Skip to main content
Log in

Oxidative responses in soybean foliage to herbivory by bean leaf beetle and three-cornered alfalfa hopper

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

Abstract

Variation in induced responses in soybean is shown to be dependent, in part, upon herbivore species. Herbivory by the phloem-feeding three-cornered alfalfa hopper caused increases in the activities of several oxidative enzymes including lipoxygenases, peroxidases, ascorbate oxidase, and polyphenol oxidase. Bean leaf beetle defoliation caused increased lipoxygenase activity, but had little effect upon peroxidase, polyphenol oxidase, ascorbate oxidase, or trypsin inhibitor levels in either field or greenhouse studies. In one field experiment, prior herbivory by the bean leaf beetle subsequently reduced the suitability of foliage to the corn earwormHelicoverpa zea. The contribution of these findings to emerging theories of insect-plant interactions is 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

  • Ahmad, S. 1992. Biochemical defence of pro-oxidant plant allelochemicals by herbivorous insects.Biochem. Syst. Ecol. 20:269–296.

    Google Scholar 

  • Ahmad, S., andPardini, R.S. 1990. Antioxidant defense of the cabbage looper,Trichoplusia ni: Enzymatic responses to the superoxide-generating flavonoid, quercetin, and photodynamic furanocoumarin, xanthotoxin.Photochem. Photobiol. 51:305–311.

    Google Scholar 

  • Apostol, I., Bohlmann, H., andReimann-Philipp, U.R. 1989. Rapid stimulation of an oxidative burst during the elicitation of cultured plant cells.Plant Physiol. 90:109–116.

    Google Scholar 

  • Aucoin, R.R., Fields, P., Lewis, M.A., Philogene, B.J.R., andArnason, J.T. 1990. The protective effects of antioxidants to a phototoxin-sensitive insect herbivore,Manduca sexta.J. Chem. Ecol. 16:2913–2924.

    Google Scholar 

  • Baysal, E., Sullivan, S.G., andStern, A. 1989. Prooxidant and antioxidant effects of ascorbate ont-BuOOH-induced erythrocyte membrane damage.Int. J. Biochem. 21:1109–1113.

    PubMed  Google Scholar 

  • Bell, A.A., Stipanovich, R.D., Elzen, G.W., andWilliams, H.J., Jr. 1987. Structural and genetic variation of natural pesticides in pigment glands of cotton (Gossypium), pp. 477–490, G.R. Waller (ed.). Allelochemicals: Role in Agriculture and Forestry. American Chemical Society, Washington, D.C.

    Google Scholar 

  • Berenbaum, M.R. 1978. Toxicity of a furanocoumarin to armyworms: A case of biosynthetic escape from insect herbivores.Science 201:532–534.

    Google Scholar 

  • Broadway, R.M., andColvin, A.A. 1992. Influence of cabbage proteinase inhibitorsin situ on the growth of larvalTrichoplusia ni andPieris rapae.J. Chem. Ecol. 18:1009–1024.

    Google Scholar 

  • Chamulitrat, W., Hughes, M.F., Eling, T.E., andMason, R.P. 1991. Superoxide and peroxyl radical generation from the reduction of polyunsaturated fatty acid hydroperoxides by soybean lipoxygenase.Arch. Biochem. Biophys. 290:153–159.

    PubMed  Google Scholar 

  • Cheynier, V.F., andVan Hulst, M.W.J. 1988. Oxidation oftrans-caftaric acid and 2-S-glutathionylicaftaric acid in model solutions.J. Agric. Food Chem. 36:10–14.

    Google Scholar 

  • Chiang, H.S., Norris, D.M., Ciepiela, A., Shapiro, P. andOosterwyk, A. 1987. Inducible versus constitutive PI 227687 soybean resistance to Mexican bean beetle,Epilachna varivestis.J. Chem. Ecol. 13:741–749.

    Google Scholar 

  • Chippendale, G.M. 1970. Metamorphic changes in fat body proteins of the southwestern corn borerDiatraea grandiosella.J. Insect. Physiol. 16:1057–1068.

    PubMed  Google Scholar 

  • Duffey, S.S., andFelton, G.W. 1991. Enzymatic antinutritive defenses of the tomato plant against insects, pp. 166–197,in P.A. Hedin (ed). Naturally Occurring Pest Bioregulators. American Chemical Society, Washington, D.C.

    Google Scholar 

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

    PubMed  Google Scholar 

  • Esaka, M., Nishitani, I., Fukui, H., Suzuki, K., andKubota, K. 1989. Stimulation of ascorbate oxidase secretion from cultured pumpkin cells by divalent cations.Phytochemistry 28:2655–2658.

    Google Scholar 

  • Faeth, S.H. 1986. Indirect interactions between temporally separated herbivores mediated by the host plant.Ecology 67:479–494.

    Google Scholar 

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

    PubMed  Google Scholar 

  • Farmer, E.E., andRyan, C.A. 1992. Octadeconoid precursors of jasmonic acid activate the synthesis of wound-inducible proteinase inhibitors.Plant Cell 4:129–134.

