Moth Sex Pheromone Receptors and Deceitful Parapheromones

Diogo M. Vidal,Walter S. Leal,Pingxi Xu,Michel Renou,Young-Moo Choo,Elizabeth Atungulu,Caio H. L. Zitelli,Stephen F. Garczynski,Zainulabeuddin Syed

doi:10.1371/journal.pone.0041653

Abstract

The insect's olfactory system is so selective that male moths, for example, can discriminate female-produced sex pheromones from compounds with minimal structural modifications. Yet, there is an exception for this “lock-and-key” tight selectivity. Formate analogs can be used as replacement for less chemically stable, long-chain aldehyde pheromones, because male moths respond physiologically and behaviorally to these parapheromones. However, it remained hitherto unknown how formate analogs interact with aldehyde-sensitive odorant receptors (ORs). Neuronal responses to semiochemicals were investigated with single sensillum recordings. Odorant receptors (ORs) were cloned using degenerate primers, and tested with the Xenopus oocyte expression system. Quality, relative quantity, and purity of samples were evaluated by gas chromatography and gas chromatography-mass spectrometry. We identified olfactory receptor neurons (ORNs) housed in trichoid sensilla on the antennae of male navel orangeworm that responded equally to the main constituent of the sex pheromone, (11Z,13Z)-hexadecadienal (Z11Z13-16Ald), and its formate analog, (9Z,11Z)-tetradecen-1-yl formate (Z9Z11-14OFor). We cloned an odorant receptor co-receptor (Orco) and aldehyde-sensitive ORs from the navel orangeworm, one of which (AtraOR1) was expressed specifically in male antennae. AtraOR1•AtraOrco-expressing oocytes responded mainly to Z11Z13-16Ald, with moderate sensitivity to another component of the sex pheromone, (11Z,13Z)-hexadecadien-1-ol. Surprisingly, this receptor was more sensitive to the related formate than to the natural sex pheromone. A pheromone receptor from Heliothis virescens, HR13 ( = HvirOR13) showed a similar profile, with stronger responses elicited by a formate analog than to the natural sex pheromone, (11Z)-hexadecenal thus suggesting this might be a common feature of moth pheromone receptors.

Highlights

Insects achieve their prominence through successful reproduction, which in turn relies heavily on an acute olfactory system
Because the chemical structure of Z914OFor resembles that of the major pheromone components of these species, namely, (11Z)-hexadecenal ( = Z11-16Ald) [10], it became evident that formate analogs may be used as replacement for chemically less stable aldehyde pheromones
Behavioral observations in wind tunnel experiments led to the conclusion that a mixture of Z11Z13-16Ald, Z11Z13-16OH, and (3Z,6Z,9Z,12Z,15Z)-tricosapentaene is necessary and sufficient for full attraction of male moths [17]

Summary

Introduction

Insects achieve their prominence through successful reproduction, which in turn relies heavily on an acute olfactory system. It was later demonstrated that olfactory receptor neurons (ORNs) involved in the detection of Z11-16Ald, the major component of H. zea sex pheromone, responds almost to the formate analog, Z914OFor [11].

Results

Conclusion