title: Ancient and novel small RNA pathways compensate for the loss of piRNAs in multiple independent nematode lineages.
abstract: 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.
authors: MRC Clinical Sciences Centre, Imperial College London, London, United Kingdom.
authors: Peter
authors: P
authors: Sarkies
authors: Department of Life Sciences, Imperial College London, London, United Kingdom.
authors: Murray E
authors: ME
authors: Selkirk
authors: The James Hutton Institute, Invergowrie, Dundee, United Kingdom.
authors: John T
authors: JT
authors: Jones
authors: The James Hutton Institute, Invergowrie, Dundee, United Kingdom.
authors: Vivian
authors: V
authors: Blok
authors: Department of Biology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of America.
authors: Thomas
authors: T
authors: Boothby
authors: Department of Biology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of America.
authors: Bob
authors: B
authors: Goldstein
authors: Center for Evolutionary and Theoretical Immunology, Department of Biology, University of New Mexico, Albuquerque, New Mexico, United States of America.
authors: Ben
authors: B
authors: Hanelt
authors: Department of Botany, University of British Columbia, Vancouver, British Columbia, Canada.
authors: Alex
authors: A
authors: Ardila-Garcia
authors: Department of Botany, University of British Columbia, Vancouver, British Columbia, Canada.
authors: Naomi M
authors: NM
authors: Fast
authors: Zoologisches Institut, Universität zu Köln, Cologne, NRW, Germany.
authors: Phillip M
authors: PM
authors: Schiffer
authors: Zoologisches Institut, Universität zu Köln, Cologne, NRW, Germany.
authors: Christopher
authors: C
authors: Kraus
authors: Molecular and Biochemical Parasitology, Liverpool School of Tropical Medicine, Liverpool, United Kingdom.
authors: Mark J
authors: MJ
authors: Taylor
authors: Institute of Evolutionary Biology, University of Edinburgh, Edinburgh, United Kingdom.
authors: Georgios
authors: G
authors: Koutsovoulos
authors: Institute of Evolutionary Biology, University of Edinburgh, Edinburgh, United Kingdom.
authors: Mark L
authors: ML
authors: Blaxter
authors: Wellcome Trust/Cancer Research UK Gurdon Institute, Cambridge, United Kingdom.
authors: Eric A
authors: EA
authors: Miska
mesh_terms: D000595:Amino Acid Sequence; D000818:Animals; D001483:Base Sequence; D005075:Biological Evolution; D017173:Caenorhabditis elegans / Q000235:genetics* / Q000276:immunology / Q000378:metabolism; D029742:Caenorhabditis elegans Proteins / Q000235:genetics* / Q000378:metabolism; D019175:DNA Methylation; D004251:DNA Transposable Elements / Q000276:immunology; D004331:Drosophila melanogaster / Q000235:genetics / Q000276:immunology / Q000378:metabolism; D005786:Gene Expression Regulation; D006801:Humans; D035683:MicroRNAs / Q000235:genetics* / Q000378:metabolism; D008969:Molecular Sequence Data; D009348:Nematoda / Q000145:classification / Q000235:genetics* / Q000276:immunology / Q000378:metabolism; D010802:Phylogeny; D034741:RNA, Small Interfering / Q000235:genetics* / Q000378:metabolism; D012324:RNA-Dependent RNA Polymerase / Q000235:genetics / Q000378:metabolism; D043244:Ribonuclease III / Q000235:genetics / Q000378:metabolism
chemical_list: D029742:Caenorhabditis elegans Proteins; D004251:DNA Transposable Elements; D035683:MicroRNAs; D034741:RNA, Small Interfering; D012324:RNA-Dependent RNA Polymerase; D043244:Ribonuclease III