GAF is essential for zygotic genome activation and chromatin accessibility in the early Drosophila embryo

Abstract
Data availability
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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.

The following data sets were generated

(2020) GAF is essential for zygotic genome activation and chromatin accessibility in the early Drosophila embryo
NCBI Gene Expression Omnibus, GSE152773.

https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE152773

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
NCBI Gene Expression Omnibus, GSE30757.

https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE30757
1. Guertin MJ
(2013) The Genomic Binding Profile of GAGA Element Associated Factor (GAF) in Drosophila S2 cells
NCBI Gene Expression Omnibus, GSE40646.

https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi? acc=GSE40646
(2019) Targeting of the dosage-compensated male X-chromosome during early Drosophila development
NCBI Gene Expression Omnibus, GSE133637.

https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE133637
1. Lott SE
2. Eisen MB
(2011) Non-canonical compensation of zygotic X transcription in Drosophila melanogaster development revealed through single embryo RNA-Seq
NCBI Gene Expression Omnibus, GSE25180.

https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE25180
1. Li XY
2. Harrison MM
3. Kaplan T
4. Eisen MB
(2014) Establishment of regions of genomic activity during the Drosophila maternal-to-zygotic transition
NCBI Gene Expression Omnibus, GSE58935.

https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE58935
1. Rieder LE
2. Koreski KP
3. Boltz KA
4. Kuzu G
5. Urban JA
6. Bowman S
7. Zeidman A
8. Jordan III WT
9. Tolstorukov MY
10. Marzluff WF
11. Duronio RJ
12. Larschan EN
(2017) Histone locus regulation by the Drosophila dosage compensation adaptor protein CLAMP
NCBI Gene Expression Omnibus, GSE10292.

https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE102922
(2017) Concentration dependent binding states of the Bicoid Homeodomain Protein
NCBI Gene Expression Omnibus, GSE86966.

https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE86966
1. McDaniel SL
2. Gibson TJ
3. Schulz KN
4. Garcia MF
5. Nevil M
6. Jain SU
7. Lewis PW
8. Zaret KS
9. Harrison MM
(2019) Continued activity of the pioneer factor Zelda is required to drive zygotic genome activation
NCBI Gene Expression Omnibus, GSE121157.

https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE121157
1. Blythe SA
2. Wieschaus EF
(2016) ATAC-seq analysis of chromatin accessibility and nucleosome positioning in Drosophila melanogaster precellular blastoderm embryos
NCBI Gene Expression Omnibus, GSE83851.

https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE83851
(2020) Developmentally regulated requirement for the conserved transcription factor Grainy head in determining chromatin accessibility
NCBI Gene Expression Omnibus, GSE83851.

https://www-ncbi-nlm-nih-gov.ezproxy.u-pec.fr/geo/query/acc.cgi?acc=GSE137075

Article and author information

Author details

Marissa M Gaskill

Department of Biomolecular Chemistry, University of Wisconsin-Madison, Madison, United States

Competing interests
The authors declare that no competing interests exist.
Tyler J Gibson

Department of Biomolecular Chemistry, University of Wisconsin-Madison, Madison, United States

Competing interests
The authors declare that no competing interests exist.
Elizabeth D Larson

Department of Biomolecular Chemistry, University of Wisconsin-Madison, Madison, United States

Competing interests
The authors declare that no competing interests exist.
Melissa M Harrison

Department of Biomolecular Chemistry, University of Wisconsin-Madison, Madison, United States

For correspondence
mharrison3@wisc.edu

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-8228-6836

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.

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.