Alternative silencing states of transposable elements in Arabidopsis associated with H3K27me3
Abstract Background 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...
Saved in:
| Main Authors: | , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
BMC
2025-01-01
|
| Series: | Genome Biology |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s13059-024-03466-6 |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| _version_ | 1832585704936308736 |
|---|---|
| author | Valentin Hure Florence Piron-Prunier Tamara Yehouessi Clémentine Vitte Aleksandra E. Kornienko Gabrielle Adam Magnus Nordborg Angélique Déléris |
| author_facet | Valentin Hure Florence Piron-Prunier Tamara Yehouessi Clémentine Vitte Aleksandra E. Kornienko Gabrielle Adam Magnus Nordborg Angélique Déléris |
| author_sort | Valentin Hure |
| collection | DOAJ |
| description | Abstract Background 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. Results 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. Conclusions 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. |
| format | Article |
| id | doaj-art-4fefb5b33b0344a68fd170e26237ad77 |
| institution | Kabale University |
| issn | 1474-760X |
| language | English |
| publishDate | 2025-01-01 |
| publisher | BMC |
| record_format | Article |
| series | Genome Biology |
| spelling | doaj-art-4fefb5b33b0344a68fd170e26237ad772025-01-26T12:36:07ZengBMCGenome Biology1474-760X2025-01-0126112110.1186/s13059-024-03466-6Alternative silencing states of transposable elements in Arabidopsis associated with H3K27me3Valentin Hure0Florence Piron-Prunier1Tamara Yehouessi2Clémentine Vitte3Aleksandra E. Kornienko4Gabrielle Adam5Magnus Nordborg6Angélique Déléris7Institute for Integrative Biology of the Cell (I2BC), Université Paris-Saclay, Centre National de La Recherche Scientifique (CNRS), Commissariat À L’EnergieAtomique (CEA)Institute for Integrative Biology of the Cell (I2BC), Université Paris-Saclay, Centre National de La Recherche Scientifique (CNRS), Commissariat À L’EnergieAtomique (CEA)Institute for Integrative Biology of the Cell (I2BC), Université Paris-Saclay, Centre National de La Recherche Scientifique (CNRS), Commissariat À L’EnergieAtomique (CEA)Université Paris-Saclay, Institut National de la Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), CNRS, AgroParisTech, Génétique Quantitative et Evolution (GQE)Gregor Mendel Institute (GMI), Austrian Academy of Sciences, Vienna BioCenter (VBC)Institute of Plant Sciences Paris-Saclay (IPS2), Université Paris-Saclay, CNRS, INRAEGregor Mendel Institute (GMI), Austrian Academy of Sciences, Vienna BioCenter (VBC)Institute for Integrative Biology of the Cell (I2BC), Université Paris-Saclay, Centre National de La Recherche Scientifique (CNRS), Commissariat À L’EnergieAtomique (CEA)Abstract Background 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. Results 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. Conclusions 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.https://doi.org/10.1186/s13059-024-03466-6Transposable elements (TE)Polycomb (PcG)DNA methylationEpigeneticsEpigenomicsNatural variation |
| spellingShingle | Valentin Hure Florence Piron-Prunier Tamara Yehouessi Clémentine Vitte Aleksandra E. Kornienko Gabrielle Adam Magnus Nordborg Angélique Déléris Alternative silencing states of transposable elements in Arabidopsis associated with H3K27me3 Genome Biology Transposable elements (TE) Polycomb (PcG) DNA methylation Epigenetics Epigenomics Natural variation |
| title | Alternative silencing states of transposable elements in Arabidopsis associated with H3K27me3 |
| title_full | Alternative silencing states of transposable elements in Arabidopsis associated with H3K27me3 |
| title_fullStr | Alternative silencing states of transposable elements in Arabidopsis associated with H3K27me3 |
| title_full_unstemmed | Alternative silencing states of transposable elements in Arabidopsis associated with H3K27me3 |
| title_short | Alternative silencing states of transposable elements in Arabidopsis associated with H3K27me3 |
| title_sort | alternative silencing states of transposable elements in arabidopsis associated with h3k27me3 |
| topic | Transposable elements (TE) Polycomb (PcG) DNA methylation Epigenetics Epigenomics Natural variation |
| url | https://doi.org/10.1186/s13059-024-03466-6 |
| work_keys_str_mv | AT valentinhure alternativesilencingstatesoftransposableelementsinarabidopsisassociatedwithh3k27me3 AT florencepironprunier alternativesilencingstatesoftransposableelementsinarabidopsisassociatedwithh3k27me3 AT tamarayehouessi alternativesilencingstatesoftransposableelementsinarabidopsisassociatedwithh3k27me3 AT clementinevitte alternativesilencingstatesoftransposableelementsinarabidopsisassociatedwithh3k27me3 AT aleksandraekornienko alternativesilencingstatesoftransposableelementsinarabidopsisassociatedwithh3k27me3 AT gabrielleadam alternativesilencingstatesoftransposableelementsinarabidopsisassociatedwithh3k27me3 AT magnusnordborg alternativesilencingstatesoftransposableelementsinarabidopsisassociatedwithh3k27me3 AT angeliquedeleris alternativesilencingstatesoftransposableelementsinarabidopsisassociatedwithh3k27me3 |