Pyrethroid resistance in Sitophilus zeamais is associated with a mutation (T929I) in the voltage‐gated sodium channel

The maize weevil, Sitophilus zeamais, is the most important pest affecting stored grain in Brazil and its control relies heavily on the use of insecticides. The intensive use of compounds such as the pyrethroids has led to the emergence of resistance, and previous studies have suggested that resistance to both pyrethroids and 1,1,1‐trichloro‐2,2‐bis(p‐chlorophenyl)ethane (DDT) may result from reduced sensitivity of the insecticide target, the voltage‐gated sodium channel. To identify the molecular mechanisms underlying pyrethroid resistance in S. zeamais, the domain II region of the voltage‐gated sodium channel (para‐orthologue) gene was amplified by PCR and sequenced from susceptible and resistant laboratory S. zeamais strains that were selected with a discriminating dose of DDT. A single point mutation, T929I, was found in the para gene of the resistant S. zeamais populations and its presence in individual weevils was strongly associated with survival after DDT exposure. This is the first identification of a target‐site resistance mutation in S. zeamais and unusually it is a super‐kdr type mutation occurring in the absence of the more common kdr (L1014F) substitution. A high‐throughput assay based on TaqMan single nucleotide polymorphism genotyping was developed for sensitive detection of the mutation and used to screen field‐collected strains of S. zeamais. This showed that the mutation is present at low frequency in field populations and is a useful tool for informing control strategies.

[1]  Y. Nomura,et al.  A sodium channel mutation identified in Aedes aegypti selectively reduces cockroach sodium channel sensitivity to type I, but not type II pyrethroids. , 2011, Insect biochemistry and molecular biology.

[2]  S. Toda,et al.  Identification of Three Point Mutations on the Sodium Channel Gene in Pyrethroid-Resistant Thrips tabaci (Thysanoptera: Thripidae) , 2009, Journal of economic entomology.

[3]  Y. Nomura,et al.  Identification of a cluster of residues in transmembrane segment 6 of domain III of the cockroach sodium channel essential for the action of pyrethroid insecticides. , 2009, The Biochemical journal.

[4]  M. Williamson,et al.  Knockdown resistance to DDT and pyrethroids: from target-site mutations to molecular modelling. , 2008, Pest management science.

[5]  R. Guedes,et al.  Enhanced activity of carbohydrate- and lipid-metabolizing enzymes in insecticide-resistant populations of the maize weevil, Sitophilus zeamais , 2008, Bulletin of Entomological Research.

[6]  P. Usherwood,et al.  Mutations in DIIS5 and the DIIS4–S5 linker of Drosophila melanogaster sodium channel define binding domains for pyrethroids and DDT , 2007, FEBS letters.

[7]  John Vontas,et al.  Detection of knockdown resistance (kdr) mutations in Anopheles gambiae: a comparison of two new high-throughput assays with existing methods , 2007, Malaria Journal.

[8]  P. De Marco,et al.  Competition between insecticide-susceptible and -resistant populations of the maize weevil, Sitophilus zeamais. , 2007, Chemosphere.

[9]  R. Guedes,et al.  Partial characterization of glutathione S-transferases in pyrethroid-resistant and -susceptible populations of the maize weevil, Sitophilus zeamais , 2007 .

[10]  P. Usherwood,et al.  DDT, pyrethrins, pyrethroids and insect sodium channels , 2007, IUBMB life.

[11]  K. Dong Insect sodium channels and insecticide resistance , 2007, Invertebrate Neuroscience.

[12]  J. Vontas,et al.  Identification of mutations in the para sodium channel of Bemisia tabaci from Crete, associated with resistance to pyrethroids , 2006 .

[13]  B. Wallace,et al.  Modelling insecticide-binding sites in the voltage-gated sodium channel. , 2006, The Biochemical journal.

[14]  S. Morin,et al.  Multiple origins of pyrethroid resistance in sympatric biotypes of Bemisia tabaci (Hemiptera: Aleyrodidae). , 2006, Insect biochemistry and molecular biology.

[15]  E. Campbell,et al.  Voltage Sensor of Kv1.2: Structural Basis of Electromechanical Coupling , 2005, Science.

[16]  E. Campbell,et al.  Crystal Structure of a Mammalian Voltage-Dependent Shaker Family K+ Channel , 2005, Science.

[17]  A. Devonshire,et al.  Identification of mutations in the houseflypara-type sodium channel gene associated with knockdown resistance (kdr) to pyrethroid insecticides , 1996, Molecular and General Genetics MGG.

[18]  P. Jewess,et al.  6.1 – Pyrethroids , 2005 .

[19]  M. Williamson,et al.  Identification of mutations associated with pyrethroid resistance in the para-type sodium channel of the cat flea, Ctenocephalides felis. , 2004, Insect biochemistry and molecular biology.

[20]  R. Guedes,et al.  Glutathione S‐transferase detoxification as a potential pyrethroid resistance mechanism in the maize weevil, Sitophilus zeamais , 2003 .

[21]  P. Usherwood,et al.  Mutations of the para sodium channel of Drosophila melanogaster identify putative binding sites for pyrethroids. , 2003, Molecular pharmacology.

