Hure Valentin, Piron-Prunier Florence, Yehouessi Tamara, Vitte Clémentine, Kornienko Aleksandra E, Adam Gabrielle, Nordborg Magnus, Déléris Angélique
Institute for Integrative Biology of the Cell (I2BC), Université Paris-Saclay, Centre National de La Recherche Scientifique (CNRS), Commissariat À L'EnergieAtomique (CEA), Gif-Sur-Yvette, 91190, France.
Université Paris-Saclay, Institut National de la Recherche pour l'Agriculture, l'Alimentation et l'Environnement (INRAE), CNRS, AgroParisTech, Génétique Quantitative et Evolution (GQE), Gif-Sur-Yvette, 91190, France.
Genome Biol. 2025 Jan 20;26(1):11. doi: 10.1186/s13059-024-03466-6.
The DNA/H3K9 methylation and Polycomb-group proteins (PcG)-H3K27me3 silencing pathways have long been considered mutually exclusive and specific to transposable elements (TEs) and genes, respectively in mammals, plants, and fungi. However, H3K27me3 can be recruited to many TEs in the absence of DNA/H3K9 methylation machinery and sometimes also co-occur with DNA methylation.
In this study, we show that TEs can also be solely targeted and silenced 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, a 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 accession. This variation can be linked to intrinsic TE features and to trans-acting factors and reveals a change in epigenetic status across the 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.
长期以来，DNA/H3K9甲基化和多梳蛋白组（PcG）-H3K27me3沉默途径在哺乳动物、植物和真菌中分别被认为是相互排斥的，且分别特异地作用于转座元件（TEs）和基因。然而，在缺乏DNA/H3K9甲基化机制的情况下，H3K27me3可以被招募到许多TEs上，有时还与DNA甲基化同时出现。
在本研究中，我们表明在野生型拟南芥植物中，TEs也可以仅被H3K27me3靶向并沉默。这些被H3K27me3标记的TEs不仅包括退化的遗迹，还包括看似完整的拷贝，它们表现出响应性PcG靶基因的表观遗传特征以及活跃的H3K27me3调控。我们还表明，H3K27me3可以以TE特异性的方式沉积在新插入的转基因TE序列上，这表明沉默是由顺式作用决定的。最后，对拟南芥自然群体的比较揭示了一类TEs的存在，我们将其称为“双面体”，它们根据群体不同被DNA甲基化或H3K27me3标记。这种变异可能与TEs的内在特征和反式作用因子有关，并揭示了TEs生命周期中表观遗传状态的变化。
我们的研究揭示了开花植物中与H3K27me3而非DNA甲基化相关的TE沉默的另一种模式。它还表明在物种水平上这两种表观遗传标记之间的动态转换，这是一种可能扩展到其他多细胞真核生物的新范式。
