TY - JOUR T1 - Transposons repressed by H3K27me3 were co-opted as cis-regulatory elements of H3K27me3 controlled protein coding genes during evolution of plants JF - bioRxiv DO - 10.1101/2022.10.24.513474 SP - 2022.10.24.513474 AU - Tetsuya Hisanaga AU - Facundo Romani AU - Shuangyang Wu AU - Teresa Kowar AU - Ruth Lintermann AU - Bhagyshree Jamge AU - Sean A. Montgomery AU - Elin Axelsson AU - Tom Dierschke AU - John L. Bowman AU - Takayuki Fujiwara AU - Shunsuke Hirooka AU - Shin-ya Miyagishima AU - Liam Dolan AU - Daniel Schubert AU - Frédéric Berger Y1 - 2022/01/01 UR - http://biorxiv.org/content/early/2022/10/24/2022.10.24.513474.abstract N2 - The mobility of transposable elements (TEs) contributes to evolution of genomes 1,2. 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. It was therefore proposed that the ancestral activity of PRC2 was the deposition of H3K27me3 to silence TEs 16.To test this hypothesis we obtained mutants deprived of PRC2 activity and used genomics to analyze the role of PRC2 in extant species along the lineage of Archaeplastida. While in the red alga Cyanidioschyzon merolae more TEs than genes were repressed by PRC2, an opposite trend was observed in bryophytes Marchantia polymorpha and Anthoceros agrestis. In the red alga, TEs silenced by H3K27me3 are in subtelomeres but in bryophytes, TEs and genes marked by H3K27me3 form coregulated transcriptional units. The latter trend was also observed in the flowering plant Arabidopsis thaliana, and we identified cis-elements recognised by transcription factors in TEs flanking genes repressed by PRC2.Together with the silencing of TEs by PRC2 in ciliates that diverged early from an ancestor common with Archaeplastida, our findings support the hypothesis that PRC2 deposited H3K27me3 to silence TEs in early lineages of eukaryotes. During evolution, TE fragments marked with H3K27me3 were selected to shape transcriptional regulation that control networks of genes regulated by PRC2.Highlights H3K27me3 marks a decreasing proportion of TEs during evolution of plantsThe polycomb repressive complex 2 represses TEs in red algae and bryophytesH3K27me3-marked TEs in flowering plants contain transcription factor binding sitesTranscription factors bind TEs and regulate networks of genes controlled by PRC2Competing Interest StatementThe authors have declared no competing interest. ER -