A photoregulatory mechanism of the circadian clock in Arabidopsis

Abstract

Cryptochromes (CRYs) are photoreceptors that mediate light regulation of the circadian clock in plants and animals. Here we show that CRYs mediate blue-light regulation of N⁶-methyladenosine (m⁶A) modification of more than 10% of messenger RNAs in the Arabidopsis transcriptome, especially those regulated by the circadian clock. CRY2 interacts with three subunits of the METTL3/14-type N⁶-methyladenosine RNA methyltransferase (m⁶A writer): MTA, MTB and FIP37. Photo-excited CRY2 undergoes liquid-liquid phase separation (LLPS) to co-condense m⁶A writer proteins in vivo, without obviously altering the affinity between CRY2 and the writer proteins. mta and cry1cry2 mutants share common defects of a lengthened circadian period, reduced m⁶A RNA methylation and accelerated degradation of mRNA encoding the core component of the molecular oscillator circadian clock associated 1 (CCA1). These results argue for a photoregulatory mechanism by which light-induced phase separation of CRYs modulates m⁶A writer activity, mRNA methylation and abundance, and the circadian rhythms in plants.