Sanderman, H., jr., Van Montagu, M., Inzé, D., Van Camp, W. 1998. Defence activation and enhanced pathogen tolerance induced by H2O2 in transgenic tobacco. Proc. Natl. Acad. Sci. USA 95: 5818–5823.

    Article  PubMed  CAS  Google Scholar 

  • Chen, Z., Silva, H., Klessig, D.F. 1993. Active oxygen species in the induction of plant systemic acquired resistance by salicylic acid. Science 262: 1883–1885.

    Article  PubMed  CAS  Google Scholar 

  • Conrath, U., Chen, Z., Ricigliano, J.R., Klessig, D.F. 1995. Two inducers of plant defence responses, 2,6-dichloroisonicotinic acid and salicylic acid, inhibit catalase activity in tobacco. Proc. Natl. Acad. Sci. USA 92: 7143–7147.

    Article  PubMed  CAS  Google Scholar 

  • Croft, K.P.C., Voisey, C.R., Slusarenko, A.J. 1990. Mechanism of hypersensitive cell collapses: correlation of increased lipoxygenase activity with membrane damage in leaves of Phaseolus vulgaris (L.) inoculated with an avirulent race of Pseudomonas syringae pv. phaseolicola. Physiol. Mol. Plant Pathol. 36: 49–62.

    Article  CAS  Google Scholar 

  • Dai, Q., Yan, B., Huang, S., Liu, X., Peng, S., Miranda, M.L.L., Chavez, A.Q., Vergara, B.S., Olszyk, D.M. 1997. Response of oxidative stress defence systems in rice (Oryza sativa) leaves with supplemental UV-B radiation. Physiol. Plant. 101: 301–308.

    Article  CAS  Google Scholar 

  • Dat, J.F., Lopez-Delgado, H., Foyer, C.H., Scott, I.M. 1998. Parallel changes in H2O2 and catalase during thermotolerance induced by salicylic acid or heat acclimation in mustard seedlings. Plant Physiol. 116: 1351–1357.

    Article  PubMed  CAS  Google Scholar 

  • Deskian, R., Neill, S.J., Hancock, J.T. 1997. Generation of active oxygen in Arabidopsis thaliana. Phyton 37: 65–70.

    Google Scholar 

  • Doke, N. 1983. Involvement of superoxide anion generation in the hypersensitive response of potato tuber tissues to infection with an incompatible race of Phytophthora infestans and the hyphal cell wall material. Physiol. Plant Pathol. 23: 345–357.

    Article  CAS  Google Scholar 

  • Dong, X. 1995. Finding of the missing pieces in the puzzle of plant disease resistance. Proc. Natl. Acad. Sci. USA 92: 7137–7139.

    Article  PubMed  CAS  Google Scholar 

  • Dumas, B., Freyssinet, G., Pallett, K.E. 1995. Tissue-specific expression of germine-like oxalate oxidase during development and fungal infection of barley seedlings. Plant Physiol. 107: 1091–1096.

    PubMed  CAS  Google Scholar 

  • Durner, J., Klessig, D.F. 1995. Inhibition of ascorbate peroxidase by salicylic acid and 2,6-dichloroisonicotinic acid, two inducers of plant defence responses. Proc. Natl. Acad. Sci. USA 92: 11312–11316.

    Article  PubMed  CAS  Google Scholar 

  • Dwyer, S.C., Legendre, L., Low, P.S., Leto, T.L. 1996. Plant and human neutrophil oxidative burst complexes contain immunologically related proteins. Biochim. Biophys. Acta 1289: 231–237.

    PubMed  Google Scholar 

  • Elstner, E.F. 1991. Oxygen radicals — biochemical basis for their efficacy. Klin. Wochenschr. 69: 949–956.

    Article  PubMed  CAS  Google Scholar 

  • Gaffney, T., Friedrich, L., Vernooij, B., Negrotto, D., Nye, G., Uknes, S., Ward, E., Kessmann, H., Ryals, J. 1993. Requirement of salicylic acid for the induction of systemic acquired resistance. Science 261: 754–756.

    Article  CAS  PubMed  Google Scholar 

  • Gajewska, E., Urbanek, H. 1999. Hydrogen peroxide and enzymes metabolizing it in tomato leaves after infection with fungus. Acta Physiol. Plant. 21 (suppl.): 41

    Google Scholar 

  • Glazener, J.A., Orlandi, E.W., Baker, C.J. 1996. The active oxygen response of cell suspensions to incompatible bacteria is not sufficient to cause hypersensitive cell death. Plant Physiol. 110: 759–763.

