Long noncoding RNA repertoire and targeting by nuclear exosome, cytoplasmic exonuclease, and RNAi in fission yeast.
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Authors
Atkinson, Sophie R
Lemay, Jean-François
Smialowski, Pawel
Korber, Philipp
Bachand, François
Publication Date
2018-09Journal Title
RNA
ISSN
1355-8382
Publisher
Cold Spring Harbor Laboratory
Volume
24
Issue
9
Pages
1195-1213
Language
eng
Type
Article
Physical Medium
Print-Electronic
Metadata
Show full item recordCitation
Atkinson, S. R., Marguerat, S., Bitton, D. A., Rodríguez-López, M., Rallis, C., Lemay, J., Cotobal, C., et al. (2018). Long noncoding RNA repertoire and targeting by nuclear exosome, cytoplasmic exonuclease, and RNAi in fission yeast.. RNA, 24 (9), 1195-1213. https://doi.org/10.1261/rna.065524.118
Abstract
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.
Keywords
Cell Nucleus, Cytoplasm, Schizosaccharomyces, Exonucleases, Fungal Proteins, RNA, Fungal, Gene Expression Profiling, Sequence Analysis, RNA, Meiosis, Gene Expression Regulation, Fungal, RNA Interference, RNA Stability, Mutation, Exosomes, Molecular Sequence Annotation, RNA, Long Noncoding
Sponsorship
Biotechnology and Biological Sciences Research Council (BB/M021483/1)
Identifiers
External DOI: https://doi.org/10.1261/rna.065524.118
This record's URL: https://www.repository.cam.ac.uk/handle/1810/283578
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