Abstract
Many plant secondary compounds induce detoxification activity in herbivorous insects. Although inducibility may be advantageous as a means of reducing costs associated with maintenance of metabolism, another benefit of inducibility is that it may allow insects to tailor their detoxification profiles to multiple substrate toxins in their diets. The parsnip webworm, Depressaria pastinacella, must contend with many types of furanocoumarins, toxins present in abundance in all of its host plants. Previous studies have documented that cytochrome P-450s are responsible for metabolism of furanocoumarins in this species and that this overall activity is inducible. In this study, we examined the effects of ingestion of single furanocoumarins on metabolism of multiple furanocoumarins and the ability of webworms to adjust their metabolism profiles to match artificial diets with furanocoumarin content differing qualitatively and quantitatively from the average content found in their principal host. That detoxification rates of newly molted sixth instars prior to feeding did not differ from those of actively feeding fifth or sixth instars suggests that constitutive activities of furanocoumarin-metabolizing enzymes are maintained in the absence of substrates. All of the induction assays in this study were performed with ultimate instars. Each of the furanocoumarins assayed was found to induce metabolism of five different furanocoumarin substrates; however, the induction profile was independent of the inducing agent. Consistent with this finding, webworms were incapable of matching their detoxification profiles to diets with different furanocoumarin compositions. Thus, the profile of detoxification within individuals of this species appears to be genetically fixed, although there is considerable variation in profiles among individuals.
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REFERENCES
Ahmad, S.1986. Enzymatic adaptations of herbivorous insects and mites to phytochemicals. J. Chem. Ecol.12:533–560.
Berenbaum, M. R.1991. Coumarins, pp. 221–249, inG. A. Rosenthal and M. R. Berenbaum (eds.). Herbivores: Their Interactions with Secondary Plant Metabolites. Academic Press, New York.
Berenbaum, M.R.2002. Post-genomic chemical ecology: from genetic code to ecological interactions. J. Chem. Ecol. In press.
Berenbaum, M. R. and Zangerl, A. R.1994. Costs of inducible defense: Protein limitation, growth, and detoxification in parsnip webworms. Ecology75:2311–2317.
Berenbaum, M. R. and Zangerl, A. R.1996. Phytochemical diversity: adaptation or random variation? pp. 1–24, inJ. T. Romeo, J. A. Saunders, and P. Barbosa (eds.). Phytochemical Diversity and Redundancy in Ecological Interactions. Plenum Press, New York.
Berenbaum, M. R. and Zangerl, A. R.1998. Chemical phenotype matching between a plant and its insect herbivore. Proc. Natl. Acad. Sci. USA95:13743–13748.
Berenbaum, M. R., Zangerl, A. R., and Lee, K.1989. Chemical barriers to adaptation by a specialist herbivore. Oecologia80:501–506.
Brattsten, L. B., Wilkinson, C. F., and Eisner, T.1977. Herbivore-plant interactions: mixedfunction oxidases and secondary plant substances. Science196:1349–1352.
Cohen, M. B., Berenbaum, M. R., and Schuler, M. A.1989. Induction of cytochrome P-450-mediated detoxification of xanthotoxin in the black swallowtail. J. Chem. Ecol.15:2347–2355.
Fernald, M. L.1950. Gray' Manual of Botany, 8th ed. American Book, New York.
Harrison, T. L., Zangerl, A. R., Schuler, M. A., and Berenbaum, M. R.2001. Developmental variation in cytochrome P450 expression in Papilio polyxenesin response to xanthotoxin, a hostplant allelochemical. Arch. Insect Biochem. Physiol.48:179–189.
Hinks, C. F., Cheeseman, M. T., Erlandson, M. A., Olfert, O., and Westcott, N. D.1991. The effects of kochia, wheat and oats on digestive proteinases and the protein economy of adult grasshoppers, Melanoplus sanguinipes. J. Insect Physiol.37:417–430.
