Cargando…

Odorant receptor orthologues in conifer‐feeding beetles display conserved responses to ecologically relevant odours

Insects are able to detect a plethora of olfactory cues using a divergent family of odorant receptors (ORs). Despite the divergent nature of this family, related species frequently express several evolutionarily conserved OR orthologues. In the largest order of insects, Coleoptera, it remains unknow...

Descripción completa

Detalles Bibliográficos
Autores principales: Roberts, Rebecca E., Biswas, Twinkle, Yuvaraj, Jothi Kumar, Grosse‐Wilde, Ewald, Powell, Daniel, Hansson, Bill S., Löfstedt, Christer, Andersson, Martin N.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9321952/
https://www.ncbi.nlm.nih.gov/pubmed/35532927
http://dx.doi.org/10.1111/mec.16494
_version_ 1784756177424351232
author Roberts, Rebecca E.
Biswas, Twinkle
Yuvaraj, Jothi Kumar
Grosse‐Wilde, Ewald
Powell, Daniel
Hansson, Bill S.
Löfstedt, Christer
Andersson, Martin N.
author_facet Roberts, Rebecca E.
Biswas, Twinkle
Yuvaraj, Jothi Kumar
Grosse‐Wilde, Ewald
Powell, Daniel
Hansson, Bill S.
Löfstedt, Christer
Andersson, Martin N.
author_sort Roberts, Rebecca E.
collection PubMed
description Insects are able to detect a plethora of olfactory cues using a divergent family of odorant receptors (ORs). Despite the divergent nature of this family, related species frequently express several evolutionarily conserved OR orthologues. In the largest order of insects, Coleoptera, it remains unknown whether OR orthologues have conserved or divergent functions in different species. Using HEK293 cells, we addressed this question through functional characterization of two groups of OR orthologues in three species of the Curculionidae (weevil) family, the conifer‐feeding bark beetles Ips typographus L. (“Ityp”) and Dendroctonus ponderosae Hopkins (“Dpon”) (Scolytinae), and the pine weevil Hylobius abietis L. (“Habi”; Molytinae). The ORs of H. abietis were annotated from antennal transcriptomes. The results show highly conserved response specificities, with one group of orthologues (HabiOR3/DponOR8/ItypOR6) responding exclusively to 2‐phenylethanol (2‐PE), and the other group (HabiOR4/DponOR9/ItypOR5) responding to angiosperm green leaf volatiles (GLVs). Both groups of orthologues belong to the coleopteran OR subfamily 2B, and share a common ancestor with OR5 in the cerambycid Megacyllene caryae, also tuned to 2‐PE, suggesting a shared evolutionary history of 2‐PE receptors across two beetle superfamilies. The detected compounds are ecologically relevant for conifer‐feeding curculionids, and are probably linked to fitness, with GLVs being used to avoid angiosperm nonhost plants, and 2‐PE being important for intraspecific communication and/or playing a putative role in beetle–microbe symbioses. To our knowledge, this study is the first to reveal evolutionary conservation of OR functions across several beetle species and hence sheds new light on the functional evolution of insect ORs.
format Online
Article
Text
id pubmed-9321952
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher John Wiley and Sons Inc.
record_format MEDLINE/PubMed
spelling pubmed-93219522022-07-30 Odorant receptor orthologues in conifer‐feeding beetles display conserved responses to ecologically relevant odours Roberts, Rebecca E. Biswas, Twinkle Yuvaraj, Jothi Kumar Grosse‐Wilde, Ewald Powell, Daniel Hansson, Bill S. Löfstedt, Christer Andersson, Martin N. Mol Ecol ORIGINAL ARTICLES Insects are able to detect a plethora of olfactory cues using a divergent family of odorant receptors (ORs). Despite the divergent nature of this family, related species frequently express several evolutionarily conserved OR orthologues. In the largest order of insects, Coleoptera, it remains unknown whether OR orthologues have conserved or divergent functions in different species. Using HEK293 cells, we addressed this question through functional characterization of two groups of OR orthologues in three