Abstract
Circadian clocks are aligned to the environment via synchronizing signals, or Zeitgebers, such as daily light and temperature cycles, food availability, and social behavior. In this study, we found that genome-wide expression profiles from temperature-entrained flies show a dramatic difference in the presence or absence of a thermocycle. Whereas transcript levels appear to be modified broadly by changes in temperature, there is a specific set of temperature-entrained circadian mRNA profiles that continue to oscillate in constant conditions. There are marked differences in the biological functions represented by temperature-driven or circadian regulation. The set of temperature-entrained circadian transcripts overlaps significantly with a previously defined set of transcripts oscillating in response to a photocycle. In follow-up studies, all thermocycle-entrained circadian transcript rhythms also responded to light/dark entrainment, whereas some photocycle-entrained rhythms did not respond to temperature entrainment. Transcripts encoding the clock components Period, Timeless, Clock, Vrille, PAR-domain protein 1, and Cryptochrome were all confirmed to be rhythmic after entrainment to a daily thermocycle, although the presence of a thermocycle resulted in an unexpected phase difference between period and timeless expression rhythms at the transcript but not the protein level. Generally, transcripts that exhibit circadian rhythms both in response to thermocycles and photocycles maintained the same mutual phase relationships after entrainment by temperature or light. Comparison of the collective temperature- and light-entrained circadian phases of these transcripts indicates that natural environmental light and temperature cycles cooperatively entrain the circadian clock. This interpretation is further supported by comparative analysis of the circadian phases observed for temperature-entrained and light-entrained circadian locomotor behavior. Taken together, these findings suggest that information from both light and temperature is integrated by the transcriptional clock mechanism in the adult fly head.
Highlights
Organisms on Earth have evolved an internal timekeeping system, or circadian clock, that allows them to both respond to and predict changes in the 24h environmental day
To act as reliable time-keeping mechanisms, circadian clocks have to be able to synchronize to environmental time cues, maintain ;24-h rhythms under constant conditions, run at approximately the same pace over a range of environmental temperatures, and efficiently communicate time-of-day information to other biological systems
Clock-controlled oscillations in gene expression play an essential role in producing overt circadian rhythms
Summary
Organisms on Earth have evolved an internal timekeeping system, or circadian clock (circa 1⁄4 about, diem 1⁄4 day), that allows them to both respond to and predict changes in the 24h environmental day. Proteins encoded by the latter four genes either suppress or activate CLK and CYC [2,3,4,5,6,7,8] Feedback in these regulatory loops is thought to oscillate due to timed changes in the stabilities and subcellular localizations of component proteins, especially Period (PER) and Timeless (TIM) [9,10]. The fly molecular clock is aligned to the environment through Zeitgebers (‘‘time givers’’), the most notable being the daily light/dark cycle. This is mediated by the light-dependent degradation of the TIM protein [11,12]. A second pathway of light entrainment in the pacemaker neurons is defined by signals from visual organs that may impact TIM in a CRY-independent manner [13,16]
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