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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.

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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.

References

  1. Reik, W. & Surani, M. A. Germline and pluripotent stem cells. Cold Spring Harb. Perspect. Biol. 7, a019422 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  2. Feng, X., Zilberman, D. & Dickinson, H. A conversation across generations: soma-germ cell crosstalk in plants. Dev. Cell 24, 215–225 (2013).

    Article  CAS  PubMed  Google Scholar 

  3. Segui-Simarro, J. M. & Nuez, F. How microspores transform into haploid embryos: changes associated with embryogenesis induction and microspore-derived embryogenesis. Physiol. Plant. 134, 1–12 (2008).

    Article  CAS  PubMed  Google Scholar 

  4. Li, H. et al. The histone deacetylase inhibitor trichostatin a promotes totipotency in the male gametophyte. Plant Cell 26, 195–209 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Kota, S. K. & Feil, R. Epigenetic transitions in germ cell development and meiosis. Dev. Cell 19, 675–686 (2010).

    Article  CAS  PubMed  Google Scholar 

  6. Xu, Q. & Xie, W. Epigenome in early mammalian development: inheritance, reprogramming and establishment. Trends Cell Biol. 28, 237–253 (2018).

    Article  CAS  PubMed  Google Scholar 

  7. Heard, E. & Martienssen, R. A. Transgenerational epigenetic inheritance: myths and mechanisms. Cell 157, 95–109 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Baulcombe, D. C. & Dean, C. Epigenetic regulation in plant responses to the environment. Cold Spring Harb. Perspect. Biol. 6, a019471 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  9. Feng, S., Jacobsen, S. E. & Reik, W. Epigenetic reprogramming in plant and animal development. Science 330, 622–627 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Gehring, M. Epigenetic dynamics during flowering plant reproduction: evidence for reprogramming? N. Phytol. 224, 91–96 (2019).

    Article  Google Scholar 

  11. Berry, S. & Dean, C. Environmental perception and epigenetic memory: mechanistic insight through FLC. Plant J. 83, 133–148 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Costa, S. & Dean, C. Storing memories: the distinct phases of Polycomb-mediated silencing of Arabidopsis FLC. Biochem. Soc. Trans. 47, 1187–1196 (2019).

    Article  CAS  PubMed  Google Scholar 

  13. Crevillen, P. et al. Epigenetic reprogramming that prevents transgenerational inheritance of the vernalized state. Nature 515, 587–590 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Tao, Z. et al. Embryonic epigenetic reprogramming by a pioneer transcription factor in plants. Nature 551, 124–128 (2017).

    Article  PubMed  Google Scholar 

  15. Sheldon, C. C. et al. Resetting of FLOWERING LOCUS C expression after epigenetic repression by vernalization. Proc. Natl Acad. Sci. USA 105, 2214–2219 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Xu, G., Tao, Z. & He, Y. Embryonic reactivation of FLOWERING LOCUS C by ABSCISIC ACID-INSENSITIVE 3 establishes the vernalization requirement in each Arabidopsis generation. Plant Cell 34, 2205–2221 (2022).

    Article  PubMed  PubMed Central  Google Scholar 

  17. Luo, X., Ou, Y., Li, R. & He, Y. Maternal transmission of the epigenetic ‘memory of winter cold’ in Arabidopsis. Nat. Plants 6, 1211–1218 (2020).

    Article  CAS  PubMed  Google Scholar 

  18. Rathke, C., Baarends, W. M., Awe, S. & Renkawitz-Pohl, R. Chromatin dynamics during spermiogenesis. Biochim. Biophys. Acta 1839, 155–168 (2014).

    Article  CAS  PubMed  Google Scholar 

  19. Hammoud, S. S. et al. Distinctive chromatin in human sperm packages genes for embryo development. Nature 460, 473–478 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Jung, Y. H. et al. Chromatin states in mouse sperm correlate with embryonic and adult regulatory landscapes. Cell Rep. 18, 1366–1382 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Carone, B. R. et al. High-resolution mapping of chromatin packaging in mouse embryonic stem cells and sperm. Dev. Cell 30, 11–22 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Samans, B. et al. Uniformity of nucleosome preservation pattern in mammalian sperm and its connection to repetitive DNA elements. Dev. Cell 30, 23–35 (2014).

    Article  CAS  PubMed  Google Scholar 

  23. Walker, J. et al. Sexual-lineage-specific DNA methylation regulates meiosis in Arabidopsis. Nat. Genet. 50, 130–137 (2018).

    Article  CAS  PubMed  Google Scholar 

  24. Calarco, J. P. et al. Reprogramming of DNA methylation in pollen guides epigenetic inheritance via small RNA. Cell 151, 194–205 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Slotkin, R. K. et al. Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell 136, 461–472 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Ibarra, C. A. et al. Active DNA demethylation in plant companion cells reinforces transposon methylation in gametes. Science 337, 1360–1364 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Borg, M. et al. Targeted reprogramming of H3K27me3 resets epigenetic memory in plant paternal chromatin. Nat. Cell Biol. 22, 621–629 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Ingouff, M. et al. Zygotic resetting of the HISTONE 3 variant repertoire participates in epigenetic reprogramming in Arabidopsis. Curr. Biol. 20, 2137–2143 (2010).

    Article  CAS  PubMed  Google Scholar 

  29. Misra, C. S. et al. Transcriptomics of Arabidopsis sperm cells at single-cell resolution. Plant Reprod. 32, 29–38 (2019).

    Article  CAS  PubMed  Google Scholar 

  30. Twell, D. Male gametogenesis and germline specification in flowering plants. Sex. Plant Reprod. 24, 149–160 (2011).

    Article  PubMed  Google Scholar 

  31. Zhang, J. et al. Sperm cells are passive cargo of the pollen tube in plant fertilization. Nat. Plants 3, 17079 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  32. Huang, J., Dong, J. & Qu, L. J. From birth to function: male gametophyte development in flowering plants. Curr. Opin. Plant Biol. 63, 102118 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Santos, M. R., Bispo, C. & Becker, J. D. Isolation of Arabidopsis pollen, sperm cells, and vegetative nuclei by Fluorescence-Activated Cell Sorting (FACS). Methods Mol. Biol. 1669, 193–210 (2017).

    Article  CAS  PubMed  Google Scholar 

  34. Borg, M. et al. Epigenetic reprogramming rewires transcription during the alternation of generations in Arabidopsis. eLife 10, e61894 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. You, Y. et al. Temporal dynamics of gene expression and histone marks at the Arabidopsis shoot meristem during flowering. Nat. Commun. 8, 15120 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Cartagena, J. A. et al. The Arabidopsis SDG4 contributes to the regulation of pollen tube growth by methylation of histone H3 lysines 4 and 36 in mature pollen. Dev. Biol. 315, 355–368 (2008).

    Article  CAS  PubMed  Google Scholar 

  37. Chanvivattana, Y. et al. Interaction of Polycomb-group proteins controlling flowering in Arabidopsis. Development 131, 5263–5276 (2004).

    Article  CAS  PubMed  Google Scholar 

  38. Gu, Y. & Rasmussen, C. G. Cell biology of primary cell wall synthesis in plants. Plant Cell. 34, 103–128 (2021).

    Article  PubMed Central  Google Scholar 

  39. Lafon-Placette, C. & Kohler, C. Embryo and endosperm, partners in seed development. Curr. Opin. Plant Biol. 17, 64–69 (2014).

    Article  PubMed  Google Scholar 

  40. Yanofsky, M. F. et al. The protein encoded by the Arabidopsis homeotic gene agamous resembles transcription factors. Nature 346, 35–39 (1990).

    Article  CAS  PubMed  Google Scholar 

  41. Goto, K. & Meyerowitz, E. M. Function and regulation of the Arabidopsis floral homeotic gene PISTILLATA. Genes Dev. 8, 1548–1560 (1994).

    Article  CAS  PubMed  Google Scholar 

  42. Pelaz, S., Ditta, G. S., Baumann, E., Wisman, E. & Yanofsky, M. F. B and C floral organ identity functions require SEPALLATA MADS-box genes. Nature 405, 200–203 (2000).

    Article  CAS  PubMed  Google Scholar 

  43. Bowman, J. L., Smyth, D. R. & Meyerowitz, E. M. The ABC model of flower development: then and now. Development 139, 4095–4098 (2012).

    Article  CAS  PubMed  Google Scholar 

  44. Shi, X. et al. GLUCAN SYNTHASE-LIKE 5 (GSL5) plays an essential role in male fertility by regulating callose metabolism during microsporogenesis in rice. Plant Cell Physiol. 56, 497–509 (2015).

    Article  CAS  PubMed  Google Scholar 

  45. Enns, L. C. et al. Two callose synthases, GSL1 and GSL5, play an essential and redundant role in plant and pollen development and in fertility. Plant Mol. Biol. 58, 333–349 (2005).

    Article  CAS  PubMed  Google Scholar 

  46. Gazzarrini, S., Tsuchiya, Y., Lumba, S., Okamoto, M. & McCourt, P. The transcription factor FUSCA3 controls developmental timing in Arabidopsis through the hormones gibberellin and abscisic acid. Dev. Cell 7, 373–385 (2004).

    Article  CAS  PubMed  Google Scholar 

  47. Zhao, C., Avci, U., Grant, E. H., Haigler, C. H. & Beers, E. P. XND1, a member of the NAC domain family in Arabidopsis thaliana, negatively regulates lignocellulose synthesis and programmed cell death in xylem. Plant J. 53, 425–436 (2008).

    Article  CAS  PubMed  Google Scholar 

  48. Baylis, T., Cierlik, I., Sundberg, E. & Mattsson, J. SHORT INTERNODES/STYLISH genes, regulators of auxin biosynthesis, are involved in leaf vein development in Arabidopsis thaliana. N. Phytol. 197, 737–750 (2013).

    Article  CAS  Google Scholar 

  49. Liu, J. et al. WOX11 and 12 are involved in the first-step cell fate transition during de novo root organogenesis in Arabidopsis. Plant Cell 26, 1081–1093 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Ge, Z. et al. Arabidopsis pollen tube integrity and sperm release are regulated by RALF-mediated signaling. Science 358, 1596–1600 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Boisson-Dernier, A. et al. Disruption of the pollen-expressed FERONIA homologs ANXUR1 and ANXUR2 triggers pollen tube discharge. Development 136, 3279–3288 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Miyazaki, S. et al. ANXUR1 and 2, sister genes to FERONIA/SIRENE, are male factors for coordinated fertilization. Curr. Biol. 19, 1327–1331 (2009).

    Article  CAS  PubMed  Google Scholar 

  53. Chen, K. et al. Broad H3K4me3 is associated with increased transcription elongation and enhancer activity at tumor-suppressor genes. Nat. Genet. 47, 1149–1157 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Dahl, J. A. et al. Broad histone H3K4me3 domains in mouse oocytes modulate maternal-to-zygotic transition. Nature 537, 548–552 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Zhang, B. et al. Allelic reprogramming of the histone modification H3K4me3 in early mammalian development. Nature 537, 553–557 (2016).

    Article  CAS  PubMed  Google Scholar 

  56. Liu, X. et al. Distinct features of H3K4me3 and H3K27me3 chromatin domains in pre-implantation embryos. Nature 537, 558–562 (2016).

    Article  CAS  PubMed  Google Scholar 

  57. Belhocine, M. et al. Dynamic of broad H3K4me3 domains uncover an epigenetic switch between cell identity and cancer-related genes. Genome Res. 32, 1328–1342 (2021).

    Article  PubMed  Google Scholar 

  58. Voigt, P., Tee, W. W. & Reinberg, D. A double take on bivalent promoters. Genes Dev. 27, 1318–1338 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Harikumar, A. & Meshorer, E. Chromatin remodeling and bivalent histone modifications in embryonic stem cells. EMBO Rep. 16, 1609–1619 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Azuara, V. et al. Chromatin signatures of pluripotent cell lines. Nat. Cell Biol. 8, 532–538 (2006).

    Article  CAS  PubMed  Google Scholar 

  61. Bernstein, B. E. et al. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125, 315–326 (2006).

    Article  CAS  PubMed  Google Scholar 

  62. Brookes, E. et al. Polycomb associates genome-wide with a specific RNA polymerase II variant, and regulates metabolic genes in ESCs. Cell Stem Cell 10, 157–170 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Voigt, P. et al. Asymmetrically modified nucleosomes. Cell 151, 181–193 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Schmidl, C., Rendeiro, A. F., Sheffield, N. C. & Bock, C. ChIPmentation: fast, robust, low-input ChIP–seq for histones and transcription factors. Nat. Methods 12, 963–965 (2015).

  65. Xu, W., Ye, Y., Sharrocks, A. D., Zhang, W. & Chen, X. Genome-wide interrogation of protein-DNA interactions in mammalian cells using ChIPmentation. STAR Protoc. 1, 100187 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  66. Wang, Z. P. et al. Egg cell-specific promoter-controlled CRISPR/Cas9 efficiently generates homozygous mutants for multiple target genes in Arabidopsis in a single generation. Genome Biol. 16, 144 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  67. Brind’Amour, J. et al. An ultra-low-input native ChIP–seq protocol for genome-wide profiling of rare cell populations. Nat. Commun. 6, 6033 (2015).

  68. Picelli, S. et al. Full-length RNA-seq from single cells using Smart-seq2. Nat. Protoc. 9, 171–181 (2014).

    Article  CAS  PubMed  Google Scholar 

  69. Zheng, J. et al. A modified SMART-Seq method for single-cell transcriptomic analysis of embryoid body differentiation. Methods Mol. Biol. 2520, 233–259 (2022).

    Article  CAS  PubMed  Google Scholar 

  70. Hagemann-Jensen, M. et al. Single-cell RNA counting at allele and isoform resolution using Smart-seq3. Nat. Biotechnol. 38, 708–714 (2020).

    Article  CAS  PubMed  Google Scholar 

  71. Chen, S., Zhou, Y., Chen, Y. & Gu, J. fastp: An ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34, i884–i890 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  72. Kim, D., Paggi, J. M., Park, C., Bennett, C. & Salzberg, S. L. Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype. Nat. Biotechnol. 37, 907–915 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Li, H. et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078–2079 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  74. Zhang, Y. et al. Model-based analysis of ChIP–Seq (MACS). Genome Biol. 9, R137 (2008).

  75. Heinz, S. et al. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol. Cell 38, 576–589 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Quinlan, A. R. & Hall, I. M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841–842 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Trapnell, C. et al. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat. Protoc. 7, 562–578 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Yan, W. et al. Dynamic and spatial restriction of Polycomb activity by plant histone demethylases. Nat. Plants 4, 681–689 (2018).

    Article  CAS  PubMed  Google Scholar 

  79. Hofmann, F., Schon, M. A. & Nodine, M. D. The embryonic transcriptome of Arabidopsis thaliana. Plant Reprod. 32, 77–91 (2019).

    Article  CAS  PubMed  Google Scholar 

  80. Kaminow, B., Yunusov, D. & Dobin, A. STARsolo: accurate, fast and versatile mapping/quantification of single-cell and single-nucleus RNA-seq data. Preprint at https://doi.org/10.1101/2021.05.05.442755 (2021).

  81. Hao, Y. et al. Integrated analysis of multimodal single-cell data. Cell 184, 3573–3587 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Yu, G., Wang, L. G., Han, Y. & He, Q. Y. clusterProfiler: an R package for comparing biological themes among gene clusters. OMICS 16, 284–287 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Kent, W. J. et al. The human genome browser at UCSC. Genome Res. 12, 996–1006 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Lopez-Delisle, L. et al. pyGenomeTracks: reproducible plots for multivariate genomic datasets. Bioinformatics 37, 422–423 (2021).

    Article  CAS  PubMed  Google Scholar 

  85. Zhu, D. et al. Distinct chromatin signatures in the Arabidopsis male gametophyte. https://doi.org/10.5281/zenodo.7578051 (2023).

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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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