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

Abstract

Background Olfaction and gustation underlie behaviors that are crucial for insect fitness, such as host and mate selection. The detection of semiochemicals is mediated via proteins from large and rapidly evolving chemosensory gene families; however, the links between a species’ ecology and the diversification of these genes remain poorly understood. Hence, we annotated the chemosensory genes from genomes of wood-boring coleopterans, and compared the gene repertoires from stenophagous species with those from polyphagous species. Results We annotated 86 odorant receptors (ORs), 60 gustatory receptors (GRs), 57 ionotropic receptors (IRs), 4 sensory neuron membrane proteins (SNMPs), 36 odorant binding proteins (OBPs), and 11 chemosensory proteins (CSPs) in the mountain pine beetle (Dendroctonus ponderosae), and 47 ORs, 30 GRs, 31 IRs, 4 SNMPs, 12 OBPs, and 14 CSPs in the emerald ash borer (Agrilus planipennis). Four SNMPs and 17 CSPs were annotated in the polyphagous wood-borer Anoplophora glabripennis. The gene repertoires in the stenophagous D. ponderosae and A. planipennis are reduced compared with those in the polyphagous A. glabripennis and T. castaneum, which is largely manifested through small gene lineage expansions and entire lineage losses. Alternative splicing of GR genes was limited in D. ponderosae and apparently absent in A. planipennis, which also seems to have lost one carbon dioxide receptor (GR1). A. planipennis has two SNMPs, which are related to SNMP3 in T. castaneum. D. ponderosae has two alternatively spliced OBP genes, a novel OBP “tetramer”, and as many as eleven IR75 members. Simple orthology was generally rare in beetles; however, we found one clade with orthologues of putative bitter-taste GRs (named the "GR215 clade"), and conservation of IR60a from Drosophila melanogaster. Conclusions Our genome annotations represent important quantitative and qualitative improvements of the original datasets derived from transcriptomes of D. ponderosae and A. planipennis, facilitating evolutionary analysis of chemosensory genes in the Coleoptera where only a few genomes were previously annotated. Our analysis suggests a correlation between chemosensory gene content and host specificity in beetles. Future studies should include additional species to consolidate this correlation, and functionally characterize identified proteins as an important step towards improved control of these pests.

Putative ligand binding sites of two functionally characterized bark beetle odorant receptors

“…Additionally, I. typographus lacked ORs in groups 3, 4, 5B, and 6, which is also true for D. ponderosae. In contrast to previous studies 39,40 , our tree did not recapitulate the monophyly of OR group 2, with the two group 4 OR members from the cerambycid Anoplophora glabripennis being associated with the 2B group. This discrepancy is likely explained by the limited number of group 4 ORs in the analysis, in combination with the comparatively low node support for the 2A/2B distinction observed previously 39 .…”

“…Transcripts did not always encode full-length OR sequences. Hence, suffixes were added to gene names following established practice 40 , with NTE and CTE suffixes given to genes with the Nterminus or C-terminus missing, respectively. A FIX suffix was given to genes that were annotated on transcripts which were manually corrected using raw RNAseq reads or following the other current or previously published assemblies 38 .…”

“…The amino acid sequences of the ItypORs were aligned with the ORs from the genomes of D. ponderosae (Dpon) 40 and A. glabripennis (Agla) 58 using MAFFT 7.017 ref60 , implemented in Geneious software package 7.1.9. The three functionally characterized ORs from M. caryae (Mcar) (Cerambycidae) 37 were also included to indicate their positions in the phylogeny.…”

The draft genome of the specialist flea beetle Altica viridicyanea (Coleoptera: Chrysomelidae)

“…Yet there is a single outlier to this trend; Agrilus planipennis (132 genes and two pseudogenes), a species that is intermediate in host range, has fewer chemosensory genes than A. viridicyanea. These ndings are generally consistent with the hypothesis that chemosensory gene content and host speci city should correlate in phytophagous beetles [52], although there is clearly an exception to this rule.…”

“…Interestingly, we also found a large expansion in A. viridicyanea in Group 4 that contained 17 ORs. By comparison, no more than four Group 4 OR genes have been previously identi ed in any other surveyed beetle species [52,55].…”