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

Roberts, Rebecca E. LU ; Biswas, Twinkle LU orcid ; Yuvaraj, Jothi Kumar LU ; Grosse-Wilde, Ewald ; Powell, Daniel LU ; Hansson, Bill S. ; Löfstedt, Christer LU and Andersson, Martin N. LU (2022) In Molecular Ecology 31(13). p.3693-3707
Abstract

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... (More)

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.

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author
; ; ; ; ; ; and
organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
Coleoptera, Curculionidae, de-orphanization, evolutionary conservation, functional characterization, HEK293 cells
in
Molecular Ecology
volume
31
issue
13
pages
3693 - 3707
publisher
Wiley-Blackwell
external identifiers
  • pmid:35532927
  • scopus:85130622826
ISSN
0962-1083
DOI
10.1111/mec.16494
project
Olfaction in bark beetles
language
English
LU publication?
yes
additional info
Publisher Copyright: © 2022 The Authors. Molecular Ecology published by John Wiley & Sons Ltd.
id
3f6d8506-b738-474d-b9cc-4576682458c6
date added to LUP
2022-06-13 16:13:24
date last changed
2024-06-11 07:48:54
@article{3f6d8506-b738-474d-b9cc-4576682458c6,
  abstract     = {{<p>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.</p>}},
  author       = {{Roberts, Rebecca E. and Biswas, Twinkle and Yuvaraj, Jothi Kumar and Grosse-Wilde, Ewald and Powell, Daniel and Hansson, Bill S. and Löfstedt, Christer and Andersson, Martin N.}},
  issn         = {{0962-1083}},
  keywords     = {{Coleoptera; Curculionidae; de-orphanization; evolutionary conservation; functional characterization; HEK293 cells}},
  language     = {{eng}},
  month        = {{05}},
  number       = {{13}},
  pages        = {{3693--3707}},
  publisher    = {{Wiley-Blackwell}},
  series       = {{Molecular Ecology}},
  title        = {{Odorant receptor orthologues in conifer-feeding beetles display conserved responses to ecologically relevant odours}},
  url          = {{http://dx.doi.org/10.1111/mec.16494}},
  doi          = {{10.1111/mec.16494}},
  volume       = {{31}},
  year         = {{2022}},
}