Diversification of chromatin organization in eukaryotes

Transposons repressed by H3K27me3 were co-opted as cis-regulatory elements of H3K27me3 controlled protein coding genes during evolution of plants

“…The overlap between TE or PCG annotations and H3K27me3 peaks showed 4.7% of PCGs and 48% of TEs were covered by H3K27me3 and there was no significant enrichment of specific TE families among them (Figure S1A). Because half of the TEs were not covered by H3K27me3 we investigated the presence of other repressive marks such as methylation of the lysine 9 of histone H3 (H3K9me1) and DNA (5methyl-C (5mC)), which mark TEs in many eukaryotes including flowering plants 5,6 . In the genome of C. merolae , five putative SET domain histone methyltransferases are encoded (four with homology to H3K4 methyltransferases, one with homology to the PRC2 methyltransferase Enhancer of Zeste (E(z)).…”

“…Meanwhile, their uncontrolled activity causes genomic instability and therefore expression of TEs is silenced by host genomes 3,4 . TEs are marked with DNA and H3K9 methylation that are associated with silencing in flowering plants 5 , animals, and fungi 6 . Yet, in distantly related eukaryotes TEs are instead marked by H3K27me3 deposited by the Polycomb Repressive Complex 2 (PRC2) 7–11 , an epigenetic mark associated with gene silencing in multicellular eukaryotes 12–15 .…”

The ancestral chromatin landscape of land plants

“…In flowering plants, TEs are enriched in pericentromeric heterochromatin while PCGs are enriched along chromosomal arms (Jamge and Berger, 2022; Sequeira-Mendes et al, 2014). By contrast, both TEs and PCGs are distributed evenly over the entire chromosomes of bryophytes (Montgomery et al, 2020; Lang et al, 2018; Zhang et al, 2020; Li et al, 2020).…”

“…In yeast and animals H3K9me3 is bound by heterochromatin protein 1 (HP1) which promotes compaction of heterochromatin and could phase separate by recruiting other heterochromatin interacting proteins (Larson and Narlikar, 2018). In flowering plants, H3K9me2 does not bind to HP1, but instead recruits the plant-specific DNA methyltransferases CHROMOMETHYLASE (CMT) 2 and 3 (Jamge and Berger, 2022). CMT2/3 deposits methyl groups specifically on cytosines in CHG context (Du et al, 2012).…”

“…The difference of the mechanisms of DNA methylation and histone modification in mosses and liverworts and the absence of data in the sister group of hornworts have made it impossible to reconstruct the ancestral state (Jamge and Berger, 2022). To reconstruct the ancestral chromatin landscape of bryophytes, we investigated DNA methylation and a set of five PTMs in the chromatin of the model hornwort Anthoceros agrestis and compared it to P. patens and M. polymorpha .…”