The expansion and diversification of epigenetic regulatory networks underpins major transitions in the evolution of land plants

By incorporating genomic phylostratigraphy, we show how genes of differing evolutionary age are partitioned into distinct epigenetic states in plants, with evolutionarily young genes incorporated into developmental programs controlled by H3K9 methylation in Arabidopsis. We further reveal a major wave of PRC2 recruitment to genes that emerged during land terrestrialisation and flowering plant evolution, and identify an ancestral PRC2 network with a shared functional topology in green algae through to land plants, providing a glimpse of the earliest types of genes regulated by PRC2 during the course of plant evolution.

Finally, we analyse the potential regulation of these ancestral PRC2 target genes and find a strong enrichment of motifs bound by ancient AP2/ERF transcription factors (TFs) known to interact with PRC2, which we hypothesise were key determinants in shaping some of the first gene regulatory networks controlled by PRC2 in plants. Our data thus reveal pivotal epigenetic adaptations that occurred during a significant period in the evolutionary history of plants, which likely contributed to key regulatory innovations that influenced major morphological and developmental change into the modern-day.

More broadly, our findings offer insight into the evolutionary dynamics and molecular triggers that drive the adaptation and elaboration of epigenetic regulation, laying the groundwork for its future consideration in other major eukaryotic lineages.