4.6 Article

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

Journal

MOLECULAR SYSTEMS BIOLOGY
Volume 18, Issue 3, Pages -

Publisher

WILEY
DOI: 10.15252/msb.202010140

Keywords

circadian clock; coordination; coupling; noise; plant

Funding

  1. Gatsby Charitable Foundation [GAT3395/GLC]
  2. Japan Society for the Promotion of Science [17H06313, 18H02477, 20K11875]
  3. Grants-in-Aid for Scientific Research [18H02477, 17H06313, 20K11875] Funding Source: KAKEN

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Individual plant cells possess a circadian clock that times internal processes to the day-night cycle. This clock is regulated by a genetic network and is sensitive to light. The cells communicate their timing through local or long-distance sharing of clock components, allowing for spatial coordination. Local coupling minimizes timing errors caused by noisy light-dark cycles and maintains different clock phases in different plant regions.
Individual plant cells possess a genetic network, the circadian clock, that times internal processes to the day-night cycle. Mathematical models of the clock are typically either whole-plant that ignore tissue or cell type-specific clock behavior, or phase-only that do not include molecular components. To address the complex spatial coordination observed in experiments, here we implemented a clock network model on a template of a seedling. In our model, the sensitivity to light varies across the plant, and cells communicate their timing via local or long-distance sharing of clock components, causing their rhythms to couple. We found that both varied light sensitivity and long-distance coupling could generate period differences between organs, while local coupling was required to generate the spatial waves of clock gene expression observed experimentally. We then examined our model under noisy light-dark cycles and found that local coupling minimized timing errors caused by the noise while allowing each plant region to maintain a different clock phase. Thus, local sensitivity to environmental inputs combined with local coupling enables flexible yet robust circadian timing.

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