Mechanical control of tissue shape and morphogenetic flows during vertebrate body axis elongation

Abstract Shaping embryonic tissues into their functional morphologies requires cells to control the physical state of the tissue in space and time. While regional variations in cellular forces or cell proliferation have been typically assumed to be the main physical factors controlling tissue morpho...

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Autores principales:	Samhita P. Banavar, Emmet K. Carn, Payam Rowghanian, Georgina Stooke-Vaughan, Sangwoo Kim, Otger Campàs
Formato:	article
Lenguaje:	EN
Publicado:	Nature Portfolio 2021
Materias:	Medicine R Science Q
Acceso en línea:	https://doaj.org/article/5eebb36daa444d34aa7da9b300373d7b
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spelling	oai:doaj.org-article:5eebb36daa444d34aa7da9b300373d7b2021-12-02T18:27:48ZMechanical control of tissue shape and morphogenetic flows during vertebrate body axis elongation10.1038/s41598-021-87672-32045-2322https://doaj.org/article/5eebb36daa444d34aa7da9b300373d7b2021-04-01T00:00:00Zhttps://doi.org/10.1038/s41598-021-87672-3https://doaj.org/toc/2045-2322Abstract Shaping embryonic tissues into their functional morphologies requires cells to control the physical state of the tissue in space and time. While regional variations in cellular forces or cell proliferation have been typically assumed to be the main physical factors controlling tissue morphogenesis, recent experiments have revealed that spatial variations in the tissue physical (fluid/solid) state play a key role in shaping embryonic tissues. Here we theoretically study how the regional control of fluid and solid tissue states guides morphogenetic flows to shape the extending vertebrate body axis. Our results show that both the existence of a fluid-to-solid tissue transition along the anteroposterior axis and the tissue surface tension determine the shape of the tissue and its ability to elongate unidirectionally, with large tissue tensions preventing unidirectional elongation and promoting blob-like tissue expansions. We predict both the tissue morphogenetic flows and stresses that enable unidirectional axis elongation. Our results show the existence of a sharp transition in the structure of morphogenetic flows, from a flow with no vortices to a flow with two counter-rotating vortices, caused by a transition in the number and location of topological defects in the flow field. Finally, comparing the theoretical predictions to quantitative measurements of both tissue flows and shape during zebrafish body axis elongation, we show that the observed morphogenetic events can be explained by the existence of a fluid-to-solid tissue transition along the anteroposterior axis. These results highlight the role of spatiotemporally-controlled fluid-to-solid transitions in the tissue state as a physical mechanism of embryonic morphogenesis.Samhita P. BanavarEmmet K. CarnPayam RowghanianGeorgina Stooke-VaughanSangwoo KimOtger CampàsNature PortfolioarticleMedicineRScienceQENScientific Reports, Vol 11, Iss 1, Pp 1-14 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Medicine R Science Q
spellingShingle	Medicine R Science Q Samhita P. Banavar Emmet K. Carn Payam Rowghanian Georgina Stooke-Vaughan Sangwoo Kim Otger Campàs Mechanical control of tissue shape and morphogenetic flows during vertebrate body axis elongation
description	Abstract Shaping embryonic tissues into their functional morphologies requires cells to control the physical state of the tissue in space and time. While regional variations in cellular forces or cell proliferation have been typically assumed to be the main physical factors controlling tissue morphogenesis, recent experiments have revealed that spatial variations in the tissue physical (fluid/solid) state play a key role in shaping embryonic tissues. Here we theoretically study how the regional control of fluid and solid tissue states guides morphogenetic flows to shape the extending vertebrate body axis. Our results show that both the existence of a fluid-to-solid tissue transition along the anteroposterior axis and the tissue surface tension determine the shape of the tissue and its ability to elongate unidirectionally, with large tissue tensions preventing unidirectional elongation and promoting blob-like tissue expansions. We predict both the tissue morphogenetic flows and stresses that enable unidirectional axis elongation. Our results show the existence of a sharp transition in the structure of morphogenetic flows, from a flow with no vortices to a flow with two counter-rotating vortices, caused by a transition in the number and location of topological defects in the flow field. Finally, comparing the theoretical predictions to quantitative measurements of both tissue flows and shape during zebrafish body axis elongation, we show that the observed morphogenetic events can be explained by the existence of a fluid-to-solid tissue transition along the anteroposterior axis. These results highlight the role of spatiotemporally-controlled fluid-to-solid transitions in the tissue state as a physical mechanism of embryonic morphogenesis.
format	article
author	Samhita P. Banavar Emmet K. Carn Payam Rowghanian Georgina Stooke-Vaughan Sangwoo Kim Otger Campàs
author_facet	Samhita P. Banavar Emmet K. Carn Payam Rowghanian Georgina Stooke-Vaughan Sangwoo Kim Otger Campàs
author_sort	Samhita P. Banavar
title	Mechanical control of tissue shape and morphogenetic flows during vertebrate body axis elongation
title_short	Mechanical control of tissue shape and morphogenetic flows during vertebrate body axis elongation
title_full	Mechanical control of tissue shape and morphogenetic flows during vertebrate body axis elongation
title_fullStr	Mechanical control of tissue shape and morphogenetic flows during vertebrate body axis elongation
title_full_unstemmed	Mechanical control of tissue shape and morphogenetic flows during vertebrate body axis elongation
title_sort	mechanical control of tissue shape and morphogenetic flows during vertebrate body axis elongation
publisher	Nature Portfolio
publishDate	2021
url	https://doaj.org/article/5eebb36daa444d34aa7da9b300373d7b
work_keys_str_mv	AT samhitapbanavar mechanicalcontroloftissueshapeandmorphogeneticflowsduringvertebratebodyaxiselongation AT emmetkcarn mechanicalcontroloftissueshapeandmorphogeneticflowsduringvertebratebodyaxiselongation AT payamrowghanian mechanicalcontroloftissueshapeandmorphogeneticflowsduringvertebratebodyaxiselongation AT georginastookevaughan mechanicalcontroloftissueshapeandmorphogeneticflowsduringvertebratebodyaxiselongation AT sangwookim mechanicalcontroloftissueshapeandmorphogeneticflowsduringvertebratebodyaxiselongation AT otgercampas mechanicalcontroloftissueshapeandmorphogeneticflowsduringvertebratebodyaxiselongation
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Mechanical control of tissue shape and morphogenetic flows during vertebrate body axis elongation

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