Overexpression of glutamate-gated chloride channel in the integument is mainly responsible for emamectin benzoate resistance in the western flower thrips Frankliniella occidentalis.

Abstract

Western flower thrips Frankliniella occidentalis is a serious polyphagous pest worldwide. In this study, we investigated the potential mechanisms of resistance including enhanced metabolism and target site insensitivity in an emamectin benzoate (EB)-resistant (EB-R) strain. The EB-R strain of F. occidentalis showed 356-fold increased resistance compared to a susceptible RDA strain. Analysis of cross-resistance to four other insecticides confirmed that EB resistance is highly specific to the contact toxicity of EB. Synergistic bioassay and quantitative PCR of cytochrome P450 monooxygenase (CYP) genes revealed that three overexpressed Cyps were likely involved in resistance. Among three putative glutamate-gated chloride channel (GluCl) genes identified, FoGluClc showed four radical amino acid substitutions and 3.8-fold and 31-fold transcription level in the head and integument in the EB-R strain when compared to the RDA strain. Backcrossing analysis and RNA interference confirmed that both amino acid substitution and overexpression of FoGluClc are responsible for EB resistance. In situ hybridization revealed that FoGluClc is mainly distributed in the integument in the EB-R strain. Cross-comparison of known genomes and transcriptomes of thrips species revealed that FoGluClc is unique to the Frankliniella genus. While mutations and overexpression of FoGluClc play major roles in EB resistance, the overexpressed Cyps are partially involved as metabolic factors. Higher expression of FoGluClc in the integument may suggest its role in the first-line defense against EB in the EB-R strain. Unique distribution of FoGluClc in the Frankliniella genus but not in other thrips species further suggests that FoGluClc may be a surplus channel not having an essential endogenous function and is thus recruited as a defense barrier against xenobiotics. © 2022 Society of Chemical Industry.