Abstract

In Lepidoptera, RNA sequencing has become a useful tool in identifying chemosensory genes from antennal transcriptomes, but little attention is paid to non-antennal tissues. Though the antennae are primarily responsible for olfaction, studies have found that a certain number of chemosensory genes are exclusively or highly expressed in the non-antennal tissues, such as proboscises, legs and abdomens. In this study, we report a global transcriptome of 16 tissues from Dioryctria abietella, including chemosensory and non-chemosensory tissues. Through Illumina sequencing, totally 952,658,466 clean reads were generated, summing to 142.90 gigabases of data. Based on the transcriptome, 235 chemosensory-related genes were identified, comprising 42 odorant binding proteins (OBPs), 23 chemosensory proteins (CSPs), 75 odorant receptors (ORs), 62 gustatory receptors (GRs), 30 ionotropic receptors (IRs), and 3 sensory neuron membrane proteins (SNMPs). Compared to a previous study in this species, 140 novel genes were found. A transcriptome-wide analysis combined with PCR results revealed that except for GRs, the majority of other five chemosensory gene families in Lepidoptera were expressed in the antennae, including 160 chemosensory genes in D. abietella. Using phylogenetic and expression profiling analyses, members of the six chemosensory gene repertoires were characterized, in which 11 DabiORs were candidates for detecting female sex pheromones in D. abietella, and DabiOR23 may be involved in the sensing of plant-derived phenylacetaldehyde. Intriguingly, more than half of the genes were detected in the proboscises, and one fourth of the genes were found to have the expression in the legs. Our study not only greatly extends and improves the description of chemosensory genes in D. abietella, but also identifies potential molecular targets involved in olfaction, gustation and non-chemosensory functions for control of this pest.

Highlights

  • Over the last decade, Illumina sequencing has been applied to a diverse range of insects regarding tissue transcriptomes (Kawahara et al, 2019; McKenna et al, 2019)

  • To compare the numbers of chemosensory genes expressed in antennae of adult Lepidoptera, we summarized the studies on chemosensory genes identified from antennal transcriptomes

  • Based on RNA sequencing (RNA–Seq) results, we found that almost all the A–ionotropic receptors (IRs) were expressed in the antennae at a considerable level (FPKM > 1), with the exception of DabiIR40a that appeared to be predominant in the antennae but remarkably low levels

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Summary

Introduction

Illumina sequencing has been applied to a diverse range of insects regarding tissue transcriptomes (Kawahara et al, 2019; McKenna et al, 2019). Chemosensory Genes in Dioryctria abietella study, have described chemosensory gene families involved in olfaction, gustation, development, insecticide resistance and even the sensation of humidity and temperature, i.e., odorant binding proteins (OBPs), chemosensory proteins (CSPs), odorant receptors (ORs), gustatory receptors (GRs), ionotropic receptors (IRs) and sensory neuron membrane proteins (SNMPs) (Agnihotri et al, 2016; Pelosi et al, 2018; Robertson, 2019; Xu, 2020; Montagné et al, 2021) Such great attention to chemosensory genes in moth antennae is attributable to their importance during the processes of smell and taste reception, as they mediate chemosensory-related behaviors of moths, such as the seeking of feeding or ovipositing host plants, the escape of dangerous signals and the recognition of conspecific partners Some members of OBPs or CSPs that are exclusively or highly expressed in gustatory or non-sensory organs have been found to be involved in additional physiological roles, such as taste, development, flight and insecticide resistance (Pelosi et al, 2018; Wang et al, 2020)

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