Extensive N4 cytosine methylation is essential for Marchantia sperm function

N4-methylcytosine (4mC) is an important DNA modification in prokaryotes, but its relevance and even its presence in eukaryotes have been mysterious. Here we show that spermatogenesis in the liverwort Marchantia polymorpha involves two waves of extensive DNA methylation reprogramming. First, 5-methylcytosine (5mC) expands from transposons to the entire genome. Notably, the second wave installs 4mC throughout genic regions, covering over 50% of CG sites in sperm. 4mC requires a methyltransferase (MpDN4MT1a) that is specifically expressed during late spermiogenesis. Deletion of MpDN4MT1a alters the sperm transcriptome, causes sperm swimming and fertility defects, and impairs post-fertilization development. Our results reveal extensive 4mC in a eukaryote, identify a family of eukaryotic methyltransferases, and elucidate the biological functions of 4mC in reproductive development, thereby expanding the repertoire of functional eukaryotic DNA modifications.

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Publication Details

Journal
Cell
Published
2025-04-09
DOI
https://doi.org/10.1016/j.cell.2025.03.014
Citations
13
Primary Topic
Plant Molecular Biology Research
Type
article
Field-Weighted Citation Impact
22.75

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article

Extensive N4 cytosine methylation is essential for Marchantia sperm function

James W. Walker, Weizhi Ouyang, Liam Dolan, Yiming Yu et al.
13 citations
Cell
Plant Molecular Biology Research
22.75
article

Extensive N4 cytosine methylation is essential for Marchantia sperm function

James W. Walker, Weizhi Ouyang, Liam Dolan, Yiming Yu, Martin Vickers, Keiji Nakajima, Xiaoqi Feng, Jingyi Zhang, Yalin Liu, Shujuan Xu, Judit Tálas
article en
13 citations

Abstract

N4-methylcytosine (4mC) is an important DNA modification in prokaryotes, but its relevance and even its presence in eukaryotes have been mysterious. Here we show that spermatogenesis in the liverwort Marchantia polymorpha involves two waves of extensive DNA methylation reprogramming. First, 5-methylcytosine (5mC) expands from transposons to the entire genome. Notably, the second wave installs 4mC throughout genic regions, covering over 50% of CG sites in sperm. 4mC requires a methyltransferase (MpDN4MT1a) that is specifically expressed during late spermiogenesis. Deletion of MpDN4MT1a alters the sperm transcriptome, causes sperm swimming and fertility defects, and impairs post-fertilization development. Our results reveal extensive 4mC in a eukaryote, identify a family of eukaryotic methyltransferases, and elucidate the biological functions of 4mC in reproductive development, thereby expanding the repertoire of functional eukaryotic DNA modifications.

CellVol. 188(11)
John Innes Centre (GB), Gregor Mendel Institute of Molecular Plant Biology (AT), Institute of Science and Technology Austria (AT), Nara Institute of Science and Technology (JP)
European Molecular Biology Organization, Biotechnology and Biological Sciences Research Council, HORIZON EUROPE European Research Council
Zero hunger
Openalex Percentile: Top 0%
Plant Molecular Biology Research
22.75
DOIOpen Access PDFOpenAlex
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