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 indicate that
support cells in an olfactory organ serve a sensory function as light
responsive 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.