Germline/soma distinction in Drosophila embryos requires regulators of zygotic genome activation

In Drosophila melanogaster embryos, somatic versus germline identity is the first cell fate decision. Zygotic genome activation (ZGA) orchestrates regionalized gene expression, imparting specific identity on somatic cells. ZGA begins with a minor wave that commences at nuclear cycle (NC)8 under the...

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Main Authors: Megan M Colonnetta, Paul Schedl, Girish Deshpande
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2023-01-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/78188
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author Megan M Colonnetta
Paul Schedl
Girish Deshpande
author_facet Megan M Colonnetta
Paul Schedl
Girish Deshpande
author_sort Megan M Colonnetta
collection DOAJ
description In Drosophila melanogaster embryos, somatic versus germline identity is the first cell fate decision. Zygotic genome activation (ZGA) orchestrates regionalized gene expression, imparting specific identity on somatic cells. ZGA begins with a minor wave that commences at nuclear cycle (NC)8 under the guidance of chromatin accessibility factors (Zelda, CLAMP, GAF), followed by the major wave during NC14. By contrast, primordial germ cell (PGC) specification requires maternally deposited and posteriorly anchored germline determinants. This is accomplished by a centrosome coordinated release and sequestration of germ plasm during the precocious cellularization of PGCs in NC10. Here, we report a novel requirement for Zelda and CLAMP during the establishment of the germline/soma distinction. When their activity is compromised, PGC determinants are not properly sequestered, and specification is disrupted. Conversely, the spreading of PGC determinants from the posterior pole adversely influences transcription in the neighboring somatic nuclei. These reciprocal aberrations can be correlated with defects in centrosome duplication/separation that are known to induce inappropriate transmission of the germ plasm. Interestingly, consistent with the ability of bone morphogenetic protein (BMP) signaling to influence specification of embryonic PGCs, reduction in the transcript levels of a BMP family ligand, decapentaplegic (dpp), is exacerbated at the posterior pole.
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spelling doaj.art-36455ee220944790b7983aeb1b8ef2b62023-01-04T16:33:28ZengeLife Sciences Publications LtdeLife2050-084X2023-01-011210.7554/eLife.78188Germline/soma distinction in Drosophila embryos requires regulators of zygotic genome activationMegan M Colonnetta0https://orcid.org/0000-0001-5685-1670Paul Schedl1Girish Deshpande2https://orcid.org/0000-0002-5200-7090Department of Molecular Biology, Princeton University, Princeton, United StatesDepartment of Molecular Biology, Princeton University, Princeton, United StatesDepartment of Molecular Biology, Princeton University, Princeton, United StatesIn Drosophila melanogaster embryos, somatic versus germline identity is the first cell fate decision. Zygotic genome activation (ZGA) orchestrates regionalized gene expression, imparting specific identity on somatic cells. ZGA begins with a minor wave that commences at nuclear cycle (NC)8 under the guidance of chromatin accessibility factors (Zelda, CLAMP, GAF), followed by the major wave during NC14. By contrast, primordial germ cell (PGC) specification requires maternally deposited and posteriorly anchored germline determinants. This is accomplished by a centrosome coordinated release and sequestration of germ plasm during the precocious cellularization of PGCs in NC10. Here, we report a novel requirement for Zelda and CLAMP during the establishment of the germline/soma distinction. When their activity is compromised, PGC determinants are not properly sequestered, and specification is disrupted. Conversely, the spreading of PGC determinants from the posterior pole adversely influences transcription in the neighboring somatic nuclei. These reciprocal aberrations can be correlated with defects in centrosome duplication/separation that are known to induce inappropriate transmission of the germ plasm. Interestingly, consistent with the ability of bone morphogenetic protein (BMP) signaling to influence specification of embryonic PGCs, reduction in the transcript levels of a BMP family ligand, decapentaplegic (dpp), is exacerbated at the posterior pole.https://elifesciences.org/articles/78188ZGAgerm cellsDrosophila melanogasterembryonic developmentstem cells
spellingShingle Megan M Colonnetta
Paul Schedl
Girish Deshpande
Germline/soma distinction in Drosophila embryos requires regulators of zygotic genome activation
eLife
ZGA
germ cells
Drosophila melanogaster
embryonic development
stem cells
title Germline/soma distinction in Drosophila embryos requires regulators of zygotic genome activation
title_full Germline/soma distinction in Drosophila embryos requires regulators of zygotic genome activation
title_fullStr Germline/soma distinction in Drosophila embryos requires regulators of zygotic genome activation
title_full_unstemmed Germline/soma distinction in Drosophila embryos requires regulators of zygotic genome activation
title_short Germline/soma distinction in Drosophila embryos requires regulators of zygotic genome activation
title_sort germline soma distinction in drosophila embryos requires regulators of zygotic genome activation
topic ZGA
germ cells
Drosophila melanogaster
embryonic development
stem cells
url https://elifesciences.org/articles/78188
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AT paulschedl germlinesomadistinctionindrosophilaembryosrequiresregulatorsofzygoticgenomeactivation
AT girishdeshpande germlinesomadistinctionindrosophilaembryosrequiresregulatorsofzygoticgenomeactivation