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A paternal protein facilitates sperm RNA delivery to regulate zygotic development

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Abstract

Sperm contributes essential paternal factors, including the paternal genome, centrosome, and oocyte-activation signals, to sexual reproduction. However, it remains unresolved how sperm contributes its RNA molecules to regulate early embryonic development. Here, we show that the Caenorhabditis elegans paternal protein SPE-11 assembles into granules during meiotic divisions of spermatogenesis and later matures into a perinuclear structure where sperm RNAs localize. We reconstitute an SPE-11 liquid-phase scaffold in vitro and find that SPE-11 condensates incorporate the nematode RNA, which, in turn, promotes SPE-11 phase separation. Loss of SPE-11 does not affect sperm motility or fertilization but causes pleiotropic development defects in early embryos, and spe-11 mutant males reduce mRNA levels of genes crucial for an oocyte-to-embryo transition or embryonic development. These results reveal that SPE-11 undergoes phase separation and associates with sperm RNAs that are delivered to oocytes during fertilization, providing insights into how a paternal protein regulates early embryonic development.

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Acknowledgements

This work was supported by the Ministry of Science and Technology of China (2019YFA0508401), the National Natural Science Foundation of China (31871394, 82121004, 32100538), Shanghai Municipal Science and Technology Major Project (2018SHZDZX01), the China Postdoctoral Science Foundation (2022M711844), the Young Elite Scientists Sponsorship Program by CAST (YESS20220102), and ZJ Lab and Shanghai Center for Brain Science and Brain-Inspired Technology.

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Authors and Affiliations

  1. Tsinghua-Peking Center for Life Sciences, Beijing Frontier Research Center for Biological Structure, McGovern Institute for Brain Research, School of Life Sciences and MOE Key Laboratory for Protein Science, Tsinghua University, Beijing, 100084, China

    Dongdong Li, Yongping Chai, Jing Gong, Qiangfeng Cliff Zhang & Guangshuo Ou

  2. Department of Neurosurgery, Huashan Hospital, the Shanghai Key Laboratory of Medical Epigenetics, Institutes of Biomedical Sciences, State Key Laboratory of Medical Neurobiology and MOE Frontiers Center for Brain Science, National Center for Neurological Disorders, School of Basic Medical Sciences, Fudan University, Shanghai, 200032, China

    Shijing Huang, Ruiqian Zhao & Wenyu Wen

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  1. Dongdong Li
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Correspondence to Guangshuo Ou or Wenyu Wen.

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Li, D., Huang, S., Chai, Y. et al. A paternal protein facilitates sperm RNA delivery to regulate zygotic development. Sci. China Life Sci. 66, 2342–2353 (2023). https://doi.org/10.1007/s11427-022-2332-5

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