A carboxylesterase, Esterase-6, modulates sensory physiological and behavioral response dynamics to pheromone in Drosophila.
BACKGROUND
Insects 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.


RESULTS
We 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.


CONCLUSIONS
Our 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.
Université Pierre et Marie Curie, UMR, Physiologie de l'Insecte, Signalisation et Communication, Paris, France.
Thomas
T
Chertemps
Adrien
A
François
Nicolas
N
Durand
Gloria
G
Rosell
Teun
T
Dekker
Philippe
P
Lucas
Martine
M
Maïbèche-Coisne
D000085:Acetates / Q000494:pharmacology; D000374:Aggression / Q000187:drug effects; D000818:Animals; D057506:Arthropod Antennae / Q000201:enzymology; D001522:Behavior, Animal / Q000187:drug effects*; D043182:Carboxylesterase / Q000378:metabolism*; D003380:Courtship; D029721:Drosophila Proteins / Q000378:metabolism*; D004331:Drosophila melanogaster / Q000187:drug effects / Q000201:enzymology* / Q000502:physiology*; D005260:Female; D005502:Food; D007659:Ketones / Q000494:pharmacology; D008297:Male; D009154:Mutation / Q000235:genetics; D009812:Odorants; D009829:Oleic Acids / Q000494:pharmacology; D018034:Olfactory Receptor Neurons / Q000187:drug effects / Q000502:physiology; D010675:Pheromones / Q000494:pharmacology*; D012677:Sensation / Q000187:drug effects*; D058618:Sensilla / Q000187:drug effects / Q000502:physiology; D012903:Smell / Q000187:drug effects
D000085:Acetates; D029721:Drosophila Proteins; D007659:Ketones; D009829:Oleic Acids; D010675:Pheromones; C505385:cis-vaccenyl acetate; D043182:Carboxylesterase; C468266:Est-6 protein, Drosophila