    PubMed  Google Scholar 

  • Felton, G.W., andDuffey, S.S. 1991. Protective action of midgut catalase in lepidopteran larvae against oxidative plant defenses.J. Chem. Ecol. 17:1715–1732.

    Google Scholar 

  • Felton, G.W., andSummers, C.B. 1993. Potential role of ascorbate oxidase as a plant defense protein against insect herbivory.J. Chem. Ecol. 19:1553–1568.

    Google Scholar 

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

    Google Scholar 

  • Felton, G.W., Workman, J., andDuffey, S.S. 1992a. Avoidance of antinutritive plant defense: Role of midgut pH in Colorado potato beetle.J. Chem Ecol. 18:571–583.

    Google Scholar 

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

    Google Scholar 

  • Fehr, W.R., andCaviness, C.E. 1977. Stages of soybean development. Iowa Cooperative Extension Service Report 80.

  • Gaspar, T., Prel, C., Thorpe, T.A., andGreppin, H. 1981. Peroxidases, 1970–1981. University of Geneva Press, Geneva.

    Google Scholar 

  • Grankvist, K. 1989. Gossypol-induced free radical toxicity to isolated islet cells.Int. J. Biochem. 21:853–856.

    PubMed  Google Scholar 

  • Grayburn, W.S., Schneider, G.R., Hamilton-Kemp, T.R., Bookjans, G., Ali, K., andHildebrand, D.F. 1991. Soybean leaves contain multiple lipoxygenases.Plant Physiol. 95:1214–1218.

    Google Scholar 

  • Grimes, H.D., Koetje, D.S., andFranceschi, V.R. 1992. Expression, activity, and cellular accumulation of methyl jasmonate-responsive lipoxygenase in soybean seedlings.Plant Physiol. 100:433–443.

    Google Scholar 

  • Halliwell, B. 1991. The biological toxicity of free radicals and other reactive oxygen species, pp. 37–58,in O.I. Arouma and B. Halliwell (eds.) Free Radicals and Food Additives. Taylor and Francis, New York.

    Google Scholar 

  • Hanham, A.F., Dunn, B.P., andStich, H.F. 1983. Clastogenic activity of caffeic acid and it relationship to hydrogen peroxide generated during autooxidation.Mutat. Res. 116:333–339.

    PubMed  Google Scholar 

  • Harrison, S., andKarban, R. 1986. Effects of any early season folivorous moth on the success of a later-season species, mediated by a change in the quality of the shared host,Lupinus arboreus Sims.Oecologia 69:354–359.

    Google Scholar 

  • Hildebrand, D.F. 1992. Altering fatty acid metabolism in plants.Food Technol. 46:71–74.

    Google Scholar 

  • Hildebrand, D.F., Rodriguez, J.G., Brown, G.C., andVolden, C.S. 1986a. Twospotted spider mite (Acari: Tetranychidae) infestations on soybeans: Effect on composition and growth of susceptible and resistant cultivars.J. Econ. Entomol. 79:915–921.

    Google Scholar 

  • Hildebrand, D.F., Rodriguez, J.G., Brown, G.C., Luu, K.T., andVolden, C.S. 1986b. Peroxidative responses of leaves in two soybean genotypes injured by twospotted spider mites (Acari: Tetranychidae).J. Econ. Entomol. 79:1459–1465.

    Google Scholar 

  • Hildebrand, D.F., Hamilton-Kemp, T.R., Legg, C.S., andBookjans, G. 1988. Plant lipoxygenases: Occurrence, properties and possible functions.Curr. Top. Plant. Biochem. Physiol. 7:201–219.

    Google Scholar 

  • Hildebrand, D.F., Rodriguez, J.G., Legg, C.S., Brown, G.C., andBookjans, G. 1989. The effects of wounding and mite infestation on soybean leaf lipoxygenase levels.Z. Naturforsch. 44:655–659.

    Google Scholar 

  • Hodnick, W.F., Kalyanaraman, B., Pristos, C.A., andPardini, R.S. 1989. The production of hydroxyl and semiquinone free radicals during the autoxidation of redox active flavonoids, pp. 149–152,in M.G. Simic, K.A. Taylor, J.F. Ward, and C. von Sonntag (eds.) Oxygen Radicals in Biology and Medicine. Plenum Press, New York.

    Google Scholar 

  • Iyengar, S., Arnason, J.T., Philogene, B.J.R., Morand, P., Werstiuk, N.H. andTimmins, G. 1987. Toxicokinetics of the phototoxic allelochemical α-terthienyl in three herbivorous Lepidoptera.Pestic. Biochem. Physiol. 29:1–5.

    Google Scholar 

  • Joshi, P.C. andPathak, M.A. 1983. Production of singlet oxygen and superoxide radicals by psoralens and their biological significance.Biochem. Biophys. Res. Commun. 112:638–646.

    PubMed  Google Scholar 

  • Kanofsky, J.R., andAxelrod, B. 1986. Singlet oxygen production by soybean lipoxygenase isozymes.J. Biol. Chem. 261:1099–1104.

