Abstract
Activation of the plant defensin gene PDF1.2 in Arabidopsis by pathogens has been shown previously to be blocked in the ethylene response mutant ein2-1 and the jasmonate response mutant coi1-1. In this work, we have further investigated the interactions between the ethylene and jasmonate signal pathways for the induction of this defense response. Inoculation of wild-type Arabidopsis plants with the fungus Alternaria brassicicola led to a marked increase in production of jasmonic acid, and this response was not blocked in the ein2-1 mutant. Likewise, A. brassicicola infection caused stimulated emission of ethylene both in wild-type plants and in coi1-1 mutants. However, treatment of either ein2-1 or coi1-1 mutants with methyl jasmonate or ethylene did not induce PDF1.2, as it did in wild-type plants. We conclude from these experiments that both the ethylene and jasmonate signaling pathways need to be triggered concomitantly, and not sequentially, to activate PDF1.2 upon pathogen infection. In support of this idea, we observed a marked synergy between ethylene and methyl jasmonate for the induction of PDF1.2 in plants grown under sterile conditions. In contrast to the clear interdependence of the ethylene and jasmonate pathways for pathogen-induced activation of PDF1.2, functional ethylene and jasmonate signaling pathways are not required for growth responses induced by jasmonate and ethylene, respectively.
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- Beffa R., Szell M., Meuwly P., Pay A., Vögeli-Lange R., Métraux J. P., Neuhaus G., Meins F., Jr, Nagy F. Cholera toxin elevates pathogen resistance and induces pathogenesis-related gene expression in tobacco. EMBO J. 1995 Dec 1;14(23):5753–5761. doi: 10.1002/j.1460-2075.1995.tb00264.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bent A. F., Innes R. W., Ecker J. R., Staskawicz B. J. Disease development in ethylene-insensitive Arabidopsis thaliana infected with virulent and avirulent Pseudomonas and Xanthomonas pathogens. Mol Plant Microbe Interact. 1992 Sep-Oct;5(5):372–378. doi: 10.1094/mpmi-5-372. [DOI] [PubMed] [Google Scholar]
- Berger S., Bell E., Mullet J. E. Two Methyl Jasmonate-Insensitive Mutants Show Altered Expression of AtVsp in Response to Methyl Jasmonate and Wounding. Plant Physiol. 1996 Jun;111(2):525–531. doi: 10.1104/pp.111.2.525. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bleecker A. B., Estelle M. A., Somerville C., Kende H. Insensitivity to Ethylene Conferred by a Dominant Mutation in Arabidopsis thaliana. Science. 1988 Aug 26;241(4869):1086–1089. doi: 10.1126/science.241.4869.1086. [DOI] [PubMed] [Google Scholar]
- Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1006/abio.1976.9999. [DOI] [PubMed] [Google Scholar]
- Brederode F. T., Linthorst H. J., Bol J. F. Differential induction of acquired resistance and PR gene expression in tobacco by virus infection, ethephon treatment, UV light and wounding. Plant Mol Biol. 1991 Dec;17(6):1117–1125. doi: 10.1007/BF00028729. [DOI] [PubMed] [Google Scholar]
- Broekaert W. F., Terras F. R., Cammue B. P., Osborn R. W. Plant defensins: novel antimicrobial peptides as components of the host defense system. Plant Physiol. 1995 Aug;108(4):1353–1358. doi: 10.1104/pp.108.4.1353. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chang C., Kwok S. F., Bleecker A. B., Meyerowitz E. M. Arabidopsis ethylene-response gene ETR1: similarity of product to two-component regulators. Science. 1993 Oct 22;262(5133):539–544. doi: 10.1126/science.8211181. [DOI] [PubMed] [Google Scholar]
- Creelman Robert A., Mullet John E. BIOSYNTHESIS AND ACTION OF JASMONATES IN PLANTS. Annu Rev Plant Physiol Plant Mol Biol. 1997 Jun;48(NaN):355–381. doi: 10.1146/annurev.arplant.48.1.355. [DOI] [PubMed] [Google Scholar]
- Delaney T. P., Uknes S., Vernooij B., Friedrich L., Weymann K., Negrotto D., Gaffney T., Gut-Rella M., Kessmann H., Ward E., Ryals J. A central role of salicylic Acid in plant disease resistance. Science. 1994 Nov 18;266(5188):1247–1250. doi: 10.1126/science.266.5188.1247. [DOI] [PubMed] [Google Scholar]
- Ecker J. R. The ethylene signal transduction pathway in plants. Science. 1995 May 5;268(5211):667–675. doi: 10.1126/science.7732375. [DOI] [PubMed] [Google Scholar]
- Feys BJF., Benedetti C. E., Penfold C. N., Turner J. G. Arabidopsis Mutants Selected for Resistance to the Phytotoxin Coronatine Are Male Sterile, Insensitive to Methyl Jasmonate, and Resistant to a Bacterial Pathogen. Plant Cell. 1994 May;6(5):751–759. doi: 10.1105/tpc.6.5.751. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Friedrich L., Vernooij B., Gaffney T., Morse A., Ryals J. Characterization of tobacco plants expressing a bacterial salicylate hydroxylase gene. Plant Mol Biol. 1995 Dec;29(5):959–968. doi: 10.1007/BF00014969. [DOI] [PubMed] [Google Scholar]
