Skip to main content Accessibility help
×
×
Home

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

  • I. Eleftherianos (a1), S.P. Foster (a1), M.S. Williamson (a2) and I. Denholm (a1)
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.

Copyright
Corresponding author
*Author for correspondence Fax: +33 388 606 922 E-mail: Ioannis.Eleftherianos@ibmc.u-strasbg.fr
References
Hide All
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.
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.
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.
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.
Busvine, J.R. (1951) Mechanism of resistance to insecticide in houseflies. Nature 168, 193195.
Catterall, W.A. (2000) From ionic currents to molecular mechanisms: The structure and function of voltage-gated sodium channels. Neuron 26, 1325.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
McCaffery, A. & Nauen, R. (2006) The Insecticide Resistance Action Committee (IRAC): Public responsibility and enlightened industrial self-interest. Outlooks on Pest Management 17, 1115.
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.
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.
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.
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.
Robertson, J.L. & Preisler, H.K. (1992) Pesticide Bioassays with Arthropods. 127 pp. Boca Raton, FL, USA, CRC Press.
Roush, R.T. & McKenzie, J.A. (1987) Ecological genetics of insecticide and acaricide resistance. Annual Review of Entomology 32, 361380.
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.
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.
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.
Soderlund, D.M. & Knipple, D.C. (2003) The molecular biology of knockdown resistance to pyrethroid insecticides. Insect Biochemistry and Molecular Biology 33, 563577.
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.
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.
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.
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.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Bulletin of Entomological Research
  • ISSN: 0007-4853
  • EISSN: 1475-2670
  • URL: /core/journals/bulletin-of-entomological-research
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed