Abstract
The transcriptional circuits of circadian clocks control physiological and behavioral rhythms. Light may affect such overt rhythms in two ways: (1) by entraining the clock circuits and (2) via clock-independent molecular pathways. In this study we examine the relationship between autonomous transcript oscillations and light-driven transcript responses. Transcript profiles of wild-type and arrhythmic mutant Drosophila were recorded both in the presence of an environmental photocycle and in constant darkness. Systematic autonomous oscillations in the 12- to 48-h period range were detectable only in wild-type flies and occurred preferentially at the circadian period length. However, an extensive program of light-driven expression was confirmed in arrhythmic mutant flies. Many light-responsive transcripts are preferentially expressed in the compound eyes and the phospholipase C component of phototransduction, NORPA (no receptor potential), is required for their light-dependent regulation. Although there is evidence for the existence of multiple molecular clock circuits in cyanobacteria, protists, plants, and fungi, Drosophila appears to possess only one such system. The sustained photic expression responses identified here are partially coupled to the circadian clock and may reflect a mechanism for flies to modulate functions such as visual sensitivity and synaptic transmission in response to seasonal changes in photoperiod.
Highlights
The circadian clocks of cyanobacteria, protists, plants, fungi, and animals produce self-sustained physiological rhythmicity that resonates with daily fluctuations in the environment
Persistence of light responses was detected in three out of five cases for the per 0 mutant and nine out of 14 cases for the Clk jrk mutant (Figure 7A, columns 7 and 8). These results confirm that the light-dependent responses that we identified generally do not require a functional circadian clock, they indicate that at least some of them are affected by the state of specific clock genes
A new strategy for analyzing oscillatory patterns in microarrray data has allowed us to answer general questions about oscillatory gene systems in the fly head. By applying this strategy to 17 d of data, we were able to conclusively demonstrate that there are more than a hundred circadian transcript oscillations in the fly head
Summary
The circadian clocks of cyanobacteria, protists, plants, fungi, and animals produce self-sustained physiological rhythmicity that resonates with daily fluctuations in the environment. Feedback circuits regulated at the level of clock gene expression, clock protein accumulation, and clock protein degradation are thought to form most if not all circadian clocks. Interactions among these circuits appear to promote molecular oscillations of the clock components themselves and rhythmic gene activities that are subordinate to the clock. Entrainment of circadian clocks to environmental cycles of light and dark is best understood in Drosophila and Neurospora. In the former, the clock protein TIM (timeless) is rapidly degraded in response to light, causing resetting of the oscillating mechanism. In Neurospora, light induces expression of the clock gene frequency, which encodes the central transcriptional repressor in the Neurospora clockworks (for reviews, see [1,2,3,4,5,6,7,8,9])
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