Genome-scale transcriptome augmentation during Arabidopsis thaliana photomorphogenesis

Plant photomorphogenesis is a light-induced developmental switch that combines massive reprogramming of gene expression and a general enhancement in RNA Polymerase II activity. Yet, transcriptome analyses have failed to demonstrate any tendency toward gene upregulation. To solve this conundrum, we use a spike-in RNA-seq experimental and bioinformatic pipeline, enabling to reconcile transcriptome dynamics with epigenomic and cytogenetic observations of Arabidopsis thaliana cotyledon photomorphogenesis. During the transition, a quasi-unilateral impact of light, with 94% of the differentially expressed genes being upregulated within the first six hours, triggers a two-fold increase in cellular transcript levels. This augmentation of the transcriptome is detected at a similar strength in spike-free RNA-seq datasets re-normalized using stable endogenous transcript levels that mimic the spike-in information. Reanalyzing light-mediated gene regulatory pathways from this standpoint further reveals a quasi-exclusive positive effect of ELONGATED HYPOCOTYL 5 (HY5) and other key light-induced transcription factors on target genes. This study provides a paradigm shift for understanding global genome regulation by light and opens the way to investigate transcriptome size control during other developmentally or environmentally controlled cellular transitions in plants.