Harnessing model organisms to study insecticide resistance

Crow, 1957, Genetics of insect resistance to chemicals, Ann Rev Entomol, 2, 227, 10.1146/annurev.en.02.010157.001303 Ffrench-Constant, 2004, The genetics and genomics of insecticide resistance, Trends Genet, 20, 163, 10.1016/j.tig.2004.01.003 Perry, 2011, The biology of insecticidal activity and resistance, Insect Biochem Mol Biol, 41, 411, 10.1016/j.ibmb.2011.03.003 Jinek, 2012, A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity, Science, 337, 816, 10.1126/science.1225829 Jinek, 2013, RNA-programmed genome editing in human cells, Elife, 2, e00471, 10.7554/eLife.00471 Gratz, 2013, Genome engineering of Drosophila with the CRISPR RNA-guided Cas9 nuclease, Genetics, 194, 1029, 10.1534/genetics.113.152710 Port, 2014, Optimized CRISPR/Cas tools for efficient germline and somatic genome engineering in Drosophila, Proc Natl Acad Sci U S A, 111, E2967, 10.1073/pnas.1405500111 Liu, 2005, A nicotinic acetylcholine receptor mutation conferring target-site resistance to imidacloprid in Nilaparvata lugens (brown planthopper), Proc Natl Acad Sci U S A, 102, 8420, 10.1073/pnas.0502901102 Perry, 2008, Mutations in Dalpha1 or Dbeta2 nicotinic acetylcholine receptor subunits can confer resistance to neonicotinoids in Drosophila melanogaster, Insect Biochem Mol Biol, 38, 520, 10.1016/j.ibmb.2007.12.007 Bao, 2014, Spinosad resistance of melon thrips, Thrips palmi, is conferred by G275E mutation in alpha6 subunit of nicotinic acetylcholine receptor and cytochrome P450 detoxification, Pestic Biochem Physiol, 112, 51, 10.1016/j.pestbp.2014.04.013 Baxter, 2010, Mis-spliced transcripts of nicotinic acetylcholine receptor alpha6 are associated with field evolved spinosad resistance in Plutella xylostella (L.), PLoS Genet, 6, e1000802, 10.1371/journal.pgen.1000802 Hsu, 2012, Truncated transcripts of nicotinic acetylcholine subunit gene Bdalpha6 are associated with spinosad resistance in Bactrocera dorsalis, Insect Biochem Mol Biol, 42, 806, 10.1016/j.ibmb.2012.07.010 Puinean, 2013, A nicotinic acetylcholine receptor transmembrane point mutation (G275E) associated with resistance to spinosad in Frankliniella occidentalis, J Neurochem, 124, 590, 10.1111/jnc.12029 Perry, 2007, A Dalpha6 knockout strain of Drosophila melanogaster confers a high level of resistance to spinosad, Insect Biochem Mol Biol, 37, 184, 10.1016/j.ibmb.2006.11.009 Perry, 2015, Expression of insect alpha6-like nicotinic acetylcholine receptors in Drosophila melanogaster highlights a high level of conservation of the receptor:spinosyn interaction, Insect Biochem Mol Biol, 64, 106, 10.1016/j.ibmb.2015.01.017 Somers, 2015, In vivo functional analysis of the Drosophila melanogaster nicotinic acetylcholine receptor Dalpha6 using the insecticide spinosad, Insect Biochem Mol Biol, 64, 116, 10.1016/j.ibmb.2015.01.018 Watson, 2010, A spinosyn-sensitive Drosophila melanogaster nicotinic acetylcholine receptor identified through chemically induced target site resistance, resistance gene identification, and heterologous expression, Insect Biochem Mol Biol, 40, 376, 10.1016/j.ibmb.2009.11.004 Zimmer, 2016, A CRISPR/Cas9 mediated point mutation in the alpha 6 subunit of the nicotinic acetylcholine receptor confers resistance to spinosad in Drosophila melanogaster, Insect Biochem Mol Biol, 73, 62, 10.1016/j.ibmb.2016.04.007 Kwon, 2010, A point mutation in a glutamate-gated chloride channel confers abamectin resistance in the two-spotted spider mite, Tetranychus urticae Koch, Insect Mol Biol, 19, 583 Wang, 