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

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cam.issuedOnline2018-06-18
dc.contributor.authorAtkinson, Sophie R
dc.contributor.authorMarguerat, Samuel
dc.contributor.authorBitton, Danny A
dc.contributor.authorRodríguez-López, Maria
dc.contributor.authorRallis, Charalampos
dc.contributor.authorLemay, Jean-François
dc.contributor.authorCotobal, Cristina
dc.contributor.authorMalecki, Michal
dc.contributor.authorSmialowski, Pawel
dc.contributor.authorMata, Juan
dc.contributor.authorKorber, Philipp
dc.contributor.authorBachand, François
dc.contributor.authorBähler, Jürg
dc.contributor.orcidMarguerat, Samuel [0000-0002-2402-3165]
dc.contributor.orcidBitton, Danny A [0000-0003-3282-1017]
dc.contributor.orcidRodríguez-López, Maria [0000-0002-2066-0589]
dc.contributor.orcidRallis, Charalampos [0000-0002-4390-0266]
dc.contributor.orcidCotobal, Cristina [0000-0002-5877-2228]
dc.contributor.orcidMalecki, Michal [0000-0002-1525-5036]
dc.contributor.orcidBähler, Jürg [0000-0003-4036-1532]
dc.date.accessioned2018-10-10T17:30:43Z
dc.date.available2018-10-10T17:30:43Z
dc.date.issued2018-09
dc.description.abstractLong 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.
dc.format.mediumPrint-Electronic
dc.identifier.doi10.17863/CAM.30940
dc.identifier.eissn1469-9001
dc.identifier.issn1355-8382
dc.identifier.urihttps://www.repository.cam.ac.uk/handle/1810/283578
dc.languageeng
dc.language.isoeng
dc.publisherCold Spring Harbor Laboratory
dc.publisher.urlhttp://dx.doi.org/10.1261/rna.065524.118
dc.rightsAttribution 4.0 International
dc.rights.urihttps://creativecommons.org/licenses/by/4.0/
dc.subjectNMD pathway
dc.subjectRNA degradation
dc.subjectSchizosaccharomyces pombe
dc.subjectantisense RNA
dc.subjectcytoplasmic exonuclease
dc.subjectpervasive transcription
dc.subjectCell Nucleus
dc.subjectCytoplasm
dc.subjectExonucleases
dc.subjectExosomes
dc.subjectFungal Proteins
dc.subjectGene Expression Profiling
dc.subjectGene Expression Regulation, Fungal
dc.subjectMeiosis
dc.subjectMolecular Sequence Annotation
dc.subjectMutation
dc.subjectRNA Interference
dc.subjectRNA Stability
dc.subjectRNA, Fungal
dc.subjectRNA, Long Noncoding
dc.subjectSchizosaccharomyces
dc.subjectSequence Analysis, RNA
dc.titleLong noncoding RNA repertoire and targeting by nuclear exosome, cytoplasmic exonuclease, and RNAi in fission yeast.
dc.typeArticle
dcterms.dateAccepted2018-06-14
prism.endingPage1213
prism.issueIdentifier9
prism.publicationDate2018
prism.publicationNameRNA
prism.startingPage1195
prism.volume24
pubs.funder-project-idBiotechnology and Biological Sciences Research Council (BB/M021483/1)
rioxxterms.licenseref.startdate2018-09
rioxxterms.licenseref.urihttp://www.rioxx.net/licenses/all-rights-reserved
rioxxterms.typeJournal Article/Review
rioxxterms.versionVoR
rioxxterms.versionofrecord10.1261/rna.065524.118

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