{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,28]],"date-time":"2026-10-28T00:16:16Z","timestamp":1793146576113,"version":"4.5.0"},"update-to":[{"DOI":"10.1371\/journal.pgen.1010814","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2023,7,12]],"date-time":"2023-07-12T00:00:00Z","timestamp":1689120000000}}],"reference-count":69,"publisher":"Public Library of Science (PLoS)","issue":"6","license":[{"start":{"date-parts":[[2023,6,29]],"date-time":"2023-06-29T00:00:00Z","timestamp":1687996800000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100012166","name":"National Key Research and Development Program of China","doi-asserted-by":"publisher","award":["2022YFD1400900"],"award-info":[{"award-number":["2022YFD1400900"]}],"id":[{"id":"10.13039\/501100012166","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["31871995"],"award-info":[{"award-number":["31871995"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.plosgenetics.org"],"crossmark-restriction":false},"short-container-title":["PLoS Genet"],"abstract":"<jats:p>\n                    Meta-diamides (e.g. broflanilide) and isoxazolines (e.g. fluralaner) are novel insecticides that target the resistant to dieldrin (RDL) subunit of insect \u03b3-aminobutyric acid receptors (GABARs). In this study, we used\n                    <jats:italic>in silico<\/jats:italic>\n                    analysis to identify residues that are critical for the interaction between RDL and these insecticides. Substitution of glycine at the third position (G3\u2019) in the third transmembrane domain (TMD3) with methionine (G3\u2019M\n                    <jats:sub>TMD3<\/jats:sub>\n                    ), which is present in vertebrate GABARs, had the strongest effect on fluralaner binding. This was confirmed by expression of RDL from the rice stem borer,\n                    <jats:italic>Chilo suppressalis<\/jats:italic>\n                    (\n                    <jats:italic>Cs<\/jats:italic>\n                    RDL) in oocytes of the African clawed frog,\n                    <jats:italic>Xenopus laevis<\/jats:italic>\n                    , where the G3\u2019M\n                    <jats:sub>TMD3<\/jats:sub>\n                    mutation almost abolished the antagonistic action of fluralaner. Subsequently, G3\u2019M\n                    <jats:sub>TMD3<\/jats:sub>\n                    was introduced into the\n                    <jats:italic>Rdl<\/jats:italic>\n                    gene of the fruit fly,\n                    <jats:italic>Drosophila melanogaster<\/jats:italic>\n                    , using the CRISPR\/Cas9 system. Larvae of heterozygous lines bearing G3\u2019M\n                    <jats:sub>TMD3<\/jats:sub>\n                    did not show significant resistance to avermectin, fipronil, broflanilide, and fluralaner. However, larvae homozygous for G3\u2019M\n                    <jats:sub>TMD3<\/jats:sub>\n                    were highly resistant to broflanilide and fluralaner whilst still being sensitive to fipronil and avermectin. Also, homozygous lines showed severely impaired locomotivity and did not survive to the pupal stage, indicating a significant fitness cost associated with G3\u2019M\n                    <jats:sub>TMD3<\/jats:sub>\n                    . Moreover, the M3\u2019G\n                    <jats:sub>TMD3<\/jats:sub>\n                    mutation in the mouse\n                    <jats:italic>Mus musculus<\/jats:italic>\n                    \u03b11\u03b22 GABAR increased sensitivity to fluralaner. Taken together, these results provide convincing\n                    <jats:italic>in vitro<\/jats:italic>\n                    and\n                    <jats:italic>in vivo<\/jats:italic>\n                    evidence for both broflanilide and fluralaner acting on the same amino acid site, as well as insights into potential mechanisms leading to target-site resistance to these insecticides. In addition, our findings could guide further modification of isoxazolines to achieve higher selectivity for the control of insect pests with minimal effects on mammals.