Journal
NATURE CELL BIOLOGY
Volume 22, Issue 2, Pages 235-+Publisher
NATURE PORTFOLIO
DOI: 10.1038/s41556-020-0462-7
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Funding
- NIH Office of Research Infrastructure Programs [P40 OD010440]
- Institut Pasteur, the CNRS
- European Research Council (ERC) under the EU Horizon 2020 research and innovation programme [ERC-StG-679243]
- EU [665807]
- Pasteur-Cantarini Fellowship program
- Region Ile-de-France
- Fondation pour la Recherche Medicale grants
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PIWI-interacting RNAs (piRNAs) promote fertility in many animals. However, whether this is due to their conserved role in repressing repetitive elements (REs) remains unclear. Here, we show that the progressive loss of fertility in Caenorhabditis elegans lacking piRNAs is not caused by derepression of REs or other piRNA targets but, rather, is mediated by epigenetic silencing of all of the replicative histone genes. In the absence of piRNAs, downstream components of the piRNA pathway relocalize from germ granules and piRNA targets to histone mRNAs to synthesize antisense small RNAs (sRNAs) and induce transgenerational silencing. Removal of the downstream components of the piRNA pathway restores histone mRNA expression and fertility in piRNA mutants, and the inheritance of histone sRNAs in wild-type worms adversely affects their fertility for multiple generations. We conclude that sRNA-mediated silencing of histone genes impairs the fertility of piRNA mutants and may serve to maintain piRNAs across evolution. Barucci et al. show that the progressive loss of fertility in Caenorhabditis elegans lacking piRNAs is mediated by the epigenetic silencing of all of the replicative histone genes.
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