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 require 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 3,503 circadian-regulated genes and for the concentration of cytosolic-free calcium to quantify the magnitude and timing of regulation by circadian oscillators and light-signaling pathways. Bioinformatic and experimental analysis show that rapid light-induced regulation of circadian outputs is associated with seasonal rephasing of the output rhythm. We identify that external coincidence is required for rephasing 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 findings uncover a fundamental design principle of circadian regulation, and identify the importance of rapid light-signaling pathways in temporal control.
Dalchau
Neil
N
Department of Plant Sciences, University of Cambridge, Cambridge CB2 3EA, United Kingdom.
Hubbard
Katharine E
KE
Robertson
Fiona C
FC
Hotta
Carlos T
CT
Briggs
Helen M
HM
Stan
Guy-Bart
GB
Gonçalves
Jorge M
JM
Webb
Alex A R
AA
D017360:Arabidopsis / Q000235:genetics / Q000378:metabolism* / Q000528:radiation effects*; D029681:Arabidopsis Proteins / Q000378:metabolism; D002940:Circadian Rhythm / Q000528:radiation effects*; D018506:Gene Expression Regulation, Plant / Q000528:radiation effects; D008027:Light; D055537:Light Signal Transduction / Q000528:radiation effects; D045342:Light-Harvesting Protein Complexes / Q000378:metabolism; D008954:Models, Biological; D012333:RNA, Messenger / Q000235:genetics / Q000378:metabolism; D015203:Reproducibility of Results
D029681:Arabidopsis Proteins; C423618:CAB2 protein, Arabidopsis; D045342:Light-Harvesting Protein Complexes; D012333:RNA, Messenger