species of the Curculionidae (weevil) family, the conifer‐feeding bark beetles Ips typographus L. (“Ityp”) and Dendroctonus ponderosae Hopkins (“Dpon”) (Scolytinae), and the pine weevil Hylobius abietis L. (“Habi”; Molytinae). The ORs of H. abietis were annotated from antennal transcriptomes. The results show highly conserved response specificities, with one group of orthologues (HabiOR3/DponOR8/ItypOR6) responding exclusively to 2‐phenylethanol (2‐PE), and the other group (HabiOR4/DponOR9/ItypOR5) responding to angiosperm green leaf volatiles (GLVs). Both groups of orthologues belong to the coleopteran OR subfamily 2B, and share a common ancestor with OR5 in the cerambycid Megacyllene caryae, also tuned to 2‐PE, suggesting a shared evolutionary history of 2‐PE receptors across two beetle superfamilies. The detected compounds are ecologically relevant for conifer‐feeding curculionids, and are probably linked to fitness, with GLVs being used to avoid angiosperm nonhost plants, and 2‐PE being important for intraspecific communication and/or playing a putative role in beetle–microbe symbioses. To our knowledge, this study is the first to reveal evolutionary conservation of OR functions across several beetle species and hence sheds new light on the functional evolution of insect ORs. John Wiley and Sons Inc. 2022-05-26 2022-07 /pmc/articles/PMC9321952/ /pubmed/35532927 http://dx.doi.org/10.1111/mec.16494 Text en © 2022 The Authors. Molecular Ecology published by John Wiley & Sons Ltd. https://creativecommons.org/licenses/by-nc-nd/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc-nd/4.0/ (https://creativecommons.org/licenses/by-nc-nd/4.0/) License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non‐commercial and no modifications or adaptations are made.
spellingShingle ORIGINAL ARTICLES
Roberts, Rebecca E.
Biswas, Twinkle
Yuvaraj, Jothi Kumar
Grosse‐Wilde, Ewald
Powell, Daniel
Hansson, Bill S.
Löfstedt, Christer
Andersson, Martin N.
Odorant receptor orthologues in conifer‐feeding beetles display conserved responses to ecologically relevant odours
title Odorant receptor orthologues in conifer‐feeding beetles display conserved responses to ecologically relevant odours
title_full Odorant receptor orthologues in conifer‐feeding beetles display conserved responses to ecologically relevant odours
title_fullStr Odorant receptor orthologues in conifer‐feeding beetles display conserved responses to ecologically relevant odours
title_full_unstemmed Odorant receptor orthologues in conifer‐feeding beetles display conserved responses to ecologically relevant odours
title_short Odorant receptor orthologues in conifer‐feeding beetles display conserved responses to ecologically relevant odours
title_sort odorant receptor orthologues in conifer‐feeding beetles display conserved responses to ecologically relevant odours
topic ORIGINAL ARTICLES
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9321952/
https://www.ncbi.nlm.nih.gov/pubmed/35532927
http://dx.doi.org/10.1111/mec.16494
work_keys_str_mv AT robertsrebeccae odorantreceptororthologuesinconiferfeedingbeetlesdisplayconservedresponsestoecologicallyrelevantodours
AT biswastwinkle odorantreceptororthologuesinconiferfeedingbeetlesdisplayconservedresponsestoecologicallyrelevantodours
AT yuvarajjothikumar odorantreceptororthologuesinconiferfeedingbeetlesdisplayconservedresponsestoecologicallyrelevantodours
AT grossewildeewald odorantreceptororthologuesinconiferfeedingbeetlesdisplayconservedresponsestoecologicallyrelevantodours
AT powelldaniel odorantreceptororthologuesinconiferfeedingbeetlesdisplayconservedresponsestoecologicallyrelevantodours
AT hanssonbills odorantreceptororthologuesinconiferfeedingbeetlesdisplayconservedresponsestoecologicallyrelevantodours
AT lofstedtchrister odorantreceptororthologuesinconiferfeedingbeetlesdisplayconservedresponsestoecologicallyrelevantodours
AT anderssonmartinn odorantreceptororthologuesinconiferfeedingbeetlesdisplayconservedresponsestoecologicallyrelevantodours