    PubMed  Google Scholar 

  • Karban, R., 1986. Interspecific competition between folivorous insects onErigeron glaucus.Ecology 67:1063–1072.

    Google Scholar 

  • Karban, R., andEnglish-Loeb, G.M. 1990. A “vaccination” of Willamette spider mites (Acari: Tetranychidae) to prevent large populations of Pacific spider mites on grapevines.J. Econ. Entomol. 83:2252–2257.

    Google Scholar 

  • Kraemer, M.E., Rangappa, M., Gade, W., andBenepal, P.S., 1987. Induction of trypsin inhibitors in soybean leaves by Mexican bean beetle (Coleoptera: Cocinellidae) defoliation.J. Econ. Entomol. 80:327–341.

    Google Scholar 

  • Lee, K., andBerenbaum, M.R., 1989. Action of antioxidant enzymes and cytochrome P-450 monoxygenases in the cabbage looper in response to plant phototoxins,Arch. Insect Biochem. Physiol. 10:151–162.

    Google Scholar 

  • Lee, K., andBerenbaum, M.R. 1990. Defense of parsnip webworm against phototoxic furanocoumarins: Role of antioxidant enzymes.J. Chem. Ecol. 16:2451–2460.

    Google Scholar 

  • Legendre, L., Rueter, S., Heinstein, P.F., andLow, P.S., 1993. Characterization of the oligogalacturonide-induced oxidative burst in cultured soybean (Glycine max) cells.Plant Physiol. 102:233–240.

    PubMed  Google Scholar 

  • MacAdam, J.W., Nelson, C.J., Sharp, R.E., 1992. Peroxidase activity in the leaf elongation zone of tall fescue.Plant Physiol. 99:872–878.

    Google Scholar 

  • Mohri, S., Endo, Y., Matsuda, K., Kitamura, K., andFujimoto, K. 1990. Physiological effects of soybean seed lipoxygenases on insects.Agric. Biol. Chem. 54:2265–2270.

    Google Scholar 

  • Neupane, F.P., andNorris, D.M. 1991a. Sulfhydryl-reagent alteration of soybean resistance to the cabbage looper,Trichoplusia ni.Entomol. Exp. Appl. 60:239–245.

    Google Scholar 

  • Neupane, F.P., andNorris, D.M. 1991b. α-Tocopherol alteration of soybean antiherbivory toTrichoplusia ni.J. Chem. Ecol. 17:1941–1951.

    Google Scholar 

  • Nishimura, K., Ohtsura, M., andNigota, K. 1989. Effect of ascorbic acid and dehydroascorbic acid on ovalbumin.J. Agric. Food Chem. 37:1544–1547.

    Google Scholar 

  • Pierpoint, W.S. 1983. Reactions of phenolic compounds with proteins, and their relevance to the production of leaf protein, pp. 235–267,in L. Telek and H. Graham (eds.) Leaf Protein Concentrates. Avi Publishing, Westport, Connecticut.

    Google Scholar 

  • Rubinstein, B. 1992. Similarities between plants and animals for avoiding predation and disease.Physiol. Zool. 65:473–492.

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Sutherland, M.W. 1991. The generation of oxygen radicals during host plant responses to infection.Physiol. Mol. Plant Pathol. 39:79–83.

    Google Scholar 

  • Tallamy, D., andKrischik, V.A. 1989. Variation and function of cucurbitacins inCucurbita: an examination of current hypotheses.Am. Nat. 133:766–786.

    Google Scholar 

  • Vera-Estrella, T., Blumwald, E., andHiggins, V.J. 1992. Effect of specific elicitors ofCladosporium fulvum on tomato suspension cells.Plant Physiol. 99:1208–1215.

    Google Scholar 

  • Vianello, A., andMacri, F. 1991. Generation of superoxide anion and hydrogen peroxide at the surface of plant cells.J. Bioenerg. Biomembr. 23:409–423.

    PubMed  Google Scholar 

  • Waldbauer, G.P. 1968. The consumption and utilization of food by insects.Adv. Insect Physiol. 5:229–288.

    Google Scholar 

  • Zacheo, G. andBleve-Zacheo, T. 1988. Involvement of superoxide dismutases and superoxide radicals in the susceptibility and resistance of tomato plants toMeliodogyne incognita attack.Physiol. Mol. Plant Pathol. 32:313–322.

    Google Scholar 

  • Zangerl, A.R. 1990. Furanocoumarin induction in wild parsnip: Evidence for an induced defense against herbivores.Ecology 71:1926–1932.

    Google Scholar 

  • Zangerl, A.R., andBerenbaum, M.R. 1990. Furanocoumarin induction in parsnip: Genetics and population variation.Ecology 71:1933–1940.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Felton, G.W., Summers, C.B. & Mueller, A.J. Oxidative responses in soybean foliage to herbivory by bean leaf beetle and three-cornered alfalfa hopper. J Chem Ecol 20, 639–650 (1994). https://doi.org/10.1007/BF02059604

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02059604

Key Words

Navigation