Insects detect and discriminate a diverse array of chemicals using odorant receptors (ORs), which are ligand-gated ion channels comprising a divergent odorant-sensing OR and a conserved odorant receptor co-receptor (Orco). In this work, we report structures of the Ap OR5-Orco heterocomplex from the pea aphid Acyrthosiphon pisum alone and bound to its known activating ligand, geranyl acetate. In these structures, three Ap Orco subunits serve as scaffold components that cannot bind the ligand and remain relatively unchanged. Upon ligand binding, the pore-forming helix S7b of Ap OR5 shifts outward from the central pore axis, causing an asymmetrical pore opening for ion influx. Our study provides insights into odorant recognition and channel gating of the OR-Orco heterocomplex and offers structural resources to support development of innovative insecticides and repellents for pest control.

BACKGROUND: The insect olfactory system can recognize odorants for feeding, courtship, oviposition and avoiding natural enemies. Odorant cues from host plants play important roles in insect behaviours. Tobacco (Nicotiana tabacum) is the main cultivated host of the oriental tobacco budworm Helicoverpa assult. Volatiles of tobacco plants attract and stimulate oviposition in female moths. However, it is still not known how female H. assulta recognize tobacco volatiles and which odorant compounds are used as oviposition cues.RESULTS: We detected 14 volatile compounds emitted from a tobacco plant during vegetative growth, using gas chromatography–mass spectrometry. Electroantennogram tests indicated that eight of the 14 compounds induced responses in female H. assulta. Among these eight volatiles, nonanal greatly increased oviposition preference. Single‐sensillum recording (SSR) results showed that many neurons housed in three types of short basiconic sensilla and four types of long basiconic sensilla responded to nonanal and heptanal as its structural analogue. The responses to nonanal were significantly stronger than those to the other compounds. Nonanal was the main ligand of OR67, an odorant receptor from H. assulta. This was demonstrated using an in vitro Xenopus oocytes expression system that supported the SSR results.CONCLUSION: Nonanal is a key signal volatile of tobacco plants that attracts female H. assulta moths to oviposit. © 2020 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.