Arabidopsis circadian clock genes control the rhythmicity and phase synchronization of the diel proteome to a greater degree than the diel transcriptome.
The plant circadian clock is a genetic circuit composed of multiple mutually-regulating transcription factors that together synchronize internal biological rhythms to the ~24-hour period of planetary rotation. While it has been known for over a decade that nearly 40% of the transcriptome in the model plant Arabidopsis oscillates with a circadian rhythm, it is yet unclear to what extent this translates to the proteome. Here, through parallel time course quantitative proteome and transcriptome profiling of Arabidopsis wild-type plants and a panel of clock gene knockout mutants, we show that specific clock genes exercise extensive control over rhythmic proteins, and to a much greater extent than they do rhythmic transcripts. This control results in a clock-dependent synchronization of rhythmic proteins along a bimodal phase distribution that is lost in circadian clock knockout mutants. This suggests pervasive post-translational control of gene expression by specific elements of the circadian system, notably the morning expressed LHY/CCA1 module. Our findings imply that the circadian clock exercises much greater control of gene expression through proteostasis mechanisms than previously recognised, necessitating a rethink in our current understanding of clock proteins as primarily transcriptional regulators.