Journal Article

Drosophila Ionotropic Receptor 25a mediates circadian clock resetting by temperature

Chen, Chenghao, Croset, Vincent, Buhl, Edgar, Benton, Richard, Xu, Min, Hodge, James J. L., Stanewsky, Ralf, Lilley, Kathryn S., Rees, Johanna S.

2015

Overview

A Drosophila chemosensory receptor, expressed in leg sensory neurons, is necessary for behavioural and molecular synchronization of the fly’s circadian clock to low-amplitude temperature cycles; this temperature-sensing pathway functions independently from the known temperature sensors of the fly’s antennae. Temperature rhythm sets the body clock The roughly 24-hour period of circadian clocks is largely independent of ambient temperature but the phase can be synchronized, in the absence of light variations, to the cycle of warmer (day) and colder (night) temperatures, with a sensitivity as fine as ±2° C. Now Ralf Stanewsky and colleagues identify the chemosensory receptor IR25a, expressed in internal stretch (chordotonal) sensory neurons in the leg of Drosophila , as necessary for both behavioural and molecular synchronization of the animal's circadian clock to low-amplitude temperature cycles. They further show that this new temperature-sensing pathway functions independently from the known temperature sensors of the fly's antennas. Circadian clocks are endogenous timers adjusting behaviour and physiology with the solar day 1 . Synchronized circadian clocks improve fitness 2 and are crucial for our physical and mental well-being 3 . Visual and non-visual photoreceptors are responsible for synchronizing circadian clocks to light 4 , 5 , but clock-resetting is also achieved by alternating day and night temperatures with only 2–4 °C difference 6 , 7 , 8 . This temperature sensitivity is remarkable considering that the circadian clock period (~24 h) is largely independent of surrounding ambient temperatures 1 , 8 . Here we show that Drosophila Ionotropic Receptor 25a (IR25a) is required for behavioural synchronization to low-amplitude temperature cycles. This channel is expressed in sensory neurons of internal stretch receptors previously implicated in temperature synchronization of the circadian clock 9 . IR25a is required for temperature-synchronized clock protein oscillations in subsets of central clock neurons. Extracellular leg nerve recordings reveal temperature- and IR25a-dependent sensory responses, and IR25a misexpression confers temperature-dependent firing of heterologous neurons. We propose that IR25a is part of an input pathway to the circadian clock that detects small temperature differences. This pathway operates in the absence of known ‘hot’ and ‘cold’ sensors in the Drosophila antenna 10 , 11 , revealing the existence of novel periphery-to-brain temperature signalling channels.

• Publisher: Nature Publishing Group UK,Nature Publishing Group
• Subject: 631/378/1385/1330 / 631/378/3917 / Ambient temperature / Animals / Atmospheric temperature / Circadian Clocks - physiology / Circadian rhythm / Circadian Rhythm - physiology / Circadian rhythms / CLOCK Proteins - metabolism / Drosophila / Drosophila melanogaster - cytology / Drosophila melanogaster - physiology / Drosophila Proteins - genetics / Drosophila Proteins - metabolism / Environmental aspects / Extremities - innervation / Female / Humanities and Social Sciences / Insects / Ion channels / letter / Male / Mechanoreceptors - cytology / Mechanoreceptors - metabolism / multidisciplinary / Neurons / Physiological aspects / Receptors, Ionotropic Glutamate - genetics / Receptors, Ionotropic Glutamate - metabolism / Science / Sensory Receptor Cells - metabolism / Temperature