Highly dynamic mechanical transitions in embryonic cell populations during Drosophila gastrulation

Abstract During development, three-dimensional morphology arises from the balance of forces acting on cells and tissues, and their material properties. Cellular forces have been investigated, however the characterisation and specification of cell material properties remains poorly understood. Here,...

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Main Authors: Juan Manuel Gomez, Carlo Bevilacqua, Abhisha Thayambath, Jean-Karim Heriche, Maria Leptin, Julio M. Belmonte, Robert Prevedel
Format: Article
Language:English
Published: Nature Portfolio 2025-07-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-61702-4
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author Juan Manuel Gomez
Carlo Bevilacqua
Abhisha Thayambath
Jean-Karim Heriche
Maria Leptin
Julio M. Belmonte
Robert Prevedel
author_facet Juan Manuel Gomez
Carlo Bevilacqua
Abhisha Thayambath
Jean-Karim Heriche
Maria Leptin
Julio M. Belmonte
Robert Prevedel
author_sort Juan Manuel Gomez
collection DOAJ
description Abstract During development, three-dimensional morphology arises from the balance of forces acting on cells and tissues, and their material properties. Cellular forces have been investigated, however the characterisation and specification of cell material properties remains poorly understood. Here, we characterise and spatially map in three dimensions the dynamics of the longitudinal modulus at GHz frequencies to characterise the evolving blastoderm material properties during Drosophila gastrulation utilising line-scan Brillouin microscopy. We find that blastoderm cells undergo rapid and spatially varying changes in their material properties and that these differ in cells with different fates and behaviours. We identify microtubules as potential mechano-effectors, and develop a physical model to understand the role of localised and dynamic changes in material properties during tissue folding. Our work provides the first spatio-temporal description of evolving material properties during organismal morphogenesis, and highlights the potential of Brillouin microscopy for studying the dynamic changes in cell shape and cell material properties simultaneously.
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spelling doaj-art-90b0db7b4b3f4337a520d792256a6ab22025-08-20T04:03:02ZengNature PortfolioNature Communications2041-17232025-07-0116111710.1038/s41467-025-61702-4Highly dynamic mechanical transitions in embryonic cell populations during Drosophila gastrulationJuan Manuel Gomez0Carlo Bevilacqua1Abhisha Thayambath2Jean-Karim Heriche3Maria Leptin4Julio M. Belmonte5Robert Prevedel6Cell Biology and Biophysics Unit, European Molecular Biology Laboratory (EMBL)Cell Biology and Biophysics Unit, European Molecular Biology Laboratory (EMBL)Quantitative and Computational Developmental Biology Cluster, North Carolina State UniversityCell Biology and Biophysics Unit, European Molecular Biology Laboratory (EMBL)Developmental Biology Unit, European Molecular Biology Laboratory (EMBL)Quantitative and Computational Developmental Biology Cluster, North Carolina State UniversityCell Biology and Biophysics Unit, European Molecular Biology Laboratory (EMBL)Abstract During development, three-dimensional morphology arises from the balance of forces acting on cells and tissues, and their material properties. Cellular forces have been investigated, however the characterisation and specification of cell material properties remains poorly understood. Here, we characterise and spatially map in three dimensions the dynamics of the longitudinal modulus at GHz frequencies to characterise the evolving blastoderm material properties during Drosophila gastrulation utilising line-scan Brillouin microscopy. We find that blastoderm cells undergo rapid and spatially varying changes in their material properties and that these differ in cells with different fates and behaviours. We identify microtubules as potential mechano-effectors, and develop a physical model to understand the role of localised and dynamic changes in material properties during tissue folding. Our work provides the first spatio-temporal description of evolving material properties during organismal morphogenesis, and highlights the potential of Brillouin microscopy for studying the dynamic changes in cell shape and cell material properties simultaneously.https://doi.org/10.1038/s41467-025-61702-4
spellingShingle Juan Manuel Gomez
Carlo Bevilacqua
Abhisha Thayambath
Jean-Karim Heriche
Maria Leptin
Julio M. Belmonte
Robert Prevedel
Highly dynamic mechanical transitions in embryonic cell populations during Drosophila gastrulation
Nature Communications
title Highly dynamic mechanical transitions in embryonic cell populations during Drosophila gastrulation
title_full Highly dynamic mechanical transitions in embryonic cell populations during Drosophila gastrulation
title_fullStr Highly dynamic mechanical transitions in embryonic cell populations during Drosophila gastrulation
title_full_unstemmed Highly dynamic mechanical transitions in embryonic cell populations during Drosophila gastrulation
title_short Highly dynamic mechanical transitions in embryonic cell populations during Drosophila gastrulation
title_sort highly dynamic mechanical transitions in embryonic cell populations during drosophila gastrulation
url https://doi.org/10.1038/s41467-025-61702-4
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