Abstract
BackgroundCircadian clocks are internal daily time keeping mechanisms that allow organisms to anticipate daily changes in their environment and to organize their behavior and physiology in a coherent schedule. Although circadian clocks use temperature compensation mechanisms to maintain the same pace over a range of temperatures, they are also capable of synchronizing to daily temperature cycles. This study identifies key properties of this process.ResultsGradually ramping daily temperature cycles are shown here to synchronize behavioral and molecular daily rhythms in Drosophila with a remarkable efficiency. Entrainment to daily temperature gradients of amplitudes as low as 4°C persisted even in the context of environmental profiles that also included continuous gradual increases or decreases in absolute temperature. To determine which elements of daily temperature gradients acted as the key determinants of circadian activity phase, comparative analyses of daily temperature gradients with different wave forms were performed. The phases of ascending and descending temperature acted together as key determinants of entrained circadian phase. In addition, circadian phase was found to be modulated by the relative temperature of release into free running conditions. Release at or close to the trough temperature of entrainment consistently resulted in phase advances. Re-entrainment to daily temperature gradients after large phase shifts occurred relatively slowly and required several cycles, allowing flies to selectively respond to periodic rather than anecdotal signals. The temperature-entrained phase relationship between clock gene expression rhythms and locomotor activity rhythms strongly resembled that previously observed for light entrainment. Moreover, daily temperature gradient and light/dark entrainment reinforced each other if the phases of ascending and descending temperature were in their natural alignment with the light and dark phases, respectively.ConclusionThe present study systematically examined the entrainment of clock-controlled behavior to daily environmental temperature gradients. As a result, a number of key properties of circadian temperature entrainment were identified. Collectively, these properties represent a circadian temperature entrainment mechanism that is optimized in its ability to detect the time-of-day information encoded in natural environmental temperature profiles. The molecular events synchronized to the daily phases of ascending and descending temperature are expected to play an important role in the mechanism of circadian entrainment to daily temperature cycles.
Highlights
Circadian clocks are internal daily time keeping mechanisms that allow organisms to anticipate daily changes in their environment and to organize their behavior and physiology in a coherent schedule
Peak locomotor activity synchronizes to peak temperature in a daily temperature gradient Analyses of temperature-entrained locomotor behavior such as those shown in Figure 1 suggested that the entrained activity peak phase was determined by the phase of the temperature maximum. This hypothesis was systematically tested by comparing the peak phase of synchronized locomotor activity with that of the entraining daily temperature gradient for eight different temperature protocols varying in amplitude, peak phase, absolute temperature, relative duration of thermophase, cryophase, temperature ascent or descent
The present study systematically examined the entrainment of clock-controlled behavior to daily environmental temperature gradients
Summary
Circadian clocks are internal daily time keeping mechanisms that allow organisms to anticipate daily changes in their environment and to organize their behavior and physiology in a coherent schedule. Internal daily biological timekeepers, termed circadian clocks, have evolved These circadian clocks provide organisms with the ability to reliably predict regular daily changes in their environment and to organize their bodily functions and behavior in a coherent daily schedule [1,2,3,4,5,6]. The defining properties of circadian clocks include (1) ~24-h (circadian) periodicity, (2) autonomous time keeping under constant conditions, (3) entrainment to environmental time cues such as light or temperature, (4) control of overt biological rhythms, and (5) maintenance of a constant pace over a range of environmental temperatures [1,2,3,4,5,6]. Elaborate posttranslational mechanisms are at work to ensure that gene expression oscillations are produced with a stable circadian period length
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