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Widespread pyrethroid resistance in Australian diamondback moth, Plutella xylostella (L.), is related to multiple mutations in the para sodium channel gene

Published online by Cambridge University Press:  23 February 2011

N.M. Endersby ,
K. Viduka ,
S.W. Baxter ,
J. Saw ,
D.G. Heckel  and
S.W. McKechnie
N.M. Endersby*
Affiliation:
School of Biological Sciences, Monash University, Victoria 3800, Australia
K. Viduka
Affiliation:
School of Biological Sciences, Monash University, Victoria 3800, Australia
S.W. Baxter
Affiliation:
Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, UK
J. Saw
Affiliation:
School of Biological Sciences, Monash University, Victoria 3800, Australia
D.G. Heckel
Affiliation:
Department of Entomology, Max Planck Institute for Chemical Ecology, Hans-Knöll-Straße 8, D-07745 Jena, Germany
S.W. McKechnie
Affiliation:
School of Biological Sciences, Monash University, Victoria 3800, Australia
*
*Author for correspondence Fax: +61 3 8344 2279 E-mail: [email protected]
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Abstract

Populations of Plutella xylostella, extending over 3800 km in southern Australia, show no genetic structure as assessed by microsatellite markers; yet outbreaks of pyrethroid resistance occur sporadically in cropping areas. Since mutations in the para voltage-gated sodium channel gene have been implicated in pyrethroid resistance, we looked for DNA sequence variation at this target among Australian moths. We found two resistance mutations previously reported for this species (L1014F and T929I), as well as a novel substitution (F1020S). Of the eight possible haplotypes formed by combinations of these three biallelic polymorphisms, only four were found in Australian populations: the wild-type allele (w), the kdr mutation allele (kdr) with only L1014F, the super-kdr-like combination of L1014F and T929I (skdrl), and the crashdown allele with only F1020S (cdr). Comparison of genotype frequencies among survivors of permethrin assays with those from untreated controls identified three resistant genotypes: skdrl homozygotes, cdr homozygotes and the corresponding heterozygote, cdr/skrdl – the heterozygote being at least as resistant as either homozygote. Spatial heterogeneity of allele frequencies was conspicuous, both across the continent and among local collections, consistent with reported spatial heterogeneity of pyrethroid resistance. Further, high resistance samples were sometimes associated with high frequency of cdr, sometimes high frequency of skdrl, or sometimes with a high combined cdr+skdrl frequency. The skdrl and cdr alleles explain a high proportion of the Australia-wide resistance variation. These data add to evidence that nerve insensitivity by mutations in the para-sodium channel gene is a common pyrethroid resistance mechanism in P. xylostella.

Keywords

Plutella xylostellasodium channelkdrpyrethroidinsecticide resistance
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 101 , Issue 4 , August 2011 , pp. 393 - 405
Copyright
Copyright © Cambridge University Press 2011

