Functional Characterization Supports Multiple Evolutionary Origins of Pheromone Receptors in Bark Beetles.

Publisher: Oxford University Press Country of Publication: United States NLM ID: 8501455 Publication Model: Print Cited Medium: Internet ISSN: 1537-1719 (Electronic) Linking ISSN: 07374038 NLM ISO Abbreviation: Mol Biol Evol Subsets: MEDLINE

Publication: 2003- : New York, NY : Oxford University Press
Original Publication: [Chicago, Ill.] : University of Chicago Press, [c1983-

Coleoptera*/genetics ; Coleoptera*/metabolism ; Receptors, Pheromone*/genetics ; Receptors, Pheromone*/metabolism ; Evolution, Molecular* ; Phylogeny*; Animals ; Male ; Pheromones/metabolism ; Female ; Monoterpenes/metabolism ; Insect Proteins/genetics ; Insect Proteins/metabolism ; Insect Proteins/chemistry ; Biological Evolution ; Receptors, Odorant/genetics ; Receptors, Odorant/metabolism ; Bicyclic Monoterpenes

Chemical communication using pheromones is thought to have contributed to the diversification and speciation of insects. The species-specific pheromones are detected by specialized pheromone receptors (PRs). Whereas the evolution and function of PRs have been extensively studied in Lepidoptera, only a few PRs have been identified in beetles, which limits our understanding of their evolutionary histories and physiological functions. To shed light on these questions, we aimed to functionally characterize potential PRs in the spruce bark beetle Ips typographus ("Ityp") and explore their evolutionary origins and molecular interactions with ligands. Males of this species release an aggregation pheromone comprising 2-methyl-3-buten-2-ol and (4S)-cis-verbenol, which attracts both sexes to attacked trees. Using two systems for functional characterization, we show that the highly expressed odorant receptor (OR) ItypOR41 responds specifically to (4S)-cis-verbenol, with structurally similar compounds eliciting minor responses. We next targeted the closely related ItypOR40 and ItypOR45. Whereas ItypOR40 was unresponsive, ItypOR45 showed an overlapping response profile with ItypOR41, but a broader tuning. Our phylogenetic analysis shows that these ORs are present in a different OR clade as compared to all other known beetle PRs, suggesting multiple evolutionary origins of PRs in bark beetles. Next, using computational analyses and experimental validation, we reveal two amino acid residues (Gln179 and Trp310) that are important for ligand binding and pheromone specificity of ItypOR41 for (4S)-cis-verbenol, possibly via hydrogen bonding to Gln179. Collectively, our results shed new light on the origins, specificity, and ligand binding mechanisms of PRs in beetles.
Competing Interests: Conflict of Interest The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
(© The Author(s) 2024. Published by Oxford University Press on behalf of Society for Molecular Biology and Evolution.)

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2022-03597 Swedish research councils VR; Foundation in Memory of Oscar and Lili Lamm; CTS17:25 Carl; Royal Physiographic Society in Lund; Max Planck center

Keywords: Ips typographus; Xenopus laevis oocytes; cis-verbenol; HEK293 cells; homology modeling; ligand docking; odorant receptor (OR)

0 (Receptors, Pheromone)
0 (Pheromones)
G0F32F922S (verbenol)
0 (Monoterpenes)
0 (Insect Proteins)
0 (Receptors, Odorant)
0 (Bicyclic Monoterpenes)

Date Created: 20240917 Date Completed: 20241004 Latest Revision: 20241006

20241006

PMC11451568

10.1093/molbev/msae196

39288326