Skip to main content
Log in

A cluster of at least three esterase genes inLucilia cuprina includes malathion carboxylesterase and two other esterases implicated in resistance to organophosphates

  • Published:
Biochemical Genetics Aims and scope Submit manuscript

Abstract

Three distinct malathion carboxylesterase (MCE) phenotypes have been identified among strains ofLucilia cuprina. The high-activity phenotype shows 1.6-and 33-fold more MCE specific activity than the intermediate- and low-activity phenotypes, respectively. Flies with high MCE activity are 1000-fold more resistant to malathion than flies with either low or intermediate MCE phenotypes, which are equally susceptible. High and low MCE specific activity are allelic and encoded by theRmal gene on chromosome 4.Rmal is clustered within one map unit of two other esterase genes,Rop1 andE9, which are implicated in resistance to other organophosphate insecticides. Intermediate MCE specific activity is also inherited within the cluster, although its allelism toRmal, Rop1, orE9 is unclear. The cluster does not contain the gene for the hemolymph esterase E4, which maps 6.1 map units fromRop1, on the other side of thebubbled wing marker. The cluster appears to be homologous to part of a tandem array of 11 esterase genes on chromosome 3R ofDrosophila melanogaster.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Arnold, J. T. A., and Whitten, M. J. (1976). The genetic basis for organophosphorus resistance in the Australian sheep blowfly,Lucilia cuprina (Weidemann) (Diptera: Calliphoridae).Bull. Entomol. Res. 66561.

    Google Scholar 

  • Bradford, M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilising the principle of protein-dye binding.Anal. Biochem. 72248.

    Google Scholar 

  • Collet, C., Nielsen, K. M., Russell, R. J., Karl, M., Oakeshott, J. G., and Richmond, R. C. (1990). Molecular analysis of duplicated esterase genes inDrosophila melanogaster.Mol. Biol. Evol. 79.

    Google Scholar 

  • Dyte, C. E., and Rowlands, D. G. (1968). The metabolism and synergism of malathion in resistant and susceptible strains ofTribolium castaneum (Herbst) (Coleoptera, Tenebrionidae).J. Stored Prod. Res. 4157.

    Google Scholar 

  • Finney, D. J. (1971).Probit Analysis. Cambridge, England, Cambridge University Press.

    Google Scholar 

  • Foster, G. G., Maddern, R. H., and Mill, A. T. (1980a). Genetic instability in mass-rearing colonies of a sex-linked translocation strain ofLucilia cuprina (Wiedemann) (Diptera: Calliphoridae) during a field trial of genetic control.Theor. Appl. Genet. 58169.

    Google Scholar 

  • Foster, G. G., Whitten, M. J., Konovalov, C., Bedo, D. G., Maddern, R. H., and Boon, D. J. (1980b). Cytogenetic studies ofLucilia cuprina dorsalis R.-D. (Diptera: Calliphoridae). Polytene chromosome maps of the autosomes and cytogenetic locations of visible markers.Chromosoma 81151.

    Google Scholar 

  • Foster, G. G., Whitten, M. J., Konovalov, C., Arnold, J. T. A., and Maffi, G. (1981). Autosomal genetic maps of the Australian sheep blowfly,Lucilia cuprina dorsalis R-D. (Diptera: Calliphoridae) and possible correlations with the linkage maps ofMusca domestica L. andDrosophila melanogaster (Mg.),Genet. Res. Cambr. 3755.

    Google Scholar 

  • Foster, G. G., Weller, G. L., and Clarke, G. M. (1991). Male crossing over and genetic sexing systems in the Australian sheep blowflyLucilia cuprina.Heredity 67365.

    Google Scholar 

  • Franco, M. G., and Oppenoorth, F. J. (1962). Genetical experiments on the gene for low aliesterase activity and organophosphate resistance inMusca domestica L.Entomol. Exp. Appl. 5119.

    Google Scholar 

  • Healy, M. J., Dumancic, M. M., and Oakeshott, J. G. (1991). Biochemical and physiological studies of soluble esterases fromDrosophila melanogaster.Biochem. Genet. 29365.

    Google Scholar 

  • Hemingway, J. (1985). Malathion carboxylesterase enzymes inAnopheles arabiensis from Sudan.Pestic. Biochem. Physiol. 23309.

    Google Scholar 

  • Hughes, P. B., and Devonshire, A. L. (1982). The biochemical basis of resistance to organophosphorus insecticides in the sheep blowfly,Lucilia cuprina.Pestic. Biochem. Physiol. 18289.

    Google Scholar 

  • Hughes, P. B., and Raftos, D. A. (1985). Genetics of an esterase associated with resistance to organophosphorus insecticides in the sheep blowfly,Lucilia cuprina (Wiedemann) (Diptera: Calliphoridae).Bull. Entomol. Res. 75535.

    Google Scholar 

  • Hughes, P. B., Green, P. E., and Reichmann, K. G. (1984). Specific resistance to malathion in laboratory and field populations of the Australian sheep blowfly,Lucilia cuprina (Diptera: Calliphoridae).J. Econ. Entomol. 771400.

    Google Scholar 

  • Lai-Fook, J., and Smith, P. H. (1992). Genetics of the hemolymph esterases ofLucilia cuprina (Diptera: Calliphoridae).Biochem. Genet. 30123.

    Google Scholar 

  • Maddern, R. H., Foster, G. G., Whitten, M. J., Clarke, G. M., Konovalov, C. A., Arnold, J. T. A., and Maffi, G. (1986). The genetic mutations ofLucilia cuprina dorsalis R.-D. (Diptera: Calliphoridae). CSIRO, Division of Entomology Report No. 37, Canberra, Australia.

  • McKenzie, J. A., Parker, A. P., and Yen, J. L. (1992). Polygenic and single gene responses to selection for resistance to Diazinon inLucilia cuprina.Genetics 130613.

    Google Scholar 

  • Miyata, T., and Saito, T. (1976). Mechanisms of malathion resistance in the green rice leafhopper,Nephotettix cincticeps Uhler (Hemiptera: Deltocephalidae).J. Pestic. Sci. 123.

    Google Scholar 

  • Nguy, V. D., and Busvine, J. R. (1960). Studies of the genetics of resistance to parathion and malathion in the housefly.Bull. WHO 22531.

    Google Scholar 

  • Oppenoorth, F. J. (1985). Biochemistry and genetics of insecticide resistance. In Kerkut, G. A., and Gilbert, L. I. (eds.),Comprehensive Insect Physiology, Biochemistry, and Pharmacology Pergamon Press, Oxford, Vol. 12, p. 731.

    Google Scholar 

  • Oppenoorth, F. J., and van Asperen, K. (1960). Allelic genes in the housefly producing modified enzymes that cause organophosphate resistance.Science 132298.

    Google Scholar 

  • Parker, A. G., Russell, R. J., Delves, A. C., and Oakeshott, J. G. (1991). Biochemistry and physiology of esterases in organophosphate-susceptible and resistant strains of the Australian sheep blowfly,Lucilia cuprina.Pestic. Biochem. Physiol. 41305.

    Google Scholar 

  • Picollo de Villar, M. I., van Der Pas, L. J. T., Smissaert, H. R., and Oppenoorth, F. J. (1983). An unusual type of malathion-carboxylesterase in a Japanese strain of house fly.Pestic. Biochem. Physiol. 1960.

    Google Scholar 

  • Plapp, F. W., Jr. (1984). The genetic basis of insecticide resistance in the house fly: Evidence that a single gene plays a role in metabolic resistance to insecticides.Pestic. Biochem. Physiol. 22194.

    Google Scholar 

  • Plapp, F. W., Jr., and Eddy, G. W. (1961). Synergism of malathion against resistant insects.Science 3342043.

    Google Scholar 

  • Raftos, D. A. (1986). The biochemical basis of malathion resistance in the sheep blowfly.Pestic. Biochem. Physiol. 26302.

    Google Scholar 

  • Raftos, D. A., and Hughes, P. B. (1986). Genetic basis of a specific resistance to malathion in the Australian sheep blowfly,Lucilia cuprina (Diptera: Calliphoridae).J. Econ. Entomol. 79553.

    Google Scholar 

  • SAS Technical Report P-179 (1988).Additional SAS/STAT Procedures, Release 6.03, SAS Institute Inc., Cary, NC.

  • Shono, T. (1983). Linkage group analysis of carboxylesterase in a malathion resistant strain of the housefly,Musca domestica L. (Diptera: Muscidae).Appl. Entomol. Zool. 18407.

    Google Scholar 

  • Smyth, K. A., Boyce, T. M., Russell, R. J., and Oakeshott, J. G. (1995). Negative cross-resistance to organophosphate insecticides inLucilia cuprina (submitted for publication).

  • Spackman, M. E., Oakeshott, J. G., Smyth, K. A., Medveczky, K. M., and Russell, R. J. (1994). A cluster of esterase genes on chromosome 3R ofDrosophila melanogaster includes homologues of esterase genes conferring insecticide resistance inLucilia cuprina.Biochem. Genet. 3239.

    Google Scholar 

  • Townsend, M. G., and Busvine, J. R. (1969). The mechanism of malathion resistance in the blowflyChrysomya putoria.Entomol. Exp. Appl. 12243.

    Google Scholar 

  • Umetsu, N., Grose, F. H., Allahyari, R., Abu-El-Haj, S., and Fukuto, T. R. (1977). Effect of impurities on the mammalian toxicity of technical malathion and acephate.J. Agr. Food Chem. 24946.

    Google Scholar 

  • van Asperen, K., and Oppenoorth, F. J. (1959). Organophosphate resistance and esterase activity in houseflies.Entomol. Exp. Appl. 248.

    Google Scholar 

  • Weller, G. L., and Foster, G. G. (1993). Genetic maps of the sheep blowflyLucilia cuprina: Linkage-group correlations with other dipteran genera.Genome 36495.

    Google Scholar 

  • White, N. D. G., and Bell, R. J. (1988). Inheritance of malathion resistance in a strain ofTribolium castaneum (Coleoptera: Tenebrionidae) and effects of resistance genotypes on fecundity and larval survival in malathion-treated wheat.J. Econ. Entomol. 81381.

    Google Scholar 

  • Whyard, S., Downe, A. E. R., and Walker, V. K. (1994a). Isolation of an esterase conferring insecticide resistance in the mosquitoCulex tarsalis.Insect Biochem. Mol. Biol. 24819.

    Google Scholar 

  • Whyard, S., Russell, R., and Walker, V. K. (1994b). Insecticide resistance and malathion carboxylesterase in the sheep blowfly,Lucilia cuprina.Biochem. Genet. 329.

    Google Scholar 

  • Wilkinson, C. F. (1971). Insecticide synergists and their mode of action. In Tahori, A. S. (ed.),International IUPAC Congress of Pesticide Chemistry Gordon and Breach, New York, Vol. 2, p. 117.

    Google Scholar 

  • Ziegler, R., Whyard, S., Downe, A. E. R., Wyatt, G. R., and Walker, V. K. (1987). General esterase, malathion carboxylesterase, and malathion resistance inCulex tarsalis.Pestic. Biochem. Physiol. 28279.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Smyth, KA., Russell, R.J. & Oakeshott, J.G. A cluster of at least three esterase genes inLucilia cuprina includes malathion carboxylesterase and two other esterases implicated in resistance to organophosphates. Biochem Genet 32, 437–453 (1994). https://doi.org/10.1007/BF00566064

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00566064

Key words

Navigation