biologia plantarum

International journal on Plant Life established by Bohumil Nìmec in 1959

Biologia plantarum 45:105-115, 2002 | DOI: 10.1023/A:1015112926955

Hydrogen Peroxide Generated Via the Octadecanoid Pathway is Neither Necessary nor Sufficient for Methyl Jasmonate-Induced Hypersensitive Cell Death in Woody Plants

V. Repka1
1 Laboratory of Molecular Biology and Virology, Research Institute of Viticulture and Enology (CRIVE), Bratislava, Slovakia

Exogenously applied methyl jasmonate (MeJA) might induce the formation of necrotic lesions that closely resemble hypersensitive response lesions. Cellular damage, restricted to the infiltrated zone, was accompanied with the production of H2O2 from the oxidative burst. H2O2 generated in response to MeJA can be histochemically detected in cells surrounding the necrotic lesions as well as in the vascular tissues. The response is systemic and maximizes with time. Among 12 plant species from different families that were assayed for both hypersensitive reaction (HR)-like response and H2O2 generation, only woody species exhibited both MeJA-inducible HR cell death and the generation of H2O2. To assess the role of H2O2 in MeJA-induced HR-like cell death, a gain and loss of function strategy was employed. The cumulative results indicate that H2O2 is neither necessary nor sufficient for MeJA-inducible cell death and that O2- rather than H2O2 might be responsible.

Keywords: hypersensitive reaction; jasmonates; programmed cell death; reactive oxygen intermediates
Subjects: Acer pseudoplatanus; Aesculus hippocastanum; Aglaonema modestum; barley, methyl jasmonate; bean, methyl jasmonate; Catalpa bignoioides; cucumber, methyl jasmonate; Cucumis sativa; French bean, methyl jasmonate; grapevine, methyl jasmonate; Hibiscus rosa-chinensis; Hordeum vulgare; horse-chestnut, methyl jasmonate; hydrogen peroxide generation, octadecanoid pathway; hypersensitive reaction; jasmonates; lime-tree, methyl jasmonate; maple, methyl jasmonate; methyl jasmonate; Nicotiana tabacum; oak, methyl jasmonate; octadecanoid pathway, H2O2 generation; Peperomia serpens; Phaseolus vulgaris; programmed cell death; Quercus petraea; reactive oxygen species; Tilia platyphyllos; tobacco, methyl jasmonate; Vitis vinifera

Published: March 1, 2002  Show citation

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Repka, V. (2002). Hydrogen Peroxide Generated Via the Octadecanoid Pathway is Neither Necessary nor Sufficient for Methyl Jasmonate-Induced Hypersensitive Cell Death in Woody Plants. Biologia plantarum, 45(1), 105-115. doi: 10.1023/A:1015112926955
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    References

