CCA1 alternative splicing as a way of linking the circadian clock to temperature response in Arabidopsis

Most living organisms on the earth have the circadian clock to synchronize their biochemical processes and physiological activities with environmental changes to optimize their propagation and survival. CIRCADIAN CLOCK-ASSOCIATED1 (CCA1) is one of the core clock components in Arabidopsis. Notably, it is also associated with cold acclimation. However, it is largely unknown how CCA1 activity is modulated by low temperatures. We found that the CCA1 activity is self-regulated by a splice variant CCA1 beta and the CCA1 beta production is modulated by low temperatures, linking the circadian clock with cold acclimation. CCA1 beta competitively inhibits the activities of functional CCA1 alpha and LATE ELONGATED HYPOCOTYL (LHY) transcription factors by forming nonfunctional CCA1 alpha-CCA1 beta and LHY-CCA1 beta heterodimers. Consequently, CCA1 beta-overexpressing plants (35S:CCA1 beta) exhibit shortened circadian periods as observed in cca1 lhy double mutants. In addition, elongated hypocotyls and petioles and delayed flowering of CCA1 alpha-overexpressing plants (35S:CCA1 alpha) were rescued by coexpression of CCA1 beta. Interestingly, low temperatures suppress CCA1 alternative splicing and thus derepress the CCA1 alpha activity in inducing cold tolerance. These observations indicate that a cold-responsive self-regulatory circuit of CCA1 plays a role in plant responses to low temperatures.