Abstract
The insect olfactory system, particularly the peripheral sensory system for sex pheromone reception in male moths, is highly selective, but specificity determinants at the receptor level are hitherto unknown. Using the Xenopus oocyte recording system, we conducted a thorough structure-activity relationship study with the sex pheromone receptor of the silkworm moth, Bombyx mori, BmorOR1. When co-expressed with the obligatory odorant receptor co-receptor (BmorOrco), BmorOR1 responded in a dose-dependent fashion to both bombykol and its related aldehyde, bombykal, but the threshold of the latter was about one order of magnitude higher. Solubilizing these ligands with a pheromone-binding protein (BmorPBP1) did not enhance selectivity. By contrast, both ligands were trapped by BmorPBP1 leading to dramatically reduced responses. The silkworm moth pheromone receptor was highly selective towards the stereochemistry of the conjugated diene, with robust response to the natural (10E,12Z)-isomer and very little or no response to the other three isomers. Shifting the conjugated diene towards the functional group or elongating the carbon chain rendered these molecules completely inactive. In contrast, an analogue shortened by two omega carbons elicited the same or slightly higher responses than bombykol. Flexibility of the saturated C1–C9 moiety is important for function as addition of a double or triple bond in position 4 led to reduced responses. The ligand is hypothesized to be accommodated by a large hydrophobic cavity within the helical bundle of transmembrane domains.
Highlights
The identification of bombykol, (10E,12Z)-hexadecadien-1-ol (1), the sex pheromone for the silkworm moth, Bombyx mori [1], more than five decades ago triggered physiologists’ interest in insect olfaction, and paved the way for current molecular studies
Probing the system with earlier techniques such as electroantennogram (EAG) and single-sensillum recordings (SSR), pioneers in the field unraveled an inordinate sensitivity and selectivity of the insect’s olfactory system [2]. These earlier studies clearly demonstrated that structural modifications dramatically reduce neuronal responses or render the molecules completely inactive [3], but it remains mostly unknown how pheromone molecules interact with odorant receptors (ORs) housed in these neurons, various moth sex pheromone receptors have been deorphanized to date [4,5,6,7,8,9,10,11]
Selectivity of the Functional Group First, we examined the response of BmorOR1NBmorOrcoexpressing oocytes to bombykol
Summary
The identification of bombykol, (10E,12Z)-hexadecadien-1-ol (1), the sex pheromone for the silkworm moth, Bombyx mori [1], more than five decades ago triggered physiologists’ interest in insect olfaction, and paved the way for current molecular studies. Probing the system with earlier techniques such as electroantennogram (EAG) and single-sensillum recordings (SSR), pioneers in the field unraveled an inordinate sensitivity and selectivity of the insect’s olfactory system [2]. These earlier studies clearly demonstrated that structural modifications dramatically reduce neuronal responses or render the molecules completely inactive [3], but it remains mostly unknown how pheromone molecules interact with odorant receptors (ORs) housed in these neurons, various moth sex pheromone receptors have been deorphanized to date [4,5,6,7,8,9,10,11]. We show that the stereochemistry of the double bonds, flexibility of saturated moiety, the functional group, and the number of carbons atoms after the unsaturations are specificity determinants of the pheromone molecule
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