Transcriptional Dynamics and Chromatin Accessibility in the Regulation of Shade-Responsive Genes in Arabidopsis

Open chromatin regions host DNA regulatory motifs that are accessible to transcription factors and the transcriptional machinery. In Arabidopsis, responses to light are heavily regulated at the transcriptional level. Shade, for example, can limit photosynthesis and is rapidly perceived by phytochromes as a reduction of red to far-red light ratio (LRFR). Under shade, phytochromes become inactive, enabling PHYTOCHROME INTERACTING FACTORs (PIFs), particularly PIF7, to promote genome-wide reprogramming essential for LRFR responses. An initial strong and fast regulation of shade-responsive genes is followed by attenuation of this response under prolonged shade. We wanted to determine whether the transcriptional response to shade depends on chromatin accessibility. For this, we used ATAC-seq to profile the chromatin of seedlings exposed to short (1h) and long (25h) simulated shade. We found that PIF7 binding sites were accessible for most early target genes before LRFR treatment. The transcription pattern of most acute shade-responsive genes correlated with a rapid increase in PIF levels and chromatin association at 1h, and its decrease at 25h of shade exposure. For a small subset of acutely responding genes, PIFs also modulate chromatin accessibility at their binding sites early and/or late in the response to shade. Our results suggest that in seedlings a state of open chromatin conformation allows PIFs to easily access and recognize their binding motifs, rapidly initiating gene expression triggered by shade. This transcriptional response primarily depends on a transient increase in PIF stability and gene occupancy, accompanied by changes in chromatin accessibility in a minority of genes.