Identification and functional analysis of olfactory receptor family reveal unusual characteristics of the olfactory system in the migratory locust

Abstract

Locusts represent the excellent model of insect olfaction because the animals are equipped with an unusual olfactory system and display remarkable density-dependent olfactory plasticity. However, information regarding receptor molecules involved in the olfactory perception of locusts is very limited. On the basis of genome sequence and antennal transcriptome of the migratory locust, we conduct the identification and functional analysis of two olfactory receptor families: odorant receptors (ORs) and ionotropic receptors (IRs). In the migratory locust, there is an expansion of OR family (142 ORs) while distinctly lower number of IR genes (32 IRs) compared to the repertoires of other insects. The number of the locust OR genes is much less than that of glomeruli in antennal lobe, challenging the general principle of the “one glomerulus-one receptor” observed in other insects. Most OR genes are found in tandem arrays, forming two large lineage-specific subfamilies in the phylogenetic tree. The “divergent IR” subfamily displays a significant contraction, and most of the IRs belong to the “antennal IR” subfamily in the locust. Most ORs/IRs have olfactory-specific expression while some broadly- or internal-expressed members are also found. Differing from holometabolous insects, the migratory locust contains very similar expression profiles of ORs/IRs between nymph and adult stages. RNA interference and behavioral assays indicate that an OR-based signaling pathway, not IR-based, mediates the attraction of locusts to aggregation pheromones. These discoveries provide insights into the unusual olfactory system of locusts and enhance our understanding of the evolution of insect olfaction.Electronic supplementary materialThe online version of this article (doi:10.1007/s00018-015-2009-9) contains supplementary material, which is available to authorized users.

Identification and tissue expression profile of genes from three chemoreceptor families in an urban pest, Periplaneta americana

“…Moreover, 4 PameORs ( 17, 74, 75 , and 81 ) and 4 PameIRs ( 21, 31, 35 and 42 , and six iGluRs ( iGluR1–6 ) exhibited non-chemosensory organ-biased expression. All of them expressed in the legs to a certain extent, which was consistent with some previous studies364748. However, we could not ignore their olfactory function; as reported earlier, IR expression in the legs affected the mating behaviour of fly47.…”

“…The number of ORs was much higher than in the two other Blattaria species, Z. nevadensis (60 ORs, genome data)31 and B. germanica (5 ORs, antennal transcriptome data)30. It was also higher than the 62 ORs found in D. melanogaster 15 and the 79 ORs in A. gambiae 635, but was much lower than the number of ORs reported in T. castaneum (259 ORs)8, A. mellifera (170 ORs)7, and L. moratoria (142 ORs)36. The number of IRs was lower than the numbers found in Z. nevadensis (136 IRs)31 and higher than those found in B. germanica (5 IRs, antennal transcriptome data)30, but it was much higher than the 14 IRs found in A. gossypii 24 and Sogatella furcifera 23, 57 in D. melanogaster 202237, and 22 in A. gambiae 38.…”

Identification and expression analysis of an olfactory receptor gene family in green plant bug Apolygus lucorum (Meyer-Dür)

“…The expression of broadly expressed OR genes in non-olfactory tissues suggested that they might have diverse physiological functions in other organs. The co-expression of LmigOR95 and LmigOrco were also observed in the fat body of migratory locust37. In locusts and mosquitoes, the testis-enhanced OR genes supposed to participate in the sperm chemotaxis, fertilization, or the activation of spermatozoa3745.…”

“…Nevertheless, because the ORF of some ORs is incomplete, we cannot exclude the possibility that some of these ORs might be pseudogenes. The sequence number is much lower compared with species including Apis mellifera (163 ORs)35, Tribolium castaneum (341ORs)36, and Locusta migratoria (142 ORs)37. This may be caused by adaptation of distinct species to their hosts during evolution38.…”

“…Results showed that AlucOR genes exhibited diverse expression patterns, which could be briefly classified into five types: antennal highly expressed ORs, head highly expressed ORs, abdomen highly expressed ORs, wing highly expressed ORs, and broadly expressed ORs (Supplementary Table 2). It was also reported that some ORs could be expressed in a variety of tissues apart from the olfactory organs3739. Antennae are important sensory organs for insect, so the majority of AlucOR genes displayed high expressions in antennae, including female and male antennal highly expressed genes.…”