Correct regionalization of a tissue primordium is essential for coordinated morphogenesis

During organ development, tubular organs often form from flat epithelial primordia. In the placodes of the forming tubes of the salivary glands in the Drosophila embryo, we previously identified spatially defined cell behaviors of cell wedging, tilting, and cell intercalation that are key to the ini...

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Autores principales:	Yara E Sánchez-Corrales, Guy B Blanchard, Katja Röper
Formato:	article
Lenguaje:	EN
Publicado:	eLife Sciences Publications Ltd 2021
Materias:	organogenesis tubulogenesis morphogenesis morphometrics apical constriction intercalation Medicine R Science Q Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/b2be314643c54509853136f36d3e88c6
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id	oai:doaj.org-article:b2be314643c54509853136f36d3e88c6
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spelling	oai:doaj.org-article:b2be314643c54509853136f36d3e88c62021-11-24T12:22:18ZCorrect regionalization of a tissue primordium is essential for coordinated morphogenesis10.7554/eLife.723692050-084Xe72369https://doaj.org/article/b2be314643c54509853136f36d3e88c62021-11-01T00:00:00Zhttps://elifesciences.org/articles/72369https://doaj.org/toc/2050-084XDuring organ development, tubular organs often form from flat epithelial primordia. In the placodes of the forming tubes of the salivary glands in the Drosophila embryo, we previously identified spatially defined cell behaviors of cell wedging, tilting, and cell intercalation that are key to the initial stages of tube formation. Here, we address what the requirements are that ensure the continuous formation of a narrow symmetrical tube from an initially asymmetrical primordium whilst overall tissue geometry is constantly changing. We are using live-imaging and quantitative methods to compare wild-type placodes and mutants that either show disrupted cell behaviors or an initial symmetrical placode organization, with both resulting in severe impairment of the invagination. We find that early transcriptional patterning of key morphogenetic transcription factors drives the selective activation of downstream morphogenetic modules, such as GPCR signaling that activates apical-medial actomyosin activity to drive cell wedging at the future asymmetrically placed invagination point. Over time, transcription of key factors expands across the rest of the placode and cells switch their behavior from predominantly intercalating to predominantly apically constricting as their position approaches the invagination pit. Misplacement or enlargement of the initial invagination pit leads to early problems in cell behaviors that eventually result in a defective organ shape. Our work illustrates that the dynamic patterning of the expression of transcription factors and downstream morphogenetic effectors ensures positionally fixed areas of cell behavior with regards to the invagination point. This patterning in combination with the asymmetric geometrical setup ensures functional organ formation.Yara E Sánchez-CorralesGuy B BlanchardKatja RöpereLife Sciences Publications Ltdarticleorganogenesistubulogenesismorphogenesismorphometricsapical constrictionintercalationMedicineRScienceQBiology (General)QH301-705.5ENeLife, Vol 10 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	organogenesis tubulogenesis morphogenesis morphometrics apical constriction intercalation Medicine R Science Q Biology (General) QH301-705.5
spellingShingle	organogenesis tubulogenesis morphogenesis morphometrics apical constriction intercalation Medicine R Science Q Biology (General) QH301-705.5 Yara E Sánchez-Corrales Guy B Blanchard Katja Röper Correct regionalization of a tissue primordium is essential for coordinated morphogenesis
description	During organ development, tubular organs often form from flat epithelial primordia. In the placodes of the forming tubes of the salivary glands in the Drosophila embryo, we previously identified spatially defined cell behaviors of cell wedging, tilting, and cell intercalation that are key to the initial stages of tube formation. Here, we address what the requirements are that ensure the continuous formation of a narrow symmetrical tube from an initially asymmetrical primordium whilst overall tissue geometry is constantly changing. We are using live-imaging and quantitative methods to compare wild-type placodes and mutants that either show disrupted cell behaviors or an initial symmetrical placode organization, with both resulting in severe impairment of the invagination. We find that early transcriptional patterning of key morphogenetic transcription factors drives the selective activation of downstream morphogenetic modules, such as GPCR signaling that activates apical-medial actomyosin activity to drive cell wedging at the future asymmetrically placed invagination point. Over time, transcription of key factors expands across the rest of the placode and cells switch their behavior from predominantly intercalating to predominantly apically constricting as their position approaches the invagination pit. Misplacement or enlargement of the initial invagination pit leads to early problems in cell behaviors that eventually result in a defective organ shape. Our work illustrates that the dynamic patterning of the expression of transcription factors and downstream morphogenetic effectors ensures positionally fixed areas of cell behavior with regards to the invagination point. This patterning in combination with the asymmetric geometrical setup ensures functional organ formation.
format	article
author	Yara E Sánchez-Corrales Guy B Blanchard Katja Röper
author_facet	Yara E Sánchez-Corrales Guy B Blanchard Katja Röper
author_sort	Yara E Sánchez-Corrales
title	Correct regionalization of a tissue primordium is essential for coordinated morphogenesis
title_short	Correct regionalization of a tissue primordium is essential for coordinated morphogenesis
title_full	Correct regionalization of a tissue primordium is essential for coordinated morphogenesis
title_fullStr	Correct regionalization of a tissue primordium is essential for coordinated morphogenesis
title_full_unstemmed	Correct regionalization of a tissue primordium is essential for coordinated morphogenesis
title_sort	correct regionalization of a tissue primordium is essential for coordinated morphogenesis
publisher	eLife Sciences Publications Ltd
publishDate	2021
url	https://doaj.org/article/b2be314643c54509853136f36d3e88c6
work_keys_str_mv	AT yaraesanchezcorrales correctregionalizationofatissueprimordiumisessentialforcoordinatedmorphogenesis AT guybblanchard correctregionalizationofatissueprimordiumisessentialforcoordinatedmorphogenesis AT katjaroper correctregionalizationofatissueprimordiumisessentialforcoordinatedmorphogenesis
_version_	1718415068873359360

Correct regionalization of a tissue primordium is essential for coordinated morphogenesis

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