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Malathion-specific resistance in a strain of the rust red grain beetle Cryptolestes ferrugineus (Coleoptera: Cucujidae)

Published online by Cambridge University Press:  10 July 2009

A.G. Spencer*
Affiliation:
School of Animal and Microbial Sciences, University of Reading, Reading, Berkshire, RG6 6AJ, UK
N.R. Price
Affiliation:
Ministry of Agriculture Fisheries and Food, Central Science Laboratory, Sand Hutton, York, YO4 1LZ, UK
A. Callaghan
Affiliation:
School of Animal and Microbial Sciences, University of Reading, Reading, Berkshire, RG6 6AJ, UK
*
*Danish Pest Infestation Laboratory, Skovbrynet 14, DK-2800 Lyngby, Denmark. Fax: 0045 45931155 E-mail: a.spencer@ssl.dk

Abstract

A strain of Cryptolestes ferrugineus (Stephens) bred for malathion-specific resistance was found to be 650 fold resistant at LD50 when compared with a susceptible strain bred from the same stock. Resistance was more than 98% synergized by triphenyl phosphate and S,S,S-tributyl phosphorotrithioate, but unaffected by piperonyl butoxide. AChE inhibition by malaoxon varied slightly between the strains. Non-specific esterase activity as measured by the hydrolysis of α-naphthyl acetate was slightly reduced in the resistant strain whereas there were no inter-strain differences in the hydrolysis of β-naphthyl acetate. Products of in vitro metabolism of malathion were identified by thin-layer chromatography and gas chromatography-mass spectrometry as α- and β-malathion mono-acids. It was therefore concluded that resistance was due to the hydrolytic breakdown of malathion by a malathion-specific carboxylesterase. The rate of in vitro malathion hydrolysis was found to be 31 times greater in the resistant strain. In vitro inhibition studies indicated that resistance is attributable to a carboxylesterase unique to the resistant strain. The implications of these results are discussed in relation to work recently carried out on malathion-specific resistance in dipterous species.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 1998

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References

Abdel-Aal, Y.A.I., Lampert, E.P., Roe, R.M. & Semtner, P.J.(1992) Diagnostic esterases and insecticide resistance in the tobacco aphid, Myzus nicotianae Blackman (Homoptera: Aphididae). Pesticide Biochemistry and Physiology 43, 123133.CrossRefGoogle Scholar
Anon. (1974) Recommended methods for the detection and measurement of resistance of agricultural pests to pesticides. Tentative method for adults of some major beetle pests of stored cereals with malathion or lindane. FAO method 15. Plant Protection Bulletin 22, 127137.Google Scholar
Bigley, W.S. & Plapp, F.W. (1962) Metabolism of malathion and malaoxon by the mosquito Culex tarsalis. Journal of Insect Physiology 8, 545557.CrossRefGoogle Scholar
Bradford, M. (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principal of protein dye-binding. Analytical Biochemistry 72, 248.CrossRefGoogle Scholar
Campbell, P.M., Trott, J.F., Claudianos, C., Smyth, K.A., Russell, R.J. & Oakeshott, J.G. (1997) Biochemistry of esterases associated with organophosphate resistance in Lucilia cuprina with comparisons to putative orthologues in other Diptera. Biochemical Genetics 35, 1740.CrossRefGoogle ScholarPubMed
Doichuanngam, K. & Thornhill, R.A. (1989) The role of non-specific esterases in insecticide resistance to malathion in the diamondback moth Plutella xylostella. Comparative Biochemistry and Physiology 93C, 8186.Google Scholar