\n                  <\/jats:p>","DOI":"10.1371\/journal.pgen.1010814","type":"journal-article","created":{"date-parts":[[2023,6,29]],"date-time":"2023-06-29T14:21:35Z","timestamp":1688048495000},"page":"e1010814","update-policy":"https:\/\/doi.org\/10.1371\/journal.pgen.corrections_policy","source":"Crossref","is-referenced-by-count":42,"title":["G3\u2019MTMD3 in the insect GABA receptor subunit, RDL, confers resistance to broflanilide and fluralaner"],"prefix":"10.1371","volume":"19","author":[{"given":"Yichi","family":"Zhang","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qiutang","family":"Huang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chengwang","family":"Sheng","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Genyan","family":"Liu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kexin","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhongqiang","family":"Jia","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tao","family":"Tang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xin","family":"Mao","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Andrew K.","family":"Jones","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhaojun","family":"Han","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7942-488X","authenticated-orcid":true,"given":"Chunqing","family":"Zhao","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2023,6,29]]},"reference":[{"issue":"3","key":"pgen.1010814.ref001","doi-asserted-by":"crossref","first-page":"430","DOI":"10.1038\/s41559-018-0793-y","article-title":"The global burden of pathogens and pests on major food crops.","volume":"3","author":"S Savary","year":"2019","journal-title":"Nat Ecol Evol"},{"issue":"3\u20134","key":"pgen.1010814.ref002","doi-asserted-by":"crossref","first-page":"163","DOI":"10.1080\/01677063.2016.1229781","article-title":"Ion channels as insecticide targets","volume":"30","author":"RH ffrench-Constant","year":"2016","journal-title":"J Neurogenet"},{"key":"pgen.1010814.ref003","doi-asserted-by":"crossref","first-page":"22","DOI":"10.1016\/j.pestbp.2014.11.006","article-title":"Novel GABA receptor pesticide targets","volume":"121","author":"JE Casida","year":"2015","journal-title":"Pest Biochem Physiol"},{"issue":"6","key":"pgen.1010814.ref004","doi-asserted-by":"crossref","first-page":"2609","DOI":"10.1002\/ps.6254","article-title":"Insecticide resistance management and industry: the origins and evolution of the Insecticide Resistance Action Committee (IRAC) and the mode of action classification scheme.","volume":"77","author":"TC Sparks","year":"2021","journal-title":"Pest Manag Sci"},{"issue":"5","key":"pgen.1010814.ref005","doi-asserted-by":"crossref","first-page":"1733","DOI":"10.1093\/jee\/83.5.1733","article-title":"Isolation of dieldrin resistance from field populations of Drosophila melanogaster (Diptera: Drosophilidae).","volume":"83","author":"RH ffrench-Constant","year":"1990","journal-title":"J Econ Entomol"},{"issue":"2","key":"pgen.1010814.ref006","doi-asserted-by":"crossref","first-page":"646","DOI":"10.1603\/EC10391","article-title":"The A2\u2032N mutation of the RDL gamma-aminobutyric acid receptor conferring fipronil resistance in Laodelphax