Abstract
Insects express chemical receptors within sensory neurons that are activated by specific cues in the environment, thereby influencing the acquisition of critical resources. A significant gap in our current understanding of insect chemical ecology is defining the molecular mechanisms that underlie sensitivity to plant-emitted volatiles. Linalool is a commonly-occurring monoterpene that has various effects on insect behavior, either acting as an attractant or a repellent, and existing in nature as one of two possible stereoisomers, (R)-(–)-linalool and (S)-(+)-linalool. In this study, we have used a cell-based functional assay to identify linalool and structurally-related compounds as ligands of Odorant receptor 29, a labellum-expressed receptor in the malaria vector mosquito, Anopheles gambiae (AgamOr29). While (R)-(–)-linalool activates AgamOr29, a mixture of the (R) and (S) stereoisomers activates the receptor with higher potency, implying enantiomeric selectivity. Orthologs of Or29 are present in the genomes of Anophelines within the Cellia subgenus. The conservation of this receptor across Anopheline lineages suggests that this ecologically important compound might serve as an attraction cue for nectar-seeking mosquitoes. Moreover, the characterization of a mosquito terpene receptor could serve as a foundation for future ligand-receptor studies of plant volatiles and for the discovery of compounds that can be integrated into push-pull vector control strategies.
Highlights
Mosquitoes use sensory receptors to detect environmental chemical cues that influence resource acquisition success
Anopheline Or29 orthologs are very similar in length (384 aa) and have pairwise identities ranging from 70% to 99%, with conserved residues spanning their entire lengths (S2 Table; S1 Fig)
The Or29 relationships conform to previously described phylogenies of the Anophelines [37, 41, 42], with Or29 orthologs encoded in the genomes of species in the A. gambiae complex appearing as a single clade with 100% bootstrap support (Fig 2)
Summary
Mosquitoes use sensory receptors to detect environmental chemical cues that influence resource acquisition success. Among these are the characteristically female behaviors of animal host seeking [1,2] and oviposition site selection [3,4], plus the female and male behaviors of nectar locating [5] and resting site selection [6]. Chemosensory receptor proteins are expressed in sensory neurons and comprise three major families in insects: odorant receptors (Ors) [7], gustatory receptors (Grs) [8], and variant ionotropic glutamate receptors (Irs) [9]. The interactions between chemoreceptors and their environmental ligands, while studied extensively in some insects, remain uncharacterized for the vast majority of mosquito species and are of interest for further scientific inquiry [7].
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