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Dev Cell. 2019 Jan 30. pii: S1534-5807(18)31126-2. doi: 10.1016/j.devcel.2018.12.026. [Epub ahead of print]

Comparative Epigenomics Reveals that RNA Polymerase II Pausing and Chromatin Domain Organization Control Nematode piRNA Biogenesis.

Author information

1
MRC London Institute of Medical Sciences, London W12 0NN, UK; Institute of Clinical Sciences, Imperial College London, London W12 0NN, UK.
2
Institute of Evolutionary Biology, School of Biological Sciences, University of Edinburgh, Edinburgh EH9 3TF, UK.
3
Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA 91125, USA.
4
Department of Biology, New York University, New York, NY 10003, USA; Center for Genomics and Systems Biology, New York University, New York, NY 10003, USA; Center for Genomics and Systems Biology, New York University Abu Dhabi, Abu Dhabi, United Arab Emirates.
5
The Gurdon Institute and Department of Genetics, University of Cambridge, Cambridge, UK.
6
Institute of Evolutionary Biology, School of Biological Sciences, University of Edinburgh, Edinburgh EH9 3TF, UK. Electronic address: mark.blaxter@ed.ac.uk.
7
MRC London Institute of Medical Sciences, London W12 0NN, UK; Institute of Clinical Sciences, Imperial College London, London W12 0NN, UK. Electronic address: psarkies@imperial.ac.uk.

Abstract

Piwi-interacting RNAs (piRNAs) are important for genome regulation across metazoans, but their biogenesis evolves rapidly. In Caenorhabditis elegans, piRNA loci are clustered within two 3-Mb regions on chromosome IV. Each piRNA locus possesses an upstream motif that recruits RNA polymerase II to produce an ∼28 nt primary transcript. We used comparative epigenomics across nematodes to gain insight into the origin, evolution, and mechanism of nematode piRNA biogenesis. We show that the piRNA upstream motif is derived from core promoter elements controlling snRNA transcription. We describe two alternative modes of piRNA organization in nematodes: in C. elegans and closely related nematodes, piRNAs are clustered within repressive H3K27me3 chromatin, while in other species, typified by Pristionchus pacificus, piRNAs are found within introns of active genes. Additionally, we discover that piRNA production depends on sequence signals associated with RNA polymerase II pausing. We show that pausing signals synergize with chromatin to control piRNA transcription.

KEYWORDS:

C. elegans; chromatin; comparative epigenomics; epigenetics; evolution; nematodes; piwi-interacting small RNAs

PMID:
30713076
DOI:
10.1016/j.devcel.2018.12.026
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