striatellus (Hemiptera: Delphacidae).","volume":"104","author":"T Nakao","year":"2011","journal-title":"J Econ Entomol"},{"key":"pgen.1010814.ref007","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1016\/j.ibmb.2013.11.009","article-title":"The novel isoxazoline ectoparasiticide fluralaner: Selective inhibition of arthropod \u03b3-aminobutyric acid- and L-glutamate-gated chloride channels and insecticidal\/acaricidal activity","volume":"45","author":"M Gassel","year":"2014","journal-title":"Insect Biochem Mol Biol"},{"issue":"1","key":"pgen.1010814.ref008","doi-asserted-by":"crossref","first-page":"530","DOI":"10.1186\/s13071-017-2470-4","article-title":"The novel isoxazoline ectoparasiticide lotilaner (Credelio\u2122): a non-competitive antagonist specific to invertebrates \u03b3-aminobutyric acid-gated chloride channels (GABACls).","volume":"10","author":"L Rufener","year":"2017","journal-title":"Parasites Vectors"},{"key":"pgen.1010814.ref009","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1016\/j.pestbp.2018.02.002","article-title":"Fluxametamide: A novel isoxazoline insecticide that acts via distinctive antagonism of insect ligand-gated chloride channels.","volume":"151","author":"M Asahi","year":"2018","journal-title":"Pest Biochem Physiol"},{"issue":"4","key":"pgen.1010814.ref010","doi-asserted-by":"crossref","first-page":"366","DOI":"10.1016\/j.ibmb.2013.02.002","article-title":"Meta-diamide insecticides acting on distinct sites of RDL GABA receptor from those for conventional noncompetitive antagonists","volume":"43","author":"T Nakao","year":"2013","journal-title":"Insect Biochem Mol Biol"},{"issue":"3","key":"pgen.1010814.ref011","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1584\/jpestics.D13-024","article-title":"A comparison of the modes of action of novel meta-diamide insecticides and conventional noncompetitive antagonists on the Spodoptera litura RDL GABA receptor","volume":"38","author":"T Nakao","year":"2013","journal-title":"J Pestic Sci"},{"key":"pgen.1010814.ref012","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1016\/j.pestbp.2019.11.001","article-title":"Effects of intersubunit amino acid substitutions on GABA receptor sensitivity to the ectoparasiticide fluralaner","volume":"163","author":"K Yamato","year":"2020","journal-title":"Pest Biochem Physiol"},{"key":"pgen.1010814.ref013","doi-asserted-by":"crossref","first-page":"105217","DOI":"10.1016\/j.pestbp.2022.105217","article-title":"The mode of action of isocycloseram: A novel isoxazoline insecticide.","volume":"187","author":"J Blythe","year":"2022","journal-title":"Pest Biochem Physiol."},{"issue":"1","key":"pgen.1010814.ref014","doi-asserted-by":"crossref","first-page":"188","DOI":"10.1111\/1744-7917.12917","article-title":"Resistance and fitness costs in diamondback moths after selection using broflanilide, a novel meta-diamide insecticide.","volume":"29","author":"X Sun","year":"2022","journal-title":"Insect Sci."},{"key":"pgen.1010814.ref015","doi-asserted-by":"crossref","first-page":"39","DOI":"10.1016\/j.pestbp.2014.09.010","article-title":"Minireview: Mode of action of meta-diamide insecticides.","volume":"121","author":"T Nakao","year":"2015","journal-title":"Pest Biochem Physiol"},{"issue":"1","key":"pgen.1010814.ref016","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1017\/S0016672300028986","article-title":"Gene mapping and cross-resistance in cyclodiene insecticide-resistant Drosophila melanogaster (Mg.).","volume":"57","author":"RH ffrench-Constant","year":"1991","journal-title":"Genet Res"},{"issue":"3","key":"pgen.1010814.ref017","doi-asserted-by":"crossref","first-page":"914","DOI":"10.1093\/jee\/99.3.914","article-title":"Investigation