Skip to main content
SpringerLink
Log in

Trade-Offs in Plant Defense Against Pathogens and Herbivores: A Field Demonstration of Chemical Elicitors of Induced Resistance

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

Two signaling pathways, one involving salicylic acid and another involving jasmonic acid, participate in the expression of plant resistance to pathogens and insect herbivores. In this study, we report that stimulation of systemic acquired resistance in field-grown tomato plants with the salicylate mimic, benzothiadiazole: (1) attenuates the jasmonate-induced expression of the antiherbivore defense-related enzyme polyphenol oxidase, and (2) compromises host-plant resistance to larvae of the beet armyworm, Spodoptera exigua. Conversely, treatment of plants with jasmonic acid at concentrations that induce resistance to insects reduces pathogenesis-related protein gene expression induced by benzothiadiazole, and partially reverses the protective effect of benzothiadiazole against bacterial speck disease caused by Pseudomonas syringae pv. tomato. We conclude that effective utilization of induced plant resistance to the multiple pests typically encountered in agriculture will require understanding potential signaling conflicts in plant defense responses.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

REFERENCES

  • Ajlan, A. M., and Potter, D. A. 1992. Lack of effect of tobacco mosaic virus-induced systemic acquired resistance on arthropod herbivores in tobacco. Phytopathology 82:647-651.

    Google Scholar 

  • Alborn, H. T., Turlings, T. C. J., Jones, T. H., Stenhagen, G., Loughrin, J. H., and Tumlinson, J. H. 1997. An elicitor of plant volatiles from beet armyworm oral secretion. Science 276:945-949.

    Google Scholar 

  • Apriyanto, D., and Potter, D. A. 1990. Pathogen-activated induced resistance in cucumber: Response of arthropod herbivores to systemically protected leaves. Oecologia 85:25-31.

    Google Scholar 

  • Bennett, R. N., and Wallsgrove, R. M. 1994. Tanksley review no. 72: Secondary metabolites in plant defence mechanisms. New Phytol. 127:617-633.

    Google Scholar 

  • Broadway, R. M., Duffey, S. S., Pearce, G., and Ryan, C. A. 1986. Plant proteinase inhibitors: A defense against herbivorous insects? Entomol. Exp. Appl. 41:33-38.

    Google Scholar 

  • Carroll, C. R., and Hoffman, C. A. 1980. Chemical feeding deterrent mobilized in response to insect herbivory and counteradaptation. Science 209:414-416.

    Google Scholar 

  • Chen, Z., Ricigliano, J., and Klessig, D. 1993. Purification and characterization of a soluble salicylic-acid binding protein from tobacco. Proc. Natl. Acad. Sci. U.S.A. 90:9533-9537.

    Google Scholar 

  • Choi, D., Bostock, R. M., Avdiushko, S., and Hildebrand, D. F. 1994. Lipid-derived signals that discriminate wound-and pathogen-responsive antimicrobial isoprenoid pathways in plants: Methyl jasmonate and the fungal elicitor arachidonic acid induce different 3-hydroxy-3-methylglutaryl-coenzyme A reductase genes in Solanum tuberosum L. Proc. Natl. Acad. Sci. U.S.A. 91:2329-2333.

    Google Scholar 

  • Dicke, M., Sabelis, M. W., Takabayashi, J., Bruin, J., and Posthumus, M. A. 1990. Plant strategies of manipulating predator-prey interactions through allelochemicals: prospects for application in pest control. J. Chem. Ecol. 16:3091-3118.

    Google Scholar 

  • Doares, S. H., Narvaez-Vasquez, J., Conconi, A., and Ryan, C. A. 1995. Salicylic acid inhibits synthesis of proteinase inhibitors in tomato leaves induced by systemin and jasmonic acid. Plant Physiol. 108:1741-1746.

    Google Scholar 

  • Doherty, H. M., Selvendran, R. R., and D. J. Bowles. 1988. The wound response of tomato plants can be inhibited by aspirin and related hydroxybenzoic acids. Physiol. Mol. Plant Pathol. 33:377-384.

    Google Scholar 

  • Drukker, B., Scutareanu, P., and Sabelis, M. W. 1995. Do anthocorid predators respond to synomones from Psylla-infested pear trees under field conditions? Entomol. Exp. Appl. 77:193-203.

    Google Scholar 

  • Duffey, S. S., and Felton, G. W. 1989. Plant enzymes in resistance to insects, pp. 289-313, in J. Whittaker and P. Sonnet (eds.). Biocatalysis in Agricultural Biotechnology. American Chemical Society, Washington, D.C.

    Google Scholar 

  • Durner, J., Shah, J., and Klessig, D. 1997. Salicylic acid and disease resistance in plants. Trends Plant Sci. 2:266-274.

