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The 40-Year Mystery of Insect Odorant-Binding Proteins

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biomolecules Review The 40-Year Mystery of Insect Odorant-Binding Proteins Karen Rihani *,† , Jean-François Ferveur and Loïc Briand * Dijon, CNRS, INRAE, Université de Bourgogne Franche-Comté, Centre des Sciences du Goût et de l’Alimentation, 21000 Dijon, France; [email protected] * Correspondence: [email protected] (K.R.); [email protected] (L.B.) † Current address: Department of Evolutionary Neuroethology, Max Planck Institute for Chemical Ecology, Hans-Knoell-Str. 8, 07745 Jena, Germany. Abstract: The survival of insects depends on their ability to detect molecules present in their environ- ment. Odorant-binding proteins (OBPs) form a family of proteins involved in chemoreception. While OBPs were initially found in olfactory appendages, recently these proteins were discovered in other chemosensory and non-chemosensory organs. OBPs can bind, solubilize and transport hydrophobic stimuli to chemoreceptors across the aqueous sensilla lymph. In addition to this broadly accepted “transporter role”, OBPs can also buffer sudden changes in odorant levels and are involved in hygro- reception. The physiological roles of OBPs expressed in other body tissues, such as mouthparts, pheromone glands, reproductive organs, digestive tract and venom glands, remain to be investigated. This review provides an updated panorama on the varied structural aspects, binding properties, tissue expression and functional roles of insect OBPs. Keywords: insect; olfaction; taste; chemosensory functions; non-chemosensory functions; odorant- protein-binding assay; Drosophila melanogaster Citation: Rihani, K.; Ferveur, J.-F.; Briand, L. The 40-Year Mystery of 1. Introduction Insect Odorant-Binding Proteins. Chemoperception allows organisms to detect nutritive food and avoid toxic com- Biomolecules 2021, 11, 509. pounds. Moreover, chemoperception is necessary for animals to identify suitable ecological https://doi.org/10.3390/biom niches and mating partners. Chemoreception is mediated by chemosensory receptors that 11040509 interact with a variety of semio-chemicals, (odorants, pheromones and sapid molecules), allowing their detection and eliciting an adapted behaviour. In insects, the dendrites Academic Editor: Dov Borovsky of the sensory neurons found in olfactory and gustatory sensilla are bathed in an aque- ous phase called the sensillar lymph. Therefore, volatile and non-volatile chemical com- Received: 28 February 2021 pounds contacting sensory organs should be solubilized and transported across the internal Accepted: 19 March 2021 Published: 30 March 2021 aqueous phase before reaching the sensory receptors. These carrier mechanisms, called “peri-receptor events” [1], involve several families of proteins, including odorant-binding Publisher’s Note: MDPI stays neutral proteins (OBPs). OBPs are small soluble proteins found in high concentration in both the with regard to jurisdictional claims in nasal mucus of vertebrates and the chemo-sensilla lymph of insects [2–7]. OBPs were published maps and institutional affil- initially discovered during the early 1980s in parallel by two research groups working on iations. the cow [8–10] and on the giant moth Antheraea Polyphemus [11]. A large number of DNA sequences encoding OBPs were later identified in several vertebrate species, including rat [12], pig [13,14], xenopus [15], and human [16,17]. OBPs were also detected in more than one hundred insect species, such as the silk moth Bombyx mori [18,19], the gypsy moth Lymntria dispar [20], the turnip moth Agrotis segetum [21,22], the stemborer Sesamia nona- Copyright: © 2021 by the authors. grioides Helicoverpa armigera Licensee MDPI, Basel, Switzerland. [23], the cotton bollworm and the oriental tobacco budworm This article is an open access article Helicoverpa assulta [24]. distributed under the terms and OBPs have been widely studied for more than 30 years. Here, we present the latest conditions of the Creative Commons discoveries made on the structural and binding properties of insect OBPs. We focus on the Attribution (CC BY) license (https:// properties of insect OBPs and, more specifically, on their tissue and cellular expression. We creativecommons.org/licenses/by/ also present the varied functional roles, both classical and non-conventional, of currently 4.0/). known OBPs. Biomolecules 2021, 11, 509. https://doi.org/10.3390/biom11040509 https://www.mdpi.com/journal/biomolecules Biomolecules 2021, 11, x 2 of 30 Biomolecules 2021, 11, x 2 of 30 Biomolecules 2021, 11, x 2 of 30 expression. We also present the varied functional roles, both classical and non- Biomolecules 2021, 11, x expression. We also present the varied functional roles, both classical and 2 non-of 30 conventional,expression. We