IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v16y2025i1d10.1038_s41467-025-61702-4.html
   My bibliography  Save this article

Highly dynamic mechanical transitions in embryonic cell populations during Drosophila gastrulation

Author

Listed:
  • Juan Manuel Gomez

    (European Molecular Biology Laboratory (EMBL))

  • Carlo Bevilacqua

    (European Molecular Biology Laboratory (EMBL))

  • Abhisha Thayambath

    (North Carolina State University
    North Carolina State University)

  • Jean-Karim Heriche

    (European Molecular Biology Laboratory (EMBL))

  • Maria Leptin

    (European Molecular Biology Laboratory (EMBL)
    European Molecular Biology Laboratory (EMBL)
    University of Cologne)

  • Julio M. Belmonte

    (North Carolina State University
    North Carolina State University)

  • Robert Prevedel

    (European Molecular Biology Laboratory (EMBL)
    European Molecular Biology Laboratory (EMBL)
    European Molecular Biology Laboratory (EMBL)
    German Center for Lung Research (DZL))

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.

Suggested Citation

  • Juan Manuel Gomez & Carlo Bevilacqua & Abhisha Thayambath & Jean-Karim Heriche & Maria Leptin & Julio M. Belmonte & Robert Prevedel, 2025. "Highly dynamic mechanical transitions in embryonic cell populations during Drosophila gastrulation," Nature Communications, Nature, vol. 16(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:16:y:2025:i:1:d:10.1038_s41467-025-61702-4
    DOI: 10.1038/s41467-025-61702-4
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-025-61702-4
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-025-61702-4?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Adam C. Martin & Matthias Kaschube & Eric F. Wieschaus, 2009. "Pulsed contractions of an actin–myosin network drive apical constriction," Nature, Nature, vol. 457(7228), pages 495-499, January.
    2. Juan Manuel Gomez & Lyubov Chumakova & Natalia A. Bulgakova & Nicholas H. Brown, 2016. "Microtubule organization is determined by the shape of epithelial cells," Nature Communications, Nature, vol. 7(1), pages 1-13, December.
    3. Darren Gilmour & Martina Rembold & Maria Leptin, 2017. "From morphogen to morphogenesis and back," Nature, Nature, vol. 541(7637), pages 311-320, January.
    4. Matteo Rauzi & Uros Krzic & Timothy E. Saunders & Matej Krajnc & Primož Ziherl & Lars Hufnagel & Maria Leptin, 2015. "Embryo-scale tissue mechanics during Drosophila gastrulation movements," Nature Communications, Nature, vol. 6(1), pages 1-12, December.
    5. Yu-Chiun Wang & Zia Khan & Matthias Kaschube & Eric F. Wieschaus, 2012. "Differential positioning of adherens junctions is associated with initiation of epithelial folding," Nature, Nature, vol. 484(7394), pages 390-393, April.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Hannah J. Gustafson & Nikolas Claussen & Stefano Renzis & Sebastian J. Streichan, 2022. "Patterned mechanical feedback establishes a global myosin gradient," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    2. Aurélien Villedieu & Lale Alpar & Isabelle Gaugué & Amina Joudat & François Graner & Floris Bosveld & Yohanns Bellaïche, 2023. "Homeotic compartment curvature and tension control spatiotemporal folding dynamics," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    3. Amrita Singh & Sameedha Thale & Tobias Leibner & Lucas Lamparter & Andrea Ricker & Harald Nüsse & Jürgen Klingauf & Milos Galic & Mario Ohlberger & Maja Matis, 2024. "Dynamic interplay of microtubule and actomyosin forces drive tissue extension," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    4. Nicolas Roby & Matteo Rauzi, 2025. "Nuclear position controls the activity of cortical actomyosin networks powering simultaneous morphogenetic events," Nature Communications, Nature, vol. 16(1), pages 1-15, December.
    5. Angus Inman & Elisabeth Spiritosanto & Bridget L. Evans & Judith E. Lutton & Masazumi Tada & Till Bretschneider & Pierre A. Haas & Michael Smutny, 2025. "A multi-tiered mechanical mechanism shapes the early neural plate," Nature Communications, Nature, vol. 16(1), pages 1-17, December.
    6. Sijia Zhou & Peng Li & Jiaying Liu & Juan Liao & Hao Li & Lin Chen & Zhihua Li & Qiongyu Guo & Karine Belguise & Bin Yi & Xiaobo Wang, 2022. "Two Rac1 pools integrate the direction and coordination of collective cell migration," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    7. Anchel de Jaime-Soguero & Janina Hattemer & Anja Bufe & Alexander Haas & Jeroen Berg & Vincent Batenburg & Biswajit Das & Barbara Marco & Stefania Androulaki & Nicolas Böhly & Jonathan J. M. Landry & , 2024. "Developmental signals control chromosome segregation fidelity during pluripotency and neurogenesis by modulating replicative stress," Nature Communications, Nature, vol. 15(1), pages 1-22, December.
    8. Amlan Barai & Matis Soleilhac & Wang Xi & Shao-Zhen Lin & Marc Karnat & Elsa Bazellières & Sylvie Richelme & Brice Lecouffe & Claire Chardès & Dominique Berrebi & Frank Rümmele & Manuel Théry & Jean-F, 2025. "A multicellular star-shaped actin network underpins epithelial organization and connectivity," Nature Communications, Nature, vol. 16(1), pages 1-19, December.
    9. Julien Fierling & Alphy John & Barthélémy Delorme & Alexandre Torzynski & Guy B. Blanchard & Claire M. Lye & Anna Popkova & Grégoire Malandain & Bénédicte Sanson & Jocelyn Étienne & Philippe Marmottan, 2022. "Embryo-scale epithelial buckling forms a propagating furrow that initiates gastrulation," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    10. Ngoc Minh Nguyen & Emmanuel Farge, 2024. "Mechanical induction in metazoan development and evolution: from earliest multi-cellular organisms to modern animal embryos," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    11. Guilherme Ventura & Aboutaleb Amiri & Raghavan Thiagarajan & Mari Tolonen & Amin Doostmohammadi & Jakub Sedzinski, 2022. "Multiciliated cells use filopodia to probe tissue mechanics during epithelial integration in vivo," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    12. repec:plo:pcbi00:1005443 is not listed on IDEAS
    13. repec:plo:pone00:0075051 is not listed on IDEAS
    14. Lijuan Du & Alex Sohr & Yujia Li & Sougata Roy, 2022. "GPI-anchored FGF directs cytoneme-mediated bidirectional contacts to regulate its tissue-specific dispersion," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    15. Christophe Royer & Elizabeth Sandham & Elizabeth Slee & Falk Schneider & Christoffer B. Lagerholm & Jonathan Godwin & Nisha Veits & Holly Hathrell & Felix Zhou & Karolis Leonavicius & Jemma Garratt & , 2022. "ASPP2 maintains the integrity of mechanically stressed pseudostratified epithelia during morphogenesis," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    16. Aki Teranishi & Misato Mori & Rihoko Ichiki & Satoshi Toda & Go Shioi & Satoru Okuda, 2024. "An actin bracket-induced elastoplastic transition determines epithelial folding irreversibility," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    17. Bibi Najma & Minu Varghese & Lev Tsidilkovski & Linnea Lemma & Aparna Baskaran & Guillaume Duclos, 2022. "Competing instabilities reveal how to rationally design and control active crosslinked gels," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    18. Natalia M. Ziojła & Magdalena Socha & M. Cecilia Guerra & Dorota Kizewska & Katarzyna Blaszczyk & Edyta Urbaniak & Sara Henry & Malgorzata Grabowska & Kathy K. Niakan & Aryeh Warmflash & Malgorzata Bo, 2025. "ETVs dictate hPSC differentiation by tuning biophysical properties," Nature Communications, Nature, vol. 16(1), pages 1-21, December.
    19. Jaeseung Youn & Dohui Kim & Hyunsu Kwak & Anna Lee & Dong Sung Kim, 2024. "Tissue-scale in vitro epithelial wrinkling and wrinkle-to-fold transition," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    20. Özge Özgüç & Ludmilla de Plater & Varun Kapoor & Anna Francesca Tortorelli & Andrew G Clark & Jean-Léon Maître, 2022. "Cortical softening elicits zygotic contractility during mouse preimplantation development," PLOS Biology, Public Library of Science, vol. 20(3), pages 1-23, March.
    21. Alexis Villars & Alexis Matamoro-Vidal & Florence Levillayer & Romain Levayer, 2022. "Microtubule disassembly by caspases is an important rate-limiting step of cell extrusion," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    22. Nabila Founounou & Reza Farhadifar & Giovanna M. Collu & Ursula Weber & Michael J. Shelley & Marek Mlodzik, 2021. "Tissue fluidity mediated by adherens junction dynamics promotes planar cell polarity-driven ommatidial rotation," Nature Communications, Nature, vol. 12(1), pages 1-16, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:16:y:2025:i:1:d:10.1038_s41467-025-61702-4. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.