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P granules protect RNA interference genes from silencing by piRNAs

John Paul T. Ouyang, View ORCID ProfileAndrew Folkmann, Lauren Bernard, View ORCID ProfileChih-Yung Lee, Uri Seroussi, Amanda G. Charlesworth, Julie M. Claycomb, View ORCID ProfileGeraldine Seydoux
doi: https://doi.org/10.1101/707562
John Paul T. Ouyang
1HHMI and Dept. of Molecular Biology and Genetics, Johns Hopkins University School of Medicine, Baltimore MD USA
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Andrew Folkmann
1HHMI and Dept. of Molecular Biology and Genetics, Johns Hopkins University School of Medicine, Baltimore MD USA
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Lauren Bernard
1HHMI and Dept. of Molecular Biology and Genetics, Johns Hopkins University School of Medicine, Baltimore MD USA
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Chih-Yung Lee
1HHMI and Dept. of Molecular Biology and Genetics, Johns Hopkins University School of Medicine, Baltimore MD USA
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Uri Seroussi
2Department of Molecular Genetics, University of Toronto, Toronto, Canada
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Amanda G. Charlesworth
2Department of Molecular Genetics, University of Toronto, Toronto, Canada
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Julie M. Claycomb
2Department of Molecular Genetics, University of Toronto, Toronto, Canada
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Geraldine Seydoux
1HHMI and Dept. of Molecular Biology and Genetics, Johns Hopkins University School of Medicine, Baltimore MD USA
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  • ORCID record for Geraldine Seydoux
  • For correspondence: gseydoux@jhmi.edu
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SUMMARY

P granules are perinuclear condensates in C. elegans germ cells proposed to serve as hubs for self/non-self RNA discrimination by Argonautes. We report that a mutant (meg-3 meg-4) that does not assemble P granules in primordial germ cells loses competence for RNA-interference over several generations and accumulates silencing small RNAs against hundreds of endogenous genes, including the RNA-interference genes rde-11 and sid-1. In wild-type, rde-11 and sid-1 transcripts are heavily targeted by piRNAs, accumulate in P granules, but maintain expression. In the primordial germ cells of meg-3 meg-4 mutants, rde-11 and sid-1 transcripts disperse in the cytoplasm with the small RNA biogenesis machinery, become hyper-targeted by secondary sRNAs, and are eventually silenced. Silencing requires the PIWI-class Argonaute PRG-1 and the nuclear Argonaute HRDE-1 that maintains trans-generational silencing of piRNA targets. These observations support a “safe harbor” model for P granules in protecting germline transcripts from piRNA-initiated silencing.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted July 18, 2019.
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P granules protect RNA interference genes from silencing by piRNAs
John Paul T. Ouyang, Andrew Folkmann, Lauren Bernard, Chih-Yung Lee, Uri Seroussi, Amanda G. Charlesworth, Julie M. Claycomb, Geraldine Seydoux
bioRxiv 707562; doi: https://doi.org/10.1101/707562
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P granules protect RNA interference genes from silencing by piRNAs
John Paul T. Ouyang, Andrew Folkmann, Lauren Bernard, Chih-Yung Lee, Uri Seroussi, Amanda G. Charlesworth, Julie M. Claycomb, Geraldine Seydoux
bioRxiv 707562; doi: https://doi.org/10.1101/707562

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