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Small RNA pathways in the nematode Ascaris in the absence of piRNAs

Author

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  • Maxim V. Zagoskin

    (University of Colorado School of Medicine
    University of Colorado School of Medicine
    University of Tennessee)

  • Jianbin Wang

    (University of Colorado School of Medicine
    University of Colorado School of Medicine
    University of Tennessee
    University of Tennessee)

  • Ashley T. Neff

    (University of Colorado School of Medicine)

  • Giovana M. B. Veronezi

    (University of Colorado School of Medicine)

  • Richard E. Davis

    (University of Colorado School of Medicine
    University of Colorado School of Medicine)

Abstract

Small RNA pathways play key and diverse regulatory roles in C. elegans, but our understanding of their conservation and contributions in other nematodes is limited. We analyzed small RNA pathways in the divergent parasitic nematode Ascaris. Ascaris has ten Argonautes with five worm-specific Argonautes (WAGOs) that associate with secondary 5’-triphosphate 22-24G-RNAs. These small RNAs target repetitive sequences or mature mRNAs and are similar to the C. elegans mutator, nuclear, and CSR-1 small RNA pathways. Even in the absence of a piRNA pathway, Ascaris CSR-1 may still function to “license” as well as fine-tune or repress gene expression. Ascaris ALG-4 and its associated 26G-RNAs target and likely repress specific mRNAs during testis meiosis. Ascaris WAGO small RNAs demonstrate target plasticity changing their targets between repeats and mRNAs during development. We provide a unique and comprehensive view of mRNA and small RNA expression throughout spermatogenesis. Overall, our study illustrates the conservation, divergence, dynamics, and flexibility of small RNA pathways in nematodes.

Suggested Citation

  • Maxim V. Zagoskin & Jianbin Wang & Ashley T. Neff & Giovana M. B. Veronezi & Richard E. Davis, 2022. "Small RNA pathways in the nematode Ascaris in the absence of piRNAs," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-28482-7
    DOI: 10.1038/s41467-022-28482-7
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    1. Christopher A. Brosnan & Alexander J. Palmer & Steven Zuryn, 2021. "Cell-type-specific profiling of loaded miRNAs from Caenorhabditis elegans reveals spatial and temporal flexibility in Argonaute loading," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
    2. Amy H. Buck & Gillian Coakley & Fabio Simbari & Henry J. McSorley & Juan F. Quintana & Thierry Le Bihan & Sujai Kumar & Cei Abreu-Goodger & Marissa Lear & Yvonne Harcus & Alessandro Ceroni & Simon A. , 2014. "Exosomes secreted by nematode parasites transfer small RNAs to mammalian cells and modulate innate immunity," Nature Communications, Nature, vol. 5(1), pages 1-12, December.
    3. Shouhong Guang & Aaron F. Bochner & Kirk B. Burkhart & Nick Burton & Derek M. Pavelec & Scott Kennedy, 2010. "Small regulatory RNAs inhibit RNA polymerase II during the elongation phase of transcription," Nature, Nature, vol. 465(7301), pages 1097-1101, June.
    4. Johan Hoogen & Stefan Geisen & Devin Routh & Howard Ferris & Walter Traunspurger & David A. Wardle & Ron G. M. Goede & Byron J. Adams & Wasim Ahmad & Walter S. Andriuzzi & Richard D. Bardgett & Michae, 2019. "Soil nematode abundance and functional group composition at a global scale," Nature, Nature, vol. 572(7768), pages 194-198, August.
    5. 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.
    6. Nico Eisenhauer & Carlos A. Guerra, 2019. "Global maps of soil-dwelling nematode worms," Nature, Nature, vol. 572(7768), pages 187-188, August.
    7. 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.
    8. 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.
    9. Mark L. Blaxter & Paul De Ley & James R. Garey & Leo X. Liu & Patsy Scheldeman & Andy Vierstraete & Jacques R. Vanfleteren & Laura Y. Mackey & Mark Dorris & Linda M. Frisse & J. T. Vida & W. Kelley Th, 1998. "A molecular evolutionary framework for the phylum Nematoda," Nature, Nature, vol. 392(6671), pages 71-75, March.
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