    Google Scholar 

  • Enyedi, A. J., Yalpani, N., Silverman, P., and Raskin, I. 1992. Signal molecules in systemic plant resistance to pathogens and pests. Cell 70:879-886.

    Google Scholar 

  • Farmer, E. E., Johnson, R. R., and Ryan, C. A. 1992. Regulation of expression of proteinase inhibitor genes by methyl jasmonate and jasmonic acid. Plant Physiol. 98:995-1002.

    Google Scholar 

  • Fidantsef, A. L., Stout, M. J., Thaler, J. S., Duffey, S. S., and Bostock, R. M. 1999. Signal interactions in pathogen and insect attack: expression of lipoxygenase, proteinase inhibitor II, and pathogenesis-related protein P4 in the tomato, Lycopersicon esculentum. Physiol. Mol. Plant Pathol. In press.

  • Ghosh, S., and Kopp, E. 1995. The effect of sodium salicylate and aspirin on nf-kappa-b-response. Science 270:2018-2019.

    Google Scholar 

  • Giamoustaris, A., and Mithen, R. 1995. The effect of modifying the glucosinolate content of leaves of oilseed rape (Brassica napus spp. oleifera) on its interaction with specialist and generalist pests. Ann. Appl. Biol. 126:357-363.

    Google Scholar 

  • Gorlach, J., Volrath, S., Knauf-Beiter, G., Hengy, G., Beckhove, U., Kogel, K. H., Oostendorp, M., Staub, T., Ward, E., Kessmann, H., and Ryals, J. 1996. Benzothiadiazole, a novel class of inducers of systemic acquired resistance, activates gene expression and disease resistance in wheat. Plant Cell 8:629-643.

    Google Scholar 

  • Graham, J., Pearce, G., Merryweather, J., Titani, K., Ericsson, L., and Ryan, C. 1985. Wound-induced proteinase inhibitors from tomato leaves. II. The c-DNA-deduced primary structure of pre-inhibitor II. J. Biol. Chem. 260:6561-6564.

    Google Scholar 

  • Herrmann, G., Lehmann, J., Peterson, A., Sembdner, G., Weidhase, R. A., and Parthier, B. 1989. Species and tissue specificity of jasmonate induced abundant proteins. Plant Physiol. 134:703-709.

    Google Scholar 

  • Karban, R., and Baldwin, I. T. 1997. Induced Responses to Herbivory. University of Chicago Press, Chicago, 319 pp.

    Google Scholar 

  • Karban, R., Adamchak, R., and Schnathorst, W. C. 1987. Induced resistance and interspecific competition between spider mites and a vascular wilt fungus. Science 235:678-679.

    Google Scholar 

  • Kessmann, H., Staub, T., Hofmann, C., Maetzke, T., Herzog, J., Ward, E., Uknes, S., and Ryals, J. 1994. Induction of systemic acquired resistance in plants by chemicals. Annu. Rev. Phytopathol. 32:439-459.

    Google Scholar 

  • Krischik, V. A., Goth, R. W., and Barbosa, R. 1991. Generalized plant defense: Effects on multiple species. Oecologia 85:562-571.

    Google Scholar 

  • Li, J., Zingen-Sell, I., and Buchenauer, H. 1996. Induction of resistance of cotton plants to Verticillium wilt and of tomato plants to Fusarium wilt by 3-aminobutyric acid and methyl jasmonate. Z. Pflanzenkr. Pflanzenschutz 103:288-299.

    Google Scholar 

  • Linhart, Y. B. 1991. Disease, parasitism and herbivory: Multidimensional changes in plant evolution. TREE 6:392-396.

    Google Scholar 

  • McIntyre, J. L., Dodds, J. A., and Hare, J. D. 1981. Effects of localized infections of Nicotiana tabacum by tobacco mosaic virus on systemic resistance against diverse pathogens and an insect. Phytopathology 71:297-301.

    Google Scholar 

  • Pan, Z., Camara, B., Gardner, H., and Backhaus, R. 1998. Aspirin inhibition and acetylation of the plant cytochrome P450, allene oxide synthase, resemble that of animal prostaglandin endoperoxide H synthase. J. Biol. Chem. 273:18139-18145.

    Google Scholar 

  • Pena-Cortes, H., Albrecht, T., Prat, S., Weiler, E. W., and Willmitzer, L. 1993. Aspirin prevents wound-induced gene expression in tomato leaves by blocking jasmonic acid biosynthesis. Planta 191:123-128.

    Google Scholar 

  • Penninckx, I. A. M. A., Eggermont, K., Terras, F. R. G., Thomma, B. P. H. J., De Samblanx, G. W., Buchala, A., Metraux, J.-P., Manners, J. M., and Broekaert, W. F. 1996. Pathogen-induced systemic activation of a plant defensin gene in Arabidopsis follows a salicylic acid-independent pathway. Plant Cell 8:2309-2323.

