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PLoS Genet. 2016 Jul 14;12(7):e1006120. doi: 10.1371/journal.pgen.1006120. eCollection 2016 Jul.

Expansion of GA Dinucleotide Repeats Increases the Density of CLAMP Binding Sites on the X-Chromosome to Promote Drosophila Dosage Compensation.

Author information

1
Department of Molecular Biology, Cellular Biology and Biochemistry, Brown University, Providence, Rhode Island, United States of America.
2
Department of Molecular Biology, Massachusetts General Hospital, Boston, Massachusetts, United States of America.
3
Department of Cell Biology, Massachusetts General Hospital Cancer Center, Boston, Massachusetts, United States of America.
4
Department of Biology, Boston University, Boston, Massachusetts, United States of America.
5
Molecular and Computational Biology Program, Department of Biological Sciences, University of Southern California, Los Angeles, California, United States of America.
6
Novartis Institutes for Biomedical Research, Cambridge, Massachusetts, United States of America.
7
Institute of Plant Protection and Microbiology, Zhejiang Academy of Agricultural Sciences, Hangzhou, China.
8
Department of Biological Sciences, North Carolina State University, Raleigh, North Carolina, United States of America.
9
Division of Genetics, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, Massachusetts, United States of America.
10
Department of Pathology, Brigham and Women's Hospital and Harvard Medical School, Boston, Massachusetts, United States of America.

Abstract

Dosage compensation is an essential process that equalizes transcript levels of X-linked genes between sexes by forming a domain of coordinated gene expression. Throughout the evolution of Diptera, many different X-chromosomes acquired the ability to be dosage compensated. Once each newly evolved X-chromosome is targeted for dosage compensation in XY males, its active genes are upregulated two-fold to equalize gene expression with XX females. In Drosophila melanogaster, the CLAMP zinc finger protein links the dosage compensation complex to the X-chromosome. However, the mechanism for X-chromosome identification has remained unknown. Here, we combine biochemical, genomic and evolutionary approaches to reveal that expansion of GA-dinucleotide repeats likely accumulated on the X-chromosome over evolutionary time to increase the density of CLAMP binding sites, thereby driving the evolution of dosage compensation. Overall, we present new insight into how subtle changes in genomic architecture, such as expansions of a simple sequence repeat, promote the evolution of coordinated gene expression.

PMID:
27414415
PMCID:
PMC4945028
DOI:
10.1371/journal.pgen.1006120
[Indexed for MEDLINE]
Free PMC Article

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