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References

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, 249–256.CrossRefGoogle ScholarPubMed
Avise, J.C. (2004) Molecular Markers, Natural History, and Evolution. 2nd edn. Sunderland, MA, USA, Sinauer Associates Inc.Google Scholar
Baker, G.J. & Kovaliski, J. (1999) Detection of insecticide resistance in Plutella xylostella (L.) (Lepidoptera: Plutellidae) populations in South Australian crucifer crops. Australian Journal of Entomology 38, 132–134.CrossRefGoogle Scholar
Black, W.C. & Krafsur, E.S. (1985) A Fortran program for the calculation and analysis of two-locus linkage disequilibrium coefficients. Theoretical and Applied Genetics 70, 491–496.CrossRefGoogle ScholarPubMed
Busvine, J.R. (1951) Mechanism of resistance to insecticide in houseflies. Nature 168, 193–195.CrossRefGoogle ScholarPubMed
Chapman, J.W., Reynolds, D.R., Smith, A.D., Riley, J.R., Pedgley, D.E. & Woiwood, I.P. (2002) High altitude migration of the diamondback moth Plutella xylostella to the UK: a study using radar, aerial netting and ground trapping. Ecological Entomology 27, 641–650.CrossRefGoogle Scholar
Davies, T.G.E. & Williamson, M.S. (2009) Interactions of pyrethroids with the voltage-gated sodium channel. Bayer Crop Science Journal 62, 159–178.Google Scholar
Endersby, N.M., McKechnie, S.W., Ridland, P.M. & Weeks, A.R. (2006) Lack of structure in populations of diamondback moth, Plutella xylostella (L.), in Australia revealed using microsatellite markers. Molecular Ecology 15, 107–118.CrossRefGoogle Scholar
Endersby, N.M., Ridland, P.M. & Hoffmann, A.A. (2008) The effects of local selection versus dispersal on insecticide resistance patterns: longitudinal evidence from diamondback moth (Plutella xylostella (Lepidoptera: Plutellidae)) in Australia evolving resistance to pyrethroids. Bulletin of Entomological Research 98, 145–157.CrossRefGoogle ScholarPubMed
Forcioli, D., Frey, B. & Frey, J.E. (2002) High nucleotide diversity in the para-like voltage-sensitive sodium channel gene sequence in the western flower thrips (Thysanoptera: Thripidae). Journal of Economic Entomology 95, 838–848.CrossRefGoogle ScholarPubMed
Garnier-Géré, P. & Dillmann, C. (1992) A computer program for testing pairwise linkage disequilibria in subdivided populations. Journal of Heredity 83, 239.CrossRefGoogle ScholarPubMed
Goudet, J., Raymond, M., de-Meeus, T. & Rousset, F. (1996) Testing differentiation in diploid populations. Genetics 144, 1933–1940.CrossRefGoogle ScholarPubMed
Guo, S.W. & Thompson, E.A. (1992) Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics 48, 361–372.CrossRefGoogle ScholarPubMed
Heckel, D.G. (2008) Molecular genetics of insecticide resistance in Lepidoptera. pp. 239–269 in Goldsmith, M.R. & Marec, F. (Eds) Molecular Biology and Genetics of the Lepidoptera. Boca Raton, FL, USA, CRC Press.Google Scholar
Honda, K. (1992) Hibernation and migration of diamondback moth in northern Japan. pp. 43–50 in Talekar, N.S. (Ed.) Diamondback Moth and Other Crucifer Pests: Proceedings of the Second International Workshop. 10–15 December 1990, Asian Vegetable Research and Development Center, Tainan, Taiwan.Google Scholar
Jamroz, R.C., Guerrero, F.D., Kammlah, D.M. & Kunz, S.E. (1998) Role of the kdr and super-kdr sodium channel mutations in pyrethroid resistance: correlation of allelic frequency to resistance level in wild and laboratory populations of horn flies (Haematobia irritans). Insect Biochemistry and Molecular Biology 28, 1031–1037.CrossRefGoogle ScholarPubMed
Kim, H.G., Hawthorne, D.J., Peters, T., Dively, G.P. & Clark, J.M. (2005) Application of DNA-based genotyping techniques for the detection of kdr-like pyrethroid resistance in field populations of Colorado potato beetle. Pesticide Biochemistry & Physiology 81, 85–96.CrossRefGoogle Scholar
Kwon, D.H., Choi, B.R., Park, H.M., Lee, S.H., Miyata, T., Clark, J.M. & Lee, S.H. (2004) Knockdown resistance allele frequency in field populations of Plutella xylostella in Korea. Pesticide Biochemistry & Physiology 80, 21–30.CrossRefGoogle Scholar
Lewontin, R.C. (1974) The Genetic Basis of Evolutionary Change. New York, USA, Columbia University Press.Google Scholar
Lin, D.Y. & Zeng, D. (2006). Likelihood-based inference on haplotype effects in genetic association studies. Journal of the American Statistical Association 101, 89–104.CrossRefGoogle Scholar
Linnean Society of New South Wales (1884) Notes and exhibits. The Proceedings of the Linnean Society of New South Wales for the year 1883 VIII, 218 & 282.Google Scholar
Liu, Q., Thorland, E.C., Heit, J.A., & Sommer, S.S. (1997) Overlapping PCR for bidirectional PCR amplification of specific alleles: A rapid one-tube method for simultaneously differentiating homozygotes and heterozygotes. Genome Biology 7, 389–398.Google ScholarPubMed
Martinez-Torres, D., 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, 265–270.3.0.CO;2-P>CrossRefGoogle Scholar
O'Reilly, A.O., Khambay, B.P., Williamson, M.S., Field, L.M., Wallace, B.A. & Davies, T.G.E. (2006) Modelling insecticide-binding sites in the voltage-gated sodium channel. Biochemical Journal 396, 255–263.CrossRefGoogle ScholarPubMed
