Establishment and maintenance of heritable chromatin structure during early Drosophila embryogenesis

Abstract
Data availability
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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

The following data sets were generated

1. Blythe SA
2. Wieschaus EF
(2016) ATAC-seq analysis of chromatin accessibility and nucleosome positioning in Drosophila melanogaster precellular blastoderm embryos
Publicly available at the NCBI Gene Expression Omnibus (accession no: GSE83851).

http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE83851

The following previously published data sets were used

1. Harrison MM
2. Li X
3. Kaplan T
4. Botchan MR
5. Eisen MB
(2011) Zelda binding in the early Drosophila melanogaster embryo marks regions subsequently activated at the maternal-to-zygotic transition
Publicly available at the NCBI Gene Expression Omnibus (accession no: GSE30757) .

http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE30757
1. Negre N
2. Brown CD
3. Morrison CA
4. Shah PK
5. White KP
(2009) Genomewide analysis of Insulator protein binding sites in Drosophila embryos at E0-12
Publicly available at the NCBI Gene Expression Omnibus (accession no: GSE16245) .

http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE16245
1. modEncode Consortium
(2009) Drosophila at different time points of development: ChIP-chip, ChIP-seq, RNA-seq
Publicly available at the NCBI Gene Expression Omnibus (accession no: GSE15292) .

https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE15292

Article and author information

Author details

Shelby A Blythe

Howard Hughes Medical Institute, Princeton University, Princeton, United States

For correspondence
sblythe@princeton.edu

Competing interests
The authors declare that no competing interests exist.
Eric F Wieschaus

Howard Hughes Medical Institute, Princeton University, Princeton, United States

For correspondence
efw@princeton.edu

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-0727-3349

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.

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.