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Induced resistance in soybean toHelicoverpa zea: Role of plant protein quality

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Resistance in soybean toHelicoverpa zea is comprised of both constitutive and inducible factors. In this study, we investigated the induction of resistance byH. zea in both greenhouse and field studies. In a greenhouse experiment, fourth-instarH. zea growth rates were reduced by 39% after 24 hr feeding and by 27% after 48 hr when larvae fed on previously wounded V3 foliage (cv. Forrest) compared with undamaged foliage. In a field study, the weight gain by larvae was more than 52% greater when larvae fed for 72 hr on undamaged R2/R3 soybean plants (cv. Braxton) compared to those that fed on previously wounded plants. A significant component of the induced resistance is due to a decline in the nutritional quality of foliar protein following foliar damage byH. zea. Foliar protein was extracted from damaged and undamaged foliage and incorporated into artificial diets. Larval growth was reduced 26% after four days and 49% after seven days on diets containing protein from damaged plants compared to larvae feeding on foliar protein from undamaged plants. Chemical analyses of protein quality also indicated a decline in quality in damaged plants compared to unwounded plants. Increases in lipoxygenase activity (53%), lipid peroxidation products (20%), and trypsin inhibitor content (34%) were observed in protein from wounded plants. Moreover, a 5.9% loss in free amines and 19% loss in total thiols occurred in protein from wounded plants. Larval feeding causes a significant increase in foliar lipoxygenase activity that varied among genotypes. Lipoxygenase isozymes were measured at pH 5.5, pH 7.0, and pH 8.5 in V3 stage plants of Forrest, Hark, D75-1069, and PI 417061 genotypes. Lipoxygenase activity in each genotype was significantly increased after 72 hr of larval feeding at each pH level tested, with the exception of lipoxygenase isozymes at pH 5.5 in genotype PI 417061. Larval feeding on R2/R3 stage plants (field-grown cv. Braxton) for six days also increased foliar lipoxygenase activity.

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References

  • Anderson, W.L., andWetlaufer, D.B. 1975. A new method for disulfide analysis of peptides.Anal. Biochem. 67:493–502.

    PubMed  Google Scholar 

  • Baldwin, I.T. 1988. The alkaloidal responses of wild tobacco to real and simulated herbivory.Oecologia 77:378–381.

    Google Scholar 

  • Bradford, M.M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding.Anal. Chem. 72:248–254.

    Google Scholar 

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

    Google Scholar 

  • Broadway, R.M., andDuffey, S.S. 1986. Plant proteinase inhibitors: mechanism of action of effect on the growth of digestive physiology of larvalHeliothis zea andSpodoptera exigua.J. Insect Physiol. 32:827–833.

    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 

  • Burton, R.L. 1969. Mass rearing the corn earworm in the laboratory. USDA-ARS. 33–124.

  • Chiang, H.S., Norris, D.M., Ciepela, A., Oosterwyk, A., Shapiro, P., andJackson, M. 1986. Comparative resistance in soybean lines to Mexican bean beetle.Entomol. Exp. Appl. 42:19–26.

    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 

  • Clark, W.J., Harris, J.A., Maxwell, F.G., andHartwig, E.E. 1972. Resistance of certain soybean cultivars to bean leaf beetles, striped blister beetle, and bollworm.J. Econ. Entomol. 65:1699–1672.

    Google Scholar 

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

    Google Scholar 

  • Dadd, R.H. 1973. Insect nutrition: Current developments and metabolic implications.Annu. Rev. Entomol. 18:381–420.

    PubMed  Google Scholar 

  • Duffey, S.S., andFelton, G.W. 1991. Enzymatic antinutritive defenses of tomato plants against insects, pp. 167–197,in P.A. Hedin (ed.). Naturally Occurring Pest Bioregulators. American Chemical Society, Washington, D.C.

    Google Scholar 

  • Eckel, C.S., Bradley, J.R., Jr., andVan Duyn, J.W. 1992. Reduction in soybean yield and quality from corn earworm flower feeding.Agron. J. 84:402–409.

    Google Scholar 

  • Enyedi, A.J., Yaipani, N., Silverman, P., andRaskin, I. 1992. Signal molecules in systemic plant resistance to pathogen and pest.Cell 70:879–886.

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Fehr, W.R., Caviness, C.E., Burmood, D.T., andPennington, J.S. 1971. Stage of development description for soybeans,Glycine max (L.) Merrill.Crop Sci. 11:929–931.

    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., 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 herbivores,Spodoptera exigua.J. Insect Physiol. 38:277–285.

    Google Scholar 

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

    Google Scholar 

  • Fischer, D.C., andKogan, M. 1989. Deterrency of Mexican bean beetle (Lepidoptera: Coccinellidae) feeding by free phenolic acids.J. Entomol. Sci. 25:230–238.

    Google Scholar 

  • Gardner, H.W. 1991. Recent investigations into the lipoxygenase pathway of plants.Biochim. 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 

  • 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 

  • Hamberg, M., andGardner, H.W., 1992. Review—oxylipin pathway to jasmonates: Biochemistry and biological significance.Biochim. Biophys. Acta 1165:1–18.

