GAF is essential for zygotic genome activation and chromatin accessibility in the early Drosophila embryo
- University of Wisconsin-Madison, United States
Abstract
Following fertilization, the genomes of the germ cells are reprogrammed to form the totipotent embryo. Pioneer transcription factors are essential for remodeling the chromatin and driving the initial wave of zygotic gene expression. In Drosophila melanogaster, the pioneer factor Zelda is essential for development through this dramatic period of reprogramming, known as the maternal-to-zygotic transition (MZT). However, it was unknown whether additional pioneer factors were required for this transition. We identified an additional maternally encoded factor required for development through the MZT, GAGA Factor (GAF). GAF is necessary to activate widespread zygotic transcription and to remodel the chromatin accessibility landscape. We demonstrated that Zelda preferentially controls expression of the earliest transcribed genes, while genes expressed during widespread activation are predominantly dependent on GAF. Thus, progression through the MZT requires coordination of multiple pioneer-like factors, and we propose that as development proceeds control is gradually transferred from Zelda to GAF.
Data availability
Sequencing data have been deposited in GEO under accession code GSE152773.
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GAF is essential for zygotic genome activation and chromatin accessibility in the early Drosophila embryoNCBI Gene Expression Omnibus, GSE152773.
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Zelda binding in the early Drosophila melanogasterNCBI Gene Expression Omnibus, GSE30757.
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The Genomic Binding Profile of GAGA Element Associated Factor (GAF) in Drosophila S2 cellsNCBI Gene Expression Omnibus, GSE40646.
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Targeting of the dosage-compensated male X-chromosome during early Drosophila developmentNCBI Gene Expression Omnibus, GSE133637.
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Establishment of regions of genomic activity during the Drosophila maternal-to-zygotic transitionNCBI Gene Expression Omnibus, GSE58935.
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Histone locus regulation by the Drosophila dosage compensation adaptor protein CLAMPNCBI Gene Expression Omnibus, GSE10292.
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Concentration dependent binding states of the Bicoid Homeodomain ProteinNCBI Gene Expression Omnibus, GSE86966.
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Continued activity of the pioneer factor Zelda is required to drive zygotic genome activationNCBI Gene Expression Omnibus, GSE121157.
Article and author information
Author details
Melissa M Harrison
Funding
National Institutes of Health (R01GM111694)
- Melissa M Harrison
National Institutes of Health (R35GM136298)
- Melissa M Harrison
Vallee Foundation
- Melissa M Harrison
National Institutes of Health (T32GM007215)
- Marissa M Gaskill
- Tyler J Gibson
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Yukiko M Yamashita, Whitehead Institute/MIT, United States
Version history
- Received: January 19, 2021
- Accepted: March 14, 2021
- Accepted Manuscript published: March 15, 2021 (version 1)
- Version of Record published: April 27, 2021 (version 2)
Copyright
© 2021, Gaskill et al.
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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GAF is essential for zygotic genome activation and chromatin accessibility in the early Drosophila embryo
eLife 10:e66668.
https://doi.org/10.7554/eLife.66668
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