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      Expressions of Olfactory Proteins in Locust Olfactory Organs and a Palp Odorant Receptor Involved in Plant Aldehydes Detection

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          Abstract

          The main chemosensory organs of locusts consisted of the antennae and the mouthparts (maxillary and labial palps), which are suggested to perform different functions. However, very few are known about the differences of these two organs at molecular level. To understand the differences of locust antennae and palps in olfaction, the electrophysiological response and olfactory gene expression of these two organs were conducted. Our electrophysiological experiments with Locusta migratoria showed that the responses of mouthpart palps and antennae to odorants are quite different. Only a few odorants, such as (E,E)-2,4-hexadienal and (E,E)-2,4-heptadienal, elicited stronger electrophysiological responses of both maxillary and labial palps in comparison to the antennae. Additionally, we obtained 114 and 11 putative odorant receptor (OR) gene segments from the antennal and palp transcriptomes, respectively. Two novel odorant-binding proteins (OBPs; OBP15 and OBP16) and one novel OR ( OR142) were identified for the first time. Out of the 16 OBP genes tested in RT-PCR and qPCR analyses, OBP8 was highly expressed in the nymphal palps. OBP4, OBP10, and OBP16 were only detected in the antennae. The other 11 OBP genes were jointly expressed in both antennae and palps. The relative expression level of OBP6 in male palps was much higher than that of female palps. Furthermore, for the 11 OR genes identified in palp transcriptome, the expression levels of OR12, OR13, OR14, and OR18 in the palps were significantly higher than those in the antennae. The OR12 in palps was demonstrated to be involved in detection of hexanal and E-2-hexenal, as well as (E,E)-2,4-heptadienal. Our results provide information on the different olfactory roles of locust antennae and palps at the molecular level.

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          Most cited references50

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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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              Odor coding in the Drosophila antenna.

              Odor coding in the Drosophila antenna is examined by a functional analysis of individual olfactory receptor neurons (ORNs) in vivo. Sixteen distinct classes of ORNs, each with a unique response spectrum to a panel of 47 diverse odors, are identified by extracellular recordings. ORNs exhibit multiple modes of response dynamics: an individual neuron can show either excitatory or inhibitory responses, and can exhibit different modes of termination kinetics, when stimulated with different odors. The 16 ORN classes are combined in stereotyped configurations within seven functional types of basiconic sensilla. One sensillum type contains four ORNs and the others contain two neurons, combined according to a strict pairing rule. We provide a functional map of ORNs, showing that each ORN class is restricted to a particular spatial domain on the antennal surface.
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                Author and article information

                Contributors
                Journal
                Front Physiol
                Front Physiol
                Front. Physiol.
                Frontiers in Physiology
                Frontiers Media S.A.
                1664-042X
                04 June 2018
                2018
                : 9
                : 663
                Affiliations
                Department of Entomology, China Agricultural University , Beijing, China
                Author notes

                Edited by: Shuang-Lin Dong, Nanjing Agricultural University, China

                Reviewed by: Chen-Zhu Wang, Institute of Zoology (CAS), China; Zhao-Qun Li, Tea Research Institute (CAAS), China; Sofía Lavista Llanos, Max-Planck-Institut für Chemische Ökologie, Germany

                *Correspondence: Long Zhang, locust@ 123456cau.edu.cn

                These authors have contributed equally to this work.

                This article was submitted to Invertebrate Physiology, a section of the journal Frontiers in Physiology

                Article
                10.3389/fphys.2018.00663
                5994405
                29915543
                189ed6cf-5461-4986-af31-6c93c7b7eaf8
                Copyright © 2018 Li, Wang, Zhang, Xu, Cao and Zhang.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 26 December 2017
                : 14 May 2018
                Page count
                Figures: 7, Tables: 1, Equations: 1, References: 59, Pages: 12, Words: 0
                Funding
                Funded by: Chinese Universities Scientific Fund 10.13039/501100005236
                Award ID: 2015NX001
                Funded by: National Natural Science Foundation of China 10.13039/501100001809
                Award ID: 31472037
                Categories
                Physiology
                Original Research

                Anatomy & Physiology
                olfactory organs,electrophysiological response,odorant binding protein,odorant receptors,locusta migratoria

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