The reshuffling of nuclear architecture and chromatin landscape is a recurring theme orchestrated in most developmental transitions. Plants display extraordinary capacities enabling them to adjust such transitions to external cues, an adaptive feature at the nexus of their high cell fate plasticity and fitness in changing environments - especially with regard to light conditions. To tackle the fundamental determinants of genome regulation and their declinations in plants, our long-term research axis exploits Arabidopsis photomorphogenesis, a developmental switch that initiates upon the initial light perception by a germinating seedling. We recently unveiled that the transition involves 1) the release from a transcriptionally quiescent status in darkness, 2) nucleus expansion, 3) the formation of subnuclear heterochromatic foci (chromocenters) aggregating most silent repeats, 4) wide changes in the epigenome landscape linked to gene expression reprogramming. In recent collaborative studies with the University of Zurich, we further identified that light sensing induces non-random changes in genome 3D topology and the formation of transcription clusters near the nucleus periphery. This transition being synchronously achieved in most cells of embryonic leaves constitutes a dynamic system perfectly suited to tackle the questions addressed by the ChromatinPhotoDynamics proposal. One such objective is to decipher the molecular frameworks that integrate light signaling at chromatin to reprogram genes during the photomorphogenic transition using both candidate factors and agnostic approaches. The second task is to determine how the sequential orchestration of heterochromatin rearrangements, 3D changes in genome topology, and epigenome dynamics, interplay to modulate both the general transcriptional regime and gene-specific expression patterns. The project further pertains to evolutionary questions on how variation in genome sequence and/or the epigenome contribute to nucleus organization “acclimation”, thereby opening long-term perspectives on the chromatin-level functions subjected to environmental and genetic constraints. Addressing both plant-specific and conserved chromatin regulation pathways, this study will contribute to current intense efforts devoted to deciphering the mechanisms underpinning cellular and organismal adaptive responses.