CLAMP and Zelda function together to promote Drosophila zygotic genome activation

During the essential and conserved process of zygotic genome activation (ZGA), chromatin accessibility must increase to promote transcription. Drosophila is a well-established model for defining mechanisms that drive ZGA. Zelda (ZLD) is a key pioneer transcription factor (TF) that promotes ZGA in th...

Full description

Bibliographic Details
Main Authors: Jingyue Duan, Leila Rieder, Megan M Colonnetta, Annie Huang, Mary Mckenney, Scott Watters, Girish Deshpande, William Jordan, Nicolas Fawzi, Erica Larschan
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2021-08-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/69937
_version_ 1811200147633209344
author Jingyue Duan
Leila Rieder
Megan M Colonnetta
Annie Huang
Mary Mckenney
Scott Watters
Girish Deshpande
William Jordan
Nicolas Fawzi
Erica Larschan
author_facet Jingyue Duan
Leila Rieder
Megan M Colonnetta
Annie Huang
Mary Mckenney
Scott Watters
Girish Deshpande
William Jordan
Nicolas Fawzi
Erica Larschan
author_sort Jingyue Duan
collection DOAJ
description During the essential and conserved process of zygotic genome activation (ZGA), chromatin accessibility must increase to promote transcription. Drosophila is a well-established model for defining mechanisms that drive ZGA. Zelda (ZLD) is a key pioneer transcription factor (TF) that promotes ZGA in the Drosophila embryo. However, many genomic loci that contain GA-rich motifs become accessible during ZGA independent of ZLD. Therefore, we hypothesized that other early TFs that function with ZLD have not yet been identified, especially those that are capable of binding to GA-rich motifs such as chromatin-linked adaptor for male-specific lethal (MSL) proteins (CLAMP). Here, we demonstrate that Drosophila embryonic development requires maternal CLAMP to (1) activate zygotic transcription; (2) increase chromatin accessibility at promoters of specific genes that often encode other essential TFs; and (3) enhance chromatin accessibility and facilitate ZLD occupancy at a subset of key embryonic promoters. Thus, CLAMP functions as a pioneer factor that plays a targeted yet essential role in ZGA.
first_indexed 2024-04-12T02:00:00Z
format Article
id doaj.art-2af79af3120c48578eb73149fd9fe6f2
institution Directory Open Access Journal
issn 2050-084X
language English
last_indexed 2024-04-12T02:00:00Z
publishDate 2021-08-01
publisher eLife Sciences Publications Ltd
record_format Article
series eLife
spelling doaj.art-2af79af3120c48578eb73149fd9fe6f22022-12-22T03:52:42ZengeLife Sciences Publications LtdeLife2050-084X2021-08-011010.7554/eLife.69937CLAMP and Zelda function together to promote Drosophila zygotic genome activationJingyue Duan0https://orcid.org/0000-0001-6416-2250Leila Rieder1Megan M Colonnetta2https://orcid.org/0000-0001-5685-1670Annie Huang3Mary Mckenney4Scott Watters5Girish Deshpande6William Jordan7Nicolas Fawzi8Erica Larschan9https://orcid.org/0000-0003-2484-4921Department of Molecular Biology, Cellular Biology, and Biochemistry, Brown University, Providence, United StatesDepartment of Biology, Emory University, Atlanta, United StatesDepartment of Molecular Biology, Princeton University, Princeton, United StatesDepartment of Molecular Biology, Cellular Biology, and Biochemistry, Brown University, Providence, United StatesDepartment of Molecular Biology, Cellular Biology, and Biochemistry, Brown University, Providence, United StatesDepartment of Molecular Pharmacology, Physiology and Biotechnology, Brown University, Providence, United StatesDepartment of Molecular Biology, Cellular Biology, and Biochemistry, Brown University, Providence, United States; Department of Molecular Biology, Princeton University, Princeton, United StatesDepartment of Molecular Biology, Cellular Biology, and Biochemistry, Brown University, Providence, United StatesDepartment of Molecular Pharmacology, Physiology and Biotechnology, Brown University, Providence, United StatesDepartment of Molecular Biology, Cellular Biology, and Biochemistry, Brown University, Providence, United StatesDuring the essential and conserved process of zygotic genome activation (ZGA), chromatin accessibility must increase to promote transcription. Drosophila is a well-established model for defining mechanisms that drive ZGA. Zelda (ZLD) is a key pioneer transcription factor (TF) that promotes ZGA in the Drosophila embryo. However, many genomic loci that contain GA-rich motifs become accessible during ZGA independent of ZLD. Therefore, we hypothesized that other early TFs that function with ZLD have not yet been identified, especially those that are capable of binding to GA-rich motifs such as chromatin-linked adaptor for male-specific lethal (MSL) proteins (CLAMP). Here, we demonstrate that Drosophila embryonic development requires maternal CLAMP to (1) activate zygotic transcription; (2) increase chromatin accessibility at promoters of specific genes that often encode other essential TFs; and (3) enhance chromatin accessibility and facilitate ZLD occupancy at a subset of key embryonic promoters. Thus, CLAMP functions as a pioneer factor that plays a targeted yet essential role in ZGA.https://elifesciences.org/articles/69937zygotic genome activationCLAMPZeldaDrosophila embryopioneer TF
spellingShingle Jingyue Duan
Leila Rieder
Megan M Colonnetta
Annie Huang
Mary Mckenney
Scott Watters
Girish Deshpande
William Jordan
Nicolas Fawzi
Erica Larschan
CLAMP and Zelda function together to promote Drosophila zygotic genome activation
eLife
zygotic genome activation
CLAMP
Zelda
Drosophila embryo
pioneer TF
title CLAMP and Zelda function together to promote Drosophila zygotic genome activation
title_full CLAMP and Zelda function together to promote Drosophila zygotic genome activation
title_fullStr CLAMP and Zelda function together to promote Drosophila zygotic genome activation
title_full_unstemmed CLAMP and Zelda function together to promote Drosophila zygotic genome activation
title_short CLAMP and Zelda function together to promote Drosophila zygotic genome activation
title_sort clamp and zelda function together to promote drosophila zygotic genome activation
topic zygotic genome activation
CLAMP
Zelda
Drosophila embryo
pioneer TF
url https://elifesciences.org/articles/69937
work_keys_str_mv AT jingyueduan clampandzeldafunctiontogethertopromotedrosophilazygoticgenomeactivation
AT leilarieder clampandzeldafunctiontogethertopromotedrosophilazygoticgenomeactivation
AT meganmcolonnetta clampandzeldafunctiontogethertopromotedrosophilazygoticgenomeactivation
AT anniehuang clampandzeldafunctiontogethertopromotedrosophilazygoticgenomeactivation
AT marymckenney clampandzeldafunctiontogethertopromotedrosophilazygoticgenomeactivation
AT scottwatters clampandzeldafunctiontogethertopromotedrosophilazygoticgenomeactivation
AT girishdeshpande clampandzeldafunctiontogethertopromotedrosophilazygoticgenomeactivation
AT williamjordan clampandzeldafunctiontogethertopromotedrosophilazygoticgenomeactivation
AT nicolasfawzi clampandzeldafunctiontogethertopromotedrosophilazygoticgenomeactivation
AT ericalarschan clampandzeldafunctiontogethertopromotedrosophilazygoticgenomeactivation