Visceral organ morphogenesis via calcium-patterned muscle constrictions

  1. Noah P Mitchell
  2. Dillon J Cislo
  3. Suraj Shankar
  4. Yuzheng Lin
  5. Boris I Shraiman
  6. Sebastian J Streichan  Is a corresponding author
  1. University of California, Santa Barbara, United States

Abstract

Organ architecture is often composed of multiple laminar tissues arranged in concentric layers. During morphogenesis, the initial geometry of visceral organs undergoes a sequence of folding, adopting a complex shape that is vital for function. Genetic signals are known to impact form, yet the dynamic and mechanical interplay of tissue layers giving rise to organs' complex shapes remains elusive. Here, we trace the dynamics and mechanical interactions of a developing visceral organ across tissue layers, from sub-cellular to organ scale in vivo. Combining deep tissue light-sheet microscopy for in toto live visualization with a novel computational framework for multilayer analysis of evolving complex shapes, we find a dynamic mechanism for organ folding using the embryonic midgut of Drosophila as a model visceral organ. Hox genes, known regulators of organ shape, control the emergence of high-frequency calcium pulses. Spatiotemporally patterned calciumpulses triggermuscle contractions via myosin light chain kinase. Muscle contractions, in turn, induce cell shape change in the adjacent tissue layer. This cell shape change collectively drives a convergent extension pattern. Through tissue incompressibility and initial organ geometry, this in-plane shape change is linked to out-of-plane organ folding. Our analysis follows tissue dynamics during organ shape change in vivo, tracing organ-scale folding to a high-frequency molecular mechanism. These findings offer a mechanical route for gene expression to induce organ shape change: genetic patterning in one layer triggers a physical process in the adjacent layer - revealing post-translational mechanisms that govern shape change.

Data availability

We have uploaded processed data for experiments spanning all figures to FigShare, available at https://figshare.com/authors/Noah_Mitchell/12456507 in project #137793: 'Visceral organ morphogenesis via calcium-patterned constrictions'. The original volumetric data from living imaging are each up to a terabyte in size. We therefore posted processed data on FigShare, including 2D pullback image sequences of the dynamic 3D tissue surfaces, volumetric data for small datasets, and processed tables. An interested researcher would be able to access the original data on our lab server. They would need to contact Sebastian Streichan (streicha@ucsb.edu) to be added to the server's list of users and could then download the original data directly.In addition to the TubULAR package detailed in reference 32, further software and scripts used to analyze the data is available at: https://github.com/npmitchell/VisceralOrganMorphogenesisViaCalciumPatternedMuscleConstrictions.

The following data sets were generated

Article and author information

Author details

  1. Noah P Mitchell

    Kavli Institute for Theoretical Physics, University of California, Santa Barbara, Santa Barbara, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Dillon J Cislo

    Department of Physics, University of California, Santa Barbara, Santa Barbara, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Suraj Shankar

    Kavli Institute for Theoretical Physics, University of California, Santa Barbara, Santa Barbara, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4615-975X
  4. Yuzheng Lin

    Department of Physics, University of California, Santa Barbara, Santa Barbara, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Boris I Shraiman

    Kavli Institute for Theoretical Physics, University of California, Santa Barbara, Santa Barbara, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0886-8990
  6. Sebastian J Streichan

    Department of Physics, University of California, Santa Barbara, Santa Barbara, United States
    For correspondence
    streicha@ucsb.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6105-9087

Funding

National Institutes of Health (R35 GM138203)

  • Sebastian J Streichan

National Institutes of Health (R00 294 HD088708)

  • Sebastian J Streichan

Helen Hay Whitney Foundation (F-1246)

  • Noah P Mitchell

National Science Foundation (PHY-1748958)

  • Boris I Shraiman

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Michel Bagnat, Duke University, United States

Publication history

  1. Preprint posted: November 8, 2021 (view preprint)
  2. Received: January 26, 2022
  3. Accepted: May 8, 2022
  4. Accepted Manuscript published: May 20, 2022 (version 1)
  5. Version of Record published: July 12, 2022 (version 2)

Copyright

© 2022, Mitchell et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Noah P Mitchell
  2. Dillon J Cislo
  3. Suraj Shankar
  4. Yuzheng Lin
  5. Boris I Shraiman
  6. Sebastian J Streichan
(2022)
Visceral organ morphogenesis via calcium-patterned muscle constrictions
eLife 11:e77355.
https://doi.org/10.7554/eLife.77355
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