Integration of Light and Temperature in the Regulation of Circadian Gene Expression in Drosophila

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.

Temperature-dependent resetting of the molecular circadian oscillator inDrosophila

“…Analyses were conducted for w 1118 control flies as well as two experimental genotypes, Hsp90 e6D/08445 and y w; tim 01 ; ftim P -tim cDNA g ('Tim 4 0 ), for which we observed accelerated temperature re-entrainment in behavioural analyses as outlined below. Transcript profiling of adult Drosophila heads revealed wide-spread temperature-driven as well as temperatureentrained circadian responses [2]. Notably, a set of heat-induced transcripts associated with the HSF1/HSP90 pathway was found to cycle in both wild-type and arrhythmic tim 01 mutant heads.…”

Synchronization of theDrosophilaCircadian Clock by Temperature Cycles

“…3), Boothroyd et al (2007) demonstrated temperatureentrained mRNA rhythms of all clock gene transcripts that also oscillate in LD cycles (per,tim,Clk,vri,cry,and Pdp1). The discrepancy could be explained by the difference in the experimental design.…”

“…1b) (Glaser and Stanewsky 2005). Moreover, in a microarray study of Drosophila genes expressed rhythmically in temperature cycles, Boothroyd et al (2007) discovered that in tim 01 flies, some of the crucial clock or clock-input genes (per, tim, Clk, and cry) are rhythmically expressed during a temperature cycle but not after release into constant conditions.…”

“…Despite these findings pointing to a prominent role of posttranscriptional mechanisms in temperature entrainment, a recent study revealed substantial rhythmic mRNA regulation using whole-genome microarrays (Boothroyd et al 2007). These authors discovered that the majority of the transcripts that oscillated in temperature cycles and DD conditions where temperature-driven.…”

“…For example, in temperature cycles, fly locomotor activity shows rapid increases immediately after the temperature transitions even in flies that do not possess a functional clock (Fig. 1b) (see, e.g., Wheeler et al 1993;Glaser and Stanewsky 2005), and transcription of many Drosophila genes can be driven by temperature cycles (Boothroyd et al 2007; see below). either mutant or lacking the cry gene but having normal eyes (Stanewsky et al 1998;Dolezelova et al 2007).…”