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.
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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RNA interference (RNAi) is a conserved pathway that utilizes Argonaute proteins and their associated small RNAs to exert gene regulatory function on complementary transcripts. While the majority of germline-expressed RNAi proteins reside in perinuclear germ granules, it is unknown whether and how RNAi pathways are spatially organized in other cell types. Here, we find that the small RNA biogenesis machinery is spatially and temporally organized during Caenorhabditis elegans embryogenesis. Specifically, the RNAi factor, SIMR-1, forms visible concentrates during mid-embryogenesis that contain an RNA-dependent RNA polymerase, a poly-UG polymerase, and the unloaded nuclear Argonaute protein, NRDE-3. Curiously, coincident with the appearance of the SIMR granules, the small RNAs bound to NRDE-3 switch from predominantly CSR-class 22G-RNAs to ERGO-dependent 22G-RNAs. NRDE-3 binds ERGO-dependent 22G-RNAs in the somatic cells of larvae and adults to silence ERGO-target genes; here we further demonstrate that NRDE-3-bound, CSR-class 22G-RNAs repress transcription in oocytes. Thus, our study defines two separable roles for NRDE-3, targeting germline-expressed genes during oogenesis to promote global transcriptional repression, and switching during embryogenesis to repress recently duplicated genes and retrotransposons in somatic cells, highlighting the plasticity of Argonaute proteins and the need for more precise temporal characterization of Argonaute-small RNA interactions.
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