2016, A point mutation in the glutamate-gated chloride channel of Plutella xylostella is associated with resistance to abamectin, Insect Mol Biol, 25, 116, 10.1111/imb.12204 Kane, 2000, Drug-resistant Drosophila indicate glutamate-gated chloride channels are targets for the antiparasitics nodulisporic acid and ivermectin, Proc Natl Acad Sci U S A, 97, 13949, 10.1073/pnas.240464697 Ingles, 1996, Characterization of voltage-sensitive sodium channel gene coding sequences from insecticide-susceptible and knockdown-resistant house fly strains, Insect Biochem Mol Biol, 26, 319, 10.1016/0965-1748(95)00093-3 Williamson, 1996, Identification of mutations in the housefly para-type sodium channel gene associated with knockdown resistance (kdr) to pyrethroid insecticides, Mol Gen Genet, 252, 51, 10.1007/BF02173204 Pittendrigh, 1997, Point mutations in the Drosophila sodium channel gene para associated with resistance to DDT and pyrethroid insecticides, Mol Gen Genet, 256, 602, 10.1007/s004380050608 Soderlund, 2003, The molecular biology of knockdown resistance to pyrethroid insecticides, Insect Biochem Mol Biol, 33, 563, 10.1016/S0965-1748(03)00023-7 Ffrench-Constant, 1994, The molecular and population genetics of cyclodiene insecticide resistance, Insect Biochem Mol Biol, 24, 335, 10.1016/0965-1748(94)90026-4 Garrood, 2017, Influence of the RDL A301S mutation in the brown planthopper Nilaparvata lugens on the activity of phenylpyrazole insecticides, Pestic Biochem Physiol, 142, 1, 10.1016/j.pestbp.2017.01.007 Ffrench-Constant, 1993, A point mutation in a Drosophila GABA receptor confers insecticide resistance, Nature, 363, 449, 10.1038/363449a0 Remnant, 2013, Gene duplication in the major insecticide target site, Rdl, in Drosophila melanogaster, Proc Natl Acad Sci U S A, 110, 14705, 10.1073/pnas.1311341110 Roditakis, 2017, Ryanodine receptor point mutations confer diamide insecticide resistance in tomato leafminer, Tuta absoluta (Lepidoptera: Gelechiidae), Insect Biochem Mol Biol, 80, 11, 10.1016/j.ibmb.2016.11.003 Troczka, 2012, Resistance to diamide insecticides in diamondback moth, Plutella xylostella (Lepidoptera: Plutellidae) is associated with a mutation in the membrane-spanning domain of the ryanodine receptor, Insect Biochem Mol Biol, 42, 873, 10.1016/j.ibmb.2012.09.001 Zuo, 2017, CRISPR/Cas9 mediated G4946E substitution in the ryanodine receptor of Spodoptera exigua confers high levels of resistance to diamide insecticides, Insect Biochem Mol Biol, 89, 79, 10.1016/j.ibmb.2017.09.005 Douris, 2017, Investigation of the contribution of RyR target-site mutations in diamide resistance by CRISPR/Cas9 genome modification in Drosophila, Insect Biochem Mol Biol, 87, 127, 10.1016/j.ibmb.2017.06.013 Cook, 2012, The generation of chromosomal deletions to provide extensive coverage and subdivision of the Drosophila melanogaster genome, Genome Biol, 13, R21, 10.1186/gb-2012-13-3-r21 Bischof, 2007, An optimized transgenesis system for Drosophila using germ-line-specific phiC31 integrases, Proc Natl Acad Sci U S A, 104, 3312, 10.1073/pnas.0611511104 Brand, 1993, Targeted gene expression as a means of altering cell fates and generating dominant phenotypes, Development, 118, 401, 10.1242/dev.118.2.401 Anstead, 2015, Lucilia cuprina genome unlocks parasitic fly biology to underpin future interventions, Nat Commun, 6, 7344, 10.1038/ncomms8344 Venken, 2006, P[acman]: A BAC transgenic platform for targeted insertion of large DNA fragments in D. melanogaster, Science, 314, 1747, 10.1126/science.1134426 Stevens, 2017, Expressing