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PLoS Biol. 2015 Feb 10;13(2):e1002061. doi: 10.1371/journal.pbio.1002061. eCollection 2015 Feb.

Ancient and novel small RNA pathways compensate for the loss of piRNAs in multiple independent nematode lineages.

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MRC Clinical Sciences Centre, Imperial College London, London, United Kingdom.
Department of Life Sciences, Imperial College London, London, United Kingdom.
The James Hutton Institute, Invergowrie, Dundee, United Kingdom.
Department of Biology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of America.
Center for Evolutionary and Theoretical Immunology, Department of Biology, University of New Mexico, Albuquerque, New Mexico, United States of America.
Department of Botany, University of British Columbia, Vancouver, British Columbia, Canada.
Zoologisches Institut, Universität zu Köln, Cologne, NRW, Germany.
Molecular and Biochemical Parasitology, Liverpool School of Tropical Medicine, Liverpool, United Kingdom.
Institute of Evolutionary Biology, University of Edinburgh, Edinburgh, United Kingdom.
Wellcome Trust/Cancer Research UK Gurdon Institute, Cambridge, United Kingdom.


Small RNA pathways act at the front line of defence against transposable elements across the Eukaryota. In animals, Piwi interacting small RNAs (piRNAs) are a crucial arm of this defence. However, the evolutionary relationships among piRNAs and other small RNA pathways targeting transposable elements are poorly resolved. To address this question we sequenced small RNAs from multiple, diverse nematode species, producing the first phylum-wide analysis of how small RNA pathways evolve. Surprisingly, despite their prominence in Caenorhabditis elegans and closely related nematodes, piRNAs are absent in all other nematode lineages. We found that there are at least two evolutionarily distinct mechanisms that compensate for the absence of piRNAs, both involving RNA-dependent RNA polymerases (RdRPs). Whilst one pathway is unique to nematodes, the second involves Dicer-dependent RNA-directed DNA methylation, hitherto unknown in animals, and bears striking similarity to transposon-control mechanisms in fungi and plants. Our results highlight the rapid, context-dependent evolution of small RNA pathways and suggest piRNAs in animals may have replaced an ancient eukaryotic RNA-dependent RNA polymerase pathway to control transposable elements.

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