A temperature-dependent molecular switch to adjust behavior to changing environmental conditions

SummaryCircadian clocks increase fitness of organisms by adapting physiological and behavioral rhythms to the daily changes of light and temperature, caused by the Earth’ 24-hr rotation around its own axis. They consist of self-sustained molecular oscillators, maintained by negative feedback regulation of several clock genes, including period (per) and timeless (tim) in the fruit fly Drosophila melanogaster. This molecular clock is synchronized by light:dark and temperature cycles (Zeitgeber), and in turn drives rhythmic biological outputs, like the daily locomotor activity rhythms. While light generally is considered to be the more dominant, daily temperature cycles are sufficient for stable circadian clock synchronization. In Drosophila constant light leads to break down of the molecular clock and arrhythmic behavior, but clock function can be restored by simultaneously exposing the flies to temperature cycles, indicating their particular importance in regions experiencing long photoperiods or constant light. Here, we reveal that during temperature cycles, the deleterious effects of constant light on the clock are avoided by repressing the activity of the photoreceptor CRYPTOCHROME (CRY), which normally leads to light-dependent degradation of TIM. We show that CRY levels are repressed by Gq-PLC-ß signaling, operating within central clock neurons, thereby stabilizing TIM and promoting clock function during constant light and temperature cycles. Consistent with these findings, we reveal that a recently evolved and less light sensitive form of TIM, does not require Gq-PLC-ß signaling for maintaining clock function during constant light and temperature cycles. In summary, our results supply the molecular explanation for temperature synchronization in constant light, and how fruit flies can maintain clock function and rhythmic behavior in northern latitudes.