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Common mechanism of transcription termination at coding and noncoding RNA genes in fission yeast

Termination of RNA polymerase II (RNAPII) transcription is a fundamental step of gene expression that is critical for determining the borders between genes. In budding yeast, termination at protein-coding genes is initiated by the cleavage/polyadenylation machinery, whereas termination of most nonco...

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Autores principales: Larochelle, Marc, Robert, Marc-Antoine, Hébert, Jean-Nicolas, Liu, Xiaochuan, Matteau, Dominick, Rodrigue, Sébastien, Tian, Bin, Jacques, Pierre-Étienne, Bachand, François
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6195540/
https://www.ncbi.nlm.nih.gov/pubmed/30341288
http://dx.doi.org/10.1038/s41467-018-06546-x
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author Larochelle, Marc
Robert, Marc-Antoine
Hébert, Jean-Nicolas
Liu, Xiaochuan
Matteau, Dominick
Rodrigue, Sébastien
Tian, Bin
Jacques, Pierre-Étienne
Bachand, François
author_facet Larochelle, Marc
Robert, Marc-Antoine
Hébert, Jean-Nicolas
Liu, Xiaochuan
Matteau, Dominick
Rodrigue, Sébastien
Tian, Bin
Jacques, Pierre-Étienne
Bachand, François
author_sort Larochelle, Marc
collection PubMed
description Termination of RNA polymerase II (RNAPII) transcription is a fundamental step of gene expression that is critical for determining the borders between genes. In budding yeast, termination at protein-coding genes is initiated by the cleavage/polyadenylation machinery, whereas termination of most noncoding RNA (ncRNA) genes occurs via the Nrd1–Nab3–Sen1 (NNS) pathway. Here, we find that NNS-like transcription termination is not conserved in fission yeast. Rather, genome-wide analyses show global recruitment of mRNA 3′ end processing factors at the end of ncRNA genes, including snoRNAs and snRNAs, and that this recruitment coincides with high levels of Ser2 and Tyr1 phosphorylation on the RNAPII C-terminal domain. We also find that termination of mRNA and ncRNA transcription requires the conserved Ysh1/CPSF-73 and Dhp1/XRN2 nucleases, supporting widespread cleavage-dependent transcription termination in fission yeast. Our findings thus reveal that a common mode of transcription termination can produce functionally and structurally distinct types of polyadenylated and non-polyadenylated RNAs.
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spelling pubmed-61955402018-10-22 Common mechanism of transcription termination at coding and noncoding RNA genes in fission yeast Larochelle, Marc Robert, Marc-Antoine Hébert, Jean-Nicolas Liu, Xiaochuan Matteau, Dominick Rodrigue, Sébastien Tian, Bin Jacques, Pierre-Étienne Bachand, François Nat Commun Article Termination of RNA polymerase II (RNAPII) transcription is a fundamental step of gene expression that is critical for determining the borders between genes. In budding yeast, termination at protein-coding genes is initiated by the cleavage/polyadenylation machinery, whereas termination of most noncoding RNA (ncRNA) genes occurs via the Nrd1–Nab3–Sen1 (NNS) pathway. Here, we find that NNS-like transcription termination is not conserved in fission yeast. Rather, genome-wide analyses show global recruitment of mRNA 3′ end processing factors at the end of ncRNA genes, including snoRNAs and snRNAs, and that this recruitment coincides with high levels of Ser2 and Tyr1 phosphorylation on the RNAPII C-terminal domain. We also find that termination of mRNA and ncRNA transcription requires the conserved Ysh1/CPSF-73 and Dhp1/XRN2 nucleases, supporting widespread cleavage-dependent transcription termination in fission yeast. Our findings thus reveal that a common mode of transcription termination can produce functionally and structurally distinct types of polyadenylated and non-polyadenylated RNAs. Nature Publishing Group UK 2018-10-19 /pmc/articles/PMC6195540/ /pubmed/30341288 http://dx.doi.org/10.1038/s41467-018-06546-x Text en © The Author(s) 2018 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Larochelle, Marc
Robert, Marc-Antoine
Hébert, Jean-Nicolas
Liu, Xiaochuan
Matteau, Dominick
Rodrigue, Sébastien
Tian, Bin
Jacques, Pierre-Étienne
Bachand, François
Common mechanism of transcription termination at coding and noncoding RNA genes in fission yeast
title Common mechanism of transcription termination at coding and noncoding RNA genes in fission yeast
title_full Common mechanism of transcription termination at coding and noncoding RNA genes in fission yeast
title_fullStr Common mechanism of transcription termination at coding and noncoding RNA genes in fission yeast
title_full_unstemmed Common mechanism of transcription termination at coding and noncoding RNA genes in fission yeast
title_short Common mechanism of transcription termination at coding and noncoding RNA genes in fission yeast
title_sort common mechanism of transcription termination at coding and noncoding rna genes in fission yeast
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6195540/
https://www.ncbi.nlm.nih.gov/pubmed/30341288
http://dx.doi.org/10.1038/s41467-018-06546-x
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