Concentration dependent chromatin states induced by the bicoid morphogen gradient

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Abstract

In Drosophila, graded expression of the maternal transcription factor Bicoid (Bcd) provides positional information to activate target genes at different positions along the anterior-posterior axis. We have measured the genome-wide binding profile of Bcd using ChIP-seq in embryos expressing single, uniform levels of Bcd protein, and grouped Bcd-bound targets into four classes based on occupancy at different concentrations. By measuring the biochemical affinity of target enhancers in these classes in vitro and genome-wide chromatin accessibility by ATAC-seq, we found that the occupancy of target sequences by Bcd is not primarily determined by Bcd binding sites, but by chromatin context. Bcd drives an open chromatin state at a subset of its targets. Our data support a model where Bcd influences chromatin structure to gain access to concentration-sensitive targets at high concentrations, while concentration-insensitive targets are found in more accessible chromatin and are bound at low concentrations. This may be a common property of developmental transcription factors that must gain early access to their target enhancers while the chromatin state of the genome is being remodeled during large-scale transitions in the gene regulatory landscape.

Data availability

The following data sets were generated

(2016) Concentration dependent binding states of the Bicoid Homeodomain Protein
GSE86966.

https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?token=atqzkaiilbalxob&acc=GSE86966

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Colleen E Hannon

Department of Molecular Biology, Princeton University, Princeton, United States

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-4402-8107
Shelby A Blythe

Department of Molecular Biology, Princeton University, Princeton, United States

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

Department of Molecular Biology, 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

Howard Hughes Medical Institute

Eric F Wieschaus

National Institutes of Health (F31HD082940)

Colleen E Hannon

National Institutes of Health (F32HD072653)

Shelby A Blythe

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

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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.