Abstract
The induction by dietary nicotine of a series of cytochrome P-450 enzyme activities was investigated in early fifth-instarManduca sexta larvae. At a low nicotine concentration in the diet (0.1 %), three of 12 midgut microsomal enzyme activities were significantly increased. At a higher concentration (0.75%) commonly found in plants of the genusNicotiana, nine of 12 activities were induced by 1.4- to 10.0-fold. Total cytochrome P-450, P-450 reductase activity, and midgut microsomal metabolism of nicotine were also increased by feeding 0.75% nicotine. Nicotine was metabolized by midgut microsomes to nicotine-1-N-oxide and cotinine-N-oxide. Fat body microsomal nicotine metabolism was low and unaffected by dietary nicotine. Isolated nerve cords were able to metabolize nicotine in vitro but this metabolism was not inducible by dietary nicotine. Nicotine-fed fifth-instarM. sexta larvae showed an increased tolerance to subsequent nicotine injection when compared to larvae fed a control diet. These results support the idea that induction of midgut cytochrome P-450-related metabolism is an adaptation ofManduca sexta to dietary nicotine.
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References
Appel, H.M., andMartin, M.M. 1992. Significance of metabolic load in the evolution of host specificity ofManduca sexta.Ecology 73:216–228.
Bentz, J.-A., andBarbosa, P. 1990. Effects of dietary nicotine (0.1 %) and parasitism byCortesia congregata on the growth and food consumption and utilization of the tobacco hornworm,Manduca sexta.Entomol. Exp. Appl. 57:1–8.
Brattsten, L.B. 1983. Cytochrome P-450 involvement in the interactions between plant terpenes and insect herbivores, pp. 173–195,in P.A. Hedin (ed.). Plant Resistance to Insects. Symposium Series No. 208, American Chemical Society, Washington D.C.
Brattsten, L.B. 1987. Inducibility of metabolic insecticide defenses in boll weevils and tobacco budworm caterpillars.Pestic. Biochem. Physiol. 27:13–23.
Brattsten, L.B., Wilkinson, C.F., andEisner, T. 1977. Herbivore-plant interactions: Mixed function oxidases and secondary plant substances.Science 196:1349–1352.
Burke, M.D., andPrough, R.A. 1978. Fluorometric and Chromatographic methods for measuring microsomal biphenyl hydroxylation.Methods Enzymol. 52:399–407.
Cohen, M.B., Berenbaum, M.R., andSchuler, M.A. 1989. Induction of cytochrome P-450-mediated detoxification of xanthotoxin in the black swallowtailJ. Chem. Ecol. 15:2347–2355.
Cohen, M.B., Berenbaum, M.R., andSchuler, M.A. 1990. Immunochemical analysis of cytochrome P-450 monooxygenase diversity in the black swallowtail caterpillar,Papilio polyxenes.Insect Biochem. 20:77–783.
Cohen, M.B., Schuler, M.A., andBerenbaum, M.R. 1992. A host-inducible cytochrome P-450 from a host-specific caterpillar: Molecular cloning and evolution.Proc. Natl. Acad. Sc. U.S.A. 89:10920–10924.
Feyereisen, R., andFarnsworth, D.E. 1985. Developmental changes of microsomal cytochrome P-450 monooxygenases in larval and adultDiploptera punctata.Insect Biochem. 15:755–761.
Feyereisen, R., andVincent, D.R. 1984. Characterization of antibodies to house fly NADPH-cytochrome P-450 reductase.Insect Biochem. 14:163–168.
Gould, F. 1984. Mixed function oxidases and herbivore polyphagy: The devil's advocate position.Ecol. Entomol. 9:29–34.
Halliday, W.R., Farnsworth, D.E., andFeyereisen, R. 1986. Hemolymph ecdysteroid titer and midgut ecdysone 20-monooxygenase activity during the last larval stage ofDiploptera punctata.Insect Biochem. 16:627–634.
Hodgson, E. 1985. Microsomal mono-oxygenases, pp. 225–321,in G.A. Kerkut and L.I. Gilbert (eds.). Comprehensive Insect Physiology, Biochemistry, and Physiology, Vol. 11. Pergamon Press, Oxford.
Ivie, G.W., Bull, D.L., Beier, R.C., Pryor, N.W., andOertli, E.H. 1983. Metabolic detoxification: Mechanism of insect resistance to plant psoralens.Science 221:374–376.
Krieger, R.I., Feeny, P.P., andWilkinson, C.F. 1971. Detoxification enzymes in the guts of caterpillars: An evolutionary answer to plant defenses.Science 172:579–581.
Kyerematen, G.A., andVesell, E.S. 1991. Metabolism of nicotine.Drug Metab. Rev. 23:3–41.
