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      Antennal transcriptome analyses and olfactory protein identification in an important wood-boring moth pest, Streltzoviella insularis (Lepidoptera: Cossidae)

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          Abstract

          Olfaction plays key roles in insect survival and reproduction, such as feeding, courtship, mating, and oviposition. The olfactory-based control strategies have been developed an important means for pest management. Streltzoviella insularis is a destructive insect pest of many street tree species, and characterization of its olfactory proteins could provide targets for the disruption of their odour recognition processes and for urban forestry protection. In this study, we assembled the antennal transcriptome of S. insularis by next-generation sequencing and annotated the main olfactory multi-gene families, including 28 odorant-binding proteins (OBPs), 12 chemosensory proteins (CSPs), 56 odorant receptors (ORs), 11 ionotropic receptors (IRs), two sensory neuron membrane proteins (SNMPs), and 101 odorant-degrading enzymes (ODEs). Sequence and phylogenetic analyses confirmed the characteristics of these proteins. We further detected tissue- and sex-specific expression patterns of OBPs, CSPs and SNMPs by quantitative real time-PCR. Most OBPs were highly and differentially expressed in the antennae of both sexes. SinsCSP10 was expressed more highly in male antennae than in other tissues. Two SNMPs were highly expressed in the antennae, with no significant difference in expression between the sexes. Our results lay a solid foundation for understanding the precise molecular mechanisms underlying S. insularis odour recognition.

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          Most cited references60

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          A spatial map of olfactory receptor expression in the Drosophila antenna.

          Insects provide an attractive system for the study of olfactory sensory perception. We have identified a novel family of seven transmembrane domain proteins, encoded by 100 to 200 genes, that is likely to represent the family of Drosophila odorant receptors. Members of this gene family are expressed in topographically defined subpopulations of olfactory sensory neurons in either the antenna or the maxillary palp. Sensory neurons express different complements of receptor genes, such that individual neurons are functionally distinct. The isolation of candidate odorant receptor genes along with a genetic analysis of olfactory-driven behavior in insects may ultimately afford a system to understand the mechanistic link between odor recognition and behavior.
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            A novel family of divergent seven-transmembrane proteins: candidate odorant receptors in Drosophila.

            Although insects have proven to be valuable models for exploring the function, organization, and development of the olfactory system, the receptor molecules that bind odors have not been identified in any insect. We have developed a novel search algorithm, used it to search the Drosophila genomic sequence database, and identified a large multigene family encoding seven transmembrane domain proteins that are expressed in olfactory organs. We show that expression is restricted to subsets of olfactory receptor neurons (ORNs) for a number of these genes. Different members of the family initiate expression at different times during antennal development. Some of the genes are not expressed in a mutant of the Acj6 POU-domain transcription factor, a mutant in which a subset of ORNs show abnormal odorant specificities.
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              Molecular evolution of the major chemosensory gene families in insects.

              Chemoreception is a crucial biological process that is essential for the survival of animals. In insects, olfaction allows the organism to recognise volatile cues that allow the detection of food, predators and mates, whereas the sense of taste commonly allows the discrimination of soluble stimulants that elicit feeding behaviours and can also initiate innate sexual and reproductive responses. The most important proteins involved in the recognition of chemical cues comprise moderately sized multigene families. These families include odorant-binding proteins (OBPs) and chemosensory proteins (CSPs), which are involved in peripheral olfactory processing, and the chemoreceptor superfamily formed by the olfactory receptor (OR) and gustatory receptor (GR) families. Here, we review some recent evolutionary genomic studies of chemosensory gene families using the data from fully sequenced insect genomes, especially from the 12 newly available Drosophila genomes. Overall, the results clearly support the birth-and-death model as the major mechanism of evolution in these gene families. Namely, new members arise by tandem gene duplication, progressively diverge in sequence and function, and can eventually be lost from the genome by a deletion or pseudogenisation event. Adaptive changes fostered by environmental shifts are also observed in the evolution of chemosensory families in insects and likely involve reproductive, ecological or behavioural traits. Consequently, the current size of these gene families is mainly a result of random gene gain and loss events. This dynamic process may represent a major source of genetic variation, providing opportunities for FUTURE specific adaptations.
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                Author and article information

                Contributors
                taojing1029@hotmail.com
                zongsx@126.com
                Journal
                Sci Rep
                Sci Rep
                Scientific Reports
                Nature Publishing Group UK (London )
                2045-2322
                29 November 2019
                29 November 2019
                2019
                : 9
                : 17951
                Affiliations
                ISNI 0000 0001 1456 856X, GRID grid.66741.32, Beijing Key Laboratory for Forest Pest Control, , Beijing Forestry University, ; Beijing, 100083 China
                Author information
                http://orcid.org/0000-0002-4137-4514
                Article
                54455
                10.1038/s41598-019-54455-w
                6884542
                31784624
                493c922a-84d1-42eb-bdd2-1a92ae67be88
                © The Author(s) 2019

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 12 June 2019
                : 14 November 2019
                Funding
                Funded by: This research was funded by Beijing’s Science and Technology Planning Project (Z171100001417005).
                Categories
                Article
                Custom metadata
                © The Author(s) 2019

                Uncategorized
                chemical ecology,next-generation sequencing,transcriptomics
                Uncategorized
                chemical ecology, next-generation sequencing, transcriptomics

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