Alternative silencing states of Transposable Elements in Arabidopsis

The DNA methylation/H3K9me2 and Polycomb-group proteins (PcG)-H3K27me3 pathways have long been considered mutually exclusive and specific to TEs and genes, respectively. However, H3K27me3 can be recruited to many TEs in the absence of DNA methylation machinery and sometimes also co-occur with DNA methylation. In this study, we show that TEs can also be solely targeted by H3K27me3 in wild-type Arabidopsis plants. These H3K27me3-marked TEs not only comprise degenerate relics but also seemingly intact copies that display the epigenetic features of responsive PcG target genes as well as an active H3K27me3 regulation. We also show that H3K27me3 can be deposited on newly inserted transgenic TE sequences in a TE-specific manner indicating that silencing is determined in cis . Finally, comparison of Arabidopsis natural accessions reveals the existence of a category of TEs - which we refer to as “ bifrons ” - that are marked by DNA methylation or H3K27me3 depending on the ecotype. This variation can be linked to intrinsic TE features and to trans - acting factors, and reveals a change in epigenetic status across TE lifespan. Our study sheds light on an alternative mode of TE silencing associated with H3K27me3 instead of DNA methylation in flowering plants. It also suggests dynamic switching between the two epigenetic marks at the species level, a new paradigm that might extend to other multicellular eukaryotes.