Drosophila PSI controls circadian period and the phase of circadian behavior under temperature cycle via tim splicing

Foley, Lauren E.; Ling, Jinli; Joshi, Radhika; Evantal, Naveh; Kadener, Sebastián; Emery, Patrick

doi:10.7554/elife.50063

Cited by 26 publications

(31 citation statements)

References 67 publications

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“…This agrees with the transcriptomic analysis of a recent publication that reveals an upregulation of eya in flies exposed to short photoperiod (10 L:14D) at 11°C for 3 wk when compared to reproductively active condition (25°C, 12 L:12D) (65). In light of the recent evidence on tim thermosensitive alternative splicing (37,38,66), we were able to confirm the induction of the tim-sc mRNA and protein at 10°C. Consistent with our model, our results support the prevalent role of the cold-induced TIM-SC isoforms in stabilizing EYA under low temperature and suggest that TIM thermosensitive splicing mechanism plays a role in regulating seasonal physiology.…”

Section: Discussionsupporting

confidence: 91%

“…At 10 °C, canonical TIM was barely detectable using our TIM antibody when compared to TIM levels at 25 °C, and no other isoforms were detected. Concomitantly, recent studies revealed that tim undergoes a thermosensitive alternative splicing controlling the relative abundance of various tim isoforms ( 37 , 38 ). Consistent with our observation, the authors found lower levels of the canonical TIM protein at 18 °C and revealed the induction of two cold-specific splice forms ( tim-cold and tim-short&cold ).…”

Section: Resultsmentioning

confidence: 99%

See 1 more Smart Citation

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

Abrieux

Xue

Cai

et al. 2020

Proc. Natl. Acad. Sci. U.S.A.

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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.

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Section: Discussionsupporting

confidence: 91%

Section: Resultsmentioning

confidence: 99%

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

Abrieux

Xue

Cai

et al. 2020

Proc. Natl. Acad. Sci. U.S.A.

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show abstract

“…This agrees with the transcriptomic analysis of a recent publication that reveals an upregulation of eya in flies exposed to short photoperiod (10 L:14D) at 11°C for 3 weeks when compared to reproductively active condition (25°C, 12 L:12D) (65). In light of the recent evidence on tim thermosensitive alternative splicing (37, 38, 66), we were able to confirm the induction of the tim-sc mRNA and protein at 10°C. Consistent with our model, our results support the prevalent role of the cold-induced TIM-SC isoforms in stabilizing EYA under low temperature and suggest that TIM thermosensitive splicing mechanism plays a role in regulating seasonal physiology.…”

Section: Discussionsupporting

confidence: 52%

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

Abrieux

Xue

Cai

et al. 2020

Preprint

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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.

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“…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 ].…”

Section: Regulation Of Gene Expression By Temperature-dependent Almentioning

confidence: 99%

“…Foley et al demonstrated that the alternative splicing regulator P-element somatic inhibitor (PSI) regulates the temperature-dependent alternative splicing of TIM in Drosophila, regulating the period of circadian rhythms and circadian behavior phase during temperature cycling [ 77 ].…”

Section: Molecular Mechanism Of Temperature-dependent Alternative mentioning

confidence: 99%

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

Shiina

Shimizu

2020

IJMS

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Multiple mRNA isoforms are often generated during processing such as alternative splicing of precursor mRNAs (pre-mRNA), resulting in a diversity of generated proteins. Alternative splicing is an essential mechanism for the functional complexity of eukaryotes. Temperature, which is involved in all life activities at various levels, is one of regulatory factors for controlling patterns of alternative splicing. Temperature-dependent alternative splicing is associated with various phenotypes such as flowering and circadian clock in plants and sex determination in poikilothermic animals. In some specific situations, temperature-dependent alternative splicing can be evoked even in homothermal animals. For example, the splicing pattern of mRNA for a cold shock protein, cold-inducible RNA-binding protein (CIRP or CIRBP), is changed in response to a marked drop in body temperature during hibernation of hamsters. In this review, we describe the current knowledge about mechanisms and functions of temperature-dependent alternative splicing in plants and animals. Then we discuss the physiological significance of hypothermia-induced alternative splicing of a cold shock protein gene in hibernating and non-hibernating animals.

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Drosophila PSI controls circadian period and the phase of circadian behavior under temperature cycle via tim splicing

Cited by 26 publications

References 67 publications

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

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

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

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

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