- Gaffney T., Friedrich L., Vernooij B., Negrotto D., Nye G., Uknes S., Ward E., Kessmann H., Ryals J. Requirement of salicylic Acid for the induction of systemic acquired resistance. Science. 1993 Aug 6;261(5122):754–756. doi: 10.1126/science.261.5122.754. [DOI] [PubMed] [Google Scholar]
- Guzmán P., Ecker J. R. Exploiting the triple response of Arabidopsis to identify ethylene-related mutants. Plant Cell. 1990 Jun;2(6):513–523. doi: 10.1105/tpc.2.6.513. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Horvath D. M., Huang D. J., Chua N. H. Four classes of salicylate-induced tobacco genes. Mol Plant Microbe Interact. 1998 Sep;11(9):895–905. doi: 10.1094/MPMI.1998.11.9.895. [DOI] [PubMed] [Google Scholar]
- Kende H., Zeevaart JAD. The Five "Classical" Plant Hormones. Plant Cell. 1997 Jul;9(7):1197–1210. doi: 10.1105/tpc.9.7.1197. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kieber J. J. The ethylene response pathway in Arabidopsis. Annu Rev Plant Physiol Plant Mol Biol. 1997;48:277–296. doi: 10.1146/annurev.arplant.48.1.277. [DOI] [PubMed] [Google Scholar]
- Lamb Chris, Dixon Richard A. THE OXIDATIVE BURST IN PLANT DISEASE RESISTANCE. Annu Rev Plant Physiol Plant Mol Biol. 1997 Jun;48(NaN):251–275. doi: 10.1146/annurev.arplant.48.1.251. [DOI] [PubMed] [Google Scholar]
- Laudert D., Weiler E. W. Allene oxide synthase: a major control point in Arabidopsis thaliana octadecanoid signalling. Plant J. 1998 Sep;15(5):675–684. doi: 10.1046/j.1365-313x.1998.00245.x. [DOI] [PubMed] [Google Scholar]
- Lawton K. A., Potter S. L., Uknes S., Ryals J. Acquired Resistance Signal Transduction in Arabidopsis Is Ethylene Independent. Plant Cell. 1994 May;6(5):581–588. doi: 10.1105/tpc.6.5.581. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lawton K., Weymann K., Friedrich L., Vernooij B., Uknes S., Ryals J. Systemic acquired resistance in Arabidopsis requires salicylic acid but not ethylene. Mol Plant Microbe Interact. 1995 Nov-Dec;8(6):863–870. doi: 10.1094/mpmi-8-0863. [DOI] [PubMed] [Google Scholar]
- Levine A., Tenhaken R., Dixon R., Lamb C. H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell. 1994 Nov 18;79(4):583–593. doi: 10.1016/0092-8674(94)90544-4. [DOI] [PubMed] [Google Scholar]
- O'Donnell PJ, Calvert C, Atzorn R, Wasternack C, Leyser HMO, Bowles DJ. Ethylene as a Signal Mediating the Wound Response of Tomato Plants. Science. 1996 Dec 13;274(5294):1914–1917. doi: 10.1126/science.274.5294.1914. [DOI] [PubMed] [Google Scholar]
- Penninckx I. A., Eggermont K., Terras F. R., Thomma B. P., 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. 1996 Dec;8(12):2309–2323. doi: 10.1105/tpc.8.12.2309. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pieterse C. M., van Wees S. C., Hoffland E., van Pelt J. A., van Loon L. C. Systemic resistance in Arabidopsis induced by biocontrol bacteria is independent of salicylic acid accumulation and pathogenesis-related gene expression. Plant Cell. 1996 Aug;8(8):1225–1237. doi: 10.1105/tpc.8.8.1225. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shirasu K., Dixon R. A., Lamb C. Signal transduction in plant immunity. Curr Opin Immunol. 1996 Feb;8(1):3–7. doi: 10.1016/s0952-7915(96)80097-5. [DOI] [PubMed] [Google Scholar]
- Shulaev V., Leon J., Raskin I. Is Salicylic Acid a Translocated Signal of Systemic Acquired Resistance in Tobacco? Plant Cell. 1995 Oct;7(10):1691–1701. doi: 10.1105/tpc.7.10.1691. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Staswick P. E., Su W., Howell S. H. Methyl jasmonate inhibition of root growth and induction of a leaf protein are decreased in an Arabidopsis thaliana mutant. Proc Natl Acad Sci U S A. 1992 Aug 1;89(15):6837–6840. doi: 10.1073/pnas.89.15.6837. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Uknes S., Mauch-Mani B., Moyer M., Potter S., Williams S., Dincher S., Chandler D., Slusarenko A., Ward E., Ryals J. Acquired resistance in Arabidopsis. Plant Cell. 1992 Jun;4(6):645–656. doi: 10.1105/tpc.4.6.645. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ward E. R., Uknes S. J., Williams S. C., Dincher S. S., Wiederhold D. L., Alexander D. C., Ahl-Goy P., Metraux J. P., Ryals J. A. Coordinate Gene Activity in Response to Agents That Induce Systemic Acquired Resistance. Plant Cell. 1991 Oct;3(10):1085–1094. doi: 10.1105/tpc.3.10.1085. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Xu Y., Chang PFL., Liu D., Narasimhan M. L., Raghothama K. G., Hasegawa P. M., Bressan R. A. Plant Defense Genes Are Synergistically Induced by Ethylene and Methyl Jasmonate. Plant Cell. 1994 Aug;6(8):1077–1085. doi: 10.1105/tpc.6.8.1077. [DOI] [PMC free article] [PubMed] [Google Scholar]