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

Olfaction is employed by the fruit fly, Drosophila melanogaster, to differentiate safe from harmful foods and for other behaviors. Here, we show that ultraviolet (UV) or blue light reduces the fly's behavioral aversion and the responses of olfactory receptor neurons (ORNs) to certain repellent odors, such as benzaldehyde. We demonstrate that cryptochrome (cry) is expressed in antennal support cells and is required for the light-dependent reduction in aversion. Light activation of Cry creates reactive oxygen species (ROS), and ROS activate the TRPA1 channel. We found that TRPA1 is required in ORNs for benzaldehyde repulsion and is activated in vitro by benzaldehyde. We propose that light-activation of Cry and creation of ROS persistently stimulates and then desensitizes TRPA1, preventing activation by benzaldehyde. Since flies begin feeding at dawn, we suggest that the light-induced reduction in odor avoidance serves to lower the barrier to feeding following the transition from night to day.