of resistance mechanisms to fipronil in diamondback moth (Lepidoptera: Plutellidae).","volume":"99","author":"A Li","year":"2006","journal-title":"J Econ Entomol"},{"issue":"4","key":"pgen.1010814.ref018","doi-asserted-by":"crossref","first-page":"1364","DOI":"10.1603\/EC11074","article-title":"Differential resistance and cross-resistance to three phenylpyrazole insecticides in the planthopper Nilaparvata lugens (Hemiptera: Delphacidae).","volume":"104","author":"X Zhao","year":"2011","journal-title":"J Econ Entomol"},{"issue":"16","key":"pgen.1010814.ref019","doi-asserted-by":"crossref","first-page":"7209","DOI":"10.1073\/pnas.88.16.7209","article-title":"Molecular cloning and transformation of cyclodiene resistance in Drosophila: an invertebrate gamma-aminobutyric acid subtype A receptor locus","volume":"88","author":"RH ffrench-Constant","year":"1991","journal-title":"Proc Natl Acad Sci U S A"},{"key":"pgen.1010814.ref020","doi-asserted-by":"crossref","first-page":"1957","DOI":"10.1073\/pnas.90.5.1957","article-title":"A single-amino acid substitution in a gamma-aminobutyric acid subtype A receptor locus is associated with cyclodiene insecticide resistance in Drosophila populations","volume":"90","author":"RH ffrench-Constant","year":"1993","journal-title":"Proc Natl Acad Sci U S A"},{"key":"pgen.1010814.ref021","doi-asserted-by":"crossref","first-page":"449","DOI":"10.1038\/363449a0","article-title":"A point mutation in a Drosophila GABA receptor confers insecticide resistance","volume":"363","author":"RH ffrench-Constant","year":"1993","journal-title":"Nature"},{"key":"pgen.1010814.ref022","doi-asserted-by":"crossref","first-page":"293","DOI":"10.1016\/j.neuro.2016.03.009","article-title":"Mechanisms of resistance to insecticides targeting RDL GABA receptors in planthoppers","volume":"60","author":"T. Nakao","year":"2017","journal-title":"Neurotoxicology"},{"issue":"1","key":"pgen.1010814.ref023","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1584\/jpestics.D11-018","article-title":"Fipronil resistance in Sogatella furcifera: Molecular cloning and functional expression of wild-type and mutant RDL GABA receptor subunits","volume":"37","author":"T Nakao","year":"2012","journal-title":"J Pestic Sci"},{"issue":"1","key":"pgen.1010814.ref024","doi-asserted-by":"crossref","first-page":"744","DOI":"10.1016\/j.bbrc.2009.11.131","article-title":"The antiparasitic isoxazoline A1443 is a potent blocker of insect ligand-gated chloride channels","volume":"391","author":"Y Ozoe","year":"2010","journal-title":"Biochem Biophys Res Commun"},{"issue":"3","key":"pgen.1010814.ref025","doi-asserted-by":"crossref","first-page":"285","DOI":"10.1016\/j.pestbp.2013.09.005","article-title":"Insecticidal 3-benzamido-N-phenylbenzamides specifically bind with high affinity to a novel allosteric site in housefly GABA receptors.","volume":"107","author":"Y Ozoe","year":"2013","journal-title":"Pest Biochem Physiol"},{"key":"pgen.1010814.ref026","doi-asserted-by":"crossref","first-page":"431","DOI":"10.1021\/bk-2015-1204.ch030","volume-title":"Discovery and Synthesis of Crop Protection Products. 