Lee, S.S., andScott, J.G. 1989. Microsomal cytochrome P-450 monooxygenases in the house fly (Musca domestica L.): Biochemical changes associated with pyrethroid resistance and phenobarbital induction.Pestic. Biochem. Physiol. 35:1–10.
Morris, C.E. 1983. Uptake and metabolism of nicotine by the CNS of a nicotine-resistant insect, the tobacco homworm (Manduca sexta).J. Insect Physiol. 29:807–817.
Nitao, J.K. 1989. Enzymatic adaptation in a specialist herbivore for feeding on furanocoumarin containing plants.Ecology 70:629–635.
Omura, T., andSato, R. 1964. The carbon monoxide binding pigment of liver microsomes. I. Evidence for its hemoprotein nature.J. Biol. Chem. 239:2370–2379.
Parr, J.C., andThurston, R. 1972. Toxicity of nicotine in synthetic diets to larvae of the tobacco hornworm.Ann. Entomol. Soc. Am. 65:1185–1188.
Prasad, S.V., Ryan, R.O., Law, J.H., andWells, M.A. 1986. Changes in lipoprotein composition during larval-pupal metamorphosis of an insect,Manduca sexta.J. Biol. Chem. 261:558–562.
Reidy, G.F., Rose, H.A., andStacey, N.H. 1987. Evidence for cytochrome P-450 multiplicity in the midgut of the cluster caterpillar,Spodoptera litura.Pestic. Biochem. Physiol. 29:176–186.
Rose, R.L., Gould, F., Levi, P.E., andHodgson, E. 1991. Differences in cytochrome P-450 activities in tobacco budworm larvae as influenced by resistance to host plant allelochemicals and induction.Comp. Biochem. Physiol. 99B:535–540.
Schoonhoven, L.M., andMeerman, J. 1978. Metabolic cost of changes in diet and neutralization of allelochemicals.Entomol. Exp. Appl. 24:489–493.
Self, L.S., Guthrie, F.E., andHodgson, E. 1964. Adaptation of tobacco homworms to the ingestion of nicotine.J. Insect Physiol. 10:907–914.
Snyder, M.J.,Walding, J.K., andFeyereisen, R. 1993. Metabolic fate of the allelochemical nicotine in the tobacco hornworm.Manduca sexta. Insect Biochem. Mol. Biol., in press.
Tate, L.G., Nakart, S.S., andHodgson, E. 1982. Comparison of detoxification activity in midgut and fat body during fifth instar development of the tobacco hornworm,Manduca sexta.Comp. Biochem. Physiol. 72C:75–81.
Vesell, E.S. 1967. Induction of drug-metabolizing enzymes in liver microsomes of mice and rats by softwood bedding.Science 157:1057–1058.
Yang, C.S., andKicha, L.P. 1978. A direct fluorometric assay of benzo[a]pyrene hydroxylase.Anal. Biochem. 84:154–163.
Yu, S.J. 1982. Induction of microsomal oxidases by host plants in the fall armyworm,Spodoptera frugiperda (I.E. Smith).Pestic. Biochem. Physiol. 17:59–67.
Yu, S.J. 1984. Interactions of allelochemicals with detoxification enzymes of insecticide-susceptible and resistant fall armyworms.Pestic. Biochem. Physiol. 22:60–68.
Yu, S.J. 1985. Microsomal sulfoxidation of phorate in the fall armyworm,Spodoptera frugiperda (J.E. Smith).Pestic. Biochem. Physiol. 23:273–281.
Yu, S.J. 1986. Consequences of induction of foreign compounds-metabolizing enzymes in insects, pp. 153–174,in L.B. Brattsten and S. Ahmad (eds.). Molecular Aspects of Insect-Plant Interactions, Plenum Press, New York.
Yu, S.J. 1987. Microsomal oxidation of allelochemicals in generalist (Spodoptera frugiperda) and semispecialist (Anticarsia gemmatalis) insect.J. Chem. Ecol. 13:423–436.
Yu, S.J. 1988. Microsomal S-demethylase activity in four lepidpterous insects.Pestic. Biochem. Physiol. 31:182–186.
Yu, S.J., andIng, R.T. 1984. Microsomal biphenyl hydroxylase of fall armyworm larvae and its induction by allelochemicals and host plants.Comp. Biochem. Physiol. 78C: 145–152.
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Snyder, M.J., Hsu, E.L. & Feyereisen, R. Induction of cytochrome P-450 activities by nicotine in the tobacco hornworm,Manduca sexta . J Chem Ecol 19, 2903–2916 (1993). https://doi.org/10.1007/BF00980591
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DOI: https://doi.org/10.1007/BF00980591