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Characterization of the M918T sodium channel gene mutation associated with strong resistance to pyrethroid insecticides in the peach-potato aphid, Myzus persicae (Sulzer)

Published online by Cambridge University Press:  13 December 2007

I. Eleftherianos*
Affiliation:
Division of Plant and Invertebrate Ecology, Rothamsted Research, Harpenden, Herts. AL5 2JQ, UK
S.P. Foster
Affiliation:
Division of Plant and Invertebrate Ecology, Rothamsted Research, Harpenden, Herts. AL5 2JQ, UK
M.S. Williamson
Affiliation:
Division of Biological Chemistry, Rothamsted Research, Harpenden, Herts. AL5 2JQ, UK
I. Denholm
Affiliation:
Division of Plant and Invertebrate Ecology, Rothamsted Research, Harpenden, Herts. AL5 2JQ, UK
*
*Author for correspondence Fax: +33 388 606 922 E-mail: Ioannis.Eleftherianos@ibmc.u-strasbg.fr

Abstract

Recent advances in the characterisation of insect sodium channel gene sequences have identified a small number of point mutations within the channel protein that are implicated in conferring target-site resistance to pyrethroid insecticides (so-called knockdown resistance or kdr). The L1014F (leucine-to-phenylalanine) mutation located in the centre of segment 6 of the domain II region (IIS6) of the sodium channel (the so-called kdr trait) has been detected in the peach-potato aphid, Myzus persicae (Sulzer), and is considered to be the primary cause of pyrethroid resistance in this species. Here we report on the characterisation of a second mutation, M918T (methione-to-threonine), within the nearby IIS4–S5 intracellular linker (the so-called super-kdr trait) in a field clone also possessing L1014F, with both mutations present in heterozygous form. The resistance phenotype of M. persicae clones possessing various combinations of L1014F and M918T to a wide range of pyrethroids (both Type I and II) was assessed in leaf-dip bioassays and to lambda-cyhalothrin applied at up to ten times the recommended field rate as foliar sprays to aphids feeding on whole plants. Bioassay results demonstrated that presence of both mutations was associated with extreme resistance to all the pyrethroids tested relative to aphids lacking the mutations. Furthermore, this resistance well exceeded that shown by aphids that were homozygous for L1014F but lacking M918T. However, pre-treatment with piperonyl butoxide in the leaf-dip bioassays failed to suppress pyrethroid resistance in aphids carrying one or both of the mutations. The relevance of these findings for monitoring and managing pyrethroid resistance in M. persicae populations in the field is discussed.

