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Embryo-scale epithelial buckling forms a propagating furrow that initiates gastrulation

Author

Listed:
  • Julien Fierling

    (LIPhy)

  • Alphy John

    (iBV)

  • Barthélémy Delorme

    (iBV)

  • Alexandre Torzynski

    (LIPhy)

  • Guy B. Blanchard

    (University of Cambridge)

  • Claire M. Lye

    (University of Cambridge)

  • Anna Popkova

    (iBV)

  • Grégoire Malandain

    (CNRS, I3S)

  • Bénédicte Sanson

    (University of Cambridge)

  • Jocelyn Étienne

    (LIPhy)

  • Philippe Marmottant

    (LIPhy)

  • Catherine Quilliet

    (LIPhy)

  • Matteo Rauzi

    (iBV)

Abstract

Cell apical constriction driven by actomyosin contraction forces is a conserved mechanism during tissue folding in embryo development. While much is now understood of the molecular mechanism responsible for apical constriction and of the tissue-scale integration of the ensuing in-plane deformations, it is still not clear if apical actomyosin contraction forces are necessary or sufficient per se to drive tissue folding. To tackle this question, we use the Drosophila embryo model system that forms a furrow on the ventral side, initiating mesoderm internalization. Past computational models support the idea that cell apical contraction forces may not be sufficient and that active or passive cell apico-basal forces may be necessary to drive cell wedging leading to tissue furrowing. By using 3D computational modelling and in toto embryo image analysis and manipulation, we now challenge this idea and show that embryo-scale force balance at the tissue surface, rather than cell-autonomous shape changes, is necessary and sufficient to drive a buckling of the epithelial surface forming a furrow which propagates and initiates embryo gastrulation.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-30493-3
    DOI: 10.1038/s41467-022-30493-3
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    References listed on IDEAS

    as
    1. Anaïs Bailles & Claudio Collinet & Jean-Marc Philippe & Pierre-François Lenne & Edwin Munro & Thomas Lecuit, 2019. "Genetic induction and mechanochemical propagation of a morphogenetic wave," Nature, Nature, vol. 572(7770), pages 467-473, August.
    2. Mélanie Gracia & Sophie Theis & Amsha Proag & Guillaume Gay & Corinne Benassayag & Magali Suzanne, 2019. "Mechanical impact of epithelial−mesenchymal transition on epithelial morphogenesis in Drosophila," Nature Communications, Nature, vol. 10(1), pages 1-17, December.
    3. 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.
    4. Soline Chanet & Callie J. Miller & Eeshit Dhaval Vaishnav & Bard Ermentrout & Lance A. Davidson & Adam C. Martin, 2017. "Actomyosin meshwork mechanosensing enables tissue shape to orient cell force," Nature Communications, Nature, vol. 8(1), pages 1-13, August.
    5. Emiliano Izquierdo & Theresa Quinkler & Stefano De Renzis, 2018. "Guided morphogenesis through optogenetic activation of Rho signalling during early Drosophila embryogenesis," Nature Communications, Nature, vol. 9(1), pages 1-13, December.
    6. Bing He & Konstantin Doubrovinski & Oleg Polyakov & Eric Wieschaus, 2014. "Apical constriction drives tissue-scale hydrodynamic flow to mediate cell elongation," Nature, Nature, vol. 508(7496), pages 392-396, April.
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    Cited by:

    1. Miho Matsuda & Jan Rozman & Sassan Ostvar & Karen E. Kasza & Sergei Y. Sokol, 2023. "Mechanical control of neural plate folding by apical domain alteration," Nature Communications, Nature, vol. 14(1), pages 1-14, December.

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