Identification and evolution of olfactory genes in the small poplar longhorn beetle Saperda populnea

Abstract

Saperda populnea is a serious pest of poplar and willow trees in the Palaearctic region, causing extensive damage to forests and the lumber industry. Until recently, there is no safe and effective chemical method to control this pest due to the lack of sufficient knowledge on the molecular basis of its olfactory genes, moreover, the evolutionary history of the olfactory gene family in subfamily Lamiinae is still fully unknown. Our RNA sequencing of the antennae of S. populnea identified 43 odorant binding proteins (OBPs), 15 chemosensory proteins (CSPs), 56 odorant receptors (ORs) and 24 inotropic receptors (IRs) in S. populnea. The RT-PCR results showed several genes were expressed in a sex specific manner, suggesting that these genes might play key role in their olfactory-sensing and sex-related behaviors. Further evolutionary studies were performed on these olfactory genes, overall comparison of the Ka/Ks values of orthologous genes in S. populnea and two other Lamiinae species showed three main conclusions: 1. olfactory genes have evolved more rapidly than the non-olfactory genes in the tested long horn beetles; 2. the IR gene family are under a strong purifying selection; 3. the OBPs of Monochamus alternatus evolved more rapidly than the other two species, which is speculated to be correlated with differentiation of selective pressure in different geographic origins. Detailed evolutionary studies on each olfactory genes showed that several OBPs and ORs are under significantly purifying/relaxed selective pressure, and several positive selection sites were also detected, modeling of SpopOR14 and SpopOBP4/5 showed that most of the positive selection sites were distributed at the N-terminus of SpopOR14, while the positive selection sites in SpopOBP4/5 were located in H-bond donors, results suggest that these sites are more likely to be linked with the selectivity of modeled olfactory genes. The research provided a better understanding of the molecular basis and evolutionary history of the olfactory genes in Lamiinae, through elaborating the mechanism whereby amino structural evolution affects specific variants in OBPs and ORs.