Chromosome-wide mechanisms to decouple gene expression from gene dose during sex-chromosome evolution
- Howard Hughes Medical Institute, University of California, Berkeley, United States
- Howard Hughes Medical Institute, University of Utah, United States
Abstract
Changes in chromosome number impair fitness by disrupting the balance of gene expression. Here we analyze mechanisms to compensate for changes in gene dose that accompanied the evolution of sex chromosomes from autosomes. Using single-copy transgenes integrated throughout the Caenorhabditis elegans genome, we show that expression of all X-linked transgenes is balanced between XX hermaphrodites and XO males. However, proximity of a dosage compensation complex (DCC) binding site (rex site) is neither necessary to repress X-linked transgenes nor sufficient to repress transgenes on autosomes. Thus, X is broadly permissive for dosage compensation, and the DCC acts via a chromosome-wide mechanism to balance transcription between sexes. In contrast, no analogous X-chromosome-wide mechanism balances transcription between X and autosomes: expression of compensated hermaphrodite X-linked transgenes is half that of autosomal transgenes. Furthermore, our results argue against an X-chromosome dosage compensation model contingent upon rex-directed positioning of X relative to the nuclear periphery.
Data availability
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SRR023579.sraPublicly available at the Sequence Read Archive + (accession no: GSE20136).
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Transcriptome Analysis of roundwormPublicly available at the NCBI Short Read Archive (accession no: GSE20136).
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Condensin Controls Recruitment of RNA Polymerase II to Achieve X-Chromosome Dosage CompensationPublicly availale at the NCBI Gene Expression Omnibus (accession no: GSE43087).
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SRR031122.sraPublicly available at the Sequence Read Archive + (accession no: GSE20136).
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SRR031123.sraPublicly available at the Sequence Read Archive + (accession no: GSE20136).
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Condensin-Driven Remodeling of X-Chromosome Topology during Dosage CompensationPublicly available at the NCBI Gene Expression Omnibus (accession no: GSE59716).
Article and author information
Author details
Funding
National Institutes of Health (1R01 GM030702)
- Barbara J Meyer
Howard Hughes Medical Institute
- Barbara J Meyer
National Institutes of Health (1F32 GM100647)
- Bayly S Wheeler
Howard Hughes Medical Institute
- Christian Frøkjær-Jensen
National Institutes of Health (1R01 GM095817)
- Erik Jorgensen
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Edith Heard, Institut Curie, France
Version history
- Received: April 29, 2016
- Accepted: August 29, 2016
- Accepted Manuscript published: August 30, 2016 (version 1)
- Accepted Manuscript updated: September 1, 2016 (version 2)
- Version of Record published: October 3, 2016 (version 3)
Copyright
© 2016, Wheeler 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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Chromosome-wide mechanisms to decouple gene expression from gene dose during sex-chromosome evolution
eLife 5:e17365.
https://doi.org/10.7554/eLife.17365
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