Journal of Chemical Ecology

, Volume 20, Issue 10, pp 2575–2594 | Cite as

Differential induction of tomato foliar proteins by arthropod herbivores

  • Michael J. Stout
  • Jeff Workman
  • Sean S. Duffey


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.

Key words

Plant-insect interactions induced defense proteinase inhibitors polyphenol oxidase peroxidase lipoxygenase Lycopersicon esculentum Helicoverpa zea Liriomyza trifolii Aculops lycopersici phenolics allelochemicals insect nutrition 


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  1. Anonymous. 1990 Integrated Pest Management for Tomatoes. University of California, Statewide Integrated Pest Management Project. Division of Agriculture and Natural Resources 3274.Google Scholar
  2. Baldwin, I.T. 1990. Herbivory simulations in ecological research.Trends Ecol. Evol. 5:91–93.CrossRefGoogle Scholar
  3. 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
  4. Bernays, E.A., andJanzen, D.H. 1988. Saturniid and Sphingid caterpillars: Two ways to eat leaves.ecology 69:1153–1160.Google Scholar
  5. Bostock, R.M., andStermer, B.A. 1989. Perspectives on wound healing in resistance to pathogens.Annu. Rev. Phytopathol. 27:343–371.CrossRefGoogle Scholar
  6. Bowles, D. 1990. Defense-related proteins in higher plants.Annu. Rev. Biochem. 59:873–907.CrossRefPubMedGoogle Scholar
  7. 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.CrossRefGoogle Scholar
  8. 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
  9. 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.PubMedGoogle Scholar
  10. 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
  11. 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
  12. 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
  13. 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.PubMedGoogle Scholar
  14. 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.CrossRefGoogle Scholar
  15. 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.CrossRefGoogle Scholar
  16. 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.CrossRefGoogle Scholar
  17. 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.CrossRefGoogle Scholar
  18. Fowler, S.V., andLawton, J.H. 1985. Rapidly induced defenses and talking trees: the devil's advocate position.Am. Nat. 126:181–195.CrossRefGoogle Scholar
  19. 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
  20. Green, T.R., andRyan, C.A. 1972. Wound-induced proteinase inhibitor in plant leaves: A possible defense against insects.Science 175:776–777.PubMedGoogle Scholar
  21. 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.Google Scholar
  22. 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.CrossRefPubMedGoogle Scholar
  23. 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.CrossRefGoogle Scholar
  24. 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
  25. 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.CrossRefGoogle Scholar
  26. Hildebrand, D.F., andHymowitz, T. 1981. Two soybean genotypes lacking lipoxygenase-1.J. Am. Oil Chem. Soc. 58:583–586.Google Scholar
  27. Hori, K. 1976. Plant growth-regulating factor in the salivary gland of several heteropterous insects.Comp. Biochem. Physiol. 53B:435–438.Google Scholar
  28. Hunter, M.D., andSchultz, J.C. 1993. Induced plant defenses breached? Phytochemical induction protects an herbivore from disease.Oecologia 94:195–203.CrossRefGoogle Scholar
  29. 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.PubMedGoogle Scholar
  30. Karban, R. 1987. Environmental conditions affecting the strength of induced resistance against mites in cotton.Oecologia 73:414–418.CrossRefGoogle Scholar
  31. Karban, R., andMyers, J.H. 1989. Induced plant responses to herbivory.Annu. Rev. Entomol. 20:331–348.Google Scholar
  32. 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.PubMedGoogle Scholar
  33. Kuć, J. 1972. Phytoalexins.Annu. Rev. Phytopathol. 10:207–232.CrossRefGoogle Scholar
  34. 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
  35. Miles, P.W. 1969. Interaction of plant phenols and salivary phenolases in the relationship between plants and Hemiptera.Entomol. Exp. Appl. 12:736–744.CrossRefGoogle Scholar
  36. 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.CrossRefPubMedGoogle Scholar
  37. 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.Google Scholar
  38. 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
  39. 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.CrossRefGoogle Scholar
  40. Ryan, J.D., Gregory, P., andTingey, W. 1982. Phenolic oxidase activities in glandular trichomes ofSolanum berthaultii.Phytochemistry 21:1885–1887.CrossRefGoogle Scholar
  41. 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.Google Scholar
  42. Siedow, J.N. 1991. Plant lipoxygenase: Structure and function.Annu. Rev. Plant Physiol. Plant Mol. Biol. 42:145–188.CrossRefGoogle Scholar
  43. Tallamy, D.W., andRaupp, M.J. 1991. Phytochemical Induction by Herbivores. John Wiley & Sons, New York. 431 pp.Google Scholar
  44. 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

Copyright information

© Plenum Publishing Corporation 1994

Authors and Affiliations

  • Michael J. Stout
    • 1
  • Jeff Workman
    • 1
  • Sean S. Duffey
    • 1
  1. 1.Department of EntomologyUniversity of California, DavisDavis

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