Type
Research Paper
Copyright
Copyright © Cambridge University Press 2007

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References

Anstead, J.A., Williamson, M.S., Eleftherianos, I.G. & Denholm, I. (2004) High-throughput detection of knockdown resistance in Myzus persicae using allelic discriminating quantitative PCR. Insect Biochemistry and MolecularBiology 34, 869875.Google ScholarPubMed
Anstead, J.A., Williamson, M.S. & Denholm, I. (2005) Evidence for multiple origins of identical insecticide resistance mutations in the aphid Myzus persicae. Insect Biochemistry and Molecular Biology 35, 249256.CrossRefGoogle ScholarPubMed
Blackman, R.L. (1988) Rearing and handling aphids. pp. 5968in Minks, A.K. & Harrewijn, P. (Eds) Aphids, their Biology, Natural Enemies and Control. Amsterdam, Elsevier.Google Scholar
Blackman, R.L., Spence, J.M., Field, L.M., Javed, N., Devine, G.J. & Devonshire, A.L. (1996) Inheritance of the amplified esterase genes responsible for insecticide resistance in Myzus persicae (Homoptera: Aphididae). Heredity 77, 154167.CrossRefGoogle Scholar
Busvine, J.R. (1951) Mechanism of resistance to insecticide in houseflies. Nature 168, 193195.CrossRefGoogle ScholarPubMed
Catterall, W.A. (2000) From ionic currents to molecular mechanisms: The structure and function of voltage-gated sodium channels. Neuron 26, 1325.CrossRefGoogle ScholarPubMed
Davies, T.G.E., Field, L.M., Usherwood, P.N.R. & Williamson, M.S. (2007) DDT, pyrethrins, pyrethroids and insect sodium channels. IUBMB Life 59, 151162.CrossRefGoogle ScholarPubMed
Devonshire, A.L., Moores, G.D. & ffrench-Constant, R.H. (1986) Detection of insecticide resistance by immunological estimation of carboxylesterase activity in Myzus persicae (Sulzer) and cross reaction the antiserum with Phorodon humuli (Schrank) (Hemiptera: Aphididae). Bulletin of Entomological Research 76, 97107.CrossRefGoogle Scholar
Dong, K. (1997) A single amino acid change in the para sodium channel protein is associated with knockdown resistance (kdr) to pyrethroid insecticides in German cockroach. Insect Biochemistry and Molecular Biology 27, 93100.CrossRefGoogle ScholarPubMed
Farnham, A.W. & Khambay, B.P.S. (1995a) The pyrethrins and related compounds. Part XXXIX – Structure activity relationships of pyrethroidal esters with cyclic side chains in the alcohol component against resistant strains of house fly (Musca domestica). Pesticide Science 44, 269275.CrossRefGoogle Scholar
Farnham, A.W. & Khambay, B.P.S. (1995b) The pyrethrins and related compounds. Part XL – Structure activity relationships of pyrethroidal esters with acyclic side chains in the alcohol component against resistant strains of house fly (Musca domestica). Pesticide Science 44, 277281.CrossRefGoogle Scholar
Farnham, A.W., Murray, A.W.A., Sawicki, R.M., Denholm, I. & White, J.C. (1987) Characterisation of the structure-activity relationship of kdr and two variants of super-kdr to pyrethroids in the house fly (Musca domestica L.). Pesticide Science 19, 209220.CrossRefGoogle Scholar
Fenton, B., Malloch, G., Woodford, J.A.T., Foster, S.P., Anstead, J., Denholm, I., King, L. & Pickup, J. (2005) The attack of the clones: tracking the movement of insecticide-resistant peach-potato aphids, Myzus persicae (Hemiptera: Aphididae). Bulletin of Entomological Research 95, 483494.CrossRefGoogle ScholarPubMed
Field, L.M., Anderson, A.P., Denholm, I., Foster, S.P., Harling, Z.K., Javed, N., Martinez-Torres, D., Moores, G.D., Williamson, M.S. & Devonshire, A.L. (1997) Use of biochemical and DNA diagnostics for characterising multiple mechanisms of insecticide resistance in the peach-potato aphid, Myzus persicae (Sulzer). Pesticide Science 51, 283289.3.0.CO;2-O>CrossRefGoogle Scholar
Foster, S.P., Denholm, I. & Thompson, R. (2002) Bioassay and field-simulator studies of the efficacy of pymetrozine against peach-potato aphids, Myzus persicae (Hemiptera: Aphididae), possessing different mechanisms of insecticide resistance. Pest Management Science 58, 805810.CrossRefGoogle ScholarPubMed
Guerrero, F.D., Jamroz, R.C., Kammlah, D. & Kunz, S.E. (1997) Toxicological and molecular characterization of pyrethroid-resistant horn flies, Haematobia irritans: identification of kdr and super-kdr point mutations. Insect Biochemistry and Molecular Biology 27, 745755.CrossRefGoogle ScholarPubMed
