Skip to main content
Log in

Differential induction of tomato foliar proteins by arthropod herbivores

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

Abstract

The effects of mechanical and chemical damage and three types of biotic damage on the activities of four foliar proteins of the tomato plant (Lycopersicon esculentum Mill var. Castlemart) were assayed. Proteinase inhibitor, polyphenol oxidase, peroxidase, and lipoxygenase activities were assayed in damaged leaflets and compared with activities in undamaged leaflets. These proteins are putative plant defenses in tomato. Differential induction of these proteins by the various damage-treatments was demonstrated, such that different subsets of the four proteins were induced by different types of damage. This study clearly demonstrates the ability of plants to respond differentially to different types of damage. Possible mechanisms for this differential induction and the implications of differential induction for plant defense are discussed.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Anonymous. 1990 Integrated Pest Management for Tomatoes. University of California, Statewide Integrated Pest Management Project. Division of Agriculture and Natural Resources 3274.

  • Baldwin, I.T. 1990. Herbivory simulations in ecological research.Trends Ecol. Evol. 5:91–93.

    Article  Google Scholar 

  • Baldwin, I.T. 1993. Chemical changes rapidly induced by folivory, pp. 1–23,in E.A. Bernays (ed). Insect-Plant Interactions, Vol. 5. CRC Press, Boca Raton, Florida. 240 pp.

    Google Scholar 

  • Bernays, E.A., andJanzen, D.H. 1988. Saturniid and Sphingid caterpillars: Two ways to eat leaves.ecology 69:1153–1160.

    Google Scholar 

  • Bostock, R.M., andStermer, B.A. 1989. Perspectives on wound healing in resistance to pathogens.Annu. Rev. Phytopathol. 27:343–371.

    Article  Google Scholar 

  • Bowles, D. 1990. Defense-related proteins in higher plants.Annu. Rev. Biochem. 59:873–907.

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Coleman, J.S., andJones, C.G. 1991. A phytocentric perspective of phytochemical induction by herbivores, pp. 3–45,in D.W. Tallamy and M.J. Raupp (eds.). Phytochemical Induction by Herbivores. John Wiley & Sons, New York. 431 pp.

    Google Scholar 

  • Droillard, M., Rouet-Mayer, M., Bureau, J., andLauriere, C. 1993. Membrane-associated and soluble lipoxygenase isoforms in tomato pericarp. Characterization and involvement in membrane alteration.Plant Physiol. 103:1211–1219.

    PubMed  CAS  Google Scholar 

  • Duffey, S.S., andFelton, G.W. 1989. Role of plant enzymes in resistance to insects, pp. 289–313, J.R. Whitaker and P.E. Sonnet (eds.)in Biocatalysis. Agricultural Biotechnology. ACS Symposium Series 389. American Chemical Society, Washington, D.C.

    Google Scholar 

  • Duffey, S.S., andFelton, G.W. 1991. Enzymatic antinutritive defenses of the tomato plant against insects, pp. 167–197in P.A. Hedin (ed.). Naturally Occurring Pest Bioregulators. ACS Symposium Series 449. Dallas, Fall, 1989. American Chemical Society, Washington, D.C.

    Google Scholar 

  • Elstner, E.F. 1980. Metabolism of activated oxygen species, pp. 253–315,in D.D. Davies (ed.). The Biochemistry of Plants. A Comprehensive Treatise. Vol. 11. Biochemistry and Metabolism. Academic Press, New York. 388 pp.

    Google Scholar 

  • Farmer, E.E., andRyan, A.R. 1990. Interplant communication: Airborne methyl jasmonate induces synthesis of proteinase inhibitors in plant leaves.Proc. Natl. Acad. Sci. U.S.A. 87:7713–7716.

    PubMed  CAS  Google Scholar 

  • Felton, G.W., Donato, K., Del Vecchio, R.J., andDuffey, S.S. 1989a. Activation of plant polyphenol oxidases by insect feeding reduces the nutritive quality of foliage for noctuid herbivores.J. Chem. Ecol. 15:2667–2694.

