Abstract

To better understand the olfactory mechanisms in a lepidopteran pest model species, the cotton leafworm Spodoptera littoralis, we have recently established a partial transcriptome from adult antennae. Here, we completed this transcriptome using next generation sequencing technologies, namely 454 and Illumina, on both adult antennae and larval tissues, including caterpillar antennae and maxillary palps. All sequences were assembled in 77,643 contigs. Their analysis greatly enriched the repertoire of chemosensory genes in this species, with a total of 57 candidate odorant-binding and chemosensory proteins, 47 olfactory receptors, 6 gustatory receptors and 17 ionotropic receptors. Using RT-PCR, we conducted the first exhaustive comparison of olfactory gene expression between larvae and adults in a lepidopteran species. All the 127 candidate olfactory genes were profiled for expression in male and female adult antennae and in caterpillar antennae and maxillary palps. We found that caterpillars expressed a smaller set of olfactory genes than adults, with a large overlap between these two developmental stages. Two binding proteins appeared to be larvae-specific and two others were adult-specific. Interestingly, comparison between caterpillar antennae and maxillary palps revealed numerous organ-specific transcripts, suggesting the complementary involvement of these two organs in larval chemosensory detection. Adult males and females shared the same set of olfactory transcripts, except two male-specific candidate pheromone receptors, two male-specific and two female-specific odorant-binding proteins. This study identified transcripts that may be important for sex-specific or developmental stage-specific chemosensory behaviors.

Highlights

  • In insects, both larvae and adults use their olfactory system to detect chemical cues in their environment, searching for food, for a mate or for adequate oviposition sites

  • Ligand spectra of large olfactory receptors (ORs) repertoires have been studied in detail only in D. melanogaster [18] and A. gambiae [19,20], but numerous lepidopteran ORs specialized in the detection of sex pheromones – the so-called pheromone receptors (PRs) – have been functionally characterized [21,22,23,24,25]

  • In each of the three GO categories, the more abundant terms were the same as those observed in the adult antennae transcriptome [43]

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Summary

Introduction

Both larvae and adults use their olfactory system to detect chemical cues in their environment, searching for food, for a mate or for adequate oviposition sites. It is expected that their molecular equipment required for odor detection should be different This has been verified in only a few model species, including the Diptera Drosophila melanogaster [1] and Anopheles gambiae [2] and the Lepidoptera Bombyx mori [3], species for which complete repertoires of olfactory genes have been described thanks to their sequenced genomes. Odorant molecules interact with receptors expressed in the ORN dentritic membrane Two families of such receptors have been described in insects, the olfactory receptors (ORs) and the ionotropic receptors (IRs) [9], that are involved in the recognition of different volatile families in D. melanogaster [10,11,12]. IRs have been first identified in D. melanogaster where they are notably involved in food odor detection [10], acid sensing [12] and in reproduction behaviour promotion [27]

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