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Single-cell three-dimensional genome structures of rice gametes and unicellular zygotes

Nature Plants volume 5, pages 795–800 (2019)Cite this article

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Abstract

Chromatin conformation capture (3C)1 and high-throughput 3C (Hi-C)2 assays allow the study of three-dimensional (3D) genome structures in cell populations or tissues, based on average proximities of folded DNA. However, differences between cells can be observed only by single-cell measurements that avoid ensemble averaging3,4,5. To study 3D chromatin organization and dynamics before and after fertilization in flowering plants, we analysed the 3D genomes of rice eggs, sperm cells, unicellular zygotes and shoot mesophyll cells. We show that chromatin architectures of rice eggs and sperm cells are comparable to those of mesophyll cells and are reorganized after fertilization. The rice single-cell 3D genomes display specific features of chromosome compartments and telomere/centromere configuration compared to those in mammalian single cells. Active and silent chromatin domains combine to form multiple foci in the nuclear space. Notably, the 3D genomes of the eggs and unicellular zygotes contain a compact silent centre (CSC) that is absent in sperm cells. CSC appears to be reorganized after fertilization, and may be involved in the regulation of zygotic genome activation (ZGA). Our results reveal specific 3D genome features of plant gametes and the unicellular zygote, and provide a spatial chromatin basis for ZGA and epigenetic regulation in plants.

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Fig. 1: Rice single-cell Hi-C 3D genome structure.
Fig. 2: Features of rice single-cell 3D genomes.
Fig. 3: Plaque distribution of active and silent chromatin domains in the rice 3D genome.
Fig. 4: Identification of a CSC in rice 3D genomes.

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Data availability

All data in support of the findings of this study, including the raw data, the output ncc files of Nuc_processing software and the final programme database files for 3D viewing of the genome in PyMOL, are deposited in the Gene Expression Omnibus (No. GSE123109) and are available from the corresponding author upon request.

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Acknowledgements

We thank X. Li and C. Luo for help with single-cell isolation. This work was supported by grants from the National Key Research and Development Programme of China (No. 2016YFD0100802), the National Natural Science Foundation of China (No. 31730049), Fundamental Research Funds for the Central Universities (No. 2662015PY228) and the National Postdoctoral Programme for Innovative Talents.

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Authors and Affiliations

  1. National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan, China

    Shaoli Zhou, Wei Jiang, Yu Zhao & Dao-Xiu Zhou

  2. Institute of Plant Science of Paris-Saclay, CNRS, INRA, Université Paris-Sud, Université Paris-Saclay, Orsay, France

    Dao-Xiu Zhou

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  1. Shaoli Zhou
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Contributions

S.Z. performed most of the experiments, analysed the data and participated in writing of the paper. W.J. and Y.Z. participated in the experimental set-up of single-cell isolation. D.-X.Z. supervised the project, analysed the data and wrote the paper, with input from S.Z.

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Correspondence to Dao-Xiu Zhou.

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The authors declare no competing interests.

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Peer review information: Nature Plants thanks Thomas Dresselhaus, Chang Liu and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Supplementary Figs. 1–11, Supplementary Methods and Supplementary Tables 1–3.

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Zhou, S., Jiang, W., Zhao, Y. et al. Single-cell three-dimensional genome structures of rice gametes and unicellular zygotes. Nat. Plants 5, 795–800 (2019). https://doi.org/10.1038/s41477-019-0471-3

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