Abstract
Insecticide resistance is an economically important example of evolution in response to intense selection pressure. Here, the genetics of resistance to the neonicotinoid insecticide imidacloprid is explored using the Drosophila Genetic Reference Panel, a collection of inbred Drosophila melanogaster genotypes derived from a single population in North Carolina. Imidacloprid resistance varied substantially among genotypes, and more resistant genotypes tended to show increased capacity to metabolize and excrete imidacloprid. Variation in resistance level was then associated with genomic and transcriptomic variation, implicating several candidate genes involved in central nervous system function and the cytochrome P450s Cyp6g1 and Cyp6g2. CRISPR-Cas9 mediated removal of Cyp6g1 suggested that it contributed to imidacloprid resistance only in backgrounds where it was already highly expressed. Cyp6g2, previously implicated in juvenile hormone synthesis via expression in the ring gland, was shown to be expressed in metabolically relevant tissues of resistant genotypes. Cyp6g2 overexpression was shown to both metabolize imidacloprid and confer resistance. These data collectively suggest that imidacloprid resistance is influenced by a variety of previously known and unknown genetic factors.
Highlights
The introduction of synthetic insecticides is often followed by the appearance of resistance phenotypes in field populations, leading to significant reductions in agricultural production[1]
P450 enzymes (P450s) which are capable of metabolizing imidacloprid and conferring resistance have been identified in several species[9,10,11]; the Cyp6g1 gene of D. melanogaster
The potential for the other 87 D. melanogaster P450s to be involved in imidacloprid resistance has yet to be tested; Cyp6g1 is so far the only P450 linked to imidacloprid resistance in this species
Summary
The introduction of synthetic insecticides is often followed by the appearance of resistance phenotypes in field populations, leading to significant reductions in agricultural production[1]. Further modifications of the AA haplotype resulted from the insertions of the transposable element HMS-Beagle and a P element upstream of Cyp6g1, creating the BA and BP haplotypes, respectively These derived haplotypes have been associated with increased levels of Cyp6g1 expression and resistance to insecticides such as DDT and azinphos-methyl[16, 17]. The structural modification of imidacloprid in biological systems includes both nitroreduction and oxidation reactions Metabolites from both pathways have been detected in plants, animals and insects, but soil bacteria produce predominantly the nitroreduction metabolites[18,19,20]. The transcriptional response to xenobiotics is often regulated by transcription factors, such as Cap ‘n’ Collar and DHR96, that regulate the expression of many P450s26, 27
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