A spatial model of the plant circadian clock reveals design principles for coordinated timing under noisy environments

Abstract

Individual plant cells possess a genetic network, the circadian clock, that times internal processes to the day-night cycle. Mathematical models of the clock network have driven a mechanistic understanding of the clock in plants. However, these models are typically either whole plant models that ignore tissue or cell type specific clock behavior, or phase only models that do not include clock network components explicitly. It is increasingly clear that in order to reveal the design principles of the plant circadian clock, clock network models must address spatial differences. This is because complex spatial behaviours have been observed in tissues and cells in plants, including period and phase differences between cells and spatial waves of gene expression between organs. Here, we implement an up to date clock network model on a spatial template of the plant. In our model, the sensitivity to light inputs varies across the plant, and cells communicate their clock timing locally via the levels of core clock mRNA levels by cell-to-cell coupling. We found that differences in sensitivities to environmental input in the model can explain the experimentally observed differences in clock periods in different organs, and we show using the model that a plausible coupling mechanism can generate the experimentally observed waves in clock gene expression across the plant. We then examined what features of the plant circadian system allow it to keep time under noisy light-dark (LD) cycles. We found that differences in sensitivity to light can allow regional flexibility in phase even under LD cycles, whilst local cell-to-cell coupling minimized variability in clock rhythms in neighboring cells. Thus, local sensitivity to environmental inputs combined with cell-to-cell coupling allows for flexible yet robust circadian timing under noisy environments.