Clock-gated photic stimulation of timeless expression at cold temperatures and seasonal adaptation in Drosophila

Numerous lines of evidence indicate that the initial photoresponse of the circadian clock in Drosophila melanogaster is the light-induced degradation of TIMELESS (TIM). This posttranslational mechanism is in sharp contrast to the well-characterized pacemakers in mammals and Neurospora, where light evokes rapid changes in the transcriptional profiles of 1 or more clock genes. The authors show that light has novel effects on D. melanogaster circadian pacemakers, acutely stimulating the expression of tim at cold but not warm temperatures. This photoinduction occurs in flies defective for the classic visual phototransduction pathway or the circadian-relevant photoreceptor CRYPTOCHROME (CRY). Cold-specific stimulation of tim RNA abundance is regulated at the transcriptional level, and although numerous lines of evidence indicate that period (per) and tim expression are activated by the same mechanism, light has no measurable acute effect on per mRNA abundance. Moreover, light-induced increases in the levels of tim RNA are abolished or greatly reduced in the absence of functional CLOCK (CLK) or CYCLE (CYC) but not PER or TIM. These findings add to a growing number of examples where molecular and behavioral photoresponses in Drosophila are differentially influenced by positive (e.g., CLK and CYC) and negative (e.g., PER and TIM) core clock elements. The acute effects of light on tim expression are temporally gated, essentially restricted to the daily rising phase in tim mRNA levels. Because the start of the daily upswing in tim expression begins several hours after dawn in long photoperiods (day length), this gating mechanism likely ensures that sunrise does not prematurely stimulate tim expression during unseasonally cold spring/summer days. The results suggest that the photic stimulation of tim expression at low temperatures is part of a seasonal adaptive response that helps advance the phase of the clock on cold days, enabling flies to exhibit preferential daytime activity despite the (usually) earlier onset of dusk. Taken together with prior findings, the ability of temperature and photoperiod to adjust trajectories in the rising phases of 1 or more clock RNAs constitutes a major mechanism contributing to seasonal adaptation of clock function.