Liu, Z., Valles, S.M. & Dong, K. (2000) Novel point mutations in the German cockroach para sodium channel gene are associated with knockdown resistance (kdr) to pyrethroid insecticides. Insect Biochemistry and Molecular Biology 30, 991997.CrossRefGoogle ScholarPubMed
Liu, Z., Tan, J., Valles, S.M. & Dong, K. (2002) Synergistic interaction between two cockroach sodium channel mutations and a tobacco budworm sodium channel mutation in reducing channel sensitivity to a pyrethroid insecticide. Insect Biochemistry and Molecular Biology 32, 397404.CrossRefGoogle Scholar
Martinez-Torres, M., Devonshire, A.L. & Williamson, M.S. (1997) Molecular studies of knockdown resistance to pyrethroids: cloning of domain II sodium channel gene sequences from insects. Pesticide Science 51, 265270.3.0.CO;2-P>CrossRefGoogle Scholar
Martinez-Torres, D., Foster, S.P., Field, L.M., Devonshire, A.L. & Williamson, M.S. (1999) A sodium channel point mutation is associated with resistance to DDT and pyrethroid insecticides in the peach-potato aphid, Myzus persicae (Sulzer) (Hemiptera: Aphididae). Insect Molecular Biology 8, 339346.CrossRefGoogle ScholarPubMed
McCaffery, A. & Nauen, R. (2006) The Insecticide Resistance Action Committee (IRAC): Public responsibility and enlightened industrial self-interest. Outlooks on Pest Management 17, 1115.Google Scholar
Miyazaki, M., Ohyama, K., Dunlap, D.Y. & Matsumura, F. (1996) Cloning and sequencing of the para-type sodium channel gene from susceptible and kdr-resistant German cockroaches (Blattella germanica) and house fly (Musca domestica). Molecular and General Genetics 252, 6168.Google ScholarPubMed
Narahashi, T. (2000) Neuroreceptors and ion channels as the basis for drug action: past, present, and future. Journal of Pharmacology and Experimental Therapeutics 294, 126.Google ScholarPubMed
Park, Y. & Taylor, M.F.J. (1997) A novel mutation L1029H in sodium channel gene hscp associated with pyrethroid resistance for Heliothis virescens (Lepidoptera: Noctuidae). Insect Biochemistry and Molecular Biology 27, 913.CrossRefGoogle ScholarPubMed
Pittendrigh, B., Reenan, R., ffrench-Constant, R.H. & Ganetzky, B. (1997) Point mutations in the Drosophila sodium channel gene para associated with resistance to DDT and pyrethroid insecticides. Molecular and General Genetics 256, 602610.CrossRefGoogle ScholarPubMed
Robertson, J.L. & Preisler, H.K. (1992) Pesticide Bioassays with Arthropods. 127 pp. Boca Raton, FL, USA, CRC Press.Google Scholar
Roush, R.T. & McKenzie, J.A. (1987) Ecological genetics of insecticide and acaricide resistance. Annual Review of Entomology 32, 361380.CrossRefGoogle ScholarPubMed
Schuler, T.H., Martinez-Torres, D., Thompson, A.J., Denholm, I., Devonshire, A.L., Duce, I.R. & Williamson, M.S. (1998) Toxicological, electrophysiological, and molecular characterisation of knockdown resistance to pyrethroid insecticides in the diamondback moth, Plutella xylostella (L.). Pesticide Biochemistry and Physiology 59, 169182.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, NY, Chapman & Hall.CrossRefGoogle Scholar
Soderlund, D.M. & Bloomquist, J.R. (1990) Molecular mechanisms of insecticide resistance. pp. 5896in Roush, R.T. & Tabashnik, B.E. (Eds) Pesticide Resistance in Arthropods. New York, NY, Chapman & Hall.CrossRefGoogle Scholar
Soderlund, D.M. & Knipple, D.C. (2003) The molecular biology of knockdown resistance to pyrethroid insecticides. Insect Biochemistry and Molecular Biology 33, 563577.CrossRefGoogle ScholarPubMed
Tan, J., Liu, Z., Tsai, T.D., Valles, S.M., Goldin, A.L. & Dong, K. (2002) Novel sodium channel gene mutations in Blattella germanica reduce the sensitivity of expressed channels to deltamethrin. Insect Biochemistry and Molecular Biology 32, 445454.CrossRefGoogle ScholarPubMed
Tan, J.G., Liu, Z.Q., Wang, R.W., Huang, Z.Y., Chen, A.C., Gurevitz, M. & Dong, K. (2005) Identification of amino acid residues in the insect sodium channel critical for pyrethroid binding. Molecular Pharmacology 67, 513522.CrossRefGoogle ScholarPubMed
Williamson, M.S., Martinez-Torres, D., Hick, C.A. & Devonshire, A.L. (1996) Identification of mutations in the house fly para-type sodium channel gene associated with knockdown resistance (kdr) to pyrethroid insecticides. Molecular and General Genetics 252, 5160.CrossRefGoogle ScholarPubMed
Zhao, Y., Park, Y. & Adams, M.E. (2000) Functional and evolutionary consequences of pyrethroid resistance mutations in S6 transmembrane segments of a voltage-gated sodium channel. Biochemical Biophysical Research Communications 278, 516521.CrossRefGoogle ScholarPubMed