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

Beltran, Toni and Barroso, Consuelo and Birkle, Timothy Y. and Stevens, Lewis and Schwartz, Hillel T. and Sternberg, Paul W. and Fradin, Hélène and Gunsalus, Kristin and Piano, Fabio and Sharma, Garima and Cerrato, Chiara and Ahringer, Julie and Martínez-Pérez, Enrique and Blaxter, Mark and Sarkies, Peter (2019) Comparative Epigenomics Reveals that RNA Polymerase II Pausing and Chromatin Domain Organization Control Nematode piRNA Biogenesis. Developmental Cell, 48 (6). pp. 793-810. ISSN 1534-5807. PMCID PMC6436959. https://resolver.caltech.edu/CaltechAUTHORS:20190201-092224279

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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.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1016/j.devcel.2018.12.026DOIArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6436959PubMed CentralArticle
ORCID:
AuthorORCID
Schwartz, Hillel T.0000-0002-3448-8652
Sternberg, Paul W.0000-0002-7699-0173
Blaxter, Mark0000-0003-2861-949X
Sarkies, Peter0000-0003-0279-6199
Additional Information:© 2019 The Author(s). Published by Elsevier under a Creative Commons license (Attribution 4.0 International (CC BY 4.0)). Received 23 February 2018, Revised 6 December 2018, Accepted 27 December 2018, Available online 31 January 2019. Work in the Sarkies laboratory is funded by a grant from the Medical Research Council MC-A652-5PY80. P.S. was funded by an Imperial College Research Fellowship. L.S. was funded by a Bailie-Gifford PhD studentship. We thank the London Institute of Medical Sciences Genomics Facility for sequencing. Some sequencing was carried out at Edinburgh Genomics, which has core support from the NERC Biomolecular Analysis Facility award UKSBS PR18037. Work in the Martínez-Pérez laboratory was funded by a grant from the Medical Research Council MC-A652-5PY60. G.S. was funded by a Newton International Fellowship (Royal Society). J.A. was funded by a Wellcome Senior Research Fellowship (101863). T.Y.B. was funded by a Genetics Society Summer Studentship to the Sarkies lab. We thank Christian Eckmann for sharing parn-1 (tm869) mutant worms and Ben Lehner, Matthias Merkenschlager, and Luis Aragón for helpful comments on the manuscript. Author Contributions: Conceptualization, P.S., M.B., and T.B.; Methodology, T.B., P.S., E.M.P., and M.B.; Investigation, T.B., P.S., C.B., T.Y.B., and L.S.; Formal Analysis, T.B. and P.S.; Resources, J.A., G.S., C.C., H.S., P.W.S., F.P., K.G., and L.S.; Writing – Original Draft, P.S. and T.B.; Writing – Editing, P.S., T.B., M.B., E.M.P., and J.A.; Supervision, P.S., E.M.P., J.A., P.W.S., F.P., K.G., and M.B. Data and Software Availability: Sequencing data has been submitted to the SRA Study SRP117954: Evolution of piRNAs in nematodes. The P. oxycercus and P. sambesii genomes have been uploaded to http://caenorhabditis.org/. The authors declare no competing interests.
Funders:
Funding AgencyGrant Number
Medical Research Council (UK)MC-A652-5PY80
Imperial College LondonUNSPECIFIED
University of OxfordUNSPECIFIED
Natural Environment Research Council (NERC)UKSBS PR18037
Medical Research Council (UK)MC-A652-5PY60
Royal SocietyUNSPECIFIED
Wellcome Trust101863
Genetics SocietyUNSPECIFIED
Subject Keywords:piwi-interacting small RNAs; C. elegans; evolution; chromatin; epigenetics; nematodes; comparative epigenomics
Issue or Number:6
PubMed Central ID:PMC6436959
Record Number:CaltechAUTHORS:20190201-092224279
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20190201-092224279
Official Citation:Toni Beltran, Consuelo Barroso, Timothy Y. Birkle, Lewis Stevens, Hillel T. Schwartz, Paul W. Sternberg, Hélène Fradin, Kristin Gunsalus, Fabio Piano, Garima Sharma, Chiara Cerrato, Julie Ahringer, Enrique Martínez-Pérez, Mark Blaxter, Peter Sarkies, Comparative Epigenomics Reveals that RNA Polymerase II Pausing and Chromatin Domain Organization Control Nematode piRNA Biogenesis, Developmental Cell, Volume 48, Issue 6, 2019, Pages 793-810, ISSN 1534-5807, https://doi.org/10.1016/j.devcel.2018.12.026. (http://www.sciencedirect.com/science/article/pii/S1534580718311262)
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:92559
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:01 Feb 2019 18:22
Last Modified:03 Oct 2019 20:45

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