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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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Autores principales: Colonnetta, Megan M, Schedl, Paul, Deshpande, Girish
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9812407/
https://www.ncbi.nlm.nih.gov/pubmed/36598809
http://dx.doi.org/10.7554/eLife.78188
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author Colonnetta, Megan M
Schedl, Paul
Deshpande, Girish
author_facet Colonnetta, Megan M
Schedl, Paul
Deshpande, Girish
author_sort Colonnetta, Megan M
collection PubMed
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 pubmed-98124072023-01-05 Germline/soma distinction in Drosophila embryos requires regulators of zygotic genome activation Colonnetta, Megan M Schedl, Paul Deshpande, Girish eLife Developmental Biology 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. eLife Sciences Publications, Ltd 2023-01-04 /pmc/articles/PMC9812407/ /pubmed/36598809 http://dx.doi.org/10.7554/eLife.78188 Text en © 2023, Colonnetta et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Developmental Biology
Colonnetta, Megan M
Schedl, Paul
Deshpande, Girish
Germline/soma distinction in Drosophila embryos requires regulators of zygotic genome activation
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 Developmental Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9812407/
https://www.ncbi.nlm.nih.gov/pubmed/36598809
http://dx.doi.org/10.7554/eLife.78188
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