Kamin-Belsky, N. and Wool, D.1993. Ecological aspects of digestive enzyme covariation in almond moth larvae, Ephestia cautella(Walker) (Lepidoptera, Phyticidae). J. Stored Prod. Res.29:323–332.
Li, W., Petersen, R. A., Schuler, M. A., and Berenbaum, M. R.submitted. Thirteen closely-related cytochrome P450 monooxygenases from P. canadensisand P. glaucus: evolutionary history and gene regulation.
Muehleisen, D. P., Benedict, J. H., Plapp, F. W., Jr., and Carino, F. A.1989. Effects of cotton allelochemicals on toxicity of insecticides and induction of detoxifying enzymes in bollworm (Lepidoptera: Noctuidae). J. Econ. Entomol.82:1554–1558.
Murray, R. D., MÉndez, J., and Brown, S. A.1982. The Natural Coumarins. John Wiley & Sons, New York.
Nitao, J. K.1989. Enzymatic adaptation in a specialist herbivore for feeding on furanocoumarincontaining plants. Ecology70:629–635.
Nitao, J. K. and Berenbaum, M. R.1988. Laboratory rearing of the parsnip webworm, Depressaria pastinacella(Lepidoptera: Oecophoridae). Ann. Entomol. Soc. Am.81:485–487.
Petersen, R. A., Zangerl, A. R., Berenbaum, M. R., and Schuler, M. A.2001. Expression of CYP6B1and CYP6B3cytochrome P450 monooxygenases and furanocoumarin metabolism in different tissues of Papilio polyxenes(Lepidoptera: Papilionidae). Insect Biochem. Mol. Biol.31:679–690.
Raubenheimer, D. and Simpson, S. J.1992. Analysis of covariance: An alternative to nutritional indices. Entomol. Exp. Appl.62:221–231.
Rosenthal, G. A. and Berenbaum, M. R.1991. Herbivores: Their Interactions with Secondary Plant Metabolites. Academic Press, New York.
Schery, R. W.1972. Plants for Man. Prentice-Hall, Englewood Cliffs, New Jersey.
Slansky, F., JR., 1992. Allelochemical-nutrient interactions in herbivore nutritional ecology. pp. 135–174, inG. A. Rosenthal and M. R. Berenbaum (eds.). Herbivores: Their Interactions with Secondary Plant Metabolites. Academic Press, New York.
Snyder, M. J. and Glendinning, J. I.1996. Causal connection between detoxification enzyme activity and consumption of a toxic plant compound. J. Comp. Physiol.179: 255–261.
Snyder, M. J., Hsu, E., and Feyereisen, R.1993. Induction of cytochrome P-450 activities by nicotine in the tobacco hornworm, Manduca Sexta. J. Chem. Ecol.19:2903–2916.
Snyder, M. J., Stevens, J. L., Andersen, J. F., and Feyereisen, R.1995. Expression of cytochrome P450 genes of the CYP4 family in midgut and fatbody of the tobacco hormworm, Manduca sexta. Arch. Biochem. Biophys. 321:13–20.
SPSS. 1999. SPSS 9.0. SPSS Inc., Chicago, Illinois.
Stevens, J. L., Snyder, M. J., Koener, J. F., and Feyereisen, R.2000. Inducible P450s of the CYP9 family from larval Manduca sextamidgut. Insect Biochem. Mol. Biol. 30:559–568.
Thompson, J. N.1977. Patch dynamics in the insect-Pastinaca sativaassociation: Life history tactics and population consequences. PhD dissertation. University of Illinois, Urbana-Champaign, Illinois.
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Cianfrogna, J.A., Zangerl, A.R. & Berenbaum, M.R. Dietary and Developmental Influences on Induced Detoxification in an Oligophage. J Chem Ecol 28, 1349–1364 (2002). https://doi.org/10.1023/A:1016292317948
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DOI: https://doi.org/10.1023/A:1016292317948