    PubMed  CAS  Google Scholar 

  • Greenberg, J.T. 1996. Programmed cell death: A way of life for plants. Proc. Natl. Acad. Sci. USA 93:12094–12097.

    Article  PubMed  CAS  Google Scholar 

  • Heath, M. 1998. Involvement of reactive oxygen species in the response of resistant (hypersensitive) or susceptible cowpeas to the cowpea rust fungus. New Phytol. 138: 251–263.

    Article  CAS  Google Scholar 

  • Hernández, J.A., Campillo, A., Jiménez, A., Alarcón, J.J., Sevilla, F. 1999. Response of antioxidant systems and leaf water relations to NaCl stress in pea plants. New Phytol. 141: 241–251.

    Article  Google Scholar 

  • Hippeli, S., Elstner, E.F. 1996. Mechanisms of oxygen activation during plant stress: biochemical effects of air pollutants. J. Plant Physiol. 148: 249–257.

    CAS  Google Scholar 

  • Hückelhoven, R., Fodor, J., Preis, C., Kogel, K-H. 1999. Hypersensitive cell death and papilla formation in barley attacked by the powdery mildew fungus are associated with hydrogen peroxide but not with salicylic acid accumulation. Plant Physiol. 119: 1251–1260.

    Article  PubMed  Google Scholar 

  • Iturbe-Ormaexte, I., Escuredo, P.R., Arrese-Igor, C., Becana, M. 1998. Oxidative damage in pea plants exposed to water deficit or paraquat. Plant Physiol. 116: 173–181.

    Article  Google Scholar 

  • Jabs, T. 1999. Reactive oxygen intermediates as mediators of programmed cell death in plants and animals. Biochem. Pharmacol., 57: 231–245.

    Article  PubMed  CAS  Google Scholar 

  • Janda, T., Szalai, G., Páldi, E. 1999. Hydroponic treatment with salicylic acid decreases the effects of chilling injury in maize (Zea mays L.) plants. Planta 208: 175–180.

    Article  CAS  Google Scholar 

  • Kato, S., Misawa, T. 1976. Lipid peroxidation during the appearance of hypersensitive reaction of cowpea leaves infected with cucumber mosaic virus. Ann. Phytopathol. Soc. Jpn. 42: 472–480.

    Google Scholar 

  • Kauss, H., Jeblick, W. 1996. Influence of salicylic acid on the induction of competence for H2O2 elicitation. Plant Physiol. 111: 755–763.

    PubMed  CAS  Google Scholar 

  • Keller, T., Damude, H.G., Werner, D., Doerner, P., Dixon, R.A., Lamb, C. 1998. A plant homolog of the neutrophil NADPH oxidase gp91phox subunit gene encodes plasma membrane protein with Ca2+ binding motifs. Plant Cell 10: 255–266.

    Article  PubMed  CAS  Google Scholar 

  • Knörzer, O.C., Durner, J., Böger, P. 1996. Alterations in the antioxidative system of suspension-cultured soybean cells (Glycine max) induced by oxidative stress. Physiol. Plant. 97: 388–396.

    Article  Google Scholar 

  • Kombrink, E., Hahlbrock, K., 1986. Responses of cultured parsley cells to elicitors from phytopathogenic fungi. Plant Physiol. 81: 216–221.

    PubMed  CAS  Google Scholar 

  • Krzymowska, M., Talarczyk, A., Hennig, J. 1997. Is tobacco response to TMV infection modulated by catalase activity? Acta Physiol. Plant. 19: 577–579.

    Article  Google Scholar 

  • Kuźniak, E., Patykowski, J., Urbanek, H. 1999. Involvement of the antioxidative system in tomato response to fusaric acid treatment. J. Phytopathol. 47: 385–390.

    Article  Google Scholar 

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

    PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Lopez-Delgado, H., Dat, J.F., Foyer, C.H., Scott, I.M. 1998. Induction of thermotolerance in potato microplants by acetylsalicylic acid and H2O2. J. Exp. Bot. 321: 713–720.

    Article  Google Scholar 

  • Low, P.S., Merida, J.R. 1996. The oxidative burst in plant defence: function and signal transduction. Physiol. Plant. 96: 533–542.