Raymond, M. & Rousset, F. (1995a) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. Journal of Heredity 86, 248–249.CrossRefGoogle Scholar
Raymond, M. & Rousset, F. (1995b) An exact test for population differentiation. Evolution 49, 1283–1286.CrossRefGoogle ScholarPubMed
Russell, R.M., Robertson, J.L. & Savin, N.E. (1977) POLO: a new computer program for probit analysis. Bulletin of the Entomological Society of America 23, 209–213.CrossRefGoogle Scholar
Sambrook, J., Fritsch, E. & Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. 2nd edn. New York, USA, Cold Spring Harbor Laboratory Press.Google Scholar
Saw, J., Endersby, N.M. & McKechnie, S.W. (2006) Lack of mtDNA diversity among Australian diamondback moth Plutella xylostella (L.) suggests isolation and a founder effect. Insect Science 13, 365–373.CrossRefGoogle Scholar
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 & Physiology 59, 169–182.CrossRefGoogle Scholar
Smith, T.J., Hyeock Lee, S., Ingles, P.J., Knipple, D.C. & Soderlund, D.M. (1997) The L1014F point mutation in the house fly Vssc sodium channel confers knockdown resistance to pyrethroids. Insect Biochemistry and Molecular Biology 27, 807–812.CrossRefGoogle Scholar
Soderlund, D.M., Bloomquist, J.R. (1989) Neurotoxic actions of pyrethroid insecticides. Annual Review of Entomology 34, 77–96.CrossRefGoogle ScholarPubMed
Soderlund, D.M. & Knipple, D.C. (2003) The molecular biology of knockdown resistance to pyrethroid insecticides. Insect Biochemistry and Molecular Biology 33, 563–577.CrossRefGoogle ScholarPubMed
Sonoda, S., Igaki, C., Ashfaq, M. & Tsumuki, H. (2006) Pyrethroid-resistant diamondback moth expresses alternatively spliced sodium channel transcripts with and without T929I mutation. Insect Biochemistry and Molecular Biology 36, 904–910.CrossRefGoogle ScholarPubMed
Sonoda, S., Igaki, C. & Tsumuki, H. (2008a) Alternatively spliced sodium channel transcripts expressed in field strains of the diamondback moth. Insect Biochemistry and Molecular Biology 38, 883–890.CrossRefGoogle ScholarPubMed
Sonoda, S., Tsukahara, Y., Ashfaq, M. & Tsumuki, H. (2008b) Genomic organization of the para-sodium channel α-subunit genes from the pyrethroid-resistant and -susceptible strains of the diamondback moth. Archives of Insect Biochemistry and Physiology 69, 1–12.CrossRefGoogle ScholarPubMed
Sun, C.N. (1992) Insecticide resistance in diamondback moth. pp. 419–426 in Talekar, N.S. (Ed.) Diamondback Moth and Other Crucifer Pests: Proceedings of the Second International Workshop. 10–15 December 1990, Asian Vegetable Research and Development Center, Tainan, Taiwan.Google Scholar
Tabashnik, B.E. & Cushing, N.L. (1987) Leaf residue vs. topical bioassays for assessing insecticide resistance in the diamondback moth, Plutella xylostella L. FAO Plant Protection Bulletin 35, 11–14.Google Scholar
Talekar, N.S. & Shelton, A.M. (1993) Biology, ecology, and management of the diamondback moth. Annual Review of Entomology 38, 275–301.CrossRefGoogle Scholar
Tryon, H. (1889) Report on insect and fungus pests No. 1. pp. 170–173. Department of Agriculture, Queensland. Brisbane, Queensland, Australia, James C Beal, Government Printer.Google Scholar
Tsukahara, Y., Sonoda, S., Fujiwara, Y., Nakasuji, F. & Tsumuki, H. (2003) Molecular analysis of the para-sodium channel gene in the pyrethroid-resistant diamondback moth, Plutella xylostella (Lepidoptera: Yponomeutidae). Applied Entomology & Zoology 38, 23–29.CrossRefGoogle Scholar
Usherwood, P.N.R., Vais, H., Khambay, B.P.S., Davies, T.G.E. & Williamson, M.S. (2005) Sensitivity of the Drosophila para sodium channel to DDT is not lowered by the super-kdr mutation M918T on the IIS4-S5 linker that profoundly reduces sensitivity to permethrin and deltamethrin. FEBS Letters 579, 6317–6325.CrossRefGoogle Scholar
Usherwood, P.N.R., Davies, T.G.E., Mellor, I.R., O'Reilly, A.O., Peng, F., Vais, H., Khambay, B.P.S., Field, L.M. & Williamson, M.S. (2007) Mutations in DIIS5 and the DIIS4-S5 linker of Drosophila melanogaster sodium channel define binding domains for pyrethroids and DDT. FEBS Letters 581, 5485–5492.CrossRefGoogle ScholarPubMed
Vais, H., Williamson, M.S., Devonshire, A.L. & Usherwood, P.N. (2001) The molecular interactions of pyrethroid insecticides with insect and mammalian sodium channels. Pest Management Science 57, 877–888.CrossRefGoogle ScholarPubMed
Vais, H., Atkinson, S., Pluteanu, F., Goodson, S.J., Devonshire, A.L., Williamson, M.S. & Usherwood, P.N.R. (2003) Mutations of the para sodium channel of Drosophila melanogaster identify putative binding sites for pyrethroids. Molecular Pharmacology 64, 914–922.CrossRefGoogle ScholarPubMed
Weir, B.S. & Cockerham, C.C. (1984) Estimating F-statistics for the analysis of population structure. Evolution 38, 1358–1370.Google ScholarPubMed
Williamson, M.S., Martinez-Torres, D., Hick, C.A. & Devonshire, A.L. (1996) Identification of mutations in the housefly para-type sodium channel gene associated with knockdown resistance (kdr) to pyrethroid insecticides. Molecular and General Genetics 252, 51–60.CrossRefGoogle ScholarPubMed