Drosophila TRPA Channel Painless Inhibits Male–Male Courtship Behavior through Modulating Olfactory Sensation

Kaiyu Wang,Fei Wang,Zuoren Wang,Yanmeng Guo,Frederic Marion-Poll

doi:10.1371/journal.pone.0025890

Abstract

The Drosophila melanogaster TRPA family member painless, expressed in a subset of multidendritic neurons embeding in the larval epidermis, is necessary for larval nociception of noxious heat or mechanical stimuli. However, the function of painless in adult flies remains largely unknown. Here we report that mutation of painless leads to a defect in male–male courtship behavior and alteration in olfaction sensitivity in adult flies. Specific downregulation of the expression of the Painless protein in the olfactory projection neurons (PNs) of the antennal lobes (ALs) resulted in a phenotype resembling that found in painless mutant flies, whereas overexpression of Painless in PNs of painless mutant males suppressed male–male courtship behavior. The downregulation of Painless exclusively during adulthood also resulted in male–male courtship behavior. In addition, mutation of the painless gene in flies caused changes in olfaction, suggesting a role for this gene in olfactory processing. These results indicate that functions of painless in the adult central nervous system of Drosophila include modulation of olfactory processing and inhibition of male–male courtship behavior.

Highlights

Transient receptor potential (TRP) channels play important roles in a variety of sensory systems [1]
Using the same Gal4 line, we found that painless is expressed in several clusters of projection neurons (PNs) of the antennal lobes (ALs), in Kenyon cells (KCs) of mushroom bodies (MBs), and in the neurons that form the ellipsoid body (Figure 1A)
To study the physiological role of Painless in the central nervous system of adult fruit flies, we examined the behavior of painless mutant flies

Summary

Introduction

Transient receptor potential (TRP) channels play important roles in a variety of sensory systems [1]. As a Drosophila TRPA channel [5], the painless gene was first identified as essential for the sensation of high temperature (above ,39uC) and for noxious mechanical stimulation in the larvae [6,7]. The Drosophila olfactory system is critical for its detection of volatile chemicals in the external environment [12,13,14]. These chemical cues are first detected and converted into electric signals by the primary olfactory receptor neurons (ORNs). The Drosophila olfactory system, which detects volatile pheromone cues, plays an important role in courtship behavior. Activity of higher-order olfactory neurons, where information from ORNs is processed and modified, may influence Drosophila courtship behavior

Methods

Results

Conclusion