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      Evolution, developmental expression and function of odorant receptors in insects

      1 , 2 , 3 , 4 , 5 , 6 , 7 , 4
      The Journal of Experimental Biology
      The Company of Biologists

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          Abstract

          Animals rely on their chemosensory system to discriminate among a very large number of attractive or repulsive chemical cues in the environment, which is essential to respond with proper action. The olfactory sensory systems in insects share significant similarities with those of vertebrates, although they also exhibit dramatic differences, such as the molecular nature of the odorant receptors (ORs): insect ORs function as heteromeric ion channels with a common Orco subunit, unlike the G-protein-coupled olfactory receptors found in vertebrates. Remarkable progress has recently been made in understanding the evolution, development and function of insect odorant receptor neurons (ORNs). These studies have uncovered the diversity of olfactory sensory systems among insect species, including in eusocial insects that rely extensively on olfactory sensing of pheromones for social communication. However, further studies, notably functional analyses, are needed to improve our understanding of the origins of the Orco–OR system, the mechanisms of ORN fate determination, and the extraordinary diversity of behavioral responses to chemical cues. Summary: A review of our understanding of the origins of the olfactory system in insects, the mechanisms of olfactory receptor fate determination, and the extraordinary diversity of behavioral responses to chemical cues.

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          The genome of the model beetle and pest Tribolium castaneum.

          Tribolium castaneum is a member of the most species-rich eukaryotic order, a powerful model organism for the study of generalized insect development, and an important pest of stored agricultural products. We describe its genome sequence here. This omnivorous beetle has evolved the ability to interact with a diverse chemical environment, as shown by large expansions in odorant and gustatory receptors, as well as P450 and other detoxification enzymes. Development in Tribolium is more representative of other insects than is Drosophila, a fact reflected in gene content and function. For example, Tribolium has retained more ancestral genes involved in cell-cell communication than Drosophila, some being expressed in the growth zone crucial for axial elongation in short-germ development. Systemic RNA interference in T. castaneum functions differently from that in Caenorhabditis elegans, but nevertheless offers similar power for the elucidation of gene function and identification of targets for selective insect control.
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            Combinatorial receptor codes for odors.

            The discriminatory capacity of the mammalian olfactory system is such that thousands of volatile chemicals are perceived as having distinct odors. Here we used a combination of calcium imaging and single-cell RT-PCR to identify odorant receptors (ORs) for odorants with related structures but varied odors. We found that one OR recognizes multiple odorants and that one odorant is recognized by multiple ORs, but that different odorants are recognized by different combinations of ORs. Thus, the olfactory system uses a combinatorial receptor coding scheme to encode odor identities. Our studies also indicate that slight alterations in an odorant, or a change in its concentration, can change its "code," potentially explaining how such changes can alter perceived odor quality.
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              Insect olfactory receptors are heteromeric ligand-gated ion channels.

              In insects, each olfactory sensory neuron expresses between one and three ligand-binding members of the olfactory receptor (OR) gene family, along with the highly conserved and broadly expressed Or83b co-receptor. The functional insect OR consists of a heteromeric complex of unknown stoichiometry but comprising at least one variable odorant-binding subunit and one constant Or83b family subunit. Insect ORs lack homology to G-protein-coupled chemosensory receptors in vertebrates and possess a distinct seven-transmembrane topology with the amino terminus located intracellularly. Here we provide evidence that heteromeric insect ORs comprise a new class of ligand-activated non-selective cation channels. Heterologous cells expressing silkmoth, fruitfly or mosquito heteromeric OR complexes showed extracellular Ca2+ influx and cation-non-selective ion conductance on stimulation with odorant. Odour-evoked OR currents are independent of known G-protein-coupled second messenger pathways. The fast response kinetics and OR-subunit-dependent K+ ion selectivity of the insect OR complex support the hypothesis that the complex between OR and Or83b itself confers channel activity. Direct evidence for odorant-gated channels was obtained by outside-out patch-clamp recording of Xenopus oocyte and HEK293T cell membranes expressing insect OR complexes. The ligand-gated ion channel formed by an insect OR complex seems to be the basis for a unique strategy that insects have acquired to respond to the olfactory environment.
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                Author and article information

                Journal
                The Journal of Experimental Biology
                J Exp Biol
                The Company of Biologists
                0022-0949
                1477-9145
                February 07 2020
                February 01 2020
                February 07 2020
                February 01 2020
                : 223
                : Suppl 1
                : jeb208215
                Affiliations
                [1 ]Department of Biology, University of Florida, Gainesville, FL 32611, USA
                [2 ]Center for Smell and Taste (UFCST), University of Florida, Gainesville, FL 32610, USA
                [3 ]Department of Molecular Biology, Umeå University, 901 87 Umeå, Sweden
                [4 ]Department of Biology, New York University, New York, NY 10003, USA
                [5 ]Department of Biology, Bucknell University, Lewisburg, PA 17837, USA
                [6 ]Guangdong Province Key Laboratory of Microbial Signals and Disease Control, Integrative Microbiology Research Centre, South China Agricultural University, 510642 Guangzhou, China
                [7 ]Howard Hughes Medical Institute (HHMI), Department of Biochemistry and Molecular Pharmacology, New York University School of Medicine, New York, NY 10016, USA
                Article
                10.1242/jeb.208215
                7790194
                32034042
                0cd39fde-1454-4bed-8592-81c43aeda461
                © 2020

                http://www.biologists.com/user-licence-1-1

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