    Article  CAS  Google Scholar 

  • Felton, G.W., Broadway, R.M., andDuffey, S.S. 1989b. Inactivation of proteinase inhibitor activity by plant-derived quinones: Complications for host-plant resistance against noctuid herbivores.J. Insect Physiol. 35:981–990.

    Article  CAS  Google Scholar 

  • Felton, G.W., Donato, K.K., Broadway, R.M., andDuffey, S.S. 1992. Impact of oxidized plant phenolics on the nutritional quality of dietary protein to a noctuid herbivore.J. Insect Physiol. 38:277–285.

    Article  CAS  Google Scholar 

  • Felton, G.W., Summers, C.B. andMueller, A.J. 1994. Oxidative responses in soybean foliage to herbivory by bean leaf beetle and three-cornered alfalfa hopper.J. Chem. Ecol. 20:639–649.

    Article  CAS  Google Scholar 

  • Fowler, S.V., andLawton, J.H. 1985. Rapidly induced defenses and talking trees: the devil's advocate position.Am. Nat. 126:181–195.

    Article  Google Scholar 

  • Gentile, I.A., Ferraris, L., andMatta, A. 1988. Variations of polyphenoloxidase activities as a consequence of stresses that induce resistance to Fusarium wilt of tomato.J. Phytopathol. 122:45–53.

    Google Scholar 

  • Green, T.R., andRyan, C.A. 1972. Wound-induced proteinase inhibitor in plant leaves: A possible defense against insects.Science 175:776–777.

    PubMed  CAS  Google Scholar 

  • Grisham, M.P., Sterling, W.L., Powell, R.D., andMorgan, W. 1987. Characterization of the induction of stress ethylene in cotton caused by the cotton fleahopper (Hemiptera: Miridae) and its microorganisms.Ann. Entomol. Soc. Am. 80:411–416.

    CAS  Google Scholar 

  • Hain, R., Reif, H., Krause, E., Langebartels, R., Kindl, H., Vornam, B., Wiese, W., Schmelzer, E., Schreier, P.H., Stocker, R.H., andStenzel, K. 1993. Disease resistance results from foreign phytoalexin expression in a novel plant.Nature 361:153.

    Article  PubMed  CAS  Google Scholar 

  • Hartley, S.E., andLawton, J.H. 1987. Effects of different types of damage on the chemistry of birch foliage, and the responses of birch feeding insects.Oecologia 74:432–437.

    Article  Google Scholar 

  • Hartley, S.E., andLawton, J.H. 1991. Biochemical aspects and significance of the rapidly induced accumulation of phenolics in birch foliage, pp. 105–132,in D.W. Tallamy and M.J. Raupp (eds.). Phytochemical Induction by Herbivores. John Wiley & Sons, New York. 431 pp.

    Google Scholar 

  • Haukioja, E., andHanhimaki, S. 1985. Rapid wound-induced resistance in white birch (Betula pubescens) foliage to the geometridEpirrita autumnata: A comparison of trees and moths within and outside the outbreak range of the moth.Oecologia 65:223–228.

    Article  Google Scholar 

  • Hildebrand, D.F., andHymowitz, T. 1981. Two soybean genotypes lacking lipoxygenase-1.J. Am. Oil Chem. Soc. 58:583–586.

    CAS  Google Scholar 

  • Hori, K. 1976. Plant growth-regulating factor in the salivary gland of several heteropterous insects.Comp. Biochem. Physiol. 53B:435–438.

    Google Scholar 

  • Hunter, M.D., andSchultz, J.C. 1993. Induced plant defenses breached? Phytochemical induction protects an herbivore from disease.Oecologia 94:195–203.

    Article  Google Scholar 

  • Johnson, R., Narvaez, J., An, G., andRyan, C.A. 1989. Expression of proteinase inhibitors I and II in transgenic tobacco plants: Effects on natural defense againstManduca sexta larvae.Proc. Natl. Acad. Sci. U.S.A. 86:9871–9875.