of currentlyalso present known the OBPs. varied functional roles, both classical and non- conventional, of currently known OBPs. Biomolecules 2021, 11, x conventional, of currently known OBPs. 2 of 30 2. Expression Pattern of Insect OBPs 2. Expression Pattern of Insect OBPs expression.2.1.2. Expression Number Weof Pattern OBP-Coding also ofpresent Insect Genes OBPsthe invaried Insects fu nctional roles, both classical and non- conventional,2.1. Number of of OBP-Coding currently known Genes OBPs. in Insects expression.2.1. NumberThe number ofWe OBP-Coding alsoof OBP-coding present Genes the genes invaried Insects is highly fu nctional variable roles, between both insect classical species, and ranging non- Biomolecules 2021, 11, 509 The number of OBP-coding genes is highly variable between insect species, ranging2 of 27 conventional,betweenThe 13number in ofsome currently of antOBP-coding species known [25] genes OBPs. to >100 is highly in several variable mosquitoes between [26]insect (Table species, 1). ranging 2.between Expression 13 in Pattern some ant of speciesInsect OBPs [25] to >100 in several mosquitoes [26] (Table 1). between 13 in some ant species [25] to >100 in several mosquitoes [26] (Table 1). 2.1.2.Table Expression Number 1. Numbers of Pattern OBP-Coding of annotated of Insect Genesodorant-binding OBPs in Insects protei ns (OBP) genes in different insects [27–29]. Table 1. Numbers of annotated odorant-binding proteins (OBP) genes in different insects [27–29]. Table2. ExpressionThe 1. Numbers number Pattern ofof annotated OBP-coding of Insect odorant-binding OBPs genes is highly protei variablens (OBP) between genes in differentinsect species, insects [27ranging–29]. 2.1. Number of OBP-Coding Genes in InsectsSpecies OBP Gene Number between2.1. Number 13 in of some OBP-Coding ant species Genes [25] in Insectsto >100 Speciesin several mosquitoes [26]OBP (Table Gene 1) Number. The number of OBP-coding genesD. is melanogasterhighlySpecies variable between OBPinsect Gene species,52 Number ranging The number of OBP-coding genesD. is melanogaster highly variable between insect species,52 ranging between 13 in some ant species [25] to >100D.D. melanogaster insimulans several mosquitoes [26] (Table52 1) . Tablebetween 1. Numbers 13 in some of annotated ant species odorant-binding [25] to >100D. simulansprotei in severalns (OBP) mosquitoes genes in different [26] (Table insects521 ). [27–29]. D. simulanssechellia 5152 Table 1. Numbers of annotated odorant-bindingD. proteisechellians (OBP) genes in different insects51 [27–29]. D.D.Species sechellia yakuba OBP Gene5551 Number Table 1. Numbers of annotated odorant-bindingD. proteinsyakuba (OBP) genes in different insects55 [27–29]. D. melanogasterD.D.Species yakuba erecta OBP Gene525055 Number D. erecta 50 D.D.D. SpeciesmelanogasterD. ananassaesimulans erecta OBP Gene5250 Number D. ananassae 50 D.D. melanogasterD.pseudoobscura ananassaesimulanssechellia 5251524550 D. pseudoobscuraD. yakuba 5545 D.D. D.pseudoobscuraD. simulans persimilissechellia 525145 D.D. sechellia persimilis 5145 D.D.D. willistonipersimilis yakuba erecta 50556245 D. yakubawillistoni 5562 D.D. D.mojavensis ananassaewillistoni erecta 504362 D.D. mojavensis erecta 5043 D.D.D.D. pseudoobscura ananassaeD. mojavensisananassae virilis 5045504143 D. virilis 41 D.D. pseudoobscuraD.D.pseudoobscuraD. persimilisgrimshaw virilis 45454641 D.D. persimilis grimshaw 4546 AnopheleD.D. willistonipersimilisgrimshaw gambiae 62456946 AnopheleD. willistonimojavensis gambiae 624369 CulexAnopheleD.D. quinquefasciatus mojavensis willistoni gambiae 431096269 Culex quinquefasciatusD. virilis 10941 CulexD. D.quinquefasciatus mojavensis virilis 4110943 D.D. grimshawD. grimshaw virilis 464641 AnopheleAedes aegypti gambiae 11169 AnopheleAedesD. grimshaw gambiae aegypti 6911146 Aedes aegypti 111 CulexCulex quinquefasciatusquinquefasciatus 109109 Anophele gambiae 69 Aedes aegypti 111 Culex quinquefasciatus 109 Aedes aegypti 111 Tribolium castaneum 49 TriboliumTribolium castaneum castaneum 4949 TriboliumAedes aegypti castaneum 11149 Tribolium castaneum 49 Apis mellifera 21 TriboliumApisApis mellifera mellifera castaneum 214921 Apis mellifera 21 Apis mellifera 21 Apis mellifera 21 Blatella germanica germanica 109109 Blatella germanica 109 Blatella germanica 109 Blatella germanica 109 Blatella germanica 109 Biomolecules 2021, 11, x Solenopsis invicta 18 3 of 30 Solenopsis invicta 18 Solenopsis invicta 18 Solenopsis invicta 18 Solenopsis invicta 18 Bombyx mori 44 SolenopsisBombyx invictamori 1844 2.2. Evolution of OBP Genes 2.2. Evolution of OBP Genes Exhaustive comparative genomic analysis of OBPs gene families in 20 Arthropoda speciesExhaustive revealed comparative a highly dynamic genomic evolution, analysis with of OBPs a high gene number families of gains
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