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A wide range of organisms features molecular machines, circadian clocks,which generate endogenous oscillations with ~24 h periodicity and therebysynchronize biological processes to diurnal environmental fluctuations.Recently, it has become clear that plants harbor more complex gene regulatorycircuits within the core circadian clocks than other organisms, inspiring afundamental question: are all these regulatory interactions between clock genesequally crucial for the establishment and maintenance of circadian rhythms? Ourmechanistic simulation for Arabidopsis thaliana demonstrates that at least halfof the total regulatory interactions must be present to express the circadianmolecular profiles observed in wild-type plants. A set of those essentialinteractions is called herein a kernel of the circadian system. The kernelstructure unbiasedly reveals four interlocked negative feedback loopscontributing to circadian rhythms, and three feedback loops among them drivethe autonomous oscillation itself. Strikingly, the kernel structure, as well asthe whole clock circuitry, is overwhelmingly composed of inhibitory, ratherthan activating, interactions between genes. We found that this tendencyunderlies plant circadian molecular profiles which often exhibitsharply-shaped, cuspidate waveforms. Through the generation of these cuspidateprofiles, inhibitory interactions may facilitate the global coordination oftemporally-distant clock events that are markedly peaked at very specific timesof day. Our systematic approach resulting in experimentally-testablepredictions provides insights into a design principle of biological clockwork,with implications for synthetic biology.

Kernel Architecture of the Genetic Circuitry of the Arabidopsis Circadian System