    PubMed  CAS  Google Scholar 

  • Karban, R. 1987. Environmental conditions affecting the strength of induced resistance against mites in cotton.Oecologia 73:414–418.

    Article  Google Scholar 

  • Karban, R., andMyers, J.H. 1989. Induced plant responses to herbivory.Annu. Rev. Entomol. 20:331–348.

    Google Scholar 

  • Koch, E., Meier, B.M., andSlusarenko, A. 1992. A lipoxygenase from leaves of tomato (Lycopersicon esculentum Mill) is induced in response to plant pathogenic pseudomonads.Plant Physiol. 99:571–576.

    PubMed  CAS  Google Scholar 

  • Kuć, J. 1972. Phytoalexins.Annu. Rev. Phytopathol. 10:207–232.

    Article  Google Scholar 

  • Lin, H., Kogan, M., andFischer, D. 1990. Induced resistancein soybean to the Mexican bean beetle (Colepotera: Coccinellidae): Comparison of inducing factors.Environ. Entomol. 19:1852–1857.

    Google Scholar 

  • Miles, P.W. 1969. Interaction of plant phenols and salivary phenolases in the relationship between plants and Hemiptera.Entomol. Exp. Appl. 12:736–744.

    Article  CAS  Google Scholar 

  • Mohan, R., andKolattukudy, P.E. 1990. Differential activation of expression of a suberizationassociated anionic peroxidase gene in near-isogenic resistant and susceptible tomato lines by elicitors ofverticillium albo-atratum.Plant Physiol. 92:276–280.

    Article  PubMed  CAS  Google Scholar 

  • Olson, M.M., andRoseland, C.R. 1991. Induction of the coumarins scopletin and ayapin in sunflower by insect-feeding stress and effects of coumarins on the feeding of sunflower beetle (Coleoptera: Chrysomelidae).Environ. Entomol. 20:1166–1172.

    CAS  Google Scholar 

  • Parrella, M.P., Jones, V.P., Youngman, R.R., andLebeck, L.M. 1985. Effect of leaf mining and leaf stippling ofLiriomyza spp. on photosynthetic rates of chrysanthemum.Ann. Entomol. Soc. Am. 78:90–93.

    Google Scholar 

  • Ryan, C.A., Bishop, P.D., Graham, J.S., Broadway, R.M., andDuffey, S.S. 1985. Plant and fungal cell wall fragments activate the expression of proteinase inhibitor genes for plant defense.J. Chem. Ecol. 12:1025–1036.

    Article  Google Scholar 

  • Ryan, J.D., Gregory, P., andTingey, W. 1982. Phenolic oxidase activities in glandular trichomes ofSolanum berthaultii.Phytochemistry 21:1885–1887.

    Article  CAS  Google Scholar 

  • Shukle, R.H., andMurdock, L.L. 1983. Lipoxygenase, trypsin inhibitor, and lectin from soybeans: Effects on larval growth of Manduca sexta (Lepidoptera: Sphingidae).Environ. Entomol. 12:787–791.

    CAS  Google Scholar 

  • Siedow, J.N. 1991. Plant lipoxygenase: Structure and function.Annu. Rev. Plant Physiol. Plant Mol. Biol. 42:145–188.

    Article  CAS  Google Scholar 

  • Tallamy, D.W., andRaupp, M.J. 1991. Phytochemical Induction by Herbivores. John Wiley & Sons, New York. 431 pp.

    Google Scholar 

  • Wolfson, J.L. 1991. The effects of induced plant proteinase inhibitors on herbivorous insects, pp. 223–244,in D.W. Tallamy and M.J. Raupp (eds.). Phytochemical Induction by Herbivores. John Wiley & Sons, New York. 431 pp.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Stout, M.J., Workman, J. & Duffey, S.S. Differential induction of tomato foliar proteins by arthropod herbivores. J Chem Ecol 20, 2575–2594 (1994). https://doi.org/10.1007/BF02036193

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02036193

Key words

Navigation