    1. Alvarez, M.E., Pennell, R.I., Meijer, P.J., Ishikawa, A., Dixon, R.A., Lamb, C.J.: Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity.-Cell 92: 773-784, 1998. Go to original source...
    2. Baker, C.J., Orlandi, E.W.: Active oxygen in plant pathogenesis.-Annu. Rev. Phytopathol. 33: 299-321, 1995. Go to original source...
    3. Bergey, D.R., Orozco-Cardenas, M.L., de Moura, D.S., Ryan, C.A.: A wound-and systemic-inducible polygalacturonase in tomato leaves.-Proc. nat. Acad. Sci. USA 96: 1756-1760, 1999. Go to original source...
    4. Bradley, D.J., Kjellbom, P., Lamb, C.J.: Elicitor-induced and wound-induced oxidative cross-linking of a proline-rich plant cell-wall protein: a novel, rapid defense response.-Cell 70: 21-30, 1992. Go to original source...
    5. Chamnongpol, S., Willekens, H., Moeder, W., Langerbartels, C., Sandermann, H., Van Montagu, M., Inzé, D., Van Camp, W.: Defense activation and enhanced pathogen tolerance induced by H2O2 in transgenic tobacco.-Proc. nat. Acad. Sci. USA 95: 5818-5823, 1998. Go to original source...
    6. Chaudry, B., Mueller-Uri, F., Cameron-Mills, V., Gough, S., Simpson, D.: The barley 60 kDa jasmonate-induced protein (JIP60) is a novel ribosome-inactivating protein.-Plant J. 6: 815-824, 1994. Go to original source...
    7. Chen, Z., Malamy, J., Henning, J., Conrath, U., Sanchez-Casas, P., Silva, H., Ricigliano, J.A., Klessig, D.F.: Induction, modification, and transduction of the salicylic acid signal in plant defense responses.-Proc. nat. Acad. Sci. USA 92: 4134-4137, 1995. Go to original source...
    8. Cohen Y., Gisi, U., Niderman, T.: Local and systemic protection against Phytophthora infestans induced in potato and tomato plants by jasmonic acid and jasmonic methyl ester.-Phytopathology 83: 1054-1062, 1993. Go to original source...
    9. Creelman, R.A., Mullet, J.E.: Biosynthesis and action of jasmonates in plants.-Annu. Rev. Plant Physiol. Plant mol. Biol. 48: 355-381, 1997. Go to original source...
    10. Creelman, R.A., Tierney, M.L., Mullet, J.E.: Jasmonic acid/methyl jasmonate accumulate in wounded soybean hypocotyls and modulate wound gene expression.-Proc. nat. Acad. Sci. USA 89: 4938-4941, 1992. Go to original source...
    11. Desikan, R., Reynolds, A., Hancock, J.T., Neil, S.J.: Harpin and hydrogen peroxide both initiate programmed cell death but have differential effects on defence gene expression in Arabidopsis suspension cultures.-Biochem. J. 330: 115-120, 1998. Go to original source...
    12. Devlin, W.S., Gustine, D.L.: Involvement of the oxidative burst in phytoalexin accumulation and hypersensitive reaction.-Plant Physiol. 100: 1189-1195, 1992. Go to original source...
    13. Doares, S.H., Nerváez-Vásquez, J., Conconi, A., Ryan, C.A.: Salicylic acid inhibits synthesis of proteinase inhibitors in tomato leaves induced by systemin and jasmonic acid.-Plant Physiol. 108: 1741-1746, 1995. Go to original source...
    14. Doke, N.: NADPH-dependent O2- generation in membrane fractions isolated from wounded potato tubers inoculated with Phytophthora infestans.-Physiol. Plant Pathol. 27: 311-322, 1985. Go to original source...
    15. Dong, X.: SA, JA, ethylene, and disease resistance in plants.-Curr. Opinions Plant Biol. 1: 316-323, 1998. Go to original source...
    16. Dorey, S., Kopp, M., Geoffroy, P., Fritig, B., Kauffmann, S.: Hydrogen peroxide from the oxidative burst is neither necessary nor sufficient for hypersensitive cell death induction, phenylalanine ammonia lyase stimulation, salicylic acid accumulation, or scopoletin consumption in cultured tobacco cells treated with elicitin.-Plant Physiol. 121: 163-171, 1999. Go to original source...
    17. Draper, J.: Salicylate, superoxide synthesis and cell suicide in plant defence.-Trends Plant Sci. 2: 162-165, 1997. Go to original source...
    18. Dubery, I.A., Teodorczuk, L.G., Louw, A.E.: Early responses in methyl jasmonate-preconditioned cells toward pathogen-derived elicitors.-Mol. Cell Biol. Res. Commun. 3: 105-110, 2000. Go to original source...
