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Antifeedant Effects of Proteinase Inhibitors on Feeding Behaviors of Adult Western Corn Rootworm (Diabrotica virgifera virgifera)

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Abstract

Low-molecular-weight peptidyl proteinase inhibitors (PIs) including leupeptin, calpain inhibitor I, and calpeptin were found to be potent antifeedants for adult western corn rootworm (WCR) against the phagostimulation of cucurbitacin B (Cuc B) or a corn pollen extract (CPE). Leupeptin was the strongest (ED50 = 0.36 and 0.55 nmol/disk for Cuc B and CPE, respectively) among PIs tested with an antifeedant potency much stronger than the steroid progesterone (ED50 = 2.29 and 5.05 nmol/disk for Cuc B and CPE, respectively), but slightly less than the reference alkaloid, strychnine (ED50 = 0.17 and 0.37 nmol/disk for Cuc B and CPE, respectively). All active PIs contain a di- or tripeptidyl aldehyde moiety, indicating that PIs exert their antifeedant effects by covalent interaction with putative sulfhydryl (SH) groups on taste receptors as do these PIs with cysteine proteinases. However, opposite inhibition potency against Cuc B versus CPE by two thiol-group reducing agents, DTT and L-cysteine, and the results with other cysteine-modifying reagents obscure the net functional role of SH groups at WCR taste chemoreceptors. Surprisingly, the model phagostimulant for diabroticites, Cuc B, was more easily counteracted by these feeding deterrents than the stimulants present in CPE. Three-dimensional structure–antifeedant relationships for the PIs suggest that a novel taste chemoreception mechanism exists for these peptidyl aldehydes or that they fit partially into a strychnine binding pocket on protein chemoreceptors. Favorable economic benefit may be achieved if PIs are discovered to be useful in adult WCR control, since both pre- and postingestive sites would be targeted.

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References

  • Berenbaum, M. 1986. Postingestive effects of phytochemicals on insects: on Paracelsus and plant products, pp. 121–153, in J. R. Miller and T. A. Miller (Eds.). Insect–Plant Interactions. Springer-Verlag, New York.

    Google Scholar 

  • Bernays, E. A. 1990. Plant secondary compounds deterrent but not toxic to the grass specialist acridid Locusta migratoria: implications for the evolution of graminivory. Entomol. Exp. Appl. 54:53–56.

    Google Scholar 

  • Bernays, E. A. 1991. Relationship between deterrence and toxicity of plant secondary compounds for the grasshopper Schistocerca americana. J. Chem. Ecol. 17:2519–2526.

    Google Scholar 

  • Bernays, E. A. and Chapman, R. F. 1994. Host Plant Selection by Phytophagous Insects. Chapman and Hall, New York.

    Google Scholar 

  • Bernays, E. A. and Chapman, R. F. 2000. Plant secondary compounds and grasshoppers: Beyond plant defenses. J. Chem. Ecol. 26:1773–1794.

    Google Scholar 

  • Blaney, W. M., Simmonds, M. S. J., Evans, S. V., and Fellows, L. E. 1984. The role of the secondary plant compound 2,5-dihydroxymethyl-3,4-dihydroxypyrrolidine as a feeding inhibitor of insects. Entomol. Exp. Appl. 36:209–216.

    Google Scholar 

  • Bryant, B. 1990. Specific inhibition of the binding of the taste stimulus, l-alanine, by sulfhydryl reagents in Ictalurus punctatus. Comp. Biochem. Physiol. 95A:533–537.

    Google Scholar 

  • Chapman, R. F., Ascoli-christensen, A., and White, P. R. 1991. Sensory coding for feeding deterrence in the grasshopper Schistocerca americana. J. Exp. Biol. 158:241–259.

    Google Scholar 

  • Chyb, S., Eichenseer, H., Hollister, B., Mullin, C. A., and Frazier, J. L. 1995. Identification of sensilla involved in taste mediation in adult western corn rootworm (Diabrotica virgifera virgifera LeConte). J. Chem. Ecol. 21:313–329.

    Google Scholar 

  • Clyne, P., Warr, C., and Carlson, J. 2000. Candidate taste receptors in Drosophila. Science 287:1830–1834.

    Google Scholar 

  • Dethier, V. G. and Bowdan, E. 1989. The effect of alkaloids on sugar receptors and the feeding behaviour of the blowfly. Physiol. Entomol. 14:127–136.