1204","author":"Y Ozoe","year":"2015"},{"issue":"5","key":"pgen.1010814.ref027","doi-asserted-by":"crossref","first-page":"546","DOI":"10.1124\/mol.117.109413","article-title":"A single amino acid substitution in the third transmembrane region has opposite impacts on the selectivity of the parasiticides fluralaner and ivermectin for ligand-gated chloride channels","volume":"92","author":"Y Nakata","year":"2017","journal-title":"Mol Pharmacol"},{"issue":"5","key":"pgen.1010814.ref028","doi-asserted-by":"crossref","first-page":"1019","DOI":"10.1021\/jf4050809","article-title":"Insect \u03b3-aminobutyric acid receptors and isoxazoline insecticides: Toxicological profiles relative to the binding sites of [3H]fluralaner, [3H]-4\u2032-ethynyl-4-n-propylbicycloorthobenzoate, and [3H]avermectin","volume":"62","author":"CQ Zhao","year":"2014","journal-title":"J Agric Food Chem"},{"issue":"4","key":"pgen.1010814.ref029","doi-asserted-by":"crossref","first-page":"560","DOI":"10.1021\/tx500520w","article-title":"Golden Age of RyR and GABA-R Diamide and Isoxazoline Insecticides: Common Genesis, Serendipity, Surprises, Selectivity, and Safety","volume":"28","author":"JE Casida","year":"2015","journal-title":"Chem Res Toxicol"},{"issue":"49","key":"pgen.1010814.ref030","doi-asserted-by":"crossref","first-page":"12922","DOI":"10.1073\/pnas.1711699114","article-title":"Molecular basis of selective resistance of the bumblebee BiNav1 sodium channel to tau-fluvalinate","volume":"114","author":"S Wu","year":"2017","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"23","key":"pgen.1010814.ref031","doi-asserted-by":"crossref","first-page":"8607","DOI":"10.1073\/pnas.1407379111","article-title":"GABAA receptor target of tetramethylenedisulfotetramine","volume":"111","author":"CQ Zhao","year":"2014","journal-title":"Proc Natl Acad Sci U S A"},{"key":"pgen.1010814.ref032","first-page":"211","volume-title":"Advances in Insect Physiology. 44. The Boulevard, Langford Lane, Kidlington, Oxford, OX51GB","author":"Y. Ozoe","year":"2013"},{"issue":"4","key":"pgen.1010814.ref033","doi-asserted-by":"crossref","first-page":"583","DOI":"10.1111\/j.1365-2583.2010.01017.x","article-title":"A point mutation in a glutamate-gated chloride channel confers abamectin resistance in the two-spotted spider mite, Tetranychus urticae Koch","volume":"19","author":"DH Kwon","year":"2010","journal-title":"Insect Mol Biol"},{"key":"pgen.1010814.ref034","doi-asserted-by":"crossref","first-page":"50","DOI":"10.1016\/j.ibmb.2017.05.006","article-title":"Mutations on M3 helix of Plutella xylostella glutamate-gated chloride channel confer unequal resistance to abamectin by two different mechanisms","volume":"86","author":"X Wang","year":"2017","journal-title":"Insect Biochem Mol Biol"},{"issue":"3","key":"pgen.1010814.ref035","doi-asserted-by":"crossref","first-page":"372","DOI":"10.1016\/j.bmc.2015.08.008","article-title":"Broflanilide: A meta-diamide insecticide with a novel mode of action","volume":"24","author":"T Nakao","year":"2016","journal-title":"Bioorg Med Chem"},{"issue":"1","key":"pgen.1010814.ref036","doi-asserted-by":"crossref","first-page":"220","DOI":"10.1016\/j.celrep.2013.06.020","article-title":"Highly efficient targeted mutagenesis of Drosophila with the CRISPR\/Cas9 system.","volume":"4","author":"R Bassett Andrew","year":"2013","journal-title":"Cell Rep."},{"issue":"4","key":"pgen.1010814.ref037","doi-asserted-by":"crossref","first-page":"1029","DOI":"10.1534\/genetics.113.152710","article-title":"Genome engineering of Drosophila with the CRISPR RNA-guided Cas9 nuclease","volume":"194","author":"SJ Gratz","year":"2013","journal-title":"Genetics"},{"issue":"47","key":"pgen.1010814.ref038","doi-asserted-by":"crossref","first-page":"19012","DOI":"10.1073\/pnas.1318481110","article-title":"Optimized gene editing technology for Drosophila melanogaster using germ line-specific Cas9","volume":"110","author":"X Ren","year":"2013","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"4","key":"pgen.1010814.ref039","doi-asserted-by":"crossref","first-page":"961","DOI":"10.1534\/genetics.113.160713","article-title":"Highly specific and efficient CRISPR\/Cas9-catalyzed homology-directed repair in Drosophila","volume":"196","author":"SJ Gratz","year":"2014","journal-title":"Genetics"},{"issue":"1","key":"pgen.1010814.ref040","doi-asserted-by":"crossref","first-page":"52","DOI":"10.4161\/fly.26828","article-title":"A simplified and efficient germline-specific CRISPR\/Cas9 system for Drosophila genomic engineering.","volume":"8","author":"ZL Sebo","year":"2014","journal-title":"Fly."