Antennal RNA-sequencing analysis reveals evolutionary aspects of chemosensory proteins in the carpenter ant, Camponotus japonicus.

Masaru K Hojo,Midori Sakura,Katsushi Yamaguchi,Kenichi Ishii,Shuji Shigenobu,Mamiko Ozaki

doi:10.1038/srep13541

Abstract

Chemical communication is essential for the coordination of complex organisation in ant societies. Recent comparative genomic approaches have revealed that chemosensory genes are diversified in ant lineages, and suggest that this diversification is crucial for social organisation. However, how such diversified genes shape the peripheral chemosensory systems remains unknown. In this study, we annotated and analysed the gene expression profiles of chemosensory proteins (CSPs), which transport lipophilic compounds toward chemosensory receptors in the carpenter ant, Camponotus japonicus. Transcriptome analysis revealed 12 CSP genes and phylogenetic analysis showed that 3 of these are lineage-specifically expanded in the clade of ants. RNA sequencing and real-time quantitative polymerase chain reaction revealed that, among the ant specific CSP genes, two of them (CjapCSP12 and CjapCSP13) were specifically expressed in the chemosensory organs and differentially expressed amongst ant castes. Furthermore, CjapCSP12 and CjapCSP13 had a ratio of divergence at non-synonymous and synonymous sites (dN/dS) greater than 1, and they were co-expressed with CjapCSP1, which is known to bind cuticular hydrocarbons. Our results suggested that CjapCSP12 and CjapCSP13 were functionally differentiated for ant-specific chemosensory events, and that CjapCSP1, CjapCSP12, and CjapCSP13 work cooperatively in the antennal chemosensilla of worker ants.

Highlights

(ORs, gustatory receptors (GRs), and IRs) are present in the ant genomes[9], compared to 183 in the European honeybee, Apis mellifera[10], genome
We demonstrated that some chemosensory proteins (CSPs) genes (CjapCSP1, 3, 7, 12, and 13) were highly expressed in the chemosensory organs of workers (Fig. 3), and they showed differential expression among the antennae of the three castes, except for CjapCSP7 (Fig. 2)
These results suggested that CjapCSP1, 3, 4, 7, 12 and 13 were mainly involved in peripheral chemosensory events

Summary

Introduction

(ORs, GRs, and IRs) are present in the ant genomes[9], compared to 183 in the European honeybee, Apis mellifera[10], genome These results suggest that the diversification of chemosensory genes is crucial for the complex social organisation and ecological dominance of ants[6,9]. The odorants carried by OBPs and CSPs are decoded when olfactory receptors (ORs) and possibly, gustatory receptors (GRs) selectively bind adequate stimulus chemicals Binding proteins such as OBPs and CSPs are small, globular, water-soluble proteins with an inner hydrophobic pocket for lipophilic ligand binding, characterized by a specific domain of six α -helices. In the light of our findings, we discuss how ant-specific CSPs shape the peripheral chemosensory systems in ants

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Results

Conclusion