Chromatin-associated DEK proteins maintain H3K27me3 balance and coordinate developmental transitions in plants

Chromatin organization and histone modifications play essential roles in regulating gene expression during development. DEK is a conserved chromatin-associated protein implicated in DNA topology and transcriptional regulation, yet its in vivo function in plants has remained elusive. To uncover DEK function, we used Arabidopsis thaliana dek mutants and performed genome-wide analyses of histone modifications. Genetic and physical interactions with Polycomb Repressive Complex 2 (PRC2)-associated proteins were examined, and transcriptome comparisons were conducted among single and multiple mutants. Loss of DEK function led to a genome-wide increase in the PRC2-mediated histone modification H3K27me3. DEK genetically and physically interacts with the PRC2-associated protein LIKE HETEROCHROMATIN PROTEIN 1 (LHP1), and DEK deficiency partially restores H3K27me3 levels in the lhp1 mutant. The dek multiple mutant exhibited enhanced H3K27me3 at PRC2 target genes and ectopic accumulation at pericentromeric interstitial telomeric repeats - similar to histone H1 mutants - suggesting altered chromatin accessibility. Combined dek and lhp1 mutations intensified developmental defects and disrupted expression of many PRC2 target genes, including MADS-box transcription factors. Transcriptome analyses revealed that DEK and chromatin remodeler alpha thalassemia/mental retardation syndrome X-linked chromatin remodeler have opposing effects on gene expression. Our findings uncover DEK as a novel regulator of H3K27me3 homeostasis and chromatin structure, critical for coordinated plant development.