    19. Durner, J., Klessig, D.F.: Salicylic acid is a modulator of tobacco and mammalian catalases.-J. biol. Chem. 271: 28492-28501, 1996. Go to original source...
    20. Farmer, E.E., Caldelari, D., Pearce, G., Walker-Simmons, M.K., Ryan, C.A.: Diethyldithiocarbamic acid inhibits the octadecanoid signaling pathway for the wound induction of proteinase inhibitors in tomato leaves.-Plant Physiol. 106: 337-342, 1994. Go to original source...
    21. Glazebrook, J.: Genes controlling expression of defense responses in Arabidopsis.-Curr. Opinions Plant Biol. 2: 280-286, 1999. Go to original source...
    22. Glazener, J.A., Orlandi, E.W., Baker, C.J.: The active oxygen response of cell suspensions to incompatible bacteria is not sufficient to cause hypersensitive cell death.-Plant Physiol. 110: 759-763, 1996. Go to original source...
    23. Grant, J.J., Loake, G.J.: Role of reactive oxygen intermediates and cognate redox signaling in disease resistance.-Plant Physiol. 124: 21-29, 2000. Go to original source...
    24. Gundlach, H., Muller, M.J., Kutchan, T.M., Zenk, M.H.: Jasmonic acid is a signal transducer in elicitor-induced plant cell cultures.-Proc. nat. Acad. Sci. USA 89: 2398-2393, 1992. Go to original source...
    25. Hammond-Kosack, K.E., Jones, J.D.G.: Resistance gene-dependent plant defense responses.-Plant Cell 8: 1773-1791, 1996. Go to original source...
    26. Jabs, T., Dietrich, R.A., Dangl, J.L.: Initiation of runaway cell death in an Arabidopsis mutant by extracellular superoxide.-Science 273: 1853-1856, 1996. Go to original source...
    27. Jabs, T., Tschope, M., Colling, C., Hahlbrock, K., Scheel, D.: Elicitor-stimulated ion fluxes and O2- from the oxidative burst are essential components in triggering defense gene activation and phytoalexin synthesis in parsley.-Proc. nat. Acad. Sci. USA 94: 4800-4805, 1997. Go to original source...
    28. Johnson, R., Narvaez, J., An, G.H., Ryan, C.A.: Expression of proteinase inhibitors I and II in transgenic tobacco plants: effects on natural defense against Manduca sexta larvae.-Proc. nat. Acad. Sci. USA 86: 9871-9875, 1989. Go to original source...
    29. Kauss, H., Jeblick, W., Ziegler, J., Krabler, W.: Pretreatment of parsley (Petroselinum crispum L.) suspension cultures with methyl jasmonate enhances elicitation of activated oxygen species.-Plant Physiol. 105: 89-94, 1994. Go to original source...
    30. Kazan, K., Murray, F.R., Goulter, K.C., Llewellyn, D.J., Manners, J.M.: Induction of cell death in transgenic plants expressing a fungal glucose oxidase.-Mol. Plant-Microbe Interact. 11: 555-562, 1998. Go to original source...
    31. Levine, A., Tenhaken, R., Dixon, R.A., Lamb, C.: H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response.-Cell 79: 583-593, 1994. Go to original source...
    32. Maleck, K., Dietrich, R.A.: Defense on multiple fronts: how do plants cope with diverse enemies?-Trends Plant Sci. 6: 215-219, 1999. Go to original source...
    33. Mehdy, M.C.: Active oxygen species in plant defense against pathogens.-Plant Physiol. 105: 467-472, 1994. Go to original source...
    34. Muller-Uri, F., Parthier, B., Nover, L.: Jasmonate-induced alteration of gene expression in barley leaf segments analyzed by in vivo and in vitro protein synthesis.-Planta 176: 241-247, 1988. Go to original source...
    35. Orozco-Cárdenas, M.L., Ryan, C.A.: Hydrogen peroxide is generated systemically in plant leaves by wounding and systemin via the octadecanoid pathway.-Proc. nat. Acad. Sci. USA 96: 6553-6557, 1999. Go to original source...
    36. Orozco-Cárdenas, M.L., Narváez-Vásquez, J., Ryan, C.A.: Hydrogen peroxide acts as a second messenger for the induction of defense genes in tomato plants in response to wounding, systemin, and methyl jasmonate.-Plant Cell 13: 179-191, 2001. Go to original source...
    37. Overmyer, K., Tuominen, H., Kettunen, R., Betz, C., Langerbartels, C., Sandermann, H., Kangasjärvi, J.: Ozone-sensitive Arabidopsis rcd1 mutant reveals opposite roles for ethylene and jasmonate signaling pathways in regulating superoxide-dependent cell death.-Plant Cell 12: 1849-1862, 2000. Go to original source...
