Abstract
Drosophila melanogaster exhibits circadian (≅24 hr) regulated morning and evening bouts of activity that are separated by a mid-day siesta. Increases in daily ambient temperature are accompanied by a progressively longer mid-day siesta and delayed evening activity. Presumably, this behavioral plasticity reflects an adaptive response that endows D. melanogaster with the ability to temporally optimize daily activity levels over a wide range of physiologically relevant temperatures. For example, the shift in activity towards the cooler nighttime hours on hot days might minimize the risks associated with exposure to mid-day heat, whereas on cold days activity is favored during the warmer daytime hours. These temperature-induced shifts in the distribution of daily activity are partly based on the thermal sensitive splicing of an intron found in the 3′ untranslated region (UTR) of the circadian clock gene termed period (per). As temperature decreases, splicing of this 3′-terminal intron (termed dmpi8) is gradually increased, which is causally linked to a shorter mid-day siesta. Herein we identify several natural polymorphisms in the per 3′ UTR from wild-caught populations of flies originating along the east coast of the United States. Two non-intronic closely spaced single nucleotide polymorphisms (SNPs) modulate dmpi8 splicing efficiency, with the least efficiently spliced version associated with a longer mid-day siesta, especially at lower temperatures. Although these SNPs modulate the splicing efficiency of dmpi8 they have little to no effect on its thermal responsiveness, consistent with the notion that the suboptimal 5′ and 3′ splice sites of the dmpi8 intron are the primary cis-acting elements mediating temperature regulation. Our results demonstrate that natural variations in the per gene can modulate the splicing efficiency of the dmpi8 intron and the daily distribution of activity, providing natural examples for the involvement of dmpi8 splicing in the thermal adaptation of behavioral programs in D. melanogaster.
Highlights
Wake-sleep cycles in animals are governed by networks of cell-based circadian (>24 hr) ‘clocks’ or pacemakers located in the brain
All the dper 39 untranslated region (UTR) we analyzed from these natural populations have a sized dmpi8 intron (86 or 89 bp in length) approximately 100 bp downstream of the translation stop codon, with identical suboptimal 59 and 39ss, including the same branchpoint signal (BPS) (Fig. 1A and data not shown)
The key splicing signals of the dmpi8 intron appear highly conserved in D. melanogaster, we identified two major haplotypes of the dper 39 UTR that differ from each other by six polymorphisms (Fig. 1A and data not shown)
Summary
Wake-sleep cycles in animals are governed by networks of cell-based circadian (>24 hr) ‘clocks’ or pacemakers located in the brain. The increased mid-day activity of flies on cold days might be an adaptive response to maximize activity during the warmer daytimes hours, whereas suppressing mid-day activity with a concomitant shift towards the cooler nighttime hours on warm days might minimize the risks associated with unnecessary energy expenditure during the hot mid-day sun We showed that this temperature-dependent behavioral adaptation is at least partially controlled by thermosensitive splicing of a 39-terminal intron from the Drosophila melanogaster period (dper) transcript [3,5], which is a key circadian clock factor known for encoding species-specific circadian behavioral programs in this species [3,6,7,8]. The removal of a short intron in the 39 untranslated region (UTR) of dper RNA, named dmpi (D. melanogaster per intron 8), is inefficient at warmer temperatures, which attenuates the daily accumulation of dper mRNA, somehow leading to delayed evening activity and longer mid-day siesta [3,5]
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