},{"issue":"29","key":"pgen.1010814.ref041","doi-asserted-by":"crossref","first-page":"E2967","DOI":"10.1073\/pnas.1405500111","article-title":"Optimized CRISPR\/Cas tools for efficient germline and somatic genome engineering in Drosophila","volume":"111","author":"F Port","year":"2014","journal-title":"Proc Natl Acad Sci U S A"},{"key":"pgen.1010814.ref042","doi-asserted-by":"crossref","first-page":"116","DOI":"10.1016\/j.ibmb.2015.01.018","article-title":"In vivo functional analysis of the Drosophila melanogaster nicotinic acetylcholine receptor D\u03b16 using the insecticide spinosad","volume":"64","author":"J Somers","year":"2015","journal-title":"Insect Biochem Mol Biol"},{"issue":"51","key":"pgen.1010814.ref043","doi-asserted-by":"crossref","first-page":"14692","DOI":"10.1073\/pnas.1618258113","article-title":"Resistance mutation conserved between insects and mites unravels the benzoylurea insecticide mode of action on chitin biosynthesis","volume":"113","author":"V Douris","year":"2016","journal-title":"Proc Natl Acad Sci U S A"},{"key":"pgen.1010814.ref044","doi-asserted-by":"crossref","first-page":"62","DOI":"10.1016\/j.ibmb.2016.04.007","article-title":"A CRISPR\/Cas9 mediated point mutation in the alpha 6 subunit of the nicotinic acetylcholine receptor confers resistance to spinosad in Drosophila melanogaster","volume":"73","author":"CT Zimmer","year":"2016","journal-title":"Insect Biochem Mol Biol"},{"key":"pgen.1010814.ref045","doi-asserted-by":"crossref","first-page":"127","DOI":"10.1016\/j.ibmb.2017.06.013","article-title":"Investigation of the contribution of RyR target-site mutations in diamide resistance by CRISPR\/Cas9 genome modification in Drosophila","volume":"87","author":"V Douris","year":"2017","journal-title":"Insect Biochem Mol Biol"},{"key":"pgen.1010814.ref046","doi-asserted-by":"crossref","first-page":"105118","DOI":"10.1016\/j.pestbp.2022.105118","article-title":"Dual nicotinic acetylcholine receptor subunit gene knockouts reveal limits to functional redundancy","volume":"184","author":"W Chen","year":"2022","journal-title":"Pest Biochem Physiol"},{"key":"pgen.1010814.ref047","doi-asserted-by":"crossref","first-page":"103367","DOI":"10.1016\/j.ibmb.2020.103367","article-title":"Multiple target-site mutations occurring in lepidopterans confer resistance to diamide insecticides","volume":"121","author":"JM Huang","year":"2020","journal-title":"Insect Biochem Mol Biol"},{"issue":"4","key":"pgen.1010814.ref048","doi-asserted-by":"crossref","first-page":"1581","DOI":"10.1002\/ps.6215","article-title":"Untangling a Gordian knot: the role of a GluCl3 I321T mutation in abamectin resistance in Tetranychus urticae","volume":"77","author":"W Xue","year":"2021","journal-title":"Pest Manag Sci"},{"issue":"3","key":"pgen.1010814.ref049","doi-asserted-by":"crossref","first-page":"R21","DOI":"10.1186\/gb-2012-13-3-r21","article-title":"The generation of chromosomal deletions to provide extensive coverage and subdivision of the Drosophila melanogaster genome","volume":"13","author":"RK Cook","year":"2012","journal-title":"Genome