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      Characterization of antennal chemosensilla and associated odorant binding as well as chemosensory proteins in the parasitoid wasp Microplitis mediator (Hymenoptera: Braconidae)

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          Abstract

          Odorant binding proteins (OBPs) and chemosensory proteins (CSPs) expressed in antennal chemosensilla are believed to be important in insect chemoreception. In the current study, we fully described the morphological characteristics of the antennal sensilla in parasitoid wasp Microplitis mediator and analyzed the expression patterns of OBPs and CSPs within the antennae. In M. mediator, eight types of sensilla were observed on the antennae. Sensilla basiconica type 2 and s. placodea with wall pores may be involved in olfactory perception, whereas s. basiconica type 1 and type 3 with tip pores may play gustatory functions. Among the 18 OBPs and 3 CSPs in M. mediator, 10 OBPs and 2 CSPs were exclusively or primarily expressed in the antennae. In situ hybridization experiments indicated that the 12 antennae-enriched OBPs and CSPs were mapped to five morphological classes of antennal sensilla, including s. basiconica (type 1–3), s. placodea and s. coeloconica. Within the antennae, most of OBP and CSP genes were expressed only in one type of sensilla indicating their differentiated roles in detection of special type of chemical molecules. Our data will lay a foundation to further study the physiological roles of OBPs and CSPs in antennae of parasitoid wasps.

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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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            Beyond chemoreception: diverse tasks of soluble olfactory proteins in insects.

            Odorant-binding proteins (OBPs) and chemosensory proteins (CSPs) are regarded as carriers of pheromones and odorants in insect chemoreception. These proteins are typically located in antennae, mouth organs and other chemosensory structures; however, members of both classes of proteins have been detected recently in other parts of the body and various functions have been proposed. The best studied of these non-sensory tasks is performed in pheromone glands, where OBPs and CSPs solubilise hydrophobic semiochemicals and assist their controlled release into the environment. In some cases the same proteins are expressed in antennae and pheromone glands, thus performing a dual role in receiving and broadcasting the same chemical message. Several reports have described OBPs and CSPs in reproductive organs. Some of these proteins are male specific and are transferred to females during mating. They likely carry semiochemicals with different proposed roles, from inhibiting other males from approaching mated females, to marking fertilized eggs, but further experimental evidence is still needed. Before being discovered in insects, the presence of binding proteins in pheromone glands and reproductive organs was widely reported in mammals, where vertebrate OBPs, structurally different from OBPs of insects and belonging to the lipocalin superfamily, are abundant in rodent urine, pig saliva and vaginal discharge of the hamster, as well as in the seminal fluid of rabbits. In at least four cases CSPs have been reported to promote development and regeneration: in embryo maturation in the honeybee, limb regeneration in the cockroach, ecdysis in larvae of fire ants and in promoting phase shift in locusts. Both OBPs and CSPs are also important in nutrition as solubilisers of lipids and other essential components of the diet. Particularly interesting is the affinity for carotenoids of CSPs abundantly secreted in the proboscis of moths and butterflies and the occurrence of the same (or very similar CSPs) in the eyes of the same insects. A role as a carrier of visual pigments for these proteins in insects parallels that of retinol-binding protein in vertebrates, a lipocalin structurally related to OBPs of vertebrates. Other functions of OBPs and CSPs include anti-inflammatory action in haematophagous insects, resistance to insecticides and eggshell formation. Such multiplicity of roles and the high success of both classes of proteins in being adapted to different situations is likely related to their stable scaffolding determining excellent stability to temperature, proteolysis and denaturing agents. The wide versatility of both OBPs and CSPs in nature has suggested several different uses for these proteins in biotechnological applications, from biosensors for odours to scavengers for pollutants and controlled releasers of chemicals in the environment.
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              Soluble proteins of chemical communication: an overview across arthropods

              Detection of chemical signals both in insects and in vertebrates is mediated by soluble proteins, highly concentrated in olfactory organs, which bind semiochemicals and activate, with still largely unknown mechanisms, specific chemoreceptors. The same proteins are often found in structures where pheromones are synthesized and released, where they likely perform a second role in solubilizing and delivering chemical messengers in the environment. A single class of soluble polypeptides, called Odorant-Binding Proteins (OBPs) is known in vertebrates, while two have been identified in insects, OBPs and CSPs (Chemosensory Proteins). Despite their common name, OBPs of vertebrates bear no structural similarity with those of insects. We observed that in arthropods OBPs are strictly limited to insects, while a few members of the CSP family have been found in crustacean and other arthropods, where however, based on their very limited numbers, a function in chemical communication seems unlikely. The question we address in this review is whether another class of soluble proteins may have been adopted by other arthropods to perform the role of OBPs and CSPs in insects. We propose that lipid-transporter proteins of the Niemann-Pick type C2 family could represent likely candidates and report the results of an analysis of their sequences in representative species of different arthropods.
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                Author and article information

                Contributors
                yjzhang@ippcaas.cn
                Journal
                Sci Rep
                Sci Rep
                Scientific Reports
                Nature Publishing Group UK (London )
                2045-2322
                16 May 2018
                16 May 2018
                2018
                : 8
                : 7649
                Affiliations
                [1 ]ISNI 0000 0004 0646 9053, GRID grid.418260.9, Institute of Plant and Environment Protection, , Beijing Academy of Agriculture and Forestry Sciences, ; Beijing, 100097 China
                [2 ]GRID grid.464356.6, State Key Laboratory for Biology of Plant Diseases and Insect Pests, , Institute of Plant Protection, Chinese Academy of Agricultural Sciences, ; Beijing, 100193 China
                [3 ]ISNI 0000 0004 0530 8290, GRID grid.22935.3f, College of Plant Protection, , China Agricultural University, ; Beijing, 100193 China
                [4 ]ISNI 0000 0001 2291 4530, GRID grid.274504.0, College of Plant Protection, , Agricultural University of Hebei, ; Baoding, 071000 China
                [5 ]ISNI 0000 0004 0369 6250, GRID grid.418524.e, IPM Center of Hebei Province, , Key Laboratory of Integrated Pest Management on Crops in Northern Region of North China, Ministry of Agriculture, Plant Protection Institute, Hebei Academy of Agricultural and Forestry Sciences, Baoding, ; Hebei, 071000 China
                [6 ]Department of Entomology, Faculty of Crop Protection, Sindh Agriculture University Tandojam, Hyderabad, 70060 Pakistan
                Article
                25996
                10.1038/s41598-018-25996-3
                5955942
                29769575
                08200e44-1058-48c9-a8bb-c3dbe869774e
                © The Author(s) 2018

                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
                : 22 January 2018
                : 3 May 2018
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