Long non-coding RNA repertoire and targeting by nuclear exosome, cytoplasmic exonuclease and RNAi in fission yeast

Article


Atkinson, Sophie, Marguerat, Samuel, Bitton, Danny, Bachand, Francois, Rodriguez-Lopez, Maria, Rallis, C., Lemay, Jean-Francois, Cotobal, Cristina, Malecki, Michal, Smialowski, Pawel, Mata, Juan, Korber, Philipp and Bahler, Jurg 2018. Long non-coding RNA repertoire and targeting by nuclear exosome, cytoplasmic exonuclease and RNAi in fission yeast. RNA. 24 (9), pp. 1195-1213.
AuthorsAtkinson, Sophie, Marguerat, Samuel, Bitton, Danny, Bachand, Francois, Rodriguez-Lopez, Maria, Rallis, C., Lemay, Jean-Francois, Cotobal, Cristina, Malecki, Michal, Smialowski, Pawel, Mata, Juan, Korber, Philipp and Bahler, Jurg
Abstract

Long non-coding RNAs (lncRNAs), which are longer than 200 nucleotides but often
unstable, contribute a substantial and diverse portion to pervasive non-coding
transcriptomes. Most lncRNAs are poorly annotated and understood, although several play
important roles in gene regulation and diseases. Here we systematically uncover and
analyse 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-times 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.

JournalRNA
Journal citation24 (9), pp. 1195-1213
ISSN1355-8382
Year2018
PublisherCold Spring Harbor Laboratory Press for RNA Society
Accepted author manuscript
License
File Access Level
Repository staff only
Publisher's version
License
File Access Level
Anyone
Digital Object Identifier (DOI)doi:10.1261/rna.065524.118
Web address (URL)https://doi.org/10.1261/rna.065524.118
Publication dates
PrintSep 2018
Online18 Jun 2018
Publication process dates
Deposited22 Jun 2018
Accepted14 Jun 2018
Accepted14 Jun 2018
FunderWellcome Trust
Royal Society Wolfson Research Merit Award
Medical Research Council
Canadian Institutes of Health Research
Biotechnology and Biological Sciences Research Council
Copyright information© 2018 The authors
LicenseCC BY 4.0
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https://repository.uel.ac.uk/item/846y0

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