Sumoylation Contributes to Timekeeping and Temperature Compensation of the Plant Circadian Clock

Abstract

The transcriptional circadian clock network is tuned into a 24-h oscillator by numerous posttranslational modifications on the proteins encoded by clock genes, differentially influencing their subcellular localization or activity. Clock proteins in any circadian organism are subject to posttranslational regulation, and many of the key enzymes, notably kinases and phosphatases, are functionally conserved between the clocks of mammals, fungi, and plants. We now establish sumoylation, the posttranslational modification of target proteins by the covalent attachment of the small ubiquitin-like modifier protein SUMO, as a novel mechanism regulating key clock properties in the model plant Arabidopsis. Using 2 different approaches, we show that mutant plant lines with decreased or increased levels of global sumoylation exhibit shortened or lengthened circadian period, respectively. One known functional role of sumoylation is to protect the proteome from temperature stress. The circadian clock is characterized by temperature compensation, meaning that proper timekeeping is ensured over the full range of physiologically relevant temperatures. Interestingly, we observed that the period defects in sumoylation mutant plants are strongly differential across temperature. Increased global sumoylation leads to undercompensation of the clock against temperature and decreased sumoylation to overcompensation, implying that sumoylation buffers the plant clock system against differential ambient temperature.