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Long noncoding RNA repertoire and targeting by nuclear exosome, cytoplasmic exonuclease, and RNAi in fission yeast

Long noncoding RNAs (lncRNAs), which are longer than 200 nucleotides but often unstable, contribute a substantial and diverse portion to pervasive noncoding transcriptomes. Most lncRNAs are poorly annotated and understood, although several play important roles in gene regulation and diseases. Here w...

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Autores principales: Atkinson, Sophie R., Marguerat, Samuel, Bitton, Danny A., Rodríguez-López, Maria, Rallis, Charalampos, Lemay, Jean-François, Cotobal, Cristina, Malecki, Michal, Smialowski, Pawel, Mata, Juan, Korber, Philipp, Bachand, François, Bähler, Jürg
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory Press 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6097657/
https://www.ncbi.nlm.nih.gov/pubmed/29914874
http://dx.doi.org/10.1261/rna.065524.118
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author Atkinson, Sophie R.
Marguerat, Samuel
Bitton, Danny A.
Rodríguez-López, Maria
Rallis, Charalampos
Lemay, Jean-François
Cotobal, Cristina
Malecki, Michal
Smialowski, Pawel
Mata, Juan
Korber, Philipp
Bachand, François
Bähler, Jürg
author_facet Atkinson, Sophie R.
Marguerat, Samuel
Bitton, Danny A.
Rodríguez-López, Maria
Rallis, Charalampos
Lemay, Jean-François
Cotobal, Cristina
Malecki, Michal
Smialowski, Pawel
Mata, Juan
Korber, Philipp
Bachand, François
Bähler, Jürg
author_sort Atkinson, Sophie R.
collection PubMed
description Long noncoding RNAs (lncRNAs), which are longer than 200 nucleotides but often unstable, contribute a substantial and diverse portion to pervasive noncoding transcriptomes. Most lncRNAs are poorly annotated and understood, although several play important roles in gene regulation and diseases. Here we systematically uncover and analyze lncRNAs in Schizosaccharomyces pombe. Based on RNA-seq data from twelve RNA-processing mutants and nine physiological conditions, we identify 5775 novel lncRNAs, nearly 4× the previously annotated lncRNAs. The expression of most lncRNAs becomes strongly induced under the genetic and physiological perturbations, most notably during late meiosis. Most lncRNAs are cryptic and suppressed by three RNA-processing pathways: the nuclear exosome, cytoplasmic exonuclease, and RNAi. Double-mutant analyses reveal substantial coordination and redundancy among these pathways. We classify lncRNAs by their dominant pathway into cryptic unstable transcripts (CUTs), Xrn1-sensitive unstable transcripts (XUTs), and Dicer-sensitive unstable transcripts (DUTs). XUTs and DUTs are enriched for antisense lncRNAs, while CUTs are often bidirectional and actively translated. The cytoplasmic exonuclease, along with RNAi, dampens the expression of thousands of lncRNAs and mRNAs that become induced during meiosis. Antisense lncRNA expression mostly negatively correlates with sense mRNA expression in the physiological, but not the genetic conditions. Intergenic and bidirectional lncRNAs emerge from nucleosome-depleted regions, upstream of positioned nucleosomes. Our results highlight both similarities and differences to lncRNA regulation in budding yeast. This broad survey of the lncRNA repertoire and characteristics in S. pombe, and the interwoven regulatory pathways that target lncRNAs, provides a rich framework for their further functional analyses.
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spelling pubmed-60976572018-09-01 Long noncoding RNA repertoire and targeting by nuclear exosome, cytoplasmic exonuclease, and RNAi in fission yeast Atkinson, Sophie R. Marguerat, Samuel Bitton, Danny A. Rodríguez-López, Maria Rallis, Charalampos Lemay, Jean-François Cotobal, Cristina Malecki, Michal Smialowski, Pawel Mata, Juan Korber, Philipp Bachand, François Bähler, Jürg RNA Article Long noncoding RNAs (lncRNAs), which are longer than 200 nucleotides but often unstable, contribute a substantial and diverse portion to pervasive noncoding transcriptomes. Most lncRNAs are poorly annotated and understood, although several play important roles in gene regulation and diseases. Here we systematically uncover and analyze lncRNAs in Schizosaccharomyces pombe. Based on RNA-seq data from twelve RNA-processing mutants and nine physiological conditions, we identify 5775 novel lncRNAs, nearly 4× the previously annotated lncRNAs. The expression of most lncRNAs becomes strongly induced under the genetic and physiological perturbations, most notably during late meiosis. Most lncRNAs are cryptic and suppressed by three RNA-processing pathways: the nuclear exosome, cytoplasmic exonuclease, and RNAi. Double-mutant analyses reveal substantial coordination and redundancy among these pathways. We classify lncRNAs by their dominant pathway into cryptic unstable transcripts (CUTs), Xrn1-sensitive unstable transcripts (XUTs), and Dicer-sensitive unstable transcripts (DUTs). XUTs and DUTs are enriched for antisense lncRNAs, while CUTs are often bidirectional and actively translated. The cytoplasmic exonuclease, along with RNAi, dampens the expression of thousands of lncRNAs and mRNAs that become induced during meiosis. Antisense lncRNA expression mostly negatively correlates with sense mRNA expression in the physiological, but not the genetic conditions. Intergenic and bidirectional lncRNAs emerge from nucleosome-depleted regions, upstream of positioned nucleosomes. Our results highlight both similarities and differences to lncRNA regulation in budding yeast. This broad survey of the lncRNA repertoire and characteristics in S. pombe, and the interwoven regulatory pathways that target lncRNAs, provides a rich framework for their further functional analyses. Cold Spring Harbor Laboratory Press 2018-09 /pmc/articles/PMC6097657/ /pubmed/29914874 http://dx.doi.org/10.1261/rna.065524.118 Text en © 2018 Atkinson et al.; Published by Cold Spring Harbor Laboratory Press for the RNA Society http://creativecommons.org/licenses/by/4.0/ This article, published in RNA, is available under a Creative Commons License (Attribution 4.0 International), as described at http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Atkinson, Sophie R.
Marguerat, Samuel
Bitton, Danny A.
Rodríguez-López, Maria
Rallis, Charalampos
Lemay, Jean-François
Cotobal, Cristina
Malecki, Michal
Smialowski, Pawel
Mata, Juan
Korber, Philipp
Bachand, François
Bähler, Jürg
Long noncoding RNA repertoire and targeting by nuclear exosome, cytoplasmic exonuclease, and RNAi in fission yeast
title Long noncoding RNA repertoire and targeting by nuclear exosome, cytoplasmic exonuclease, and RNAi in fission yeast
title_full Long noncoding RNA repertoire and targeting by nuclear exosome, cytoplasmic exonuclease, and RNAi in fission yeast
title_fullStr Long noncoding RNA repertoire and targeting by nuclear exosome, cytoplasmic exonuclease, and RNAi in fission yeast
title_full_unstemmed Long noncoding RNA repertoire and targeting by nuclear exosome, cytoplasmic exonuclease, and RNAi in fission yeast
title_short Long noncoding RNA repertoire and targeting by nuclear exosome, cytoplasmic exonuclease, and RNAi in fission yeast
title_sort long noncoding rna repertoire and targeting by nuclear exosome, cytoplasmic exonuclease, and rnai in fission yeast
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6097657/
https://www.ncbi.nlm.nih.gov/pubmed/29914874
http://dx.doi.org/10.1261/rna.065524.118
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