Elevated CO2 drives epigenetic reprogramming and chromatin dynamics in Arabidopsis thaliana

The rapid increase in atmospheric CO2 levels has profound effects on plant systems, making it essential to understand how plants develop under elevated CO2. By perturbing epigenetic mechanisms necessary for plant acclimatization, we conducted in-depth analyses of the Arabidopsis thaliana 3D genome to investigate the relationship between epigenetic memory and 3D chromatin architecture. Using methylation-sensitive chromatin conformation capture (Hi-C), we reveal how elevated CO2 induces chromatin decondensation resulting from changes in 5mC levels and histone modifications at developmentally regulated loci. Utilizing integrated deep sequencing, we uncover local domains of chromatin loops in the Arabidopsis genome that orient clusters of developmentally regulated loci, revealing a topological framework for stress response pathways. At high resolution, our analyses uncover differential chromatin loops supported by transcriptionally reprogrammed anchor loci, revealing a collaboration between RNA-directed DNA Methylation (RdDM) and Polycomb group (PcG) proteins in mediating gene expression regulation. Our findings demonstrate the central role of the 3D genome and epigenetic modifications in plant development, adaptation, and resilience in changing environments. Finally, we report a mechanism by which elevated CO2 initiates epigenetic reprogramming underlying an accelerated growth phenotype.