Correct biological timing in Arabidopsis requires multiple light signaling pathways

Circadian oscillators provide rhythmic temporal cues for a range of biological processes in plants and animals, enabling anticipation of the day/night cycle and enhancing fitness associated traits. We have used engineering models to understand the control principles of a plant’s response to seasonal variation. We show that the seasonal changes in the timing of circadian outputs requires light regulation via feed-forward loops, combining rapid light signaling pathways with entrained circadian oscillators. Linear time-invariant models of circadian rhythms were computed for 3503 circadian-regulated genes and for the concentration of cytosolic-free calcium in order to quantify the magnitude and timing of regulation by circadian oscillators and light signaling pathways. Bioinformatic and experimental analysis demonstrate that rapid light-induced regulation of circadian outputs is associated with seasonal re-phasing of the output rhythm. We identify that external coincidence is required for re-phasing of multiple output rhythms, and is therefore important in general phase control in addition to specific photoperiod-dependent processes such as flowering and hypocotyl elongation. Our results uncover a new design principle of circadian regulation, and identify the importance of rapid light signaling pathways in temporal control.