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

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journal.pbio.1002061.pdf (1.545Mb)
Date
10/02/2015
Author
Sarkies, Peter
Selkirk, Murray E.
Jones, John T.
Blok, Vivian
Boothby, Thomas
Goldstein, Bob
Hanelt, Ben
Ardila-Garcia, Alex
Fast, Naomi M.
Schiffer, Phillip M.
Kraus, Christopher
Taylor, Mark J.
Koutsovoulos, Georgios
Blaxter, Mark L.
Miska, Eric A.
Keywords
C-elegans
Caenorhabditis-elegans
Functional diversification
Processing center
DNA methylation
QH301 Biology
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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.
Citation
Sarkies , P , Selkirk , M E , Jones , J T , Blok , V , Boothby , T , Goldstein , B , Hanelt , B , Ardila-Garcia , A , Fast , N M , Schiffer , P M , Kraus , C , Taylor , M J , Koutsovoulos , G , Blaxter , M L & Miska , E A 2015 , ' Ancient and novel small RNA pathways compensate for the loss of piRNAs in multiple independent nematode lineages ' , PLoS Biology , vol. 13 , no. 2 , e1002061 . https://doi.org/10.1371/journal.pbio.1002061
Publication
PLoS Biology
Status
Peer reviewed
DOI
https://doi.org/10.1371/journal.pbio.1002061
ISSN
1545-7885
Type
Journal article
Rights
© 2015 Sarkies et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Description
Date of Acceptance: 02/01/2015
Collections
  • University of St Andrews Research
URI
http://hdl.handle.net/10023/7320

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