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 a clear tendency toward gene upregulation. To solve this conundrum, we optimized a spike-in RNA-seq experimental and analysis pipeline and reconciled transcriptome dynamics with epigenomic and cytogenetic observations. We found that light induces a two-fold expansion of the transcriptome during Arabidopsis thaliana cotyledon photomorphogenesis, with 94% of the 9,128 differentially expressed genes being upregulated within the first six hours. Transcriptome augmentation was further detected at a similar strength in spike-free RNA-seq datasets from independent laboratories re- normalized using stable genes that mimic the spike-in information. On this new basis, reinterpretation of light-mediated gene regulatory pathways revealed a quasi-exclusive positive effect of HY5 and other key light-induced transcription factors at target genes. This new standpoint unveiled the unilateral impact of light on the transcriptome of Arabidopsis cotyledons at the genome scale and opens new avenues for investigating global genome regulation during plant developmental and environmental responses.

Linker histones play a pivotal role in shaping chromatin architecture, notably through their globular H1 (GH1) domain that contacts the nucleosome and linker DNA. Yet, interplays of H1 with chromatin factors along the epigenome landscape are just starting to emerge. Here, we report that Arabidopsis H1 occupies and favors both chromatin compaction and H3K27me3 enrichment on a majority of Polycomb-target protein-coding genes. In contrast, H1 prevents H3K27me3 accumulation on telomeres and pericentromeric interstitial telomeric repeats (ITRs) while orchestrating long-distance interactions regulating the 3D organization of these chromosome regions. Mechanistically, H1 prevents ITRs from being invaded by Telomere Repeat Binding 1 (TRB1), a GH1-containing telomere component with extra-telomeric functions in Polycomb recruitment. Based on these findings, we propose that H1 represses H3K27me3 accumulation on large blocks of telomeric repeats by antagonizing TRB1 association to linker DNA, conferring to linker histones an additional and sequence-specific role in modulating H3K27me3 epigenome homeostasis.

The plant nucleus provides a major hub for environmental signal integration at the chromatin level. Multiple light signaling pathways operate and exchange information by regulating a large repertoire of gene targets that shape plant responses to a changing environment. In addition to the established role of transcription factors in triggering photoregulated changes in gene expression, there are eminent reports on the significance of chromatin regulators and nuclear scaffold dynamics in promoting light-induced plant responses. Here, we report and discuss recent advances in chromatin-regulatory mechanisms modulating plant architecture and development in response to light, including the molecular and physiological roles of key modifications such as DNA, RNA and histone methylation, and/or acetylation. The significance of the formation of biomolecular condensates of key light signaling components is discussed and potential applications to agricultural practices overviewed.