A near-chromosome level genome assembly of the European hoverfly, Sphaerophoria rueppellii (Diptera: Syrphidae), provides comparative insights into insecticide resistance-related gene family evolution

Abstract

Background Sphaerophoria rueppellii, a European species of hoverfly, is a highly effective beneficial predator of hemipteran crop pests including aphids, thrips and coleopteran/lepidopteran larvae in integrated pest management (IPM) programmes. It is also a key pollinator of a wide variety of important agricultural crops. No genomic information is currently available for S. rueppellii. Without genomic information for such beneficial predator species, we are unable to perform comparative analyses of insecticide target-sites and genes encoding metabolic enzymes potentially responsible for insecticide resistance, between crop pests and their predators. These metabolic mechanisms include several gene families - cytochrome P450 monooxygenases (P450s), ATP binding cassette transporters (ABCs), glutathione-S-transferases (GSTs), UDP-glycosyltransferases (UGTs) and carboxyl/choline esterases (CCEs). Methods and findings In this study, a high-quality near-chromosome level de novo genome assembly (as well as a mitochondrial genome assembly) for S. rueppellii has been generated using a hybrid approach with PacBio long-read and Illumina short-read data, followed by super scaffolding using Hi-C data. The final assembly achieved a scaffold N50 of 87Mb, a total genome size of 537.6Mb and a level of completeness of 96% using a set of 1,658 core insect genes present as full-length genes. The assembly was annotated with 14,249 protein-coding genes. Comparative analysis revealed gene expansions of CYP6Zx P450s, epsilon-class GSTs, dietary CCEs and multiple UGT families (UGT37/302/308/430/431). Conversely, ABCs, delta-class GSTs and non-CYP6Zx P450s showed limited expansion. Differences were seen in the distributions of resistance-associated gene families across subfamilies between S. rueppellii and some hemipteran crop pests. Additionally, S. rueppellii had larger numbers of detoxification genes than other pollinator species. Conclusion and significance This assembly is the first published genome for a predatory member of the Syrphidae family and will serve as a useful resource for further research into selectivity and potential tolerance of insecticides by beneficial predators. Furthermore, the expansion of some gene families often linked to insecticide resistance and selectivity may be an indicator of the capacity of this predator to detoxify IPM selective insecticides. These findings could be exploited by targeted insecticide screens and functional studies to increase effectiveness of IPM strategies, which aim to increase crop yields by sustainably and effectively controlling pests without impacting beneficial predator populations.

Different Sensitivity of Flower-Visiting Diptera to a Neonicotinoid Insecticide: Expanding the Base for a Multiple-Species Risk Assessment Approach

“…In this regard, toxicogenomics has strong potential to elucidate the molecular mechanisms evolved by different phylogenetic groups to respond to different toxicants. Sphaerophoria rueppellii, the most sensitive non-bee species in our SSD analysis, has a greater number of genes in various detoxification families, such as GSTs and CYP450s, in comparison with bees [112]. Some studies indicate that this expansion of detoxification genes in hoverflies may have evolved as an adaptation to exposure to environments with highly heterogeneous chemical backgrounds [112][113][114][115].…”

UDP-Glycosyltransferases UGT350C3 and UGT344L7 Confer Tolerance to Neonicotinoids in Field Populations of Aphis gossypii

“…gossypii high resistance to neonicotinoids. , In addition to the mutation of target site, detoxification enzymes-mediated metabolic resistance play key roles in insecticide resistance . UGTs, as an important enzyme family in phase II of detoxification, contribute to insecticide resistance in insects by converting lipophilic xenobiotics to water-soluble glycosylated compounds. , Increased transcripts of UGT genes were detected in insecticide-resistant strains of insects, suggesting their potential roles in insecticide detoxification. − Our previous study demonstrated that the overexpression of UGT348A2 and UGT344B4 in a laboratory-selected strain of A. gossypii is implicated in thiamethoxam resistance .…”