Molecular characterization and differential expression of olfactory genes in the antennae of the black cutworm moth Agrotis ipsilon.

Ruo-Nan Yang,Liang Sun,Jing-Jiang Zhou,Xian-Chun Li,Shao-Hua Gu,Richard David Newcomb,Kong-Ming Wu,Yong-Jun Zhang,Yu-Yuan Guo

doi:10.1371/journal.pone.0103420

Abstract

Insects use their sensitive and selective olfactory system to detect outside chemical odorants, such as female sex pheromones and host plant volatiles. Several groups of olfactory proteins participate in the odorant detection process, including odorant binding proteins (OBPs), chemosensory proteins (CSPs), odorant receptors (ORs), ionotropic receptors (IRs) and sensory neuron membrane proteins (SNMPs). The identification and functional characterization of these olfactory proteins will enhance our knowledge of the molecular basis of insect chemoreception. In this study, we report the identification and differential expression profiles of these olfactory genes in the black cutworm moth Agrotis ipsilon. In total, 33 OBPs, 12 CSPs, 42 ORs, 24 IRs, 2 SNMPs and 1 gustatory receptor (GR) were annotated from the A. ipsilon antennal transcriptomes, and further RT-PCR and RT-qPCR revealed that 22 OBPs, 3 CSPs, 35 ORs, 14 IRs and the 2 SNMPs are uniquely or primarily expressed in the male and female antennae. Furthermore, one OBP (AipsOBP6) and one CSP (AipsCSP2) were exclusively expressed in the female sex pheromone gland. These antennae-enriched OBPs, CSPs, ORs, IRs and SNMPs were suggested to be responsible for pheromone and general odorant detection and thus could be meaningful target genes for us to study their biological functions in vivo and in vitro.

Highlights

Insects use their sensitive and selective antennae, which express various olfactory proteins, to detect air borne odorant molecules, such as sex pheromones and plant volatiles
It is commonly accepted that several different groups of antennae-enriched olfactory proteins participate in the first stage of the detection of olfactory signals, including odorant binding proteins (OBPs), chemosensory proteins (CSPs), odorant receptors (ORs), ionotropic receptors (IRs) and sensory neuron membrane proteins (SNMPs) [3]
In the present study, using a next-generation sequencing (NGS) 454 GS FLX platform, we have identified and annotate several families of chemosensory genes from the antennae of the black cutworm moth Agrotis ipsilon (Hufnagel) (Lepidoptera: Noctuidae), which is known as a destructive pest of many crops [52,53]

Summary

Introduction

Insects use their sensitive and selective antennae, which express various olfactory proteins, to detect air borne odorant molecules, such as sex pheromones and plant volatiles. Species-specific pheromone molecules and general plant volatiles enter the sensillum lymph of the different types of antennae sensilla via the multipores of the insect cuticle [1,2]. It is commonly accepted that several different groups of antennae-enriched olfactory proteins participate in the first stage of the detection of olfactory signals, including odorant binding proteins (OBPs), chemosensory proteins (CSPs), odorant receptors (ORs), ionotropic receptors (IRs) and sensory neuron membrane proteins (SNMPs) [3]. Insect OBPs are small water-soluble olfactory proteins that are presumed to be synthesized by non-neuronal auxiliary cells (trichogen and tormogen cells) of the sensory neurons and secreted into the sensillum lymph in high concentrations (up to 10 mM) [4,5,6,7]. In the fire ant Solenopsis invicta, the pheromone binding protein gene Gp-9 regulates the colony social organization between the monogyne social form (with a single queen) and the polygyne form (with multiple queens) [10]

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Conclusion