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Differentially-dimensioned furrow formation by zygotic gene expression and the MBT

Despite extensive work on the mechanisms that generate plasma membrane furrows, understanding how cells are able to dynamically regulate furrow dimensions is an unresolved question. Here, we present an in-depth characterization of furrow behaviors and their regulation in vivo during early Drosophila...

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Autores principales: Xie, Yi, Blankenship, J. Todd
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5786337/
https://www.ncbi.nlm.nih.gov/pubmed/29337989
http://dx.doi.org/10.1371/journal.pgen.1007174
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author Xie, Yi
Blankenship, J. Todd
author_facet Xie, Yi
Blankenship, J. Todd
author_sort Xie, Yi
collection PubMed
description Despite extensive work on the mechanisms that generate plasma membrane furrows, understanding how cells are able to dynamically regulate furrow dimensions is an unresolved question. Here, we present an in-depth characterization of furrow behaviors and their regulation in vivo during early Drosophila morphogenesis. We show that the deepening in furrow dimensions with successive nuclear cycles is largely due to the introduction of a new, rapid ingression phase (Ingression II). Blocking the midblastula transition (MBT) by suppressing zygotic transcription through pharmacological or genetic means causes the absence of Ingression II, and consequently reduces furrow dimensions. The analysis of compound chromosomes that produce chromosomal aneuploidies suggests that multiple loci on the X, II, and III chromosomes contribute to the production of differentially-dimensioned furrows, and we track the X-chromosomal contribution to furrow lengthening to the nullo gene product. We further show that checkpoint proteins are required for furrow lengthening; however, mitotic phases of the cell cycle are not strictly deterministic for furrow dimensions, as a decoupling of mitotic phases with periods of active ingression occurs as syncytial furrow cycles progress. Finally, we examined the turnover of maternal gene products and find that this is a minor contributor to the developmental regulation of furrow morphologies. Our results suggest that cellularization dynamics during cycle 14 are a continuation of dynamics established during the syncytial cycles and provide a more nuanced view of developmental- and MBT-driven morphogenesis.
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spelling pubmed-57863372018-02-09 Differentially-dimensioned furrow formation by zygotic gene expression and the MBT Xie, Yi Blankenship, J. Todd PLoS Genet Research Article Despite extensive work on the mechanisms that generate plasma membrane furrows, understanding how cells are able to dynamically regulate furrow dimensions is an unresolved question. Here, we present an in-depth characterization of furrow behaviors and their regulation in vivo during early Drosophila morphogenesis. We show that the deepening in furrow dimensions with successive nuclear cycles is largely due to the introduction of a new, rapid ingression phase (Ingression II). Blocking the midblastula transition (MBT) by suppressing zygotic transcription through pharmacological or genetic means causes the absence of Ingression II, and consequently reduces furrow dimensions. The analysis of compound chromosomes that produce chromosomal aneuploidies suggests that multiple loci on the X, II, and III chromosomes contribute to the production of differentially-dimensioned furrows, and we track the X-chromosomal contribution to furrow lengthening to the nullo gene product. We further show that checkpoint proteins are required for furrow lengthening; however, mitotic phases of the cell cycle are not strictly deterministic for furrow dimensions, as a decoupling of mitotic phases with periods of active ingression occurs as syncytial furrow cycles progress. Finally, we examined the turnover of maternal gene products and find that this is a minor contributor to the developmental regulation of furrow morphologies. Our results suggest that cellularization dynamics during cycle 14 are a continuation of dynamics established during the syncytial cycles and provide a more nuanced view of developmental- and MBT-driven morphogenesis. Public Library of Science 2018-01-16 /pmc/articles/PMC5786337/ /pubmed/29337989 http://dx.doi.org/10.1371/journal.pgen.1007174 Text en © 2018 Xie, Blankenship http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Xie, Yi
Blankenship, J. Todd
Differentially-dimensioned furrow formation by zygotic gene expression and the MBT
title Differentially-dimensioned furrow formation by zygotic gene expression and the MBT
title_full Differentially-dimensioned furrow formation by zygotic gene expression and the MBT
title_fullStr Differentially-dimensioned furrow formation by zygotic gene expression and the MBT
title_full_unstemmed Differentially-dimensioned furrow formation by zygotic gene expression and the MBT
title_short Differentially-dimensioned furrow formation by zygotic gene expression and the MBT
title_sort differentially-dimensioned furrow formation by zygotic gene expression and the mbt
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5786337/
https://www.ncbi.nlm.nih.gov/pubmed/29337989
http://dx.doi.org/10.1371/journal.pgen.1007174
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