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Functional evolution of a bark beetle odorant receptor clade detecting monoterpenoids of different ecological origins

Hou, Xiao-Qing LU ; Yuvaraj, Jothi Kumar LU ; Roberts, Rebecca E LU ; Zhang, Dan-Dan LU ; Unelius, C Rikard ; Löfstedt, Christer LU and Andersson, Martin N LU (2021) In Molecular biology and evolution 38(11). p.4934-4947
Abstract

Insects detect odors using an array of odorant receptors (ORs), which may expand through gene duplication. How and which new functions may evolve among related ORs within a species remain poorly investigated. We addressed this question by functionally characterizing ORs from the Eurasian spruce bark beetle Ips typographus, in which physiological and behavioral responses to pheromones, volatiles from host and nonhost trees, and fungal symbionts are well described. In contrast, knowledge of OR function is restricted to two receptors detecting the pheromone compounds (S)-(-)-ipsenol (ItypOR46) and (R)-(-)-ipsdienol (ItypOR49). These receptors belong to an Ips-specific OR-lineage comprising seven ItypORs. To gain insight into the functional... (More)

Insects detect odors using an array of odorant receptors (ORs), which may expand through gene duplication. How and which new functions may evolve among related ORs within a species remain poorly investigated. We addressed this question by functionally characterizing ORs from the Eurasian spruce bark beetle Ips typographus, in which physiological and behavioral responses to pheromones, volatiles from host and nonhost trees, and fungal symbionts are well described. In contrast, knowledge of OR function is restricted to two receptors detecting the pheromone compounds (S)-(-)-ipsenol (ItypOR46) and (R)-(-)-ipsdienol (ItypOR49). These receptors belong to an Ips-specific OR-lineage comprising seven ItypORs. To gain insight into the functional evolution of related ORs, we characterized the five remaining ORs in this clade using Xenopus oocytes. Two receptors responded primarily to the host tree monoterpenes (+)-3-carene (ItypOR25) and p-cymene (ItypOR27). Two receptors responded to oxygenated monoterpenoids produced in larger relative amounts by the beetle-associated fungi, with ItypOR23 specific for (+)-trans-(1R, 4S)-4-thujanol, and ItypOR29 responding to (+)-isopinocamphone and similar ketones. ItypOR28 responded to the pheromone E-myrcenol from the competitor Ips duplicatus. Overall, the OR responses match well with those of previously characterized olfactory sensory neuron classes except that neurons detecting E-myrcenol have not been identified. The characterized ORs are under strong purifying selection and demonstrate a shared functional property in that they all primarily respond to monoterpenoids. The variation in functional groups among OR ligands and their diverse ecological origins suggest that neofunctionalization has occurred early in the evolution of this OR-lineage following gene duplication.

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author
; ; ; ; ; and
organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
functional characterization, neofunctionalization, odorant receptor, olfaction, purifying selection, Xenopus oocyte
in
Molecular biology and evolution
volume
38
issue
11
pages
4934 - 4947
publisher
Oxford University Press
external identifiers
  • scopus:85114698352
  • pmid:34293158
ISSN
0737-4038
DOI
10.1093/molbev/msab218
project
The Max Planck Center on next Generation Insect Chemical Ecology
language
English
LU publication?
yes
id
c22a90dc-6259-4a60-8835-323acf127ee2
date added to LUP
2021-11-03 11:03:28
date last changed
2022-08-04 20:11:32
@article{c22a90dc-6259-4a60-8835-323acf127ee2,
  abstract     = {{<p>Insects detect odors using an array of odorant receptors (ORs), which may expand through gene duplication. How and which new functions may evolve among related ORs within a species remain poorly investigated. We addressed this question by functionally characterizing ORs from the Eurasian spruce bark beetle Ips typographus, in which physiological and behavioral responses to pheromones, volatiles from host and nonhost trees, and fungal symbionts are well described. In contrast, knowledge of OR function is restricted to two receptors detecting the pheromone compounds (S)-(-)-ipsenol (ItypOR46) and (R)-(-)-ipsdienol (ItypOR49). These receptors belong to an Ips-specific OR-lineage comprising seven ItypORs. To gain insight into the functional evolution of related ORs, we characterized the five remaining ORs in this clade using Xenopus oocytes. Two receptors responded primarily to the host tree monoterpenes (+)-3-carene (ItypOR25) and p-cymene (ItypOR27). Two receptors responded to oxygenated monoterpenoids produced in larger relative amounts by the beetle-associated fungi, with ItypOR23 specific for (+)-trans-(1R, 4S)-4-thujanol, and ItypOR29 responding to (+)-isopinocamphone and similar ketones. ItypOR28 responded to the pheromone E-myrcenol from the competitor Ips duplicatus. Overall, the OR responses match well with those of previously characterized olfactory sensory neuron classes except that neurons detecting E-myrcenol have not been identified. The characterized ORs are under strong purifying selection and demonstrate a shared functional property in that they all primarily respond to monoterpenoids. The variation in functional groups among OR ligands and their diverse ecological origins suggest that neofunctionalization has occurred early in the evolution of this OR-lineage following gene duplication. </p>}},
  author       = {{Hou, Xiao-Qing and Yuvaraj, Jothi Kumar and Roberts, Rebecca E and Zhang, Dan-Dan and Unelius, C Rikard and Löfstedt, Christer and Andersson, Martin N}},
  issn         = {{0737-4038}},
  keywords     = {{functional characterization; neofunctionalization; odorant receptor; olfaction; purifying selection; Xenopus oocyte}},
  language     = {{eng}},
  number       = {{11}},
  pages        = {{4934--4947}},
  publisher    = {{Oxford University Press}},
  series       = {{Molecular biology and evolution}},
  title        = {{Functional evolution of a bark beetle odorant receptor clade detecting monoterpenoids of different ecological origins}},
  url          = {{http://dx.doi.org/10.1093/molbev/msab218}},
  doi          = {{10.1093/molbev/msab218}},
  volume       = {{38}},
  year         = {{2021}},
}