Abstract:Highlights d The Chymomyza genus carries the ancestral low-latitude D. melanogaster-like clock d C. costata colonized high latitudes despite a low-latitude clock neuroarchitecture d High-latitude drosophilids show arrhythmicity in constant darkness d C. costata and D. ezoana achieve arrhythmicity via different strategies
“…In addition, daily cycling of eya mRNA was abolished in free-running condition, suggesting that eya transcription is not clock-controlled. This is consistent with recent findings suggesting that photoperiodic sensing appears independent of robust circadian clocks (55). Among the potential pathways involved in regulating eya transcription, Pigment Dispersing Factor (PDF) signaling represents a strong candidate.…”
Organisms possess photoperiodic timing mechanisms to anticipate variations in day length and temperature as the seasons progress. The nature of the molecular mechanisms interpreting and signaling these environmental changes to elicit downstream neuroendocrine and physiological responses are just starting to emerge. Here, we demonstrate that in Drosophila melanogaster, EYES ABSENT (EYA) acts as a seasonal sensor by interpreting photoperiodic and temperature changes to trigger appropriate physiological responses. We observed that tissue-specific genetic manipulation of eya expression is sufficient to disrupt the ability of flies to sense seasonal cues, thereby altering the extent of female reproductive dormancy. Specifically we observed that EYA proteins, which peak at night in short photoperiod and accumulate at higher levels in the cold, promote reproductive dormancy in female D. melanogaster. Furthermore, we provide evidence indicating that the role of EYA in photoperiodism and temperature sensing is aided by the stabilizing action of the light-sensitive circadian clock protein TIMELESS (TIM). We postulate that increased stability and level of TIM at night under short photoperiod together with the production of cold-induced and light-insensitive TIM isoforms facilitate EYA accumulation in winter conditions. This is supported by our observations that tim null mutants exhibit reduced incidence of reproductive dormancy in simulated winter conditions, while flies overexpressing tim show an increased incidence of reproductive dormancy even in long photoperiod.Significance StatementExtracting information on calendar time from seasonal changes in photoperiod and temperature is critical for organisms to maintain circannual cycles in physiology and behavior. Here we found that in flies, EYES ABSENT (EYA) protein act as a seasonal sensor by adjusting its abundance and circadian phase in response to changes in photoperiod and temperature. We show that the manipulation of EYA levels is sufficient to impair the ability of female Drosophila to regulate seasonal variation in reproductive dormancy. Finally, our results suggest an important role of the circadian clock protein TIMELESS (TIM) in modulating EYA level through its ability to measure night length, linking the circadian clock to seasonal timing.
“…In addition, daily cycling of eya mRNA was abolished in free-running condition, suggesting that eya transcription is not clock-controlled. This is consistent with recent findings suggesting that photoperiodic sensing appears independent of robust circadian clocks (55). Among the potential pathways involved in regulating eya transcription, Pigment Dispersing Factor (PDF) signaling represents a strong candidate.…”
Organisms possess photoperiodic timing mechanisms to anticipate variations in day length and temperature as the seasons progress. The nature of the molecular mechanisms interpreting and signaling these environmental changes to elicit downstream neuroendocrine and physiological responses are just starting to emerge. Here, we demonstrate that in Drosophila melanogaster, EYES ABSENT (EYA) acts as a seasonal sensor by interpreting photoperiodic and temperature changes to trigger appropriate physiological responses. We observed that tissue-specific genetic manipulation of eya expression is sufficient to disrupt the ability of flies to sense seasonal cues, thereby altering the extent of female reproductive dormancy. Specifically we observed that EYA proteins, which peak at night in short photoperiod and accumulate at higher levels in the cold, promote reproductive dormancy in female D. melanogaster. Furthermore, we provide evidence indicating that the role of EYA in photoperiodism and temperature sensing is aided by the stabilizing action of the light-sensitive circadian clock protein TIMELESS (TIM). We postulate that increased stability and level of TIM at night under short photoperiod together with the production of cold-induced and light-insensitive TIM isoforms facilitate EYA accumulation in winter conditions. This is supported by our observations that tim null mutants exhibit reduced incidence of reproductive dormancy in simulated winter conditions, while flies overexpressing tim show an increased incidence of reproductive dormancy even in long photoperiod.Significance StatementExtracting information on calendar time from seasonal changes in photoperiod and temperature is critical for organisms to maintain circannual cycles in physiology and behavior. Here we found that in flies, EYES ABSENT (EYA) protein act as a seasonal sensor by adjusting its abundance and circadian phase in response to changes in photoperiod and temperature. We show that the manipulation of EYA levels is sufficient to impair the ability of female Drosophila to regulate seasonal variation in reproductive dormancy. Finally, our results suggest an important role of the circadian clock protein TIMELESS (TIM) in modulating EYA level through its ability to measure night length, linking the circadian clock to seasonal timing.
“…In addition, daily cycling of eya mRNA was abolished in free-running condition, suggesting that eya transcription is not clock controlled. This is consistent with recent findings suggesting that photoperiodic sensing appears to be independent of robust circadian clocks (55). Among the potential pathways involved in regulating eya transcription, Pigment Dispersing Factor (PDF) signaling represents a strong candidate.…”
Organisms possess photoperiodic timing mechanisms to detect variations in day length and temperature as the seasons progress. The nature of the molecular mechanisms interpreting and signaling these environmental changes to elicit downstream neuroendocrine and physiological responses are just starting to emerge. Here, we demonstrate that, inDrosophila melanogaster, EYES ABSENT (EYA) acts as a seasonal sensor by interpreting photoperiodic and temperature changes to trigger appropriate physiological responses. We observed that tissue-specific genetic manipulation ofeyaexpression is sufficient to disrupt the ability of flies to sense seasonal cues, thereby altering the extent of female reproductive dormancy. Specifically, we observed that EYA proteins, which peak at night in short photoperiod and accumulate at higher levels in the cold, promote reproductive dormancy in femaleD. melanogaster. Furthermore, we provide evidence indicating that the role of EYA in photoperiodism and temperature sensing is aided by the stabilizing action of the light-sensitive circadian clock protein TIMELESS (TIM). We postulate that increased stability and level of TIM at night under short photoperiod together with the production of cold-induced and light-insensitive TIM isoforms facilitate EYA accumulation in winter conditions. This is supported by our observations thattimnull mutants exhibit reduced incidence of reproductive dormancy in simulated winter conditions, while flies overexpressingtimshow an increased incidence of reproductive dormancy even in long photoperiod.
“…17 However, organisms living in weakly rhythmic environments, such as polar and high-latitude areas, may show weaker circadian rhythms during some part of the year than those in less extreme environments, such as low-latitude environments, because of evolutionary adaptation. 18 At the molecular level, circadian rhythmicity is generated by transcriptional-translational feedback loops 2 (Figure 1). Firstly, the formation of the circadian locomotor output cycles kaput gene (Clock) and brain and muscle Arnt like protein-1 (Bmal1) heterodimer promotes the expression of Period (Per, including Per1, Per2, and Per3) and Cryptochrome (Cry, including Cry1 and Cry2) by binding an enhancer E-box (5'-CACGTG-3') in their regulatory regions.…”
Almost all living organisms have evolved autoregulatory transcriptional‐translational feedback loops that produce oscillations with a period of approximately 24‐h. These endogenous time keeping mechanisms are called circadian clocks. The main function of these circadian clocks is to drive overt circadian rhythms in the physiology of the organisms to ensure that main physiological functions are in synchrony with the external environment. Disruption of circadian rhythms caused by genetic or environmental factors has long‐term consequences for metabolic health. Of relevance, host circadian rhythmicity and lipid metabolism are increasingly recognized to cross‐regulate and the circadian clock‐lipid metabolism interplay may involve in the development of obesity. Multiple systemic and molecular mechanisms, such as hormones (ie, melatonin, leptin, and glucocorticoid), the gut microbiome, and energy metabolism, link the circadian clock and lipid metabolism, and predictably, the deregulation of circadian clock‐lipid metabolism interplay can increase the risk of obesity, which in turn may exacerbate circadian disorganization. Feeding time and dietary nutrients are two of key environmental Zeitgebers affecting the circadian rhythm‐lipid metabolism interplay, and the influencing mechanisms in obesity development are highlighted in this review. Together, the characterization of the clock machinery in lipid metabolism aimed at producing a healthy circadian lifestyle may improve obesity care.
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