Chromatin architecture transitions from zebrafish sperm through early embryogenesis
- Candice L. Wike1,
- Yixuan Guo1,
- Mengyao Tan1,
- Ryohei Nakamura2,
- Dana Klatt Shaw3,
- Noelia Díaz4,
- Aneasha F. Whittaker-Tademy1,
- Neva C. Durand5,
- Erez Lieberman Aiden5,6,7,8,
- Juan M. Vaquerizas4,9,10,
- David Grunwald3,
- Hiroyuki Takeda2 and
- Bradley R. Cairns1
- 1Howard Hughes Medical Institute, Department of Oncological Sciences and Huntsman Cancer Institute, University of Utah School of Medicine, Salt Lake City, Utah 84112, USA;
- 2Department of Biological Sciences, Graduate School of Science, The University of Tokyo, Tokyo 113-0033, Japan;
- 3Department of Human Genetics, University of Utah, Salt Lake City, Utah 84112, USA;
- 4Max Planck Institute for Molecular Biomedicine, 48149 Muenster, Germany;
- 5The Center for Genome Architecture, Baylor College of Medicine, Houston, Texas 77030, USA;
- 6Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, Texas 77030, USA;
- 7Department of Computer Science, Department of Computational and Applied Mathematics, Rice University, Houston, Texas 77005, USA;
- 8Center for Theoretical Biological Physics, Rice University, Houston, Texas 77030, USA;
- 9MRC London Institute of Medical Sciences, London W12 0NN, United Kingdom;
- 10Institute of Clinical Sciences, Faculty of Medicine, Imperial College London, London W12 0NN, United Kingdom
Abstract
Chromatin architecture mapping in 3D formats has increased our understanding of how regulatory sequences and gene expression are connected and regulated in a genome. The 3D chromatin genome shows extensive remodeling during embryonic development, and although the cleavage-stage embryos of most species lack structure before zygotic genome activation (pre-ZGA), zebrafish has been reported to have structure. Here, we aimed to determine the chromosomal architecture in paternal/sperm zebrafish gamete cells to discern whether it either resembles or informs early pre-ZGA zebrafish embryo chromatin architecture. First, we assessed the higher-order architecture through advanced low-cell in situ Hi-C. The structure of zebrafish sperm, packaged by histones, lacks topological associated domains and instead displays “hinge-like” domains of ∼150 kb that repeat every 1–2 Mbs, suggesting a condensed repeating structure resembling mitotic chromosomes. The pre-ZGA embryos lacked chromosomal structure, in contrast to prior work, and only developed structure post-ZGA. During post-ZGA, we find chromatin architecture beginning to form at small contact domains of a median length of ∼90 kb. These small contact domains are established at enhancers, including super-enhancers, and chemical inhibition of Ep300a (p300) and Crebbpa (CBP) activity, lowering histone H3K27ac, but not transcription inhibition, diminishes these contacts. Together, this study reveals hinge-like domains in histone-packaged zebrafish sperm chromatin and determines that the initial formation of high-order chromatin architecture in zebrafish embryos occurs after ZGA primarily at enhancers bearing high H3K27ac.
Footnotes
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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 https://www.genome.org/cgi/doi/10.1101/gr.269860.120.
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Freely available online through the Genome Research Open Access option.
- Received August 4, 2020.
- Accepted April 7, 2021.
This article, published in Genome Research, is available under a Creative Commons License (Attribution 4.0 International), as described at http://creativecommons.org/licenses/by/4.0/.