Biol"},{"issue":"4","key":"pgen.1010814.ref050","doi-asserted-by":"crossref","first-page":"1004","DOI":"10.1016\/j.bbrc.2020.09.077","article-title":"Drosophila ZnT1 is essential in the intestine for dietary zinc absorption","volume":"533","author":"Z Wang","year":"2020","journal-title":"Biochem Biophys Res Commun"},{"issue":"2","key":"pgen.1010814.ref051","doi-asserted-by":"crossref","first-page":"145","DOI":"10.1016\/j.ydbio.2020.02.008","article-title":"Knock-in mutations of scarecrow, a Drosophila homolog of mammalian Nkx2.1, reveal a novel function required for development of the optic lobe in Drosophila melanogaster","volume":"461","author":"S Yoo","year":"2020","journal-title":"Dev Biol"},{"issue":"1","key":"pgen.1010814.ref052","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1007\/BF00286176","article-title":"Cytogenetic analysis of chromosome region 89A of Drosophila melanogaster: isolation of deficiencies and mapping of Po, Aldox-1 and transposon insertions","volume":"235","author":"CR Nelson","year":"1992","journal-title":"Mol Gen Genet"},{"issue":"9","key":"pgen.1010814.ref053","first-page":"E2115","article-title":"GABAergic inhibition of leg motoneurons is required for normal walking behavior in freely moving Drosophila","volume":"115","author":"SBM Gowda","year":"2018","journal-title":"Proc Natl Acad Sci U S A"},{"key":"pgen.1010814.ref054","doi-asserted-by":"crossref","first-page":"409","DOI":"10.1038\/s41586-019-1610-8","article-title":"Genome editing retraces the evolution of toxin resistance in the monarch butterfly","volume":"574","author":"M Karageorgi","year":"2019","journal-title":"Nature"},{"key":"pgen.1010814.ref055","doi-asserted-by":"crossref","first-page":"A1442","DOI":"10.3389\/fphys.2019.01442","article-title":"New Drosophila Circadian Clock Mutants Affecting Temperature Compensation Induced by Targeted Mutagenesis of Timeless.","volume":"10","author":"S Singh","year":"2019","journal-title":"Front Physiol"},{"issue":"14","key":"pgen.1010814.ref056","doi-asserted-by":"crossref","first-page":"2661","DOI":"10.1111\/mec.15503","article-title":"Evolutionary trade-offs of insecticide resistance\u2014The fitness costs associated with target-site mutations in the nAChR of Drosophila melanogaster","volume":"29","author":"RA Homem","year":"2020","journal-title":"Mol Ecol"},{"issue":"2","key":"pgen.1010814.ref057","doi-asserted-by":"crossref","first-page":"127","DOI":"10.1186\/s12863-020-00934-3","article-title":"Precise single base substitution in the shibire gene by CRISPR\/Cas9-mediated homology directed repair in Bactrocera tryoni","volume":"21","author":"A Choo","year":"2020","journal-title":"BMC Genet"},{"issue":"1","key":"pgen.1010814.ref058","first-page":"1","article-title":"Genetic disruption of the putative binding site for Homer on DmGluRA reduces sleep in Drosophila.","volume":"43","author":"S Ly","year":"2019","journal-title":"Sleep"},{"issue":"4","key":"pgen.1010814.ref059","doi-asserted-by":"crossref","first-page":"1213","DOI":"10.1016\/j.aspen.2017.08.021","article-title":"Insecticidal spectrum of fluralaner to agricultural and sanitary pests.","volume":"20","author":"CW Sheng","year":"2017","journal-title":"J Asia-Pac Entomol"},{"issue":"7","key":"pgen.1010814.ref060","doi-asserted-by":"crossref","first-page":"1870","DOI":"10.1093\/molbev\/msw054","article-title":"MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for bigger datasets","volume":"33","author":"S Kumar","year":"2016","journal-title":"Mol Biol Evol"},{"issue":"2","key":"pgen.1010814.ref061","doi-asserted-by":"crossref","first-page":"283","DOI":"10.1107\/S0021889892009944","article-title":"PROCHECK: a program to check the stereochemical