    Google Scholar 

  • Pieterse, C. M., van Wees, S. C. M., van Pelt, J. A., Knoester, M., Laan, R., Gerrits, H., Weisbeck, P. J., and van Loon, L. C. 1998. A novel signaling pathway controlling induced systemic resistance in Arabidopsis. Plant Cell 10:1571-1580.

    Google Scholar 

  • RÜffer, M., Steipe, B., and Zenk, M. 1995. Evidence against specific binding of salicylic acid to plant catalase. FEBS Lett. 377:175-180.

    Google Scholar 

  • Ryals, J. A., Ward, E., Ahl-Goy, P., and Metraux, J. P. 1992. Systemic acquired resistance: An inducible defense mechanism in plants, pp. 205-229, in J. L. Wray (ed.). Inducible Plant Proteins: Their Biochemistry and Molecular Biology. Cambridge University Press, Cambridge, U.K.

    Google Scholar 

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

    Google Scholar 

  • Sano, H., and Ohashi, Y. 1995. Involvement of small GTP-binding proteins in defense signal-transduction pathways of higher plants. Proc. Natl. Acad. Sci. U.S.A. 92:4138-4144.

    Google Scholar 

  • Schneider, M., Schweizer, P., Meuwly, P., and Metraux, J. P. 1996. Systemic acquired resistance in plants. Int. Rev. Cytol. 168:303-339.

    Google Scholar 

  • Shimoda, T., Takabayashi, J., Ashihara, W., and Takafuji, A. 1997. Response of predatory insect Scolothrips takahashii toward herbivore-induced plant volatiles under laboratory and field conditions. J. Chem. Ecol. 23:2033-2048.

    Google Scholar 

  • Sih, A., Englund, G., and Wooster, D. 1998. Emergent impacts of multiple predators on prey. Trends Ecol. Evol. 13:350-355.

    Google Scholar 

  • Stout, M. J., Workman, K. V., Bostock, R. M., and Duffey, S. S. 1998. Specificity of induced resistance in the tomato, Lycopersicon esculentum. Oecologia 113:74-81.

    Google Scholar 

  • Stout, M. J., Fidantsef, A. L., Duffey, S. S., and Bostock, R. M. 1999. Signal interactions in pathogen and insect attack: systemic plant-mediated interactions between pathogens and herbivores of the tomato, Lycopersicon esculentum. Physiol. Mol. Plant Pathol. In press.

  • Strand, L. L., and Rude, P. A. (eds.). 1998. Integrated Pest Management for Tomatoes, 4th ed. University of California Statewide Integrated Pest Management Project, Division of Agriculture and Natural Resources. Publication 3274.

  • Thaler, J. S. 1999. Jasmonate-inducible plant defenses cause increased parasitism of herbivores. Nature In press.

  • Thaler, J. S., Stout, M. J., Karban, R., and Duffey, S. S. 1996. Exogenous jasmonates simulate insect wounding in tomato plants (Lycopersicon esculentum) in the laboratory and field. J. Chem. Ecol. 22:1767-1781.

    Google Scholar 

  • Thomma, B. P. H. J., Eggermont, K., Penninckx, I. A. M. A., Mauch-Mani, B., Vogelsang, R., Cammue, B. P. A., and Broekaert, W. F. 1998. Separate jasmonate-dependent and salicylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. Proc. Natl. Acad. Sci. U.S.A. 95:15107-15111.

    Google Scholar 

  • Turlings, T. C. J., Tumlinson, J. H., and Lewis, W. J. 1990. Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science 250:1251-1253.

    Google Scholar 

  • Vijayan, P., Shockey, J., Levesque, C. A., Cook, R. J., and Browse, J. 1998. A role for jasmonate in pathogen defense of Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 95:7209-7214.

    Google Scholar 

Download references

Author information

Author notes

  1. Ana L. Fidantsef

    Present address: Section of Plant Biology, University of California, Davis, California, 95616

Authors and Affiliations

  1. Department of Entomology, University of California at Davis, Davis, California, 95616

    Jennifer S. Thaler & Sean S. Duffey

  2. Department of Plant Pathology, University of California at Davis, Davis, California, 95616.

    Ana L. Fidantsef & Richard M. Bostock

Authors
  1. Jennifer S. Thaler
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ana L. Fidantsef
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sean S. Duffey
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Richard M. Bostock
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Thaler, J.S., Fidantsef, A.L., Duffey, S.S. et al. Trade-Offs in Plant Defense Against Pathogens and Herbivores: A Field Demonstration of Chemical Elicitors of Induced Resistance. J Chem Ecol 25, 1597–1609 (1999). https://doi.org/10.1023/A:1020840900595

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1020840900595

Search

Navigation