    Google Scholar 

  • Eichenseer, H. and Mullin, C. A. 1996. Maxillary appendages used by western corn rootworms, Diabrotica virgifera virgifera, to discriminate between a phagostimulant and–deterrent. Entomol. Exp. Appl. 78:237–242.

    Google Scholar 

  • Eichenseer, H. and Mullin, C. A. 1997. Antifeedant comparisons of GABA/glycinergic antagonists for diabroticite leaf beetles (Coleoptera: Chrysomelidae). J. Chem. Ecol. 23:71–82.

    Google Scholar 

  • Eichenseer, H., Mullin, C. A., and Chyb, S. 1998. Antifeedant discrimination thresholds for two populations of western corn rootworm. Physiol. Entomol. 23:220–226.

    Google Scholar 

  • Elden, T. C. 1995. Selected proteinase inhibitor effects on alfalfa weevil (Coleoptera: Cuculionidae) growth and development. J. Econ. Entomol. 88:1586–1590.

    Google Scholar 

  • Elden, T. C. 2000. Effects of proteinase inhibitors and plant lectins on the adult alfalfa weevil (Coleoptera: Cuculionidae). J. Entomol. Sci. 35:62–69.

    Google Scholar 

  • Fabrick, J., Behnke, C., Czapla, T., Bala, K., Rao, A. G., Kramer, K. J., and Reeck, G. R. 2002. Effects of a potato cysteine proteinase inhibitor on midgut proteolytic enzyme activity and growth of the southern corn rootworm, Diabrotica undecimpunctata howardi (Coleoptera: Chrysomelidae). Insect Biochem. Mol. Biol. 32:405–415.

    Google Scholar 

  • Frazier, J. L. and Chyb, S. 1995. Use of feeding inhibitors in insect control, pp. 364–381, in G. de Boer and R. F. Chapman (Eds.). Regulatory Mechanisms of Insect Feeding. Chapman and Hall, New York.

    Google Scholar 

  • Frazier, J. L. and Heitz, J. R. 1975. Inhibition of olfaction in the moth Heliothis virescens by the sulfhydryl reagent fluorescein mercuric acetate. Chem. Senses Flavor 1:271–281.

    Google Scholar 

  • González-Coloma, A., Valencia, F., Martín, N., Hoffmann, J. J., Hutter, L., Marco, J. A., and Reina, M. 2002. Silphinene sesquiterpenes as model insect antifeedants. J. Chem. Ecol. 28:117–129.

    Google Scholar 

  • Hollister, B. and Mullin, C. A. 1999. Isolation and identification of primary metabolite feeding stimulants for adult western corn rootworm, Diabrotica virgifera virgifera LeConte, from host pollens. J. Chem. Ecol. 25:1263–1280.

    Google Scholar 

  • Ishimoto, H., Matsumoto, A., and Tanimura, T. 2000. Molecular identification of a taste receptor gene for trehalose in Drosophila. Science 289:116–119.

    Google Scholar 

  • Kim, J. H. 2002. Effects of corn pollen chemistry, dietary proteinase inhibitors and beetle oral secretions on feeding behaviors and fecundity of adult western corn rootworm. PhD thesis. Pennsylvania State University, University Park, Pennsylvania.

    Google Scholar 

  • Koiwa, H., Shade, R. E., Zhu-Salzman, K., D'urzo, M. P., Murdock, L. L., Bressan, R. A., and Hasegawa, P. M. 2000. A plant defensive cystatin (soyacystatin) targets cathepsin L-like digestive cysteine proteinases (DvCALs) in the larval midgut of western corn rootworm (Diabrotica virgifera virgifera). FEBS Lett. 471:67–70.

    Google Scholar 

  • Lam, P. Y.-S. and Frazier, J. L. 1987. Model study on the mode of action of muzigadial antifeedant. Tetrahedron Lett. 28:5477–5480.

    Google Scholar 

  • Leung, D., Abbenante, G., and Fairlie, D. P. 2000. Protease inhibitors: current status and future prospects. J. Med. Chem. 43:305–341.

    Google Scholar 

  • Lin, S. and Mullin, C. A. 1999. Lipid, polyamide, and flavonol phagostimulants for adult western corn rootworm from sunflower (Helianthus annuus L.) pollen. J. Agric. Food Chem. 47:1223–1229.

    Google Scholar 

  • McConnell, R. M., Patterson-Goss, C., Godwin, W., and Stanley, B. 1998. Synthesis and 13C NMR equilibria studies of [1-13C]leupeptin and analogs. J. Org. Chem. 63:5648–5655.

