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Potential role of lipoxygenases in defense against insect herbivory

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Abstract

The potential role of the plant enzyme lipoxygenase in host resistance against the corn earwormHelicoverpa zea was examined. Lipoxygenase is present in most of the common host plants ofH. zea, with highest activity in the leguminous hosts such as soybean and redbean. Treatment of dietary proteins with linoleic acid and lipoxygenase significantly reduced the nutritive quality of soybean protein and soy foliar protein. Larval growth was reduced from 24 to 63% depending upon treatment. Feeding byH. zea on soybean plants caused damage-induced increases in foliar lipoxygenase and lipid peroxidation products. Larvae feeding on previously wounded plant tissue demonstrated decreased growth rates compared to larvae feeding on unwounded tissue. Midgut epithelium from larvae feeding on wounded tissues showed evidence of oxidative damage as indicated by significant increases in lipid peroxidation products and losses in free primary amines. The potential role of oxidative and nutritional stress as a plant defensive response to herbivory is discussed.

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References

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

    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 

  • Baggliolini, M., andWymann, M.P. 1990. Turning on the respiratory burst.Trends Biochem. Sci. 15:69–72.

    PubMed  Google Scholar 

  • Bi, J.L., Felton, G.W., andMueller, A.J. 1994. Induced resistance in soybean toHelicoverpa zea: Role of plant protein quality.J. Chem. Ecol. 20:183–198.

    Google Scholar 

  • Bronner, R., Westphal, E., andDreger, F. 1991. Enhanced peroxidase activity associated with the hypersensitive response ofSolanum dulcamara to the gall miteAceria cladophtirus (Acari: Eriophyoidea).Can. J. Bot. 69:2192–2196.

    Google Scholar 

  • Burden, B.J., andNorris, D.M. 1992. Role of the isoflavonoid coumestrol in the constitutive antixenosic properties of Davis soybeans against an oligophagous insect, the Mexican bean beetle.J. Chem. Ecol. 18:1069–1081.

    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 

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

    PubMed  Google Scholar 

  • Choudhuri, M.A., 1988. Free radicals and leaf senescence—a review.Plant. Physiol. Biochem. 15:18–29.

    Google Scholar 

  • Croft, K.P.C., Voisey, C.R., andSlusarenko, A.J. 1990. Mechanism of hypersensitive cell collapse: Correlation of increased lipoxygenase activity with membrane damage in leaves ofPhaseolus vulgaris (L.) inoculated with an avirulent race ofPseudomonas syringae pv.phaseolicola.Physiol Mol. Plant Pathol. 36:49–62.

    Google Scholar 

  • Davis, D., Merida, J., Legendre, L., Low, P.S., andHeinstein, P. 1993. Independent elicitation of the oxidative burst and phytoalexin formation in cultured plant cells.Phytochemistry 32:607–611.

    Google Scholar 

  • Dillworth, J.W., Berberet, R.C., Bergman, D.K., Neese, P.A., Edwards, R.M., andMcNew, R.W. 1991. Plant biochemistry and aphid populations: Studies on the spotted alfalfa aphid,Therioaphis maculata.Arch. Insect Biochem. Physiol. 17:235–251.

    Google Scholar 

  • Doke, N., Miura, Y., Chai, H.B., andKawakita, K. 1991. Involvement of active oxygen in induction of plant defense response against infection and injury, pp. 84–96,in E.J. Pell and K.L. Steffen (eds.). Active Oxygen/Oxidative Stress and Plant Metabolism. American Society of Plant Pathologists, Rockville, Maryland.

    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 systemic plant resistance to pathogens and pests.Cell 70:879–886.

    PubMed  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 

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

    Google Scholar 

  • Felton, G.W., andDuffey, S.S. 1991b. Reassessment of the role of gut alkalinity and detergency in insect herbivory.J. Chem. Ecol. 17:1821–1836.

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

    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. 20:639–650.

    Google Scholar 

  • Fields, R. 1972. The rapid determination of amino groups with TNBS.Methods Enzymol. 25B:464–468.

    Google Scholar 

  • Gardner, H.W. 1979. Lipid hydroperoxide reactivity with proteins and amino acids: A review.J. Agric. Food Chem. 27:220–228.

    Google Scholar 

  • Gardner, H.W. 1991. Recent investigations into the lipoxygenase pathway of plants.Biochem. Biophys. Acta 1084:221–239.

    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 

  • Hart, S.V., Kogan, M., andPaxton, J.D. 1983. Effect of soybean phytoalexins on the herbivorous insects Mexican bean beetle and soybean looper.J. Chem. Ecol. 9;657–672.

    Google Scholar 

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

    Google Scholar 

  • Hildebrand, D.F., andKito, M. 1984. Role of lipoxygenases in soybean seed protein quality.J. Agric. Food Chem. 32:815–819.