    38. Parthier, B.: Jasmonates: hormonal regulators or stress factors in leaf senescence?-J. Plant Growth Regul. 9: 1-7, 1990. Go to original source...
    39. Parthier, B.: Jasmonates new regulators of plant growth and development: many facts and few hypothesses on their action.-Bot. Acta 104: 446-456.
    40. Peng, M., Kuc, J.: Peroxidase-generated hydrogen peroxide as a source of antifungal activity in vitro and on tobacco leaf discs.-Phytopathology 82: 696-699, 1992. Go to original source...
    41. Penninckx, I.A.M.A., Eggermont, K., Terras, F.R.G., Thomma, B.P.H.J., de Samblanx, G.W., Buchala, A., Métraux, J.P., Manners, J.M., Broekaert, W.F.: Pathogen-induced systemic activation of a plant defensin gene in Arabidopsis follows a salicylic acid-independent pathway.-Plant Cell 8: 2309-2323, 1996. Go to original source...
    42. Pena-Cortéz, H., Albrecht, T., Prat, S., Weiler, E.W., Willmitzer, L.: Aspirin prevents wound-induced gene expression in tomato leaves by blocking jasmonic acid biosynthesis.-Planta 191: 123-128, 1993. Go to original source...
    43. Pieterse, C.M.J., Van Loon, L.C.: Salicylic acid-independent plant defense pathways.-Trends Plant Sci. 4: 52-56, 1999. Go to original source...
    44. Pugin, A., Franchisse, J.-M., Tavernier, E., Bligny, R., Gout, E., Douce, R., Guern, J.: Early events induced by the elicitor cryptogein in tobacco cells: involvement of a plasma membrane NADHP oxidase and activation of glycolysis and the pentose phosphate pathway.-Plant Cell 9: 2077-2091, 1997. Go to original source...
    45. Rao, M.V., Paliyath, G., Ormrod, D.P., Murr, D.P., Watkins, C.B.: Influence of salicylic acid on H2O2 production, oxidative stress and H2O2-metabolizing enzymes.-Plant Physiol. 115: 137-149, 1997. Go to original source...
    46. Repka, V., Fischerová, I., ©ilhárová, K.: Methyl jasmonate induces a hypersensitive-like response of grapevine in the absence of avirulent pathogens.-Vitis 40: 5-10, 2001.
    47. Reymond, P., Farmer, E.E.: Jasmonate and salicylate as global signals for defense gene expression.-Curr. Opinions Plant Biol. 1: 404-411, 1998. Go to original source...
    48. Schraudner, M., Moeder, W.W., Wiese, C., Van Camp, W., Inzé, D., Langerbartels, C., Sandermann, H.: Ozone-induced oxidative burst in the ozone biomonitor plant, tobacco Bel W3.-Plant J. 16: 235-245, 1998. Go to original source...
    49. Schwacke, R., Hager, A.: Fungal elicitors induce a transient release of active oxygen species from cultured spruce cells that is dependent on Ca2+ and protein-kinase activity.-Planta 187: 136-141, 1992. Go to original source...
    50. Simon-Plas, F., Rustérucci, C., Milat, M.-L., Humbert, C., Montillet, J.-L., Blein, J.P.: Active oxygen species production in tobacco cells elicited by cryptogein.-Plant Cell Environ. 20: 1573-1579, 1997. Go to original source...
    51. Staswick, P. E.: Preferential loss of an abundant storage protein from soybean pods during seed development.-Plant Physiol. 90: 1252-1255, 1989. Go to original source...
    52. Thordal-Christensen, H., Zhang, Z., Wei, Y., Collinge, D.: Subcellular localization of H2O2: H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction.-Plant J. 11: 1187-1194, 1997. Go to original source...
    53. Tsuchiya, T., Ohta, H., Okawa, K., Iwamatsu, A., Shimada, H., Masuda, T., Takamiya, K.: Cloning of chlorophyllase, the key enzyme in chrophyll degradation: finding of a lipase motif and the induction by methyl jasmonate.-Proc. nat. Acad. Sci. USA 96: 15362-15367, 1999. Go to original source...
    54. Wojtazsek, P.: Oxidative burst: an early plant response to pathogen infection.-Biochem. J. 322: 681-692, 1997. Go to original source...
    55. Xu, Y., Chang, P.F.L., Liu, D., Narasimhan, M.L., Raghothama, K.G.: Plant defense genes are synergistically induced by ethylene and methyl jasmonate.-Plant Cell 6: 1077-1085, 1994. Go to original source...

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