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Antennal Transcriptome Analysis of the Chemosensory Gene Families From Trichoptera and Basal Lepidoptera.

ABSTRACT: The chemosensory gene families of insects encode proteins that are crucial for host location, mate finding, oviposition, and avoidance behaviors. The insect peripheral chemosensory system comprises odorant receptors (ORs), gustatory receptors (GRs), ionotropic receptors (IRs), odorant binding proteins (OBPs), chemosensory proteins (CSPs), and sensory neuron membrane proteins (SNMPs). These protein families have been identified from a large number of insect species, however, they still remain unidentified from several taxa that could provide important clues to their evolution. These taxa include older lepidopteran lineages and the sister order of Lepidoptera, Trichoptera (caddisflies). Studies of these insects should improve evolutionary analyses of insect chemoreception, and in particular shed light on the origin of certain lepidopteran protein subfamilies. These include the pheromone receptors (PRs) in the "PR clade", the pheromone binding proteins (PBPs), general odorant binding proteins (GOBPs), and certain presumably Lepidoptera-specific IR subfamilies. Hence, we analyzed antennal transcriptomes from Rhyacophila nubila (Trichoptera), Eriocrania semipurpurella, and Lampronia capitella (representing two old lepidopteran lineages). We report 37 ORs, 17 IRs, 9 GRs, 30 OBPs, 7 CSPs, and 2 SNMPs in R. nubila; 37 ORs, 17 IRs, 3 GRs, 23 OBPs, 14 CSPs, and 2 SNMPs in E. semipurpurella; and 53 ORs, 20 IRs, 5 GRs, 29 OBPs, 17 CSPs, and 3 SNMPs in L. capitella. We identified IR members of the "Lepidoptera-specific" subfamilies IR1 and IR87a also in R. nubila, demonstrating that these IRs also occur in Trichoptera. Members of the GOBP subfamily were only found in the two lepidopterans. ORs grouping within the PR clade, as well as PBPs, were only found in L. capitella, a species that in contrast to R. nubila and E. semipurpurella uses a so-called Type I pheromone similar to the pheromones of most species of the derived Lepidoptera (Ditrysia). Thus, in addition to providing increased coverage for evolutionary analyses of chemoreception in insects, our findings suggest that certain subfamilies of chemosensory genes have evolved in parallel with the transition of sex pheromone types in Lepidoptera. In addition, other chemoreceptor subfamilies show a broader taxonomic occurrence than hitherto acknowledged.

SUBMITTER: Yuvaraj JK

PROVIDER: S-EPMC6171000 | biostudies-literature | 2018

REPOSITORIES: biostudies-literature

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Antennal Transcriptome Analysis of the Chemosensory Gene Families From Trichoptera and Basal Lepidoptera.

Yuvaraj Jothi Kumar JK Andersson Martin N MN Zhang Dan-Dan DD Löfstedt Christer C

Frontiers in physiology 20180927

The chemosensory gene families of insects encode proteins that are crucial for host location, mate finding, oviposition, and avoidance behaviors. The insect peripheral chemosensory system comprises odorant receptors (ORs), gustatory receptors (GRs), ionotropic receptors (IRs), odorant binding proteins (OBPs), chemosensory proteins (CSPs), and sensory neuron membrane proteins (SNMPs). These protein families have been identified from a large number of insect species, however, they still remain uni ...[more]

PMID: 30319455

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Project description:BackgroundThe peach fruit moth, Carposina sasakii Matsumura (Lepidoptera: Carposinidae), poses a serious threat to a variety of fruits and causes significant economic loss owing to difficulties in its prevention and control. The olfactory sense is generally acknowledged to be a novel target for pest control. However, a systematic study of the olfactory genes expressed in C. sasakii has not been reported yet. Here, we reported the antennal transcriptome of C. sasakii using high-throughput sequencing and annotated the main chemosensory multi-gene families.ResultsIn the chemosensory gene families, 29 odorant-binding proteins, 13 chemosensory proteins, 1 sensory neuron membrane protein, 52 odorant receptors, 8 ionotropic receptors and 11 gustatory receptors were annotated in the C. sasakii antennal transcriptome. The number of olfactory genes obtained in our transcriptome was consistent with that identified in other lepidopteran insects, confirming that we basically accomplished the annotation of the chemosensory genes of C. sasakii in the adult antennal transcriptome. All sequences were annotated and analyzed by BLAST (basic local alignment search tool), and some chemosensory genes with specific functions were named according to the BLAST results and phylogenetic trees. Based on the expression profile in the transcriptome and phylogenetic analysis, differentially expressed genes (DEGs) were analyzed in both male and female adults. Finally, fluorescence quantitative real-time PCR was used to identify the male-specific or female-specific chemosensory genes that were putatively related to odor detection and recognition. Moreover, expression levels of OR33 and PBP2 were significantly higher in males than in females, indicating that these genes may interact with sex pheromones. We found some conserved antennal IRs and GRs involved in detecting sugar compounds (GR2, GR5, GR6, GR8) and carbon dioxide (GR1), which were also identified based on phylogenetic analysis.ConclusionsThere are 114 putative chemosensory proteins expressed in C. sasakii identified in this study. The identification of these proteins will make the molecular mechanism of odor recognition accessible.

Project description:BackgroundThe European spruce bark beetle, Ips typographus, and the North American mountain pine beetle, Dendroctonus ponderosae (Coleoptera: Curculionidae: Scolytinae), are severe pests of coniferous forests. Both bark beetle species utilize aggregation pheromones to coordinate mass-attacks on host trees, while odorants from host and non-host trees modulate the pheromone response. Thus, the bark beetle olfactory sense is of utmost importance for fitness. However, information on the genes underlying olfactory detection has been lacking in bark beetles and is limited in Coleoptera. We assembled antennal transcriptomes from next-generation sequencing of I. typographus and D. ponderosae to identify members of the major chemosensory multi-gene families.ResultsGene ontology (GO) annotation indicated that the relative abundance of transcripts associated with specific GO terms was highly similar in the two species. Transcripts with terms related to olfactory function were found in both species. Focusing on the chemosensory gene families, we identified 15 putative odorant binding proteins (OBP), 6 chemosensory proteins (CSP), 3 sensory neuron membrane proteins (SNMP), 43 odorant receptors (OR), 6 gustatory receptors (GR), and 7 ionotropic receptors (IR) in I. typographus; and 31 putative OBPs, 11 CSPs, 3 SNMPs, 49 ORs, 2 GRs, and 15 IRs in D. ponderosae. Predicted protein sequences were compared with counterparts in the flour beetle, Tribolium castaneum, the cerambycid beetle, Megacyllene caryae, and the fruit fly, Drosophila melanogaster. The most notable result was found among the ORs, for which large bark beetle-specific expansions were found. However, some clades contained receptors from all four beetle species, indicating a degree of conservation among some coleopteran OR lineages. Putative GRs for carbon dioxide and orthologues for the conserved antennal IRs were included in the identified receptor sets.ConclusionsThe protein families important for chemoreception have now been identified in three coleopteran species (four species for the ORs). Thus, this study allows for improved evolutionary analyses of coleopteran olfaction. Identification of these proteins in two of the most destructive forest pests, sharing many semiochemicals, is especially important as they might represent novel targets for population control.

Dataset Information

Antennal Transcriptome Analysis of the Chemosensory Gene Families From Trichoptera and Basal Lepidoptera.

Publications

Antennal Transcriptome Analysis of the Chemosensory Gene Families From Trichoptera and Basal Lepidoptera.

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