The role of DNA content in shaping chromatin architecture and gene expression

Whole-genome duplication is an evolutionary force that drives speciation in all living kingdoms and is notably prevalent in plants. The evolutionary history of plants involved at least two genomic duplications that significantly expanded the plant morphology and physiology spectrum. Many important crops are polyploids, showing valuable features relative to morphological and stress response traits. After genome duplication, diploidization processes facilitate genomic adjustments to restore disomic inheritance. However, little is known about the chromatin changes triggered by nuclear DNA content alterations. Here, we report that synthetically induced genome duplication leads to chromatinization and significant changes in gene expression, resulting in a transcriptional landscape resembling a natural tetraploid. Interestingly, synthetic diploidization elicits only minor alterations in transcriptional activity and chromatin accessibility compared to the more pronounced effects of tetraploidization. We identified epigenetic factors, including specific histone variants, that showed increased expression following genome duplication and decreased expression after genome reduction. These changes may play a key role in the epigenetic mechanisms underlying the phenotypic complexity after tetraploidization in plants. Our findings shed light on the mechanisms that modulate chromatin accessibility remodeling and gene transcription regulation underlying plant genome adaptation in response to changes in genome size.