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Geometric control of Myosin-II orientation during axis elongation

View ORCID ProfileM.F. Lefebvre, View ORCID ProfileN.H. Claussen, View ORCID ProfileN.P. Mitchell, H.J. Gustafson, View ORCID ProfileS.J. Streichan
doi: https://doi.org/10.1101/2022.01.12.476069
M.F. Lefebvre
1Department of Physics, University of California, Santa Barbara
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N.H. Claussen
1Department of Physics, University of California, Santa Barbara
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N.P. Mitchell
1Department of Physics, University of California, Santa Barbara
2Kavli Institute for Theoretical Physics, University of California, Santa Barbara
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H.J. Gustafson
1Department of Physics, University of California, Santa Barbara
3Biomolecular Science and Engineering, University of California, Santa Barbara
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S.J. Streichan
1Department of Physics, University of California, Santa Barbara
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  • For correspondence: streicha@ucsb.edu
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Abstract

The actomyosin cytoskeleton is a crucial driver of morphogenesis. Yet how the behavior of large-scale cytoskeletal patterns in deforming tissues emerges from the interplay of geometry, genetics, and mechanics remains incompletely understood. Convergent extension flow 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 there are complex rules governing how the control of myosin anisotropy is regulated by gene expression patterns. 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 corresponding genetic patterning. We found pair rule gene expression continuously deformed, flowing with the tissue frame. In contrast, myosin anisotropy orientation remained nearly static, aligned with the stationary dorsal-ventral axis of the embryo. We propose myosin recruitment by a geometrically defined static source, potentially related to the embryo-scale epithelial tension, and account for transient deflections by the interplay of cytoskeletal turnover with 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.

Competing Interest Statement

The authors have declared no competing interest.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted January 12, 2022.
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Geometric control of Myosin-II orientation during axis elongation
M.F. Lefebvre, N.H. Claussen, N.P. Mitchell, H.J. Gustafson, S.J. Streichan
bioRxiv 2022.01.12.476069; doi: https://doi.org/10.1101/2022.01.12.476069
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Geometric control of Myosin-II orientation during axis elongation
M.F. Lefebvre, N.H. Claussen, N.P. Mitchell, H.J. Gustafson, S.J. Streichan
bioRxiv 2022.01.12.476069