[22]  M. Galera,et al.  Dissipation of pyrethroid residues in peppers, zucchinis, and green beans exposed to field treatments in greenhouses: evaluation by decline curves , 2003 .

[23]  D. M. Soderlund,et al.  The molecular biology of knockdown resistance to pyrethroid insecticides. , 2003, Insect biochemistry and molecular biology.

[24]  R. Guedes,et al.  Insecticide resistance and synergism in Brazilian populations of Sitophilus zeamais (Coleoptera: Curculionidae) , 2003 .

[25]  J. M. Martínez Vidal,et al.  Dissipation of pyrethroid residues in peppers, zucchinis, and green beans exposed to field treatments in greenhouses: evaluation by decline curves. , 2003, Journal of agricultural and food chemistry.

[26]  J. Brown,et al.  Mutations in the Bemisia tabaci para sodium channel gene associated with resistance to a pyrethroid plus organophosphate mixture. , 2002, Insect biochemistry and molecular biology.

[27]  B. Frey,et al.  High Nucleotide Diversity in the para-Like Voltage-Sensitive Sodium Channel Gene Sequence in the Western Flower Thrips (Thysanoptera: Thripidae) , 2002, Journal of economic entomology.

[28]  A. L. Goldin,et al.  Novel sodium channel gene mutations in Blattella germanica reduce the sensitivity of expressed channels to deltamethrin. , 2002, Insect biochemistry and molecular biology.

[29]  P. Usherwood,et al.  The molecular interactions of pyrethroid insecticides with insect and mammalian sodium channels. , 2001, Pest management science.

[30]  T. Narahashi,et al.  Neuroreceptors and ion channels as the basis for drug action: past, present, and future. , 2000, The Journal of pharmacology and experimental therapeutics.

[31]  A. Devonshire,et al.  Molecular Analysis of kdr-like Resistance in Permethrin-Resistant Strains of Head Lice, Pediculus capitis , 2000 .

[32]  J. George,et al.  Identification of a point mutation in the para-type sodium channel gene from a pyrethroid-resistant cattle tick. , 1999, Biochemical and biophysical research communications.

[33]  A. Devonshire,et al.  A sodium channel point mutation is associated with resistance to DDT and pyrethroid insecticides in the peach‐potato aphid, Myzus persicae (Sulzer) (Hemiptera: Aphididae) , 1999, Insect molecular biology.

[34]  D. M. Soderlund,et al.  Molecular analysis of kdr-like resistance in a permethrin-resistant strain of Colorado potato beetle. , 1999 .

[35]  J. Perez-Mendoza Survey of insecticide resistance in Mexican populations of maize weevil, Sitophilus zeamais Motschulsky (coleoptera: curculionidae) , 1999 .

[36]  A. Devonshire,et al.  Toxicological, Electrophysiological, and Molecular Characterisation of Knockdown Resistance to Pyrethroid Insecticides in the Diamondback Moth,Plutella xylostella(L.) , 1998 .

[37]  R. Guedes,et al.  Characterization of malathion resistance in a Mexican population of Rhizopertha dominica , 1998 .

[38]  R. Guedes,et al.  Biochemical mechanisms of organophosphate resistance in Rhyzopertha dominica (Coleoptera: Bostrichidae) populations from the United States and Brazil , 1997 .

[39]  S. E. Kunz,et al.  Toxicological and molecular characterization of pyrethroid-resistant horn flies, Haematobia irritans: identification of kdr and super-kdr point mutations. , 1997, Insect biochemistry and molecular biology.

[40]  Irina Afonina,et al.  Efficient priming of PCR with short oligonucleotides conjugated to a minor groove binder , 1997, Nucleic Acids Res..

[41]  K. Dong A single amino acid change in the para sodium channel protein is associated with knockdown-resistance (kdr) to pyrethroid insecticides in German cockroach. , 1997, Insect biochemistry and molecular biology.

[42]  M. Taylor,et al.  A novel mutation L1029H in sodium channel gene hscp associated with pyrethroid resistance for Heliothis virescens (Lepidoptera:Noctuidae). , 1997, Insect biochemistry and molecular biology.

[43]  Masahiro Miyazaki,et al.  Cloning and sequencing of the para-type sodium channel gene from susceptible and kdr-resistant German cockroaches (Blattella germanica) and house fly (Musca domestica) , 1996, Molecular and General Genetics MGG.

[44]  R. Guedes,et al.  Resistance to Chlorpyrifos-Methyl, Pirimiphos-Methyl, and Malathion in Brazilian and U.S. Populations of Rhyzopertha dominica (Coleopera: Bostrichidae) , 1996 .

[45]  C. Cruz,et al.  Resistance to DDT and pyrethroids in Brazilian populations of Sitophilus zeamais Motsch. (Coleoptera: Curculionidae) , 1995 .

[46]  C. Cruz,et al.  Inheritance of Deltamethrin resistance in a Brazilian strain of maize weevil (Sitophilus zeamais mots.) , 1994 .

[47]  R. M. Sawicki Unusual response of DDT-resistant houseflies to carbinol analogues of DDT , 1978, Nature.

[48]  D. Maddison,et al.  Coleoptera , 2006, Nature.