a moth abcc2 gene in transgenic Drosophila causes susceptibility to Bt Cry1Ac without requiring a cadherin-like protein receptor, Insect Biochem Mol Biol, 80, 61, 10.1016/j.ibmb.2016.11.008 Venken, 2011, MiMIC: a highly versatile transposon insertion resource for engineering Drosophila melanogaster genes, Nat Methods, 8, 737, 10.1038/nmeth.1662 Nagarkar-Jaiswal, 2015, A library of MiMICs allows tagging of genes and reversible, spatial and temporal knockdown of proteins in Drosophila, Elife, 4 Nagarkar-Jaiswal, 2015, A genetic toolkit for tagging intronic MiMIC containing genes, Elife, 4 Kanca, 2017, Gene tagging strategies to assess protein expression, localization, and function in Drosophila, Genetics, 207, 389 Neumuller, 2012, Stringent analysis of gene function and protein–protein interactions using fluorescently tagged genes, Genetics, 190, 931, 10.1534/genetics.111.136465 Senturk, 2017, Genetic strategies to tackle neurological diseases in fruit flies, Curr Opin Neurobiol, 50, 24, 10.1016/j.conb.2017.10.017 Bass, 2011, Mutation of a nicotinic acetylcholine receptor beta subunit is associated with resistance to neonicotinoid insecticides in the aphid Myzus persicae, BMC Neurosci, 12, 51, 10.1186/1471-2202-12-51 Gong, 2004, Genomic deletions of the Drosophila melanogaster Hsp70 genes, Genetics, 168, 1467, 10.1534/genetics.104.030874 Somers, 2017, pleiotropic effects of loss of the Dalpha1 subunit in Drosophila melanogaster: implications for insecticide resistance, Genetics, 205, 263, 10.1534/genetics.116.195750 Gratz, 2014, Highly specific and efficient CRISPR/Cas9-catalyzed homology-directed repair in Drosophila, Genetics, 196, 961, 10.1534/genetics.113.160713 Bier, 2018, Advances in engineering the fly genome with the CRISPR-Cas system, Genetics, 208, 1, 10.1534/genetics.117.1113 Zhang, 2014, A versatile two-step CRISPR- and RMCE-based strategy for efficient genome engineering in Drosophila, G3 (Bethesda), 4, 2409, 10.1534/g3.114.013979 Ffrench-Constant, 2017, Does resistance really carry a fitness cost?, Curr Opin Insect Sci, 21, 39, 10.1016/j.cois.2017.04.011 Forfert, 2017, Neonicotinoid pesticides can reduce honeybee colony genetic diversity, PLoS One, 12, e0186109, 10.1371/journal.pone.0186109 Eiri, 2012, A nicotinic acetylcholine receptor agonist affects honey bee sucrose responsiveness and decreases waggle dancing, J Exp Biol, 215, 2022, 10.1242/jeb.068718 Gill, 2012, Combined pesticide exposure severely affects individual- and colony-level traits in bees, Nature, 491, 105, 10.1038/nature11585 Henry, 2012, A common pesticide decreases foraging success and survival in honey bees, Science, 336, 348, 10.1126/science.1215039 Chiu, 2010, Assaying locomotor activity to study circadian rhythms and sleep parameters in Drosophila, J Vis Exp, 43, 2157 Neckameyer, 2016, Protocols to study behavior in Drosophila, Methods Mol Biol, 1478, 303, 10.1007/978-1-4939-6371-3_19 Rostant, 2017, Pleiotropic effects of DDT resistance on male size and behaviour, Behav Genet, 47, 449, 10.1007/s10519-017-9850-6 Li, 2017, Fitness trade-off associated with spinosad resistance in Frankliniella occidentalis (Thysanoptera: Thripidae), J Econ Entomol, 110, 1755, 10.1093/jee/tox122 Daborn, 2012, Using Drosophila melanogaster to validate metabolism-based insecticide resistance from insect pests, Insect Biochem Mol Biol, 42, 918, 10.1016/j.ibmb.2012.09.003 Ibrahim, 2015, Allelic variation of cytochrome P450s drives resistance to bednet insecticides in a major malaria vector, PLoS Genet, 11, e1005618, 10.1371/journal.pgen.1005618 