Genome-wide analysis of ionotropic receptor gene repertoire in Lepidoptera with an emphasis on its functions of Helicoverpa armigera

Abstract

The functions of the Ionotropic Receptor (IR) family have been well studied in Drosophila melanogaster, but only limited information is available in Lepidoptera. Here, we conducted a large-scale genome-wide analysis of the IR gene repertoire in 13 moths and 16 butterflies. Combining a homology-based approach and manual efforts, totally 996 IR candidates are identified including 31 pseudogenes and 825 full-length sequences, representing the most current comprehensive annotation in lepidopteran species. The phylogeny, expression and sequence characteristics classify Lepidoptera IRs into three sub-families: antennal IRs (A-IRs), divergent IRs (D-IRs) and Lepidoptera-specific IRs (LS-IRs), which is distinct from the case of Drosophila IRs. In comparison to LS-IRs and D-IRs, A-IRs members share a higher degree of protein identity and are distinguished into 16 orthologous groups in the phylogeny, showing conservation of gene structure. Analysis of selective forces on 27 orthologous groups reveals that these lepidopteran IRs have evolved under strong purifying selection (dN/dS≪1). Most notably, lineage-specific gene duplications that contribute primarily to gene number variations across Lepidoptera not only exist in D-IRs, but are present in the two other sub-families including members of IR41a, 76b, 87a, 100a and 100b. Expression profiling analysis reveals that over 80% (21/26) of Helicoverpa armigera A-IRs are expressed more highly in antennae of adults or larvae than other tissues, consistent with its proposed function in olfaction. However, some are also detected in taste organs like proboscises and legs. These results suggest that some A-IRs in H. armigera likely bear a dual function with their involvement in olfaction and gustation. Results from mating experiments show that two HarmIRs (IR1.2 and IR75d) expression is significantly up-regulated in antennae of mated female moths. However, no expression difference is observed between unmated female and male adults, suggesting an association with female host-searching behaviors. Our current study has greatly extended the IR gene repertoire resource in Lepidoptera, and more importantly, identifies potential IR candidates for olfactory, gustatory and oviposition behaviors in the cotton bollworm.

Genomic content of chemosensory genes correlates with host range in wood-boring beetles (Dendroctonus ponderosae, Agrilus planipennis, and Anoplophora glabripennis)

“…planipennis. Duplications have occurred for DponIR41a and AplaIR76b, which is also the case in several species of Lepidoptera [51]. Furthermore, our analysis suggests orthologues of DmelIR60a in all beetle species.…”

Genomic content of chemosensory genes correlates with host range in wood-boring beetles (Dendroctonus ponderosae, Agrilus planipennis, and Anoplophora glabripennis)

“…All members of the conserved olfactory antennal IRs [25] and members of the divergent IR100a clade were present in both D. ponderosae and A. planipennis. Duplications have occurred for DponIR41a and AplaIR76b, which is also the case in several species of Lepidoptera [51]. Furthermore, our analysis suggests orthologues of DmelIR60a in all beetle species.…”

“…Surprisingly, the genome of D. ponderosae encoded more IR75 members (11) than other beetle species. IR75 paralogs have been implicated in olfaction and/or taste in moths based on expression patterns [51], and underlie responses to propionic acid in D.…”

“…48,49]. While chemosensory genes from the Diptera, Hymenoptera, and Lepidoptera have been more thoroughly compared in this regard [50][51][52], the largest order of insects, Coleoptera, remains poorly investigated. Apart from the ORs, which recently were analyzed across ten coleopteran genomes [53], full genomic repertoires of GRs, IRs and OBPs have only been identified in three species: the flour beetle Tribolium castaneum [54,55], the Asian longhorn beetle A. glabripennis [56], and the Colorado potato beetle Leptinotarsa decemlineata [49].…”

Coupling transcriptomics and behaviour to unveil the olfactory system ofSpodoptera exigualarvae

“…Of these, aIRs are highly conserved in sequence and in Lepidoptera they clustered in 16 orthologous groups that are largely characterized by a one-to-one orthologous relationship. Here, we describe the homologous sequence of the 17 aIRs present in S. frugiperda genome (Gouin et al, 2017;Liu et al, 2018). Hence, the missing S. exigua…”