Abstract
The circadian clock is a biological mechanism that permits some organisms to anticipate daily environmental variations. This clock generates biological rhythms, which can be reset by environmental cues such as cycles of light or temperature, a process known as entrainment. After entrainment, circadian rhythms typically persist with approximately 24 hours periodicity in free-running conditions, i.e. in the absence of environmental cues. Experimental evidence also shows that a free-running period close to 24 hours is maintained across a range of temperatures, a process known as temperature compensation. In the plant Arabidopsis, the effect of light on the circadian system has been widely studied and successfully modelled mathematically. However, the role of temperature in periodicity, and the relationship between entrainment and compensation, are not fully understood. Here we adapt recent models to incorporate temperature dependence by applying Arrhenius equations to the parameters of the models that characterize transcription, translation, and degradation rates. We show that the resulting models can exhibit thermal entrainment and temperature compensation, but that these phenomena emerge from physiologically different sets of processes. Further simulations combining thermal and photic forcing in more realistic scenarios clearly distinguish between the processes of entrainment and compensation, and reveal temperature compensation as an emergent property which can arise as a result of multiple temperature-dependent interactions. Our results consistently point to the thermal sensitivity of degradation rates as driving compensation and entrainment across a range of conditions.
Highlights
The circadian clock is an interconnected network of biological processes needed for some organisms to anticipate daily environmental variations
Thermal entrainment to a 24 h period was not observed in cooler scenarios, and nor was it observed under warmer scenarios sharing the same 4°C variation. This behaviour is not unique for CLOCK ASSOCIATED 1 (CCA1)/LATE ELONGATED HYPOCOTYL (LHY); similar results were observed for ELF4/LUX, PRR9/PRR7, and PRR5/TOC1 (Figures 2, 3, and 4 in Supplementary Material)
The results demonstrate that dynamics in both of these environmental processes are instrumental in resultant clock dynamics, and that any theoretical or empirical assessment of the robustness of the clock to these changes needs to be viewed in an ecological context
Summary
The circadian clock is an interconnected network of biological processes needed for some organisms to anticipate daily environmental variations. The synchronization of the clock with the night/day cycle grants advantages such as growth and development in plants [1, 2, 3, 4, 5, 6], energy balance in mammals [7], conidium development in Neurospora [8], sleep modulation in Drosophila [9] and starvation response in Cyanobacteria [10] This biological system generates rhythmic gene expression, and mathematical models have helped to uncover the crucial molecular mechanisms of diverse living organisms [11, 12, 13, 14, 15, 16, 17, 18, 19, 20, 21]. These models have motivated hypotheses which, in parallel with experimental validation, have helped to establish not just the components of the network, and to elucidate their role [24, 35]
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