EYES ABSENT and TIMELESS integrate photoperiodic and temperature cues to regulate seasonal physiology inDrosophila

Abstract

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.

Model and Non-model Insects in Chronobiology

“…Both properties are advantageous for a life in the north. A very recent study supports the role of TIM in dormancy of D. melanogaster (Abrieux et al, 2020). The authors showed 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 under long photoperiods.…”

CK2 Inhibits TIMELESS Nuclear Export and Modulates CLOCK Transcriptional Activity to Regulate Circadian Rhythms

“…The luciferase reporter was removed using MluI/XhoI restriction sites, and a 3XFLAG-6XHIS epitope was added in frame to the C terminus of the tim coding region. PhiC31 site-directed recombination 88 was used for transgenesis to generate yw; tim 0 ; tim(WT) (also described in 82 ). Plasmids were injected into yw fly embryos carrying attP sites on chromosome 3 (attP2) (BestGene, Chino Hills, CA).…”

Temperature-Dependent Alternative Splicing of Precursor mRNAs and Its Biological Significance: A Review Focused on Post-Transcriptional Regulation of a Cold Shock Protein Gene in Hibernating Mammals

“…In addition to investigations of circadian clock genes in plants, it has also been shown that temperature-dependent alternative splicing is essential for the regulation of circadian clock in Neurospora, Drosophila, tilapia and mice [ 66 , 67 , 68 , 69 , 70 , 71 , 72 , 73 , 74 , 75 , 76 ]. These findings suggest that alternative splicing is a general mechanism of clock regulation.…”

“…In Drosophila, period (PER) and timeless (TIM) protein and mRNA products undergo daily fluctuations in relation to the circadian clock [ 66 , 71 , 73 , 74 , 77 ]. Majercak et al showed that temperature-dependent alternative splicing in the PER gene plays a key role in adaptation of a circadian clock to seasonally cold days (low temperatures and short day lengths) in Drosophila [ 73 ].…”