    Google Scholar 

  • Messchendorp, L., Smid, H. M., and Van Loon, J. J. A. 1998. The role of an epipharyngeal sensillum in the perception of feeding deterrents by Leptinotarsa decemlineata larvae. J. Comp. Physiol. A 183:255–264.

    Google Scholar 

  • Metcalf, R. L. and Metcalf, E. R. 1992. Plant Kairomones in Insect Ecology and Control. Chapman and Hall, New York.

    Google Scholar 

  • Mitchell, B. K. and Harrison, D. 1985. Effects of Solanum glycoalkaloids on chemosensilla in the Colorado potato beetle: a mechanism of feeding deterrence? J. Chem. Ecol. 11:73–83.

    Google Scholar 

  • Mullin, C. A. and Kim, J. H. 2001. Phytochemical action at amino acid chemosensory receptors: An approach to biopesticides. pp. 45–71, in O. Koul and G. S. Dhaliwal (Eds.). Advances in Biopesticide Research. Vol.1, Phytochemical Pesticides. Harwood Academic Publishers, Amsterdam.

    Google Scholar 

  • Mullin, C. A., Mason, C. H., Chou, J.-C., and Linderman, J. R. 1992. Phytochemical antagonism of γ-aminobutyric acid based resistances in Diabrotica, pp. 288–308, in C. A. Mullin and J. G. Scott (Eds.). Molecular Mechanisms of Insecticide Resistance: Diversity Among Insects. ACS Symposium Series No. 505. American Chemical Society, Washington, DC.

    Google Scholar 

  • Mullin, C. A., Chyb, S., Eichenseer, H., Hollister, B., and Frazier, J. L. 1994. Neuroreceptor mechanisms in insect gustation: a pharmacological approach. J. Insect Physiol. 40:913–931.

    Google Scholar 

  • Mullin, C. A., Gonzalez-Coloma, A., Gutierrez, C., Reina, M., Eichenseer, H., Hollister, B., and Chyb, S. 1997. Antifeedant effects of some novel terpenoids on Chrysomelidae beetles: Comparisons with alkaloids on an alkaloid-adapted and nonadapted species. J. Chem. Ecol. 23:1851–1866.

    Google Scholar 

  • Norris, D. M. 1981. Possible unifying principles in energy transduction in the chemical senses, pp. 289–307, in D. M. Norris (ed.). Perception of Behavioral Chemicals. Elsevier/North-Holland Biomedical Press, New York.

    Google Scholar 

  • Norris, D. M. 1986. Anti-feeding compounds, pp. 98–146, in G. Haug and H. Hoffmann (Eds.). Sterol Biosynthesis Inhibitors and Anti-feeding Compounds. Springer-Verlag, New York.

    Google Scholar 

  • Otto, H.-H. and Schirmeister T. 1997. Cysteine proteases and their inhibitors. Chem. Rev. 97:133–171.

    Google Scholar 

  • Purdy, R. H., Morrow, A. L., Blinn, J. R., and Paul, S. M. 1990. Synthesis, metabolism, and pharmacological activity of 3α-hydroxy steroids which potentiate GABA-receptor-mediated chloride uptake in rat cerebral cortical synaptoneurosomes. J. Med. Chem. 33:1572–1581.

    Google Scholar 

  • Renwick, J. A. A. 1999. Phytochemical modification of taste: An insect model, pp. 221–229, in H. G. Cutler and S. J. Cutler (Eds.). Biologically Active Natural Products: Agrochemicals. CRC Press, Boca Raton, Florida.

    Google Scholar 

  • Schoonhoven, L. M. 1982. Biological aspects of antifeedants. Entomol. Exp. Appl. 31:57–69.

    Google Scholar 

  • Shimada, I. 1975. Chemical treatments of the labellar sugar receptor of the fleshfly. J. Insect Physiol. 21:1565–1574.

    Google Scholar 

  • Tallamy, D. W., Gorski, P. M., and Pesek, J. D. 1997. Intra-and interspecific genetic variation in the gustatory perception of cucurbitacins by diabroticite rootworms (Coleoptera: Chrysomelidae). Environ. Entomol. 26:1364–1372.

    Google Scholar 

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Kim, J.H., Mullin, C.A. Antifeedant Effects of Proteinase Inhibitors on Feeding Behaviors of Adult Western Corn Rootworm (Diabrotica virgifera virgifera). J Chem Ecol 29, 795–810 (2003). https://doi.org/10.1023/A:1022919413625

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