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A fluid-to-solid jamming transition underlies vertebrate body axis elongation

Author

Listed:
  • Alessandro Mongera

    (University of California
    University of California
    European Molecular Biology Laboratory)

  • Payam Rowghanian

    (University of California
    University of California)

  • Hannah J. Gustafson

    (University of California
    University of California
    University of California)

  • Elijah Shelton

    (University of California
    University of California)

  • David A. Kealhofer

    (University of California)

  • Emmet K. Carn

    (University of California)

  • Friedhelm Serwane

    (University of California
    University of California
    Max Planck Institute for Medical Research)

  • Adam A. Lucio

    (University of California
    University of California)

  • James Giammona

    (University of California
    University of California)

  • Otger Campàs

    (University of California
    University of California
    University of California
    University of California)

Abstract

Just as in clay moulding or glass blowing, physically sculpting biological structures requires the constituent material to locally flow like a fluid while maintaining overall mechanical integrity like a solid. Disordered soft materials, such as foams, emulsions and colloidal suspensions, switch from fluid-like to solid-like behaviours at a jamming transition1–4. Similarly, cell collectives have been shown to display glassy dynamics in 2D and 3D5,6 and jamming in cultured epithelial monolayers7,8, behaviours recently predicted theoretically9–11 and proposed to influence asthma pathobiology8 and tumour progression12. However, little is known about whether these seemingly universal behaviours occur in vivo13 and, specifically, whether they play any functional part during embryonic morphogenesis. Here, by combining direct in vivo measurements of tissue mechanics with analysis of cellular dynamics, we show that during vertebrate body axis elongation, posterior tissues undergo a jamming transition from a fluid-like behaviour at the extending end, the mesodermal progenitor zone, to a solid-like behaviour in the presomitic mesoderm. We uncover an anteroposterior, N-cadherin-dependent gradient in yield stress that provides increasing mechanical integrity to the presomitic mesoderm, consistent with the tissue transiting from a wetter to a dryer foam-like architecture. Our results show that cell-scale stresses fluctuate rapidly (within about 1 min), enabling cell rearrangements and effectively ‘melting’ the tissue at the growing end. Persistent (more than 0.5 h) stresses at supracellular scales, rather than cell-scale stresses, guide morphogenetic flows in fluid-like tissue regions. Unidirectional axis extension is sustained by the reported rigidification of the presomitic mesoderm, which mechanically supports posterior, fluid-like tissues during remodelling before their maturation. The spatiotemporal control of fluid-like and solid-like tissue states may represent a generic physical mechanism of embryonic morphogenesis.

Suggested Citation

  • Alessandro Mongera & Payam Rowghanian & Hannah J. Gustafson & Elijah Shelton & David A. Kealhofer & Emmet K. Carn & Friedhelm Serwane & Adam A. Lucio & James Giammona & Otger Campàs, 2018. "A fluid-to-solid jamming transition underlies vertebrate body axis elongation," Nature, Nature, vol. 561(7723), pages 401-405, September.
  • Handle: RePEc:nat:nature:v:561:y:2018:i:7723:d:10.1038_s41586-018-0479-2
    DOI: 10.1038/s41586-018-0479-2
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    Citations

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    Cited by:

    1. 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.
    2. Ece Özelçi & Erik Mailand & Matthias Rüegg & Andrew C. Oates & Mahmut Selman Sakar, 2022. "Deconstructing body axis morphogenesis in zebrafish embryos using robot-assisted tissue micromanipulation," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    3. Pragya Arora & Souvik Sadhukhan & Saroj Kumar Nandi & Dapeng Bi & A. K. Sood & Rajesh Ganapathy, 2024. "A shape-driven reentrant jamming transition in confluent monolayers of synthetic cell-mimics," Nature Communications, Nature, vol. 15(1), pages 1-10, December.
    4. 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.

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