1. Physics of Living Systems

Geometric control of Myosin-II orientation during axis elongation

  1. Matthew F Lefebvre
  2. Nikolas H Claussen
  3. Noah P Mitchell
  4. Hannah J Gustafson
  5. Sebastian J Streichan  Is a corresponding author
  1. University of California, Santa Barbara, United States
https://doi.org/10.7554/eLife.78787
Share this article
Cite this article
  1. Matthew F Lefebvre
  2. Nikolas H Claussen
  3. Noah P Mitchell
  4. Hannah J Gustafson
  5. Sebastian J Streichan
(2023)
Geometric control of Myosin-II orientation during axis elongation
eLife 12:e78787.
https://doi.org/10.7554/eLife.78787
  2. Download BibTeX
  3. Download .RIS

Abstract

The actomyosin cytoskeleton is a crucial driver of morphogenesis. Yet how the behavior of largescale cytoskeletal patterns in deforming tissues emerges from the interplay of geometry, genetics, and mechanics remains incompletely understood. Convergent extension in D. melanogaster embryos provides the opportunity to establish a quantitative understanding of the dynamics of anisotropic non-muscle myosin II. Cell-scale analysis of protein localization in fixed embryos suggests that gene expression patterns govern myosin anisotropy via complex rules. However, technical limitations have impeded quantitative and dynamic studies of this process at the whole embryo level, leaving the role of geometry open. Here we combine in toto live imaging with quantitative analysis of molecular dynamics to characterize the distribution of myosin anisotropy and the corresponding genetic patterning. We found pair rule gene expression continuously deformed, flowing with the tissue frame. In contrast, myosin anisotropy orientation remained approximately static, and was only weakly deflected from the stationary dorsal-ventral axis of the embryo. We propose that myosin is recruited by a geometrically defined static source, potentially related to the embryoscale epithelial tension, and account for transient deflections by cytoskeletal turnover and junction reorientation by flow. With only one parameter, this model quantitatively accounts for the time course of myosin anisotropy orientation in wild-type, twist, and even-skipped embryos as well as embryos with perturbed egg geometry. Geometric patterning of the cytoskeleton suggests a simple physical strategy to ensure a robust flow and formation of shape.

Data availability

All data for this article is available publicly without any restrictions. In our article, we make use of two datasets: (1) confocal microscopy data of FRAP experiments, which is available on the Dryad data repository https://doi.org/10.25349/D94C8M. (2) Lightsheet microscopy data of entire embryos. The data we use in the current publication is a subset of a larger dataset, the 'Morphodynamic atlas of Drosophila development', which is publicly available on the Dryad data repository https://doi.org/10.25349/D9WW43. This collection is indexed by the fly genotype and fluorescent marker imaged, so that the movies and images used in the current publication can be found easily. Lightsheet microscopy integrates microscopy and computational processing and its computational pipeline creates intermediate, 'raw' data files, which are of very large size (TBs for a single movie). This raw data is available upon request from the corresponding author without restriction or need for a specific research proposal. The analysis code used is available on GitHub https://github.com/nikolas-claussen/Geometric-control-of-Myosin-II-orientation-during-axis-elongation.

The following data sets were generated

Article and author information

Author details

  1. Matthew F Lefebvre

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

  2. Nikolas H Claussen

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

  3. Noah P Mitchell

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

  4. Hannah J Gustafson

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

  5. 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 (5 R35 GM138203)

  • Sebastian J Streichan

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

Copyright

© 2023, Lefebvre 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.

Metrics

  • 1,730
    views
  • 219
    downloads
  • 18
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Matthew F Lefebvre
  2. Nikolas H Claussen
  3. Noah P Mitchell
  4. Hannah J Gustafson
  5. Sebastian J Streichan
(2023)
Geometric control of Myosin-II orientation during axis elongation
eLife 12:e78787.
https://doi.org/10.7554/eLife.78787

Share this article

https://doi.org/10.7554/eLife.78787

Categories and tags

Research organism

Further reading

    1. Physics of Living Systems

    Modularity of the segmentation clock and morphogenesis

    James E Hammond, Ruth E Baker, Berta Verd
    Research Article

    Vertebrates have evolved great diversity in the number of segments dividing the trunk body, however, the developmental origin of the evolvability of this trait is poorly understood. The number of segments is thought to be determined in embryogenesis as a product of morphogenesis of the pre-somitic mesoderm (PSM) and the periodicity of a molecular oscillator active within the PSM known as the segmentation clock. Here, we explore whether the clock and PSM morphogenesis exhibit developmental modularity, as independent evolution of these two processes may explain the high evolvability of segment number. Using a computational model of the clock and PSM parameterised for zebrafish, we find that the clock is broadly robust to variation in morphogenetic processes such as cell ingression, motility, compaction, and cell division. We show that this robustness is in part determined by the length of the PSM and the strength of phase coupling in the clock. As previous studies report no changes to morphogenesis upon perturbing the clock, we suggest that the clock and morphogenesis of the PSM exhibit developmental modularity.

    1. Physics of Living Systems

    Emergence of ion-channel-mediated electrical oscillations in Escherichia coli biofilms

    Emmanuel Akabuogu, Victor Carneiro da Cunha Martorelli ... Thomas A Waigh
    Research Article

    Bacterial biofilms are communities of bacteria usually attached to solid strata and often differentiated into complex structures. Communication across biofilms has been shown to involve chemical signaling and, more recently, electrical signaling in Gram-positive biofilms. We report for the first time, community-level synchronized membrane potential dynamics in three-dimensional Escherichia coli biofilms. Two hyperpolarization events are observed in response to light stress. The first requires mechanically sensitive ion channels (MscK, MscL, and MscS) and the second needs the Kch-potassium channel. The channels mediated both local spiking of single E. coli biofilms and long-range coordinated electrical signaling in E. coli biofilms. The electrical phenomena are explained using Hodgkin-Huxley and 3D fire-diffuse-fire agent-based models. These data demonstrate that electrical wavefronts based on potassium ions are a mechanism by which signaling occurs in Gram-negative biofilms and as such may represent a conserved mechanism for communication across biofilms.

    1. Cell Biology
    2. Physics of Living Systems

    A differentiable Gillespie algorithm for simulating chemical kinetics, parameter estimation, and designing synthetic biological circuits

    Krishna Rijal, Pankaj Mehta
    Research Article

    The Gillespie algorithm is commonly used to simulate and analyze complex chemical reaction networks. Here, we leverage recent breakthroughs in deep learning to develop a fully differentiable variant of the Gillespie algorithm. The differentiable Gillespie algorithm (DGA) approximates discontinuous operations in the exact Gillespie algorithm using smooth functions, allowing for the calculation of gradients using backpropagation. The DGA can be used to quickly and accurately learn kinetic parameters using gradient descent and design biochemical networks with desired properties. As an illustration, we apply the DGA to study stochastic models of gene promoters. We show that the DGA can be used to: (1) successfully learn kinetic parameters from experimental measurements of mRNA expression levels from two distinct Escherichia coli promoters and (2) design nonequilibrium promoter architectures with desired input–output relationships. These examples illustrate the utility of the DGA for analyzing stochastic chemical kinetics, including a wide variety of problems of interest to synthetic and systems biology.