    Article  CAS  Google Scholar 

  • Lu, H., Higgins, V.J., 1998. Measurement of active oxygen species generated in planta in response to elicitor AVR9 of Cladosporium fulvum. Physiol. Mol. Plant Pathol. 52: 35–51.

    Article  CAS  Google Scholar 

  • Lu, H., Higgins, V.J., 1999. The effect of hydrogen peroxide on the viability of tomato cells and of the fungal pathogen Cladosporium fulvum. Physiol. Mol. Plant Pathol. 54: 131–143.

    Article  CAS  Google Scholar 

  • McKersie, B.D., Chen, Y., de Beus, M., Bowley, S.R. Inzé, D., D’Halluin, K., Botterman, J. 1993. Superoxide dismutase enhances tolerance of freezing stress in transgenic alfalfa (Medicago sativa L.). Plant Physiol. 103: 1155–1163.

    Article  PubMed  CAS  Google Scholar 

  • Małolepsza, U., Urbanek, H. 1999. O-Hydroksyetylorutozyd jako elicytor odporności roślin pomidora na choroby infekcyjne. Streszczenia I Krajowego Kongresu Biotechnologii, Wrocław, 20-25. 09. 1999.

    Google Scholar 

  • Mehdy, M.C. 1994. Active oxygen species in plant defence against pathogens. Plant Physiol. 105: 467–472.

    PubMed  CAS  Google Scholar 

  • Morita, S., Kaminaka, H., Masumura, T., Tanaka, K. 1999. Induction of rice cytosolic ascorbate peroxidase mRNA by oxidative stress; the involvement of hydrogen peroxide in oxidative stress signaling. Plant Cell Physiol. 40: 417–422.

    CAS  Google Scholar 

  • Murphy, T.M., Huerta, A.J. 1990. Hydrogen peroxide formation in cultured rose cells in response to UV-C radiation. Physiol. Plant. 78: 247–253.

    Article  CAS  Google Scholar 

  • Okpodu, C.M., Alscher, R.G., Grabau, E.A., Cramer, C.L. 1996. Physiological, biochemical and molecular effects of sulfur dioxide. J. Plant Physiol. 148: 309–316.

    CAS  Google Scholar 

  • Orozco-Cardenas, M., Ryan, C.A. 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.

    Article  PubMed  CAS  Google Scholar 

  • Otte, O., Barz, W. 1996. The elicitor-induced oxidative burst in cultured chickpea cells drives the rapid insolubilization of two cell wall structural proteins. Planta 200: 238–246.

    Article  CAS  Google Scholar 

  • Peng, M., Kuć, J. 1992. Peroxidase-generated hydrogen peroxide as a source of antifungal activity in vitro and on tobacco leaf disks. Phytopathol. 82: 696–699.

    CAS  Google Scholar 

  • Polidoros, A.N., Scandalios, J.G. 1999. Role of hydrogen peroxide and different classes of antioxidants in the regulation of catalase and glutathione S-transferase gene expression in maize (Zea mays L.). Physiol. Plant. 106: 112–120.

    Article  CAS  Google Scholar 

  • Prasad, T.K., Anderson, M.D., Martin, B.A., Stewart, C.R. 1994. Evidence for chilling-induced oxidative stress in maize seedlings and a regulatory role of hydrogen peroxide. Plant Cell 6: 65–74.

    Article  PubMed  CAS  Google Scholar 

  • Rusterucci, C., Stallaert, V., Millat, M.-l., Pugin, A., Ricci, P., Blein, J-P. 1996. Relationship between active oxygen species, lipid peroxidation, necrosis, and phytoalexin production induced by elicitins in Nicotiana. Plant Physiol. 111: 885–891.

    PubMed  CAS  Google Scholar 

  • Ryals, J.A., Neuenschwander, U.H., Willits, M.G., Molina, A., Steiner, H-Y., Hunt, M.D. 1996. Systemic acquired resistance. Plant Cell 8: 1809–1819.

    Article  PubMed  CAS  Google Scholar 

  • Scandalios, J.G. 1993. Oxygen stress and superoxide dismutases. Plant Physiol. 101: 7–12.

    PubMed  CAS  Google Scholar 

  • Sharma, Y.K., León, J., Raskin, I., Davies, K.R. 1996. Ozone-induced responses in Arabidopsis thaliana — the role of salicylic acid in the accumulation of defence-related transcripts and induced resistance. Proc. Natl. Acad. Sci. USA 93: 5099–5104.

