Chromosome-wide mechanisms to decouple gene expression from gene dose during sex-chromosome evolution

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Data availability
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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

The following previously published data sets were used

1. Deng X
2. Hiatt JB
3. Nguyen DK
4. Ercan S
5. Sturgill D
6. Hillier LW
7. Schlesinger F
8. Davis CA
9. Reinke VJ
10. Gingeras TR
11. Shendure J
12. Waterston RH
13. Oliver B
14. Lieb JD
15. Disteche CM
(2011) SRR023579.sra
Publicly available at the Sequence Read Archive + (accession no: GSE20136).

http://sra.dnanexus.com/runs/SRR023579
1. Deng X
2. Hiatt JB
3. Nguyen DK
4. Ercan S
5. Sturgill D
6. Hillier LW
7. Schlesinger F
8. Davis CA
9. Reinke VJ
10. Gingeras TR
11. Shendure J
12. Waterston RH
13. Oliver B
14. Lieb JD
15. Disteche CM
(2011) Transcriptome Analysis of roundworm
Publicly available at the NCBI Short Read Archive (accession no: GSE20136).

http://www.ncbi.nlm.nih.gov/sra/?term=SRR023580
1. Kreusi WS
2. Core LJ
3. Waters CT
4. Lis JT
5. Meyer BJ
(2013) Condensin Controls Recruitment of RNA Polymerase II to Achieve X-Chromosome Dosage Compensation
Publicly availale at the NCBI Gene Expression Omnibus (accession no: GSE43087).

http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE43087
1. Deng X
2. Hiatt JB
3. Nguyen DK
4. Ercan S
5. Sturgill D
6. Hillier LW
7. Schlesinger F
8. Davis CA
9. Reinke VJ
10. Gingeras TR
11. Shendure J
12. Waterston RH
13. Oliver B
14. Lieb JD
15. Disteche CM
(2011) SRR031122.sra
Publicly available at the Sequence Read Archive + (accession no: GSE20136).

http://sra.dnanexus.com/runs/SRR031122
1. Deng X
2. Hiatt JB
3. Nguyen DK
4. Ercan S
5. Sturgill D
6. Hillier LW
7. Schlesinger F
8. Davis CA
9. Reinke VJ
10. Gingeras TR
11. Shendure J
12. Waterston RH
13. Oliver B
14. Lieb JD
15. Disteche CM
(2011) SRR031123.sra
Publicly available at the Sequence Read Archive + (accession no: GSE20136).

http://sra.dnanexus.com/runs/SRR031123
1. Crane E
2. Bian Q
3. McCord RP
4. Lajoie BR
5. Wheeler BS
6. Ralston EJ
7. Uzawa S
8. Dekker J
9. Meyer BJ
(2015) Condensin-Driven Remodeling of X-Chromosome Topology during Dosage Compensation
Publicly available at the NCBI Gene Expression Omnibus (accession no: GSE59716).

http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE59716

Article and author information

Author details

Bayly S Wheeler

Department of Molecular and Cell Biology, Howard Hughes Medical Institute, University of California, Berkeley, Berkeley, United States

Competing interests
The authors declare that no competing interests exist.
Erika Anderson

Department of Molecular and Cell Biology, Howard Hughes Medical Institute, University of California, Berkeley, Berkeley, United States

Competing interests
The authors declare that no competing interests exist.
Christian Frøkjær-Jensen

Department of Biology, Howard Hughes Medical Institute, University of Utah, Salt Lake City, United States

Competing interests
The authors declare that no competing interests exist.
Qian Bian

Department of Molecular and Cell Biology, Howard Hughes Medical Institute, University of California, Berkeley, Berkeley, United States

Competing interests
The authors declare that no competing interests exist.
Erik Jorgensen

Department of Biology, Howard Hughes Medical Institute, University of Utah, Salt Lake City, United States

Competing interests
The authors declare that no competing interests exist.
Barbara J Meyer

Department of Molecular and Cell Biology, Howard Hughes Medical Institute, University of California, Berkeley, Berkeley, United States

For correspondence
bjmeyer@berkeley.edu

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-6530-4588

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.

Copyright

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.