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Mutagenesis of the odorant receptor co-receptor (Orco) reveals severe olfactory defects in the crop pest moth Helicoverpa armigera

BACKGROUND: Odorant receptors (ORs) as odorant-gated ion channels play a crucial role in insect olfaction. They are formed by a heteromultimeric complex of the odorant receptor co-receptor (Orco) and a ligand-selective Or. Other types of olfactory receptor proteins, such as ionotropic receptors (IRs...

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Autores principales: Fan, Xiao-Bin, Mo, Bao-Tong, Li, Guo-Cheng, Huang, Ling-Qiao, Guo, Hao, Gong, Xin-Lin, Wang, Chen-Zhu
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9524114/
https://www.ncbi.nlm.nih.gov/pubmed/36175945
http://dx.doi.org/10.1186/s12915-022-01411-2
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author Fan, Xiao-Bin
Mo, Bao-Tong
Li, Guo-Cheng
Huang, Ling-Qiao
Guo, Hao
Gong, Xin-Lin
Wang, Chen-Zhu
author_facet Fan, Xiao-Bin
Mo, Bao-Tong
Li, Guo-Cheng
Huang, Ling-Qiao
Guo, Hao
Gong, Xin-Lin
Wang, Chen-Zhu
author_sort Fan, Xiao-Bin
collection PubMed
description BACKGROUND: Odorant receptors (ORs) as odorant-gated ion channels play a crucial role in insect olfaction. They are formed by a heteromultimeric complex of the odorant receptor co-receptor (Orco) and a ligand-selective Or. Other types of olfactory receptor proteins, such as ionotropic receptors (IRs) and some gustatory receptors (GRs), are also involved in the olfactory system of insects. Orco as an obligatory subunit of ORs is highly conserved, providing an opportunity to systematically evaluate OR-dependent olfactory responses. RESULTS: Herein, we successfully established a homozygous mutant (Orco(−/−)) of Helicoverpa armigera, a notorious crop pest, using the CRISPR/Cas9 gene editing technique. We then compared the olfactory response characteristics of wild type (WT) and Orco(−/−) adults and larvae. Orco(−/−) males were infertile, while Orco(−/−) females were fertile. The lifespan of Orco(−/−) females was longer than that of WT females. The expressions of most Ors, Irs, and other olfaction-related genes in adult antennae of Orco(−/−) moths were not obviously affected, but some of them were up- or down-regulated. In addition, there was no change in the neuroanatomical phenotype of Orco(−/−) moths at the level of the antennal lobe (including the macroglomerular complex region of the male). Using EAG and SSR techniques, we discovered that electrophysiological responses of Orco(−/−) moths to sex pheromone components and many host plant odorants were absent. The upwind flight behaviors toward sex pheromones of Orco(−/−) males were severely reduced in a wind tunnel experiment. The oviposition selectivity of Orco(−/−) females to the host plant (green pepper) has completely disappeared, and the chemotaxis toward green pepper was also lost in Orco(−/−) larvae. CONCLUSIONS: Our study indicates that OR-mediated olfaction is essential for pheromone communication, oviposition selection, and larval chemotaxis of H. armigera, suggesting a strategy in which mate searching and host-seeking behaviors of moth pests could be disrupted by inhibiting or silencing Orco expression. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-022-01411-2.
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spelling pubmed-95241142022-10-01 Mutagenesis of the odorant receptor co-receptor (Orco) reveals severe olfactory defects in the crop pest moth Helicoverpa armigera Fan, Xiao-Bin Mo, Bao-Tong Li, Guo-Cheng Huang, Ling-Qiao Guo, Hao Gong, Xin-Lin Wang, Chen-Zhu BMC Biol Research Article BACKGROUND: Odorant receptors (ORs) as odorant-gated ion channels play a crucial role in insect olfaction. They are formed by a heteromultimeric complex of the odorant receptor co-receptor (Orco) and a ligand-selective Or. Other types of olfactory receptor proteins, such as ionotropic receptors (IRs) and some gustatory receptors (GRs), are also involved in the olfactory system of insects. Orco as an obligatory subunit of ORs is highly conserved, providing an opportunity to systematically evaluate OR-dependent olfactory responses. RESULTS: Herein, we successfully established a homozygous mutant (Orco(−/−)) of Helicoverpa armigera, a notorious crop pest, using the CRISPR/Cas9 gene editing technique. We then compared the olfactory response characteristics of wild type (WT) and Orco(−/−) adults and larvae. Orco(−/−) males were infertile, while Orco(−/−) females were fertile. The lifespan of Orco(−/−) females was longer than that of WT females. The expressions of most Ors, Irs, and other olfaction-related genes in adult antennae of Orco(−/−) moths were not obviously affected, but some of them were up- or down-regulated. In addition, there was no change in the neuroanatomical phenotype of Orco(−/−) moths at the level of the antennal lobe (including the macroglomerular complex region of the male). Using EAG and SSR techniques, we discovered that electrophysiological responses of Orco(−/−) moths to sex pheromone components and many host plant odorants were absent. The upwind flight behaviors toward sex pheromones of Orco(−/−) males were severely reduced in a wind tunnel experiment. The oviposition selectivity of Orco(−/−) females to the host plant (green pepper) has completely disappeared, and the chemotaxis toward green pepper was also lost in Orco(−/−) larvae. CONCLUSIONS: Our study indicates that OR-mediated olfaction is essential for pheromone communication, oviposition selection, and larval chemotaxis of H. armigera, suggesting a strategy in which mate searching and host-seeking behaviors of moth pests could be disrupted by inhibiting or silencing Orco expression. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-022-01411-2. BioMed Central 2022-09-30 /pmc/articles/PMC9524114/ /pubmed/36175945 http://dx.doi.org/10.1186/s12915-022-01411-2 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis 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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Fan, Xiao-Bin
Mo, Bao-Tong
Li, Guo-Cheng
Huang, Ling-Qiao
Guo, Hao
Gong, Xin-Lin
Wang, Chen-Zhu
Mutagenesis of the odorant receptor co-receptor (Orco) reveals severe olfactory defects in the crop pest moth Helicoverpa armigera
title Mutagenesis of the odorant receptor co-receptor (Orco) reveals severe olfactory defects in the crop pest moth Helicoverpa armigera
title_full Mutagenesis of the odorant receptor co-receptor (Orco) reveals severe olfactory defects in the crop pest moth Helicoverpa armigera
title_fullStr Mutagenesis of the odorant receptor co-receptor (Orco) reveals severe olfactory defects in the crop pest moth Helicoverpa armigera
title_full_unstemmed Mutagenesis of the odorant receptor co-receptor (Orco) reveals severe olfactory defects in the crop pest moth Helicoverpa armigera
title_short Mutagenesis of the odorant receptor co-receptor (Orco) reveals severe olfactory defects in the crop pest moth Helicoverpa armigera
title_sort mutagenesis of the odorant receptor co-receptor (orco) reveals severe olfactory defects in the crop pest moth helicoverpa armigera
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9524114/
https://www.ncbi.nlm.nih.gov/pubmed/36175945
http://dx.doi.org/10.1186/s12915-022-01411-2
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