Mitchell, 2014, Metabolic and target-site mechanisms combine to confer strong DDT resistance in Anopheles gambiae, PLoS One, 9, e92662, 10.1371/journal.pone.0092662 Riga, 2015, Functional characterization of the Tetranychus urticae CYP392A11, a cytochrome P450 that hydroxylates the METI acaricides cyenopyrafen and fenpyroximate, Insect Biochem Mol Biol, 65, 91, 10.1016/j.ibmb.2015.09.004 Riveron, 2014, A single mutation in the GSTe2 gene allows tracking of metabolically based insecticide resistance in a major malaria vector, Genome Biol, 15, R27, 10.1186/gb-2014-15-2-r27 Zimmer, 2018, Neofunctionalization of duplicated P450 genes drives the evolution of insecticide resistance in the brown planthopper, Curr Biol, 28, 10.1016/j.cub.2017.11.060 Highfill, 2017, Naturally segregating variation at Ugt86Dd contributes to nicotine resistance in Drosophila melanogaster, Genetics, 207, 311, 10.1534/genetics.117.300058 Le Goff, 2017, Resistance evolution in Drosophila: the case of CYP6G1, Pest Manag Sci, 73, 493, 10.1002/ps.4470 Denecke, 2015, The Wiggle index: an open source bioassay to assess sub-lethal insecticide response in Drosophila melanogaster, PLoS One, 10, e0145051, 10.1371/journal.pone.0145051 Hoi, 2014, Dissecting the insect metabolic machinery using twin ion mass spectrometry: a single P450 enzyme metabolizing the insecticide imidacloprid in vivo, Anal Chem, 86, 3525, 10.1021/ac404188g Fusetto, 2017, Partitioning the roles of CYP6G1 and gut microbes in the metabolism of the insecticide imidacloprid in Drosophila melanogaster, Sci Rep, 7, 11339, 10.1038/s41598-017-09800-2 Denecke, 2017, Multiple P450s and variation in neuronal genes underpins the response to the insecticide imidacloprid in a population of Drosophila melanogaster, Sci Rep, 7, 11338, 10.1038/s41598-017-11092-5 Christesen, 2017, Transcriptome analysis of drosophila melanogaster third instar larval ring glands points to novel functions and uncovers a cytochrome p450 required for development, G3 (Bethesda), 7, 467, 10.1534/g3.116.037333 Brinzer, 2015, Metabolomic profiling of permethrin-treated Drosophila melanogaster identifies a role for tryptophan catabolism in insecticide survival, Insect Biochem Mol Biol, 67, 74, 10.1016/j.ibmb.2015.09.009 Piper, 2014, A holidic medium for Drosophila melanogaster, Nat Methods, 11, 100, 10.1038/nmeth.2731 Chintapalli, 2013, Mapping an atlas of tissue-specific Drosophila melanogaster metabolomes by high resolution mass spectrometry, PLoS One, 8, e78066, 10.1371/journal.pone.0078066 Chen, 2016, Direct interaction of avermectin with epidermal growth factor receptor mediates the penetration resistance in Drosophila larvae, Open Biol, 6, 150231, 10.1098/rsob.150231 Dermauw, 2014, The ABC gene family in arthropods: comparative genomics and role in insecticide transport and resistance, Insect Biochem Mol Biol, 45, 89, 10.1016/j.ibmb.2013.11.001 Leader, 2018, FlyAtlas 2: a new version of the Drosophila melanogaster expression atlas with RNA-Seq, miRNA-Seq and sex-specific data, Nucleic Acids Res, 46, D809, 10.1093/nar/gkx976 Sun, 2017, Mdr65 decreases toxicity of multiple insecticides in Drosophila melanogaster, Insect Biochem Mol Biol, 89, 11, 10.1016/j.ibmb.2017.08.002 Denecke, 2017, Describing the role of Drosophila melanogaster ABC transporters in insecticide biology using CRISPR-Cas9 knockouts, Insect Biochem Mol Biol, 91, 1, 10.1016/j.ibmb.2017.09.017 Seong, 2016, Splice form variant and amino acid changes in MDR49 confers DDT resistance in transgenic Drosophila, Sci Rep, 6, 23355, 10.1038/srep23355