An early-morning gene network controlled by phytochromes and cryptochromes regulates photomorphogenesis pathways in Arabidopsis

Light perception at dawn plays a key role in coordinating multiple molecular processes and in entraining the plant circadian clock. An Arabidopsis mutant lacking the main photoreceptors however still shows clock entrainment, indicating that the integration of light into the morning transcriptome is not well understood. We performed a high-resolution RNA-seq time series experiment, sampling every two-minutes from dawn. In parallel experiments, we perturbed temperature, the circadian clock, photoreceptor signalling and chloroplast-derived light signalling. We used this data to infer a gene network that describes the gene expression dynamics after light stimulus in the morning, and then we validated key edges. By sampling time points at high density, we are able to identify three light- and temperature-sensitive bursts of transcription factor activity, one of which lasts for only about eight minutes. Phytochrome and cryptochrome mutants cause a delay in the transcriptional bursts at dawn, and completely remove a burst of expression in key photomorphogenesis genes (HY5 and BBX family). Our complete network is available online (http://www-users.york.ac.uk/~de656/dawnBurst/dawnBurst.html). Taken together, our results show that phytochrome and cryptochrome signaling is required for fine-tuning the dawn transcriptional response to light, but separate pathways can robustly activate much of the programme in their absence.