Targeted reprogramming of H3K27me3 resets epigenetic memory in plant paternal chromatin

Michael Borg; Yannick Jacob; Daichi Susaki; Chantal LeBlanc; Daniel Buendía; Elin Axelsson; Tomokazu Kawashima; Philipp Voigt; Leonor Boavida; Jörg Becker; Tetsuya Higashiyama; Robert Martienssen; Frédéric Berger

doi:10.1038/s41556-020-0515-y

Targeted reprogramming of H3K27me3 resets epigenetic memory in plant paternal chromatin

Michael Borg, Yannick Jacob, Daichi Susaki, Chantal LeBlanc, Daniel Buendía, Elin Axelsson, Tomokazu Kawashima, Philipp Voigt, Leonor Boavida, Jörg Becker, Tetsuya Higashiyama, Robert Martienssen, Frédéric Berger

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Abstract

Epigenetic marks are reprogrammed in the gametes to reset genomic potential in the next generation. In mammals, paternal chromatin is extensively reprogrammed through the global erasure of DNA methylation and the exchange of histones with protamines^1,2. Precisely how the paternal epigenome is reprogrammed in flowering plants has remained unclear since DNA is not demethylated and histones are retained in sperm^3,4. Here, we describe a multi-layered mechanism by which H3K27me3 is globally lost from histone-based sperm chromatin in Arabidopsis. This mechanism involves the silencing of H3K27me3 writers, activity of H3K27me3 erasers and deposition of a sperm-specific histone, H3.10 (ref. ⁵), which we show is immune to lysine 27 methylation. The loss of H3K27me3 facilitates the transcription of genes essential for spermatogenesis and pre-configures sperm with a chromatin state that forecasts gene expression in the next generation. Thus, plants have evolved a specific mechanism to simultaneously differentiate male gametes and reprogram the paternal epigenome.

Original language	English
Pages (from-to)	621-629
Number of pages	9
Journal	Nature Cell Biology
Volume	22
Issue number	6
DOIs	https://doi.org/10.1038/s41556-020-0515-y
State	Published - Jun 1 2020

Bibliographical note

Funding Information:
We thank P. Andersen and J. M. Watson for critical reading of the manuscript, Z. Lorkovic and S. Akimcheva for guidance and technical support, T. Suzuki for sequencing the egg cell transcriptome, and Life Science Editors for editing services. We also thank the Vienna BioCenter Core Facilities for Next Generation Sequencing, Plant Science, HistoPathology, the IMP/IMBA BioOptics Facility and the MENDEL High-Performance Computing team. This work was supported through core funding from the Gregor Mendel Institute, and external grants from the FWF (P 26887 and I 4258) and ERA-CAPS (EVO-REPRO I 2163). M.B. was supported through an FWF Lise Meitner fellowship (M 1818). Y.J., C.L. and R.M. were supported by the Howard Hughes Medical Institute and NIH funding (R01 GM067014). D.S. and T.H. were supported by the Japan Society for the Promotion of Science (18J01963 to D.S. and 16H06464, 16H06465 and 16K21727 to T.H.). P.V. was supported by the Wellcome Trust (104175/Z/14/Z; Sir Henry Dale Fellowship), ERC EU Horizon 2020 research and innovation programme (ERC-STG grant agreement 639253) and core funding from the Wellcome Trust (203149).

Publisher Copyright:
© 2020, The Author(s), under exclusive licence to Springer Nature Limited.

ASJC Scopus subject areas

Cell Biology

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title = "Targeted reprogramming of H3K27me3 resets epigenetic memory in plant paternal chromatin",

abstract = "Epigenetic marks are reprogrammed in the gametes to reset genomic potential in the next generation. In mammals, paternal chromatin is extensively reprogrammed through the global erasure of DNA methylation and the exchange of histones with protamines1,2. Precisely how the paternal epigenome is reprogrammed in flowering plants has remained unclear since DNA is not demethylated and histones are retained in sperm3,4. Here, we describe a multi-layered mechanism by which H3K27me3 is globally lost from histone-based sperm chromatin in Arabidopsis. This mechanism involves the silencing of H3K27me3 writers, activity of H3K27me3 erasers and deposition of a sperm-specific histone, H3.10 (ref. 5), which we show is immune to lysine 27 methylation. The loss of H3K27me3 facilitates the transcription of genes essential for spermatogenesis and pre-configures sperm with a chromatin state that forecasts gene expression in the next generation. Thus, plants have evolved a specific mechanism to simultaneously differentiate male gametes and reprogram the paternal epigenome.",

author = "Michael Borg and Yannick Jacob and Daichi Susaki and Chantal LeBlanc and Daniel Buend{\'i}a and Elin Axelsson and Tomokazu Kawashima and Philipp Voigt and Leonor Boavida and J{\"o}rg Becker and Tetsuya Higashiyama and Robert Martienssen and Fr{\'e}d{\'e}ric Berger",

note = "Funding Information: We thank P. Andersen and J. M. Watson for critical reading of the manuscript, Z. Lorkovic and S. Akimcheva for guidance and technical support, T. Suzuki for sequencing the egg cell transcriptome, and Life Science Editors for editing services. We also thank the Vienna BioCenter Core Facilities for Next Generation Sequencing, Plant Science, HistoPathology, the IMP/IMBA BioOptics Facility and the MENDEL High-Performance Computing team. This work was supported through core funding from the Gregor Mendel Institute, and external grants from the FWF (P 26887 and I 4258) and ERA-CAPS (EVO-REPRO I 2163). M.B. was supported through an FWF Lise Meitner fellowship (M 1818). Y.J., C.L. and R.M. were supported by the Howard Hughes Medical Institute and NIH funding (R01 GM067014). D.S. and T.H. were supported by the Japan Society for the Promotion of Science (18J01963 to D.S. and 16H06464, 16H06465 and 16K21727 to T.H.). P.V. was supported by the Wellcome Trust (104175/Z/14/Z; Sir Henry Dale Fellowship), ERC EU Horizon 2020 research and innovation programme (ERC-STG grant agreement 639253) and core funding from the Wellcome Trust (203149). Publisher Copyright: {\textcopyright} 2020, The Author(s), under exclusive licence to Springer Nature Limited.",

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AU - Borg, Michael

AU - Jacob, Yannick

AU - Susaki, Daichi

AU - LeBlanc, Chantal

AU - Buendía, Daniel

AU - Axelsson, Elin

AU - Kawashima, Tomokazu

AU - Voigt, Philipp

AU - Boavida, Leonor

AU - Becker, Jörg

AU - Higashiyama, Tetsuya

AU - Martienssen, Robert

AU - Berger, Frédéric

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PY - 2020/6/1

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N2 - Epigenetic marks are reprogrammed in the gametes to reset genomic potential in the next generation. In mammals, paternal chromatin is extensively reprogrammed through the global erasure of DNA methylation and the exchange of histones with protamines1,2. Precisely how the paternal epigenome is reprogrammed in flowering plants has remained unclear since DNA is not demethylated and histones are retained in sperm3,4. Here, we describe a multi-layered mechanism by which H3K27me3 is globally lost from histone-based sperm chromatin in Arabidopsis. This mechanism involves the silencing of H3K27me3 writers, activity of H3K27me3 erasers and deposition of a sperm-specific histone, H3.10 (ref. 5), which we show is immune to lysine 27 methylation. The loss of H3K27me3 facilitates the transcription of genes essential for spermatogenesis and pre-configures sperm with a chromatin state that forecasts gene expression in the next generation. Thus, plants have evolved a specific mechanism to simultaneously differentiate male gametes and reprogram the paternal epigenome.

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Targeted reprogramming of H3K27me3 resets epigenetic memory in plant paternal chromatin

Abstract

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