    PubMed  Google Scholar 

  • Hatanaka, A., Kajimara, T., andSekiya, J. 1987. Biosynthetic pathway for C6-aldehyde formation from linolenic acid in green leaves.Chem. Phys. Lipids 44:341–361.

    Google Scholar 

  • Hatchett, J.H., Beland, G.L., andHartwig, E.E. 1976. Leaf feeding resistance to bollworm and tobacco budworm in three soybean plant introductions.Crop Sci. 16:277–280.

    Google Scholar 

  • Haukioja, E. 1990. Induction of defenses in trees.Annu. Rev. Entomol. 36:25–42.

    Google Scholar 

  • Hildebrand, D.F., andHamilton-Kemp, T.R. 1988. Plant lipoxygenase: Occurrence, properties and possible functions.Curr. Top. Plant Biochem. Physiol. 7:201–219.

    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., Luu, K.J., andVolden, C.S. 1986. Peroxidative response of leave in two soybean genotypes injured by twospotted spider mites (Acari:Tetranychidae).J. Econ. Entomol. 79:1459–1465.

    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 

  • Khan, M.B., andHarborne, J.B. 1991. A comparison of the effect of mechanical and insect damage on alkaloid levels inAtropa acuminata.Biochem. Syst. Ecol. 19:529–534.

    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 

  • Kogan, M., andKuhlman, D.E. 1982. Soybean insects: Identification and management in Illinois. Bulletin 773. Agricultural Experiment Station, University of Illinois, 58 pp.

  • 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 

  • Levine, R.L., Garland, D., Oliver, C.N., Amici, A., Climent, U.I., Lenz, A., Ahn, B., Shaltiel, S., andStadtman, E.R. 1990. Determination of carbonyl content in oxidatively modified proteins.Methods Enzymol. 186:137–162.

    PubMed  Google Scholar 

  • Lin, H., andKogan, M. 1990. Influence of induced resistance in soybean on the development and nutrition of the soybean looper and Mexican 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 

  • Mack, A.J., Peterman, T.K., andSiedow, J.N. 1987. Lipoxygenase isozymes in higher plants: Biochemical properties and physiological role. Isozymes.Curr. Top. Biol. Med. Res. 13:127–154.

    Google Scholar 

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

    Google Scholar 

  • Morse, S.S., Wratten, D., Edwards, P.J., andNiemeyer, H.M. 1991. Changes in the hydroxamic acid content of maize leaves with time and after artificial damage: implications for insects attack.Ann. Appl. Biol. 119:239–249.

    Google Scholar 

  • Nault, B.A., All, J.N., andBoerma, H.R. 1992. Resistance in vegetative and reproductive stages of a soybean breeding line to three defoliating pests (Lepidoptera: Noctuidae).J. Econ. Entomol. 85:1507–1515.

    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 

  • Olson, M.M., andRoseland, C.R. 1991. Induction of the coumarins scopoletin 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 

  • Rowan, G.B., Boerma, H.R., All, J.N., andTodd, J., 1991. Soybean cultivar resistance to defoliating insects.Crop Sci. 31:678–682.

    Google Scholar 

  • Schewe, T., Report, S.M., andKuhn, H. 1986. Enzymology and physiology of reticulocyte lipoxygenase.Adv. Enzymol. Mol. Biol. 58:191–272.

    Google Scholar 

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

    Google Scholar 

  • Smith, C.M. 1985. Expression, mechanisms and chemistry of resistance in soybean,Glycine max L. (Merr) to the soybean looper,Pseudoplusia includens (Walker).Insect Sci. Appl. 6:243–248.

    Google Scholar 

  • Smith, C.M. 1989. Plant Resistance to Insects, A Fundamental Approach. John Wiley & Sons, New York, 286 pp.

    Google Scholar 

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

    Google Scholar 

  • Stinner, R.E., Bradley, J.R., Jr., andVan Duyn, J.W. 1980. SamplingHeliothis spp. on soybean, pp. 407–421,in M. Kogan and D.C. Herzog (eds.). Sampling Method in Soybean Entomology. Spring-Verlag, New York.

    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 

  • Ueda, J., andKato, J. 1980. Isolation and identification of a senescence-promoting substance from wormwood (Artemesia absinthium L.)Plant Physiol. 66:246–249.

    Google Scholar 

  • Vick, B.A., andZimmerman, D.C. 1987. Oxidative systems for modification of fatty acids: the lipoxygenase pathway, pp. 53–90,in P.K. Stumpf (ed.). The Biochemistry of Plants: A Comprehensive Treatise, Vol. 9. Academic Press, Orlando, Florida.

    Google Scholar 

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Bi, J.L., Felton, G.W. & Mueller, A.J. Induced resistance in soybean toHelicoverpa zea: Role of plant protein quality. J Chem Ecol 20, 183–198 (1994). https://doi.org/10.1007/BF02066000

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