    Article  PubMed  CAS  Google Scholar 

  • Shirasu, K., Nakajima, H., Rajasekhar, V.K., Dixon, R.A., Lamb, C. 1997. Salicylic acid potentiates an agonist-dependent gain control that amplifies pathogen signals in the activation of defence mechanisms. Plant Cell 9: 261–270.

    Article  PubMed  CAS  Google Scholar 

  • Tenhaken, R., Levine, A., Brisson, L.F., Dixon, R.A., Lamb, C. 1995. Function of the oxidative burst in hypersensitive disease resistance. Proc. Natl. Acad. Sci. USA 92: 4158–4163.

    Article  PubMed  CAS  Google Scholar 

  • Thordal-Christensen, H., Zhang, Z., Wei, Y., Collinge, D.B. 1997. Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J. 11: 1187–1194.

    Article  CAS  Google Scholar 

  • Vallélian-Bindschedler, L., Schweizer, P., Mösinger, E., Métraux, J-P. 1998. Heat-induced resistance in barley to powdery mildew (Blumeria graminis f.sp. hordei) is associated with a burst of active oxygen species. Physiol. Mol. Plant Pathol. 52: 185–199.

    Article  Google Scholar 

  • Van Camp, W., Capiau, K., Van Montagu, M., Inzé, D., Slooten, L. 1996. Enhancement of oxidative stress tolerance in transgenic tobacco plants overexpressing Fe-superoxide dismutase in the chloroplasts. Plant Physiol. 112: 1703–1714.

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Van Gestelen, P., Asard, H., Horemans, N., Caubergs, R.J. 1998. Superoxide-producing NAD(P)H oxidases in plasma membrane vesicles from elicitor responsive bean plants. Physiol. Plant. 104: 653–660.

    Article  Google Scholar 

  • Vera-Estrella, R., Blumwald, E., Higgins, V.J. 1992. Effect of specific elicitors of Cladosporium fulvum on tomato suspension cells: evidence for the involvement of active oxygen species. Plant Physiol. 99: 1208–1215.

    Article  PubMed  CAS  Google Scholar 

  • Wisniewski, J-P., Cornille, P., Agnel, J-P., Montillet, J-L. 1999. The extensin multigene family responds differentially to superoxide or hydrogen peroxide in tomato cell cultures. FEBS Lett. 447: 264–268.

    Article  PubMed  CAS  Google Scholar 

  • Wojtaszek, P. 1997a. Mechanisms for the generation of reactive oxygen species in plant defence response. Acta Physiol. Plant. 19: 581–589.

    CAS  Google Scholar 

  • Wojtaszek, P. 1997b. Oxidative burst: an early plant response to pathogen infection. Biochem. J. 322: 681–692.

    CAS  Google Scholar 

  • Wu, G., Shortt, B.J., Lawrence, E.B., Levine, E.B., Fitzimmonis, K.C. 1995. Disease resistance conferred by expression of a gene encoding H2O2-generating glucose oxidase in transgenic potato plants. Plant Cell 7: 1357–1368.

    Article  PubMed  CAS  Google Scholar 

  • Xing, T., Higgins, J., Blumwald, E. 1997. Racespecific elicitors of Cladosporium fulvum promote translocation of cytosolic components of NADPH oxidase to the plasma membrane of tomato cells. Plant Cell 9:249–259.

    Article  PubMed  CAS  Google Scholar 

  • Yalpani, N., Enyedi, A.J., León, J., Raskin, I. 1994. Ultraviolet light and ozone stimulate accumulation of salicylic acid, pathogenesis-related proteins and virus resistance in tobacco. Planta 193: 372–376.

    Article  CAS  Google Scholar 

  • Zhang, Z., Collinge, D.B., Thordal-Christensen, H. 1995. Germine-like oxalate oxidase, a H2O2-producing enzyme, accumulates in barley attacked by the powdery mildew fungus. Plant J. 8: 139–145.

    Article  CAS  Google Scholar 

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  1. Department of Plant Physiology and Biochemistry, University of Łódź, 90-237, Łódź, Banacha 12/16

    Elżbieta Kuźniak & Henryk Urbanek

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  1. Elżbieta Kuźniak
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Kuźniak, E., Urbanek, H. The involvement of hydrogen peroxide in plant responses to stresses. Acta Physiol Plant 22, 195–203 (2000). https://doi.org/10.1007/s11738-000-0076-4

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