quality of protein structures","volume":"26","author":"RA Laskowski","year":"1993","journal-title":"J Appl Crystallogr"},{"issue":"4","key":"pgen.1010814.ref062","doi-asserted-by":"crossref","first-page":"477","DOI":"10.1007\/BF00228148","article-title":"AQUA and PROCHECK-NMR: Programs for checking the quality of protein structures solved by NMR","volume":"8","author":"RA Laskowski","year":"1996","journal-title":"J Biomol NMR"},{"key":"pgen.1010814.ref063","doi-asserted-by":"crossref","first-page":"W407","DOI":"10.1093\/nar\/gkm290","article-title":"ProSA-web: Interactive web service for the recognition of errors in three-dimensional structures of proteins","volume":"35","author":"M Wiederstein","year":"2007","journal-title":"Nucleic Acids Res"},{"key":"pgen.1010814.ref064","doi-asserted-by":"crossref","first-page":"2645","DOI":"10.1002\/ps.5059","article-title":"Fiprole insecticide resistance of Laodelphax striatellus: electrophysiological and molecular docking characterization of A2\u2032N RDL GABA receptors","volume":"74","author":"CW Sheng","year":"2018","journal-title":"Pest Manag Sci"},{"key":"pgen.1010814.ref065","doi-asserted-by":"crossref","first-page":"18","DOI":"10.1016\/j.ibmb.2018.01.003","article-title":"Molecular cloning, spatiotemporal and functional expression of GABA receptor subunits RDL1 and RDL2 of the rice stem borer Chilo suppressalis","volume":"94","author":"CW Sheng","year":"2018","journal-title":"Insect Biochem Mol Biol"},{"issue":"39","key":"pgen.1010814.ref066","doi-asserted-by":"crossref","first-page":"11582","DOI":"10.1021\/acs.jafc.1c00385","article-title":"Functional characteristics of the Lepidopteran ionotropic GABA receptor 8916 subunit interacting with the LCCH3 or the RDL subunit","volume":"69","author":"QT Huang","year":"2021","journal-title":"J Agric Food Chem"},{"issue":"1","key":"pgen.1010814.ref067","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1673\/031.003.3401","article-title":"Overlapping confidence intervals or standard error intervals: What do they mean in terms of statistical significance?","volume":"3","author":"ME Payton","year":"2003","journal-title":"J Insect Sci."},{"key":"pgen.1010814.ref068","first-page":"93","article-title":"Optimization of wrMTrck to monitor Drosophila larval locomotor activity","author":"DS Brooks","year":"2016","journal-title":"J Insect Physiol"},{"issue":"2","key":"pgen.1010814.ref069","doi-asserted-by":"crossref","first-page":"111673","DOI":"10.1016\/j.yexcr.2019.111673","article-title":"Reduction of Rpd3 suppresses defects in locomotive ability and neuronal morphology induced by the knockdown of Drosophila SLC25A46 via an epigenetic pathway","volume":"385","author":"K Suda","year":"2019","journal-title":"Exp Cell Res"}],"updated-by":[{"DOI":"10.1371\/journal.pgen.1010814","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2023,7,12]],"date-time":"2023-07-12T00:00:00Z","timestamp":1689120000000}}],"container-title":["PLOS Genetics"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pgen.1010814","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,12,15]],"date-time":"2023-12-15T22:11:49Z","timestamp":1702678309000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pgen.1010814"}},"subtitle":[],"editor":[{"given":"Subba Reddy","family":"Palli","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2023,6,29]]},"references-count":69,"journal-issue":{"issue":"6","published-online":{"date-parts":[[2023,6,29]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pgen.1010814","relation":{},"ISSN":["1553-7404"],"issn-type":[{"value":"1553-7404","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,6,29]]}}}