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Distinct chromatin signatures in the Arabidopsis male gametophyte

Nature Genetics volume 55, pages 706–720 (2023)Cite this article

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Abstract

Epigenetic reprogramming in the germline contributes to the erasure of epigenetic inheritance across generations in mammals but remains poorly characterized in plants. Here we profiled histone modifications throughout Arabidopsis male germline development. We find that the sperm cell has widespread apparent chromatin bivalency, which is established by the acquisition of H3K27me3 or H3K4me3 at pre-existing H3K4me3 or H3K27me3 regions, respectively. These bivalent domains are associated with a distinct transcriptional status. Somatic H3K27me3 is generally reduced in sperm, while dramatic loss of H3K27me3 is observed at only ~700 developmental genes. The incorporation of the histone variant H3.10 facilitates the establishment of sperm chromatin identity without a strong impact on resetting of somatic H3K27me3. Vegetative nuclei harbor thousands of specific H3K27me3 domains at repressed genes, while pollination-related genes are highly expressed and marked by gene body H3K4me3. Our work highlights putative chromatin bivalency and restricted resetting of H3K27me3 at developmental regulators as key features in plant pluripotent sperm.

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Fig. 1: Profiling the chromatin landscape in Arabidopsis sperm and vegetative nuclei.
Fig. 2: Prevalent chromatin bivalency in sperm nucleus.
Fig. 3: HBGs and CBGs are associated with different functional groups, and their chromatin landscapes are generated by different routes.
Fig. 4: Resetting of H3K27me3 in sperm.
Fig. 5: H3K27me3 patterns in sperm following loss of HTR10.
Fig. 6: Histone modification features in the vegetative nucleus.
Fig. 7: Chromatin accessibility features and correlations with histone modification patterns in Spm and Veg.
Fig. 8: Summary of distinct chromatin signatures in sperm and vegetative nuclei.

Data availability

All sequencing data generated in this study were deposited at ArrayExpress with the accession nos. E-MTAB-10965 (bulk RNA-seq), E-MTAB-10966 (ChIP–seq), E-MTAB-10967 (ATAC–seq) and E-MTAB-12137 (scRNA-seq). Previously published data analyzed in this study can be obtained from GEO via accession code nos. GSE106943 (mRNA-seq, flower)78, GSE86583 (mRNA-seq, male meiocytes)23, GSE121236 (mRNA-seq, different embryo stages)79 and GSE155369 (ATAC–seq, Spm and Veg)34.

Code availability

The code used to process the data and instructions to run the code are available at the Zenodo repository under https://doi.org/10.5281/zenodo.757805185 and in the GitHub repository at https://github.com/Blairewen/Arabidopsis-Pollen.

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Acknowledgements

We thank J. D. Becker (Instituto Gulbenkian de Ciência) for kindly providing the pollen marker line. We thank H. Guo and W. Chen from SUSTech for valuable suggestions and discussions. We thank X. Lu (SUSTech Core Research Facilities) for patient training in the usage of FACS (BD FACSAria SORP). We thank R. Zhang (Fapon. Inc.) for provision of high-quality Tn5 transposase. We thank W. Xu and J. Zheng for assistance with scRNA-seq. We thank former SUSTech undergraduate C. Liu for help with HTB7 subcloning. We thank N. Wang and J. Du for provision of the high-quality histone peptides used for checking antibody (Millipore, no. 07-449) specificity. Computational work was supported by the Center for Computational Science and Engineering at Southern University of Science and Technology. This work was supported by the National Natural Science Foundation of China (nos. 32070645 and 32270369 to D.Z. and 31970277 and 32170348 to Z.W.); Guangdong Basic and Applied Basic Research Foundation (no. 2022A1515010505); Guangdong Innovation Research Team fund (no. 2016ZT06S172); Shenzhen Innovation Committee of Science and Technology (nos. JCYJ20210324104803009 and JCYJ20190809141201671 to D.Z., 20200925153455004 and KYTDPT20181011104005 to Z.W. and ZDSYS20200811144002008 to Shenzhen Key Laboratory of Gene Regulation and Systems Biology); and Key Laboratory of Molecular Design for Plant Cell Factory of Guangdong Higher Education Institutes (no. 2019KSYS006).

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  1. These authors contributed equally: Danling Zhu, Yi Wen.

Authors and Affiliations

  1. Key Laboratory of Molecular Design for Plant Cell Factory of Guangdong Higher Education Institutes, Institute of Plant and Food Science, Department of Biology, School of Life Sciences, Southern University of Science and Technology, Shenzhen, China

    Danling Zhu, Wanyue Yao, Sixian Zhou, Qiqi Zhang & Zhe Wu

  2. Shenzhen Key Laboratory of Gene Regulation and Systems Biology, Department of Biology, School of Life Sciences, Southern University of Science and Technology, Shenzhen, China

    Yi Wen & Xi Chen

  3. Center for Advanced Biotechnology and Medicine, Biological Mass Spectrometry Facility, Rutgers University, Piscataway, NJ, USA

    Haiyan Zheng

  4. State Key Laboratory of Protein and Plant Gene Research, Peking-Tsinghua Center for Life Sciences, College of Life Sciences, Peking University, Beijing, China

    Li-Jia Qu

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Contributions

D.Z., X.C. and Z.W., designed the project. D.Z., W.Y., S.Z., Q.Z., H.Z. and Z.W. performed assays. Y.W. and X.C. analyzed ChIP–seq, RNA-seq, scRNA-seq and ATAC–seq data. D.Z., Y.W., X.C., L.-J.Q. and Z.W. interpreted the data. D.Z., X.C. and Z.W. wrote the manuscript with input from all authors.

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Correspondence to Xi Chen or Zhe Wu.

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Zhu, D., Wen, Y., Yao, W. et al. Distinct chromatin signatures in the Arabidopsis male gametophyte. Nat Genet 55, 706–720 (2023). https://doi.org/10.1038/s41588-023-01329-7

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