    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 resistance 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 function.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 

  • Jiang, Y., andMiles, P.W. 1993. Responses of a compatible lucerne variety to attack by spotted alfalfa aphid: Changes in redox balance in affected tissues.Entomol. Exp. Appl. 67:263–274.

    Google Scholar 

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

    PubMed  Google Scholar 

  • Kogan, M., andFischer, D. 1991. Inducible defenses in soybean against herbivorous insects, pp. 347–378,in D.W. Tallamy and M.J. Raupp (eds.). Phytochemical Induction by Herbivores. John Wiley & Sons, New York.

    Google Scholar 

  • Kraemer, M.E., Rangappa, M., Gade, W., andBenepal, P.S. 1987. Induction of trypsin inhibitor in soybean leaves by Mexican bean beetle (Coleoptera: Coccinellidae) defoliation.J. Econ. Entomol. 80:237–241.

    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 

  • Lin, H., andKogan, M. 1990. Influence of induced resistance in soybean on the development and nutrition of the soybean looper and the Mexican bean beetle.Entomol. Exp. Appl. 55:131–138.

    Google Scholar 

  • Liu, S.H., Norris, D.M., Hartwig, E.E., andXu, M. 1992. Inducible phytoalexins in juvenile soybean genotypes predict soybean looper resistance in fully developed plants.Plant Physiol. 100:1479–1485.

    Google Scholar 

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

    Google Scholar 

  • Milo, G.E., andSantilli, V. 1966. Changes in the ascorbate concentration of pinto bean leaves accompanying the formation of TMV-induced local lesions.Virology 31:197–206.

    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 

  • Montalbini, P. 1991. Effect of rust infection on levels of uricase, allantoinase and ureides in susceptible and hypersensitive bean leaves.Physiol. Mol. Plant Pathol. 39:173–188.

    Google Scholar 

  • Nault, B.A., All, J.N., andBoerma, H.R. 1992. Influence of soybean planting date and leaf age on resistance to corn earworm (Lepidoptera: Noctuidae).J. Econ. Entomol. 21:264–268.

    Google Scholar 

  • Neupane, F.P., andNorris, D.M. 1991a. Sulfhydryl-reagant 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 

  • Ohta, H., Shida, K., Peng, Y., Furusawa, I., Shishiyama, J., Aibara, S., andMorita, Y. 1991. A lipoxygenase pathway is activated in rice after infection with the rice blast fungusMagnaporthe grisea.Plant Physiol. 97:94–98.

    Google Scholar 

  • Orlandi, E.W., Hutcheson, S.W., andBaker, C.J. 1992. Early physiological responses associated with race-specific recognition in soybean leaf tissue and cell suspensions treated withPseudomonas syringae pvglycinea.Physiol. Mol. Plant Pathol. 40:173–180.

    Google Scholar 

  • Polle, A., andRennenberg, H. 1992. Field studies on Norway spruce trees at high altitudes: II. Defence systems against oxidative stress in needles.New Phytol. 121:635–642.

    Google Scholar 

  • Popham, P.L., andNovacky, A. 1991. Use of dimethyl sulfoxide to detect hydroxyl radical during bacteria-induced hypersensitive reaction.Plant Physiol. 96:1157–1160.

    Google Scholar 

  • Rose, R.L., Sparks, T.C., andSmith C.M. 1988. Insecticide toxicity to the soybean looper and the velvetbean caterpillar (Lepidoptera: Noctuidae) as influenced by feeding on resistant soybean (PI 227687) leaves and coumestrol.J. Econ. Entomol. 81:1288–1294.

    Google Scholar 

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

    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 

  • Slansky, F., Jr., andWheeler, G.S. 1992. Feeding and growth responses of laboratory and field strains of velvetbean caterpillars (Lepidoptera: Noctuidae) to food nutrient level and allelochemicals.J. Econ. Entomol. 85:1717–1730.

    Google Scholar 

  • Stewart, R.R.C., andBewley, J.D. 1980. Lipid peroxidation associated with accelerated aging of soybean axes.Plant. Physiol. 65:245–248.

    Google Scholar 

  • Stoscheck, C.M. 1990. Increased uniformity in the response of the Coomassie blue G protein assay to different proteins.Anal. Biochem. 184:111–116.

    PubMed  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 

  • Tranbarger, T., Franceschi, V.R., Hildebrand, D.F. andGrimes, H.D. 1991. The soybean 94-kilodalton vegetative storage protein is a lipoxygenase that is localized in paraveinal mesophyll cell vacuoles.Plant Cell 3:973–987.

    PubMed  Google Scholar 

  • Vera-Estrella, R., 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 toMeloidogyne incognita attack.Physiol. Mol. Plant Pathol. 32:313–322.

    Google Scholar 

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Felton, G.W., Bi, J.L., Summers, C.B. et al. Potential role of lipoxygenases in defense against insect herbivory. J Chem Ecol 20, 651–666 (1994). https://doi.org/10.1007/BF02059605

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