Abstract
Neuropeptides play pivotal roles in modulating circadian rhythms. Pigment-dispersing factor (PDF) is critical to the circadian rhythms in Drosophila locomotor activity. Here, we demonstrate that diuretic hormone 31 (DH31) complements PDF function in regulating free-running rhythmicity using male flies. We determined that Dh31 loss-of-function mutants (Dh31#51) showed normal rhythmicity, whereas Dh31#51;Pdf01 double mutants exhibited a severe arrhythmic phenotype compared to Pdf-null mutants (Pdf01). The expression of tethered-PDF or tethered-DH31 in clock cells, posterior dorsal neurons 1 (DN1ps), overcomes the severe arrhythmicity of Dh31#51;Pdf01 double mutants, suggesting that DH31 and PDF may act on DN1ps to regulate free-running rhythmicity in a hierarchical manner. Unexpectedly, the molecular oscillations in Dh31#51;Pdf01 mutants were similar to those in Pdf01 mutants in DN1ps, indicating that DH31 does not contribute to molecular oscillations. Furthermore, a reduction in Dh31 receptor (Dh31r) expression resulted in normal locomotor activity and did not enhance the arrhythmic phenotype caused by the Pdf receptor (Pdfr) mutation, suggesting that PDFR, but not DH31R, in DN1ps mainly regulates free-running rhythmicity. Taken together, we identify a novel role of DH31, in which DH31 and PDF hierarchically regulate free-running rhythmicity through DN1ps.
Highlights
In Drosophila, pigment-dispersing factor (PDF) is required for robust locomotor behavioral output[1]
To re-evaluate the function of diuretic hormone 31 (DH31) in regulating the circadian rhythms of locomotor activity, we focused on a double mutant of Dh31#5116 and Pdf[017] and examined the phenotypes for rhythmicity, free-running period, morning anticipation and evening activity peaks
We subsequently focused on DN1s because small LNvs project to DN1s20–22, Pigment-dispersing factor (PDF) acts on DN1ps to regulate locomotor activity[22,23], and Pdf receptor (Pdfr) expression in DN1ps restores the dampened free-running rhythm in Pdfr mutant flies[23]
Summary
In Drosophila, pigment-dispersing factor (PDF) is required for robust locomotor behavioral output[1]. In the absence of PDF (Pdf01), flies show a loss of morning anticipation, an advanced evening activity peak, shorter free-running periods, and dampened molecular oscillations in clock cells[7,8,9,10,11], suggesting that PDF is a main neuropeptide responsible for orchestrating the activity of each pacemaker neuron. We hypothesized that normal locomotor activity rhythms in Dh31 single mutants might be a result of normal PDF signaling. We determined that PDF and DH31 hierarchically function to regulate free-running rhythmicity by acting on the same clock cells (DN1ps). These neuropeptides appear to play important roles in modulating the clock networks involved in free-running rhythmicity. The identification of this novel DH31 function deepens our mechanistic understanding of the circadian rhythms of locomotor activity
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