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C. elegans germ granules sculpt both germline and somatic RNAome

Author

Listed:
  • Ian F. Price

    (The Ohio State University
    The Ohio State University
    The Ohio State University)

  • Jillian A. Wagner

    (The Ohio State University
    The Ohio State University)

  • Benjamin Pastore

    (The Ohio State University
    The Ohio State University
    The Ohio State University)

  • Hannah L. Hertz

    (The Ohio State University
    The Ohio State University)

  • Wen Tang

    (The Ohio State University
    The Ohio State University)

Abstract

Germ granules are membrane-less organelles essential for small RNA biogenesis and germline development. Among the conserved properties of germ granules is their association with the nuclear membrane. Recent studies demonstrated that LOTUS domain proteins, EGGD-1 and EGGD-2 (also known as MIP-1 and MIP-2 respectively), promote the formation of perinuclear germ granules in C. elegans. This finding presents a unique opportunity to evaluate the significance of perinuclear localization of germ granules. Here we show that loss of eggd-1 causes the coalescence of germ granules and formation of abnormal cytoplasmic aggregates. Impairment of perinuclear granules affects certain germline classes of small RNAs including Piwi-interacting RNAs. Transcriptome profiling reveals overexpression of spermatogenic and cuticle-related genes in eggd-1 hermaphrodites. We further demonstrate that disruption of germ granules activates HLH-30-mediated transcriptional program in somatic tissues. Collectively, our findings underscore the essential role of EGGD-1 in germ granule organization and reveal an unexpected germ granule-to-soma communication.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-41556-4
    DOI: 10.1038/s41467-023-41556-4
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    1. Andrew Fire & SiQun Xu & Mary K. Montgomery & Steven A. Kostas & Samuel E. Driver & Craig C. Mello, 1998. "Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans," Nature, Nature, vol. 391(6669), pages 806-811, February.
    2. Oecd, 2018. "Case Law," Nuclear Law Bulletin, OECD Publishing, vol. 2017(1), pages 71-74.
    3. 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.
    4. Louis R. Lapierre & C. Daniel De Magalhaes Filho & Philip R. McQuary & Chu-Chiao Chu & Orane Visvikis & Jessica T. Chang & Sara Gelino & Binnan Ong & Andrew E. Davis & Javier E. Irazoqui & Andrew Dill, 2013. "The TFEB orthologue HLH-30 regulates autophagy and modulates longevity in Caenorhabditis elegans," Nature Communications, Nature, vol. 4(1), pages 1-8, October.
    5. Oecd, 2018. "Case law," Nuclear Law Bulletin, OECD Publishing, vol. 2018(1), pages 84-92.
    6. 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.
    7. Bethany A. Buckley & Kirk B. Burkhart & Sam Guoping Gu & George Spracklin & Aaron Kershner & Heidi Fritz & Judith Kimble & Andrew Fire & Scott Kennedy, 2012. "A nuclear Argonaute promotes multigenerational epigenetic inheritance and germline immortality," Nature, Nature, vol. 489(7416), pages 447-451, September.
    8. Oecd, 2018. "Case law," Nuclear Law Bulletin, OECD Publishing, vol. 2016(2), pages 63-65.
    9. Xin-Xuan Lin & Ilke Sen & Georges E. Janssens & Xin Zhou & Bryan R. Fonslow & Daniel Edgar & Nicholas Stroustrup & Peter Swoboda & John R. Yates & Gary Ruvkun & Christian G. Riedel, 2018. "DAF-16/FOXO and HLH-30/TFEB function as combinatorial transcription factors to promote stress resistance and longevity," Nature Communications, Nature, vol. 9(1), pages 1-15, December.
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