Chloroplast gene expression is required for heterochromatin assembly in Arabidopsis thaliana

The importance of nuclear organization dynamics in cell specialization and transcriptional reprogramming is increasingly recognized in eukaryotic species. In plants and mammals, a key redeployment of chromatin organization during cell differentiation is the formation of repressive heterochromatin. This process has long been proposed as an instructive force that stabilizes new transcriptional programs. Unlike mammals, in which heterochromatin is established rapidly after fertilization, in the model plant Arabidopsis thaliana this reorganization occurs during post-embryonic development. We previously found that the acquisition of such ‘mature-type’ nuclear organization is tightly linked to light availability, as nuclear expansion and aggregation of pericentromeric regions, resulting in chromocenter formation, is poised until embryonic leaves perceive light. This light-triggered nuclear shift coincides with a global increase in nuclear transcription and transcriptome size.

Light serves as both the primary energy source for photosynthesis and a critical signal that controls plant development. One of the most spectacular light-controlled transitions is the switch to photomorphogenesis in germinating seedlings, where light triggers embryonic leaf expansion, greening, chloroplast biogenesis and the transition to photoautotrophy—marking a switch from a “quiescent” to an “active” metabolic state. However, the relationships between large-scale nuclear dynamics and chloroplast and metabolic transitions remain unknown. Here, we reveal a previously unrecognized role of plastid organelles in shaping Arabidopsis nuclear architecture and epigenomic landscape. Using cytogenetics and quantitative chromatin profiling, we found that blocking plastid gene expression profoundly alters heterochromatin assembly and centromere cohesion in a cell-type-specific manner, and that these nuclear defects are associated with large-scale epigenomic alterations. We have also begun exploring how metabolic sensors and the chloroplast signals contribute to the global increase in RNA-Pol II-mediated transcription.