Control of odor sensation by light and cryptochrome in the Drosophila antenna

Olfaction is a sense employed by insects to differentiate safe from harmful food options, evaluate potential mates, and identify oviposition sites. Here, we found that the fruit fly, Drosophila melanogaster, responds differently to a set of repulsive odors depending on ambient light conditions. Ultraviolet (UV) or blue light reduces the behavioral aversion and electrophysiological responses of olfactory receptor neurons (ORNs) to certain repellent odors, such as benzaldehyde. We found that cryptochrome (cry) is strongly expressed in the antennal support cells that lie adjacent to ORNs, and mutation of cry eliminates the light-dependent reduction in aversion. Thus, these data demonstrate that support cells in an olfactory organ serve a sensory function as light receptor cells. It has been shown that light activation of Cry creates reactive oxygen species (ROS), and ROS activates the TRPA1 channel. We demonstrate that the TRPA1-C isoform is expressed and required in ORNs for benzaldehyde repulsion, and that TRPA1-C is activated in vitro by benzaldehyde. Overexpression of dual oxygenase, which generates hydrogen peroxide, reduced the aversion under dark conditions. Our data support the model that light-dependent creation of hydrogen peroxide persistently activates TRPA1-C. Consequently, the channel is no longer effectively activated by benzaldehyde. Since flies sleep much more at night, and begin feeding at dawn, we propose that the light-induced reduction in aversion to certain odors provides a mechanism to lower the barrier to feeding following the transition from night to day.