Abstract
BackgroundInsects respond to the spatial and temporal dynamics of a pheromone plume, which implies not only a strong response to 'odor on', but also to 'odor off'. This requires mechanisms geared toward a fast signal termination. Several mechanisms may contribute to signal termination, among which odorant-degrading enzymes. These enzymes putatively play a role in signal dynamics by a rapid inactivation of odorants in the vicinity of the sensory receptors, although direct in vivo experimental evidences are lacking. Here we verified the role of an extracellular carboxylesterase, esterase-6 (Est-6), in the sensory physiological and behavioral dynamics of Drosophila melanogaster response to its pheromone, cis-vaccenyl acetate (cVA). Est-6 was previously linked to post-mating effects in the reproductive system of females. As Est-6 is also known to hydrolyze cVA in vitro and is expressed in the main olfactory organ, the antenna, we tested here its role in olfaction as a putative odorant-degrading enzyme.ResultsWe first confirm that Est-6 is highly expressed in olfactory sensilla, including cVA-sensitive sensilla, and we show that expression is likely associated with non-neuronal cells. Our electrophysiological approaches show that the dynamics of olfactory receptor neuron (ORN) responses is strongly influenced by Est-6, as in Est-6° null mutants (lacking the Est-6 gene) cVA-sensitive ORN showed increased firing rate and prolonged activity in response to cVA. Est-6° mutant males had a lower threshold of behavioral response to cVA, as revealed by the analysis of two cVA-induced behaviors. In particular, mutant males exhibited a strong decrease of male-male courtship, in association with a delay in courtship initiation.ConclusionsOur study presents evidence that Est-6 plays a role in the physiological and behavioral dynamics of sex pheromone response in Drosophila males and supports a role of Est-6 as an odorant-degrading enzyme (ODE) in male antennae. Our results also expand the role of Est-6 in Drosophila biology, from reproduction to olfaction, and highlight the role of ODEs in insect olfaction.
Highlights
Insects respond to the spatial and temporal dynamics of a pheromone plume, which implies a strong response to ‘odor on’, and to ‘odor off’
In Drosophila melanogaster, when olfactory receptors (Ors) genes were expressed in another olfactory receptor neuron (ORN) than their native ORN by using the ‘empty neuron’ system (Δhalo mutant), signal termination was similar to what had been observed in their native ORN, suggesting that Ors play a key role in signal dynamics [3]
Est-6 was barely detectable in legs, which bear gustatory sensilla, including sensilla responding to female-specific pheromones [30]
Summary
Insects respond to the spatial and temporal dynamics of a pheromone plume, which implies a strong response to ‘odor on’, and to ‘odor off’. This requires mechanisms geared toward a fast signal termination. Several mechanisms may contribute to signal termination, among which odorant-degrading enzymes These enzymes putatively play a role in signal dynamics by a rapid inactivation of odorants in the vicinity of the sensory receptors, direct in vivo experimental evidences are lacking. Fast degradation of odorants in the vicinity of Ors by odorant-degrading enzymes (ODEs) has been proposed as a mechanism contributing to the termination of ORN responses. Involvement of ODEs in odorant processing has never been directly demonstrated in vivo
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