Dyte, C.E. & Rowlands, D.G. (1968) The metabolism and synergism of malathion in resistant and susceptible strains of Tribolium castaneum (Herbst) (Coleoptera, Tenebrionidae). Journal of Stored Products Research 4, 157173.CrossRefGoogle Scholar
Ellman, G.L., Courtney, D.K., Andres, V. & Featherstone, R.M.(1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochemical Pharmacology 7, 8895.CrossRefGoogle ScholarPubMed
ffrench-Constant, R.H. & Bonning, B.C. (1989) Rapid microtitre plate test distinguishes insecticide resistant acetylcholinesterase genotypes in the mosquitoes Anopheles albimanus, An. nigerrimus and Culex pipiens. Medical and Veterinary Entomology 3, 916.CrossRefGoogle ScholarPubMed
Finney, D.J. (1971) Probit analysis. 3rd edn.Cambridge, Cambridge University Press.Google Scholar
Hall, L.M.C. & Spierer, P. (1986) The Ace locus of Drosophila melanogaster: structural gene for acetylcholinesterase with an unusual 5' leader. EMBO Journal 5, 29492954.CrossRefGoogle ScholarPubMed
Halliday, W.R. (1988) Tissue specific esterase and malathion carboxylesterase activity in larvae of malathion-resistant Plodia interpunctella (Huebner) (Lepidoptera, Pyralidae). Journal of Stored Products Research 24, 9199.CrossRefGoogle Scholar
Hemingway, J. (1985) Malathion carboxylesterase enzymes in Anopheles arabiensis from Sudan. Pesticide Biochemistry and Physiology 23, 309313.CrossRefGoogle Scholar
Howe, R.W. & Lefkovitch, L.P. (1957) The distribution of the storage species of Cryptolestes (Col., Cucujidae). Bulletin of Entomological Research 48, 795809.CrossRefGoogle Scholar
Hughes, P.B.,Green, P.E. & Reichmann, K.G. (1984) Specific resistance to malathion in laboratory and field populations of the Australian sheep blowfly, Lucilia cuprina (Diptera: Calliphoridae). Journal of Economic Entomology 77, 14001404.CrossRefGoogle ScholarPubMed
Kao, C.H., Motoyama, N. & Dauterman, W.C. (1984) Studies on esterases in various house fly strains and their role in malathion resistance. Pesticide Biochemistry and Physiology 22, 8692.CrossRefGoogle Scholar
Kuwahara, M., Miyata, T., Saito, T. & Eto, M. (1981) Relationship between high esterase activity and in vitro degradation of 14C-malathion by organophosphate-resistant and susceptible strains of the kanzawa spider mite Tetranychus kanzawai Kishida (Acarina: Tetranychidae), and their inhibition with specific synergists. Applied Entomology and Zoology 16, 297305.CrossRefGoogle Scholar
Lewis, J.B. (1969) Detoxification of diazinon by subcellular fractions of diazinon-resistant and susceptible house flies. Nature 224, 917.CrossRefGoogle Scholar
Matsumura, F. & Hogendijk, C.J. (1964) The enzymatic degradation of malathion in organophosphate resistant and susceptible strains of Musca domestica. Entomologia Experimentalis et Applicata 7, 179193.CrossRefGoogle Scholar
Matsumura, F. & Voss, G. (1964) Mechanisms of malathion and parathion resistance in the two-spotted spider mite Tetranychus urticae. Journal of Economic Entomology 57, 911917.CrossRefGoogle Scholar
Matthews, W.A. (1980) The metabolism of malathion in vivo by two strains of Rhyzopertha dominica (F.), the lesser grain borer. Pesticide Biochemistry and Physiology 13, 303312.CrossRefGoogle Scholar
Menn, J.J., Erwin, W.R. & Gordon, H.T. (1957) Color reaction of 2,6-dibromo-N-chloro-p-benzoquinoneimine with thiophosphate insecticides. Agricultural and Food Chemistry 5, 601602.CrossRefGoogle Scholar
Morton, R.A. & Holwerda, B.C. (1985) The oxidative metabolism of malathion and malaoxon in resistant and susceptible strains of Drosophila melanogaster. Pesticide Biochemistry and Physiology 24, 1931.CrossRefGoogle Scholar
Morton, R.A. & Singh, R.S. (1982) The association between malathion resistance and acetylcholinesterase in Drosophila melanogaster. Biochemical Genetics 20, 179198.CrossRefGoogle ScholarPubMed
Nguy, V.D. & Busvine, J.R. (1960) Studies on the genetics of resistance to parathion and malathion in the housefly. Bulletin of the World Health Organization 22, 531.Google ScholarPubMed
Niwa, Y., Miyata, T. & Saito, T. (1977) In vitro metabolism of malathion resistant and susceptible strains of houseflies, Musca domestica L. Journal of Pesticide Science (Nihon Noyaku Gakkaishi) 2, 151.CrossRefGoogle Scholar
Oppenoorth, F.J. (1959) Genetics of resistance of organophosphorus compounds and low ali-esterase activity in the housefly. Entomologia Experimentalis et Applicata 2, 304386.CrossRefGoogle Scholar
Oppenoorth, F.J. (1965) Biochemical genetics of insecticide resistance. Annual Review of Entomology 10, 185206.CrossRefGoogle Scholar
Oppenoorth, F.J. (1985) Biochemistry and genetics of insecticide resistance. pp. 731773in Kerkut, G.A. & Gilbert, L.I. (Eds) Comprehensive insect physiology biochemistry and pharmacology (Volume 12). Oxford, Pergamon Press.Google Scholar
Oppenoorth, F.J. & van Asperen, K. (1960) Allelic genes in the housefly producing modified enzymes that cause organophosphate resistance. Science 132, 298299.CrossRefGoogle ScholarPubMed
Oppenoorth, F.J. & van Asperen, K. (1961) The detoxication enzymes causing organophosphate resistance in the housefly; properties, inhibition, and the action of inhibitors as synergists. Entomologia Experimentalis et Applicata 4, 311333.CrossRefGoogle Scholar
Oppenoorth, F.J. & Voerman, S. (1975) Hydrolysis of paraoxon and malaoxon in three strains of Myzus persicae with different degrees of parathion resistance. Pesticide Biochemistry and Physiology 5, 431443.CrossRefGoogle Scholar
Picollo de Villar, M.I., Fontan, A., Wood, E.J. & Zerba, E.N. (1990) The biochemical basis of tolerance to malathion in Rhodnius prolixus. Comparative Biochemistry and Physiology 96, 361365.Google ScholarPubMed
Picollo de Villar, M.I., van der Pas, L.J.T., Smissaert, H.R. & Oppenoorth, F.J. (1983) An unusual type of malathion-carboxylesterase in a Japanese strain of the house fly. Pesticide Biochemistry and Physiology 19, 6065.CrossRefGoogle Scholar
Price, N.R. (1991) Enzymic factors in the resistance of stored-product pests to insecticides. Biochemical Society Transactions 19, 759762.CrossRefGoogle ScholarPubMed
Prickett, A.J., Muggleton, J. & Llewellin, J.A. (1990) Insecticide resistance in populations of Oryzaephilus surinamensis and Cryptolestes ferrugineus from grain stores in England and Wales. pp. 11891194 in Proceedings of the Brighton Crop Protection Conference – Pests and Diseases.Farnham, UK,The British Crop Protection Council.Google Scholar
Schlenk, H. & Gellerman, J.L. (1960) Esterification of fatty acids with diazomethane on a small scale. Analytical Chemistry 32, 14121414.CrossRefGoogle Scholar
Scott, J.G. (1990) Investigating mechanisms of insecticide resistance: methods, strategies, and pitfalls. pp. 3957in Roush, R.T. & Tabashnik, B.E. (Eds) Pesticide resistance in arthropods. New York, Chapman and Hall.CrossRefGoogle Scholar
Smyth, K.A., Russell, R.J. & Oakeshott, J.G. (1994) A cluster of at least three esterase genes in Lucilia cuprina includes malathion carboxylesterase and two other esterase genes implicated in resistance to organophosphates. Biochemical Genetics 32, 437453.CrossRefGoogle ScholarPubMed
Smyth, K.A., Walker, V.K., Russell, R.J. & Oakeshott, J.G.(1996) Biochemical and physiological differences in the malathion carboxylesterase activities of malathion-susceptible and -resistant lines of the sheep blowfly, Lucilia cuprina. Pesticide Biochemistry and Physiology 54, 4855.CrossRefGoogle Scholar
Spencer, A.G. (1995) Malathion specific resistance in a strain of the rust red grain beetle Cryptolestes ferrugineus (Stephens) (Coleoptera: Cucujidae). PhD Thesis, University of Reading.Google Scholar
van Asperen, K. (1958) Mode of action of organophospohorous insecticides. Nature 181, 355356.CrossRefGoogle ScholarPubMed
van Asperen, K. (1964) Biochemistry and genetics of esterases in houseflies (Musca domestica) with special reference to the development of resistance to organophosphorus compounds. Entomologia Experimentalis et Applicata 7, 205214.CrossRefGoogle Scholar
van Asperen, K. & Oppenoorth, F.J. (1959) Organophosphate resistance and esterase activity in houseflies. Entomologia Experimentalis et Applicata 2, 4857.CrossRefGoogle Scholar
Welling, W., Blaakmeer, P.T. & Copier, H. (1970) Separation of isomers of malathion monocarboxylic acid by thin-layer chromatography. Journal of Chromatography 47, 281283.CrossRefGoogle ScholarPubMed
Welling, W., de Vries, A.W. & Voerman, J. (1974) Oxidative cleavage of carboxylester bond as a mechanism of resistance to malaoxon in house flies. Pesticide Biochemistry and Physiology 4, 3143.CrossRefGoogle Scholar
Whyard, S. & Walker, V.K. (1994) Characterisation of malathion carboxylesterase in the Sheep Blowfly Lucilia cuprina. Pesticide Biochemistry and Physiology 50, 198206.CrossRefGoogle Scholar
Whyard, S., Downe, A.E.R. & Walker, V.K. (1994a) Isolation of an esterase conferring insecticide resistance in the mosquito Culex tarsalis. Insect Biochemistry and Molecular Biology 24, 819827.CrossRefGoogle ScholarPubMed
Whyard, S., Russell, R.J. & Walker, V.K. (1994b) Insecticide resistance and malathion carboxylesterase in the Sheep Blowfly Lucilia cuprina. Biochemical Genetics 32, 924.CrossRefGoogle ScholarPubMed
Wilkins, J.P.G. & Mason, D.J. (1987) A study of the trans-esterification products of malathion by capillary gas chromatography-mass spectrometry. Pesticide Science 20, 259270.CrossRefGoogle Scholar
Wilkinson, C.F. (1983) Role of mixed-function oxidases in insecticide resistance. pp. 175206in Georghiou, G.P. & Saito, T. (Eds) Pest resistance to pesticides. New York, Plenum Press.CrossRefGoogle Scholar
Winteringham, F.P.W. (1969) Mechanisms of selective insecticidal action. Annual Review of Entomology 14, 409442.CrossRefGoogle ScholarPubMed
Wool, D., Noiman, S., Manheim, O. & Cohen, E. (1982) Malathion resistance in Tribolium strains and their hybrids: Inheritance patterns and possible enzymatic mechanisms (Coleoptera, Tenebrionidae). Biochemical Genetics 20, 621636.CrossRefGoogle ScholarPubMed
Zayed, M.A.D., Fakhr, I.M.I. & Bahig, M.R.E. (1973) Metabolism of organophosphorus insecticides. XII. Degradation of 32P-malathion in the adult larva of the cotton leaf worm. Biochemical Pharmacology 22, 285292.CrossRefGoogle Scholar