Establishment and maintenance of heritable chromatin structure during early Drosophila embryogenesis
Abstract
During embryogenesis, the initial chromatin state is established during a period of rapid proliferative activity. We have measured with three-minute time resolution how heritable patterns of chromatin structure are initially established and maintained during the midblastula transition (MBT). We find that regions of accessibility are established sequentially, where enhancers are opened in advance of promoters and insulators. These open states are stably maintained in highly condensed mitotic chromatin to ensure faithful inheritance of prior accessibility status across cell divisions. The temporal progression of establishment is controlled by the biological timers that control the onset of the MBT. In general, acquisition of promoter accessibility is controlled by the biological timer that measures the nucleo-cytoplasmic (N:C) ratio whereas timing of enhancer accessibility is regulated independently of the N:C ratio. These different timing classes each associate with binding sites for two transcription factors, GAGA-factor and Zelda, previously implicated in controlling chromatin accessibility at ZGA.
Data availability
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ATAC-seq analysis of chromatin accessibility and nucleosome positioning in Drosophila melanogaster precellular blastoderm embryosPublicly available at the NCBI Gene Expression Omnibus (accession no: GSE83851).
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Zelda binding in the early Drosophila melanogaster embryo marks regions subsequently activated at the maternal-to-zygotic transitionPublicly available at the NCBI Gene Expression Omnibus (accession no: GSE30757) .
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Genomewide analysis of Insulator protein binding sites in Drosophila embryos at E0-12Publicly available at the NCBI Gene Expression Omnibus (accession no: GSE16245) .
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Drosophila at different time points of development: ChIP-chip, ChIP-seq, RNA-seqPublicly available at the NCBI Gene Expression Omnibus (accession no: GSE15292) .
Article and author information
Author details
Funding
National Institutes of Health (F32HD072653)
- Shelby A Blythe
Howard Hughes Medical Institute
- Shelby A Blythe
- Eric F Wieschaus
National Institutes of Health (R37HD15587)
- Eric F Wieschaus
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Allan C Spradling, Howard Hughes Medical Institute, Carnegie Institution for Science, United States
Version history
- Received: July 28, 2016
- Accepted: November 21, 2016
- Accepted Manuscript published: November 23, 2016 (version 1)
- Version of Record published: December 14, 2016 (version 2)
Copyright
© 2016, Blythe & Wieschaus
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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