Canonical nucleosome organization at promoters forms during genome activation
- Yong Zhang1,2,7,10,
- Nadine L. Vastenhouw3,7,10,
- Jianxing Feng1,8,
- Kai Fu1,2,8,9,
- Chenfei Wang1,2,
- Ying Ge1,2,
- Andrea Pauli4,
- Paul van Hummelen5,
- Alexander F. Schier4,10 and
- X. Shirley Liu1,6,10
- 1School of Life Science and Technology, Tongji University, Shanghai 200092, China;
- 2Shanghai Key Laboratory of Signaling and Disease Research, Tongji University, Shanghai 200092, China;
- 3Max Planck Institute of Molecular Cell Biology and Genetics, D-01307 Dresden, Germany;
- 4Department of Molecular and Cellular Biology, Harvard University, Cambridge, Massachusetts 02138, USA;
- 5Center for Cancer Genome Discovery, Dana-Farber Cancer Institute, Boston, Massachusetts 02115, USA;
- 6Department of Biostatistics and Computational Biology, Dana-Farber Cancer Institute, Harvard School of Public Health, Boston, Massachusetts 02115, USA
Abstract
The organization of nucleosomes influences transcriptional activity by controlling accessibility of DNA binding proteins to the genome. Genome-wide nucleosome binding profiles have identified a canonical nucleosome organization at gene promoters, where arrays of well-positioned nucleosomes emanate from nucleosome-depleted regions. The mechanisms of formation and the function of canonical promoter nucleosome organization remain unclear. Here we analyze the genome-wide location of nucleosomes during zebrafish embryogenesis and show that well-positioned nucleosome arrays appear on thousands of promoters during the activation of the zygotic genome. The formation of canonical promoter nucleosome organization is independent of DNA sequence preference, transcriptional elongation, and robust RNA polymerase II (Pol II) binding. Instead, canonical promoter nucleosome organization correlates with the presence of histone H3 lysine 4 trimethylation (H3K4me3) and affects future transcriptional activation. These findings reveal that genome activation is central to the organization of nucleosome arrays during early embryogenesis.
Footnotes
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↵7 These authors contributed equally to this work.
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↵8 These authors contributed equally to this work.
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↵9 Present address: Bioinformatics Interdepartmental Program, UCLA, Los Angeles, California 90095, USA
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↵10 Corresponding authors
E-mail xsliu{at}jimmy.harvard.edu
E-mail yzhang{at}tongji.edu.cn
Email vastenhouw{at}mpi-cbg.de
E-mail schier{at}fas.harvard.edu
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[Supplemental material is available for this article.]
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Article published online before print. Article, supplemental material, and publication date are at http://www.genome.org/cgi/doi/10.1101/gr.157750.113.
Freely available online through the Genome Research Open Access option.
- Received March 15, 2013.
- Accepted November 25, 2013.
This article, published in Genome Research, is available under a Creative Commons License (Attribution-NonCommercial 3.0 Unported), as described at http://creativecommons.org/licenses/by-nc/3.0/.
