Daily temperature cycles prolong lifespan and have sex-specific effects on peripheral clock gene expression in Drosophila melanogaster

Abstract

Circadian rhythms optimize health by coordinating the timing of physiological processes to match predictable daily environmental challenges. The circadian rhythm of body temperature is thought to be an important modulator of molecular clocks in peripheral tissues, but how daily temperature cycles impact physiological function is unclear. Here, we examined the effect of constant (25°C, TCON) and cycling (28°C/22°C during light/dark, TCYC) temperature paradigms on lifespan of Drosophila melanogaster, and the expression of clock genes, Heat shock protein 83 (Hsp83), Frost (Fst), and Senescence-associated protein 30 (smp-30). Male and female Drosophila housed at TCYC had longer median lifespans than those housed at TCON. TCYC induced robust Hsp83 rhythms and rescued the age-related decrease in smp-30 expression that was observed in flies at TCON, potentially indicating an increased capacity to cope with age-related cellular stress. Ageing under TCON led to a decrease in the amplitude of expression of all clock genes in the bodies of male flies, except for cyc, which was non-rhythmic, and for per and cry in female flies. Strikingly, housing under TCYC conditions rescued the age-related decrease in amplitude of all clock genes, and generated rhythmicity in cyc expression, in the male flies, but not the female flies. The results suggest that ambient temperature rhythms modulate Drosophila lifespan, and that the amplitude of clock gene expression in peripheral body clocks may be a potential link between temperature rhythms and longevity in male Drosophila. Longevity due to TCYC appeared predominantly independent of clock gene amplitude in female Drosophila.

Temperature-driven coordination of circadian transcriptional regulation

“…Second, our work demonstrates that a long–lasting temperature change, spanning multiple days, can alter circadian transcriptional regulation. This complements previous studies demonstrating that diurnal temperature cycles can also drive the cyclic expression of genes [ 14 , 53 , 54 ]. By assaying gene expression at constant temperatures, we isolate temperature–specific circadian oscillations from temperature–driven cycling.…”

Discovery and Visualization of Age-dependent Patterns in the Diurnal Transcriptome of Drosophila

“…Among the RLCs we found the core clock transcripts, Clk-RA, tim-RB, tim-RM, tim-RO, per-RA, Pdp1-RJ, Pdp1-RD, Pdp1-RP, vri-RA and vri-RE, indicating that the circadian clock remains rhythmic with age. Unexpectedly, we also detected rhythmicity in the cycle gene (cyc-RA), which has been considered the only clock gene with no discernable cycling [20,21]. In addition to clock transcripts, RLCs contained transcripts derived from 105 genes that were previously identified as clock-controlled in heads of young flies [17], supporting the notion that the circadian clock remains functional with age.…”

Circadian and seasonal changes in the expression of clock genes in the ovine pars tuberalis

“…It was found that housing under cycling temperature conditions rescued the age-related decrease in the amplitude of almost all clock genes in male flies, but not female flies. This suggests that the effect of temperature on peripheral clock gene expression may be sexspecific (Goh et al, 2021). However, a study on warm-blooded animals -mice -did not show such a significant effect of environmental temperature conditions on the expression of clock genes in the liver of animals (Rabearivony et al, 2020).…”