Condensin controls cellular RNA levels through the accurate segregation of chromosomes instead of directly regulating transcription
- CNRS, France
- MRC London Institute of Medical Sciences (LMS), United Kingdom
- European Molecular Biology Laboratory, Germany
Abstract
Condensins are genome organisers that shape chromosomes and promote their accurate transmission. Several studies have also implicated condensins in gene expression, although any mechanisms have remained enigmatic. Here, we report on the role of condensin in gene expression in fission and budding yeasts. In contrast to previous studies, we provide compelling evidence that condensin plays no direct role in the maintenance of the transcriptome, neither during interphase nor during mitosis. We further show that the changes in gene expression in post-mitotic fission yeast cells that result from condensin inactivation are largely a consequence of chromosome missegregation during anaphase, which notably depletes the RNA-exosome from daughter cells. Crucially, preventing karyotype abnormalities in daughter cells restores a normal transcriptome despite condensin inactivation. Thus, chromosome instability, rather than a direct role of condensin in the transcription process, changes gene expression. This knowledge challenges the concept of gene regulation by canonical condensin complexes.
Data availability
RNA-seq data are accessible from the Gene Expression Omnibus (GEO) database under the accession number GSE112281.Microarrays data are available as supplemental table in excel format
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Condensin controls cellular RNA levels through the accurate segregation of chromosomes instead of directly regulating transcriptionPublicly available at the NCBI Gene Expression Omnibus (accession no: GSE112281).
Article and author information
Author details
Sara Cuylen-Haering
Christian H Haering
Funding
Centre National de la Recherche Scientifique
- Pascal Bernard
Agence Nationale de la Recherche (ANR-15-CE12-0002-01)
- Xavier Robellet
- Pascal Bernard
Fondation ARC pour la Recherche sur le Cancer (PJA 20151203343)
- Pascal Bernard
Ligue Régionale Contre le Cancer - comité du Rhône
- Pascal Bernard
Medical Research Council
- Xi-Ming Sun
- Samuel Marguerat
European Molecular Biology Laboratory
- Sara Cuylen-Haering
- Sandra Clauder-Münster
- Lars Steinmetz
- Christian H Haering
Fondation pour la Recherche Médicale (FDT20170437039)
- Clémence Hocquet
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Job Dekker, University of Massachusetts Medical School, United States
Version history
- Received: May 20, 2018
- Accepted: September 18, 2018
- Accepted Manuscript published: September 19, 2018 (version 1)
- Version of Record published: October 5, 2018 (version 2)
Copyright
© 2018, Hocquet et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Condensin controls cellular RNA levels through the accurate segregation of chromosomes instead of directly regulating transcription
eLife 7:e38517.
https://doi.org/10.7554/eLife.38517
Further reading
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Splicing is the stepwise molecular process by which introns are removed from pre-mRNA and exons are joined together to form mature mRNA sequences. The ordering and spatial distribution of these steps remain controversial, with opposing models suggesting splicing occurs either during or after transcription. We used single-molecule RNA FISH, expansion microscopy, and live-cell imaging to reveal the spatiotemporal distribution of nascent transcripts in mammalian cells. At super-resolution levels, we found that pre-mRNA formed clouds around the transcription site. These clouds indicate the existence of a transcription-site-proximal zone through which RNA move more slowly than in the nucleoplasm. Full-length pre-mRNA undergo continuous splicing as they move through this zone following transcription, suggesting a model in which splicing can occur post-transcriptionally but still within the proximity of the transcription site, thus seeming co-transcriptional by most assays. These results may unify conflicting reports of co-transcriptional versus post-transcriptional splicing.
