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Germ granule compartments coordinate specialized small RNA production

Author

Listed:
  • Xiangyang Chen

    (University of Science and Technology of China)

  • Ke Wang

    (University of Science and Technology of China)

  • Farees Ud Din Mufti

    (University of Science and Technology of China)

  • Demin Xu

    (University of Science and Technology of China)

  • Chengming Zhu

    (University of Science and Technology of China)

  • Xinya Huang

    (University of Science and Technology of China)

  • Chenming Zeng

    (University of Science and Technology of China)

  • Qile Jin

    (University of Science and Technology of China)

  • Xiaona Huang

    (University of Science and Technology of China)

  • Yong-hong Yan

    (National Institute of Biological Sciences)

  • Meng-qiu Dong

    (National Institute of Biological Sciences)

  • Xuezhu Feng

    (Anhui Medical University)

  • Yunyu Shi

    (University of Science and Technology of China)

  • Scott Kennedy

    (Blavatnik Institute at Harvard Medical School)

  • Shouhong Guang

    (University of Science and Technology of China
    Chinese Academy of Sciences)

Abstract

Germ granules are biomolecular condensates present in most animal germ cells. One function of germ granules is to help maintain germ cell totipotency by organizing mRNA regulatory machinery, including small RNA-based gene regulatory pathways. The C. elegans germ granule is compartmentalized into multiple subcompartments whose biological functions are largely unknown. Here, we identify an uncharted subcompartment of the C. elegans germ granule, which we term the E granule. The E granule is nonrandomly positioned within the germ granule. We identify five proteins that localize to the E granule, including the RNA-dependent RNA polymerase (RdRP) EGO-1, the Dicer-related helicase DRH-3, the Tudor domain-containing protein EKL-1, and two intrinsically disordered proteins, EGC-1 and ELLI-1. Localization of EGO-1 to the E granule enables synthesis of a specialized class of 22G RNAs, which derive exclusively from 5’ regions of a subset of germline-expressed mRNAs. Defects in E granule assembly elicit disordered production of endogenous siRNAs, which disturbs fertility and the RNAi response. Our results define a distinct subcompartment of the C. elegans germ granule and suggest that one function of germ granule compartmentalization is to facilitate the localized production of specialized classes of small regulatory RNAs.

Suggested Citation

  • Xiangyang Chen & Ke Wang & Farees Ud Din Mufti & Demin Xu & Chengming Zhu & Xinya Huang & Chenming Zeng & Qile Jin & Xiaona Huang & Yong-hong Yan & Meng-qiu Dong & Xuezhu Feng & Yunyu Shi & Scott Kenn, 2024. "Germ granule compartments coordinate specialized small RNA production," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-50027-3
    DOI: 10.1038/s41467-024-50027-3
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    References listed on IDEAS

    as
    1. Gang Wan & Brandon D. Fields & George Spracklin & Aditi Shukla & Carolyn M. Phillips & Scott Kennedy, 2018. "Spatiotemporal regulation of liquid-like condensates in epigenetic inheritance," Nature, Nature, vol. 557(7707), pages 679-683, May.
    2. Piergiuseppe Quarato & Meetali Singh & Eric Cornes & Blaise Li & Loan Bourdon & Florian Mueller & Celine Didier & Germano Cecere, 2021. "Germline inherited small RNAs facilitate the clearance of untranslated maternal mRNAs in C. elegans embryos," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    3. Ian F. Price & Jillian A. Wagner & Benjamin Pastore & Hannah L. Hertz & Wen Tang, 2023. "C. elegans germ granules sculpt both germline and somatic RNAome," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    4. Aditi Shukla & Jenny Yan & Daniel J. Pagano & Anne E. Dodson & Yuhan Fei & Josh Gorham & J. G. Seidman & Marvin Wickens & Scott Kennedy, 2020. "poly(UG)-tailed RNAs in genome protection and epigenetic inheritance," Nature, Nature, vol. 582(7811), pages 283-288, June.
    5. Meetali Singh & Eric Cornes & Blaise Li & Piergiuseppe Quarato & Loan Bourdon & Florent Dingli & Damarys Loew & Simone Proccacia & Germano Cecere, 2021. "Translation and codon usage regulate Argonaute slicer activity to trigger small RNA biogenesis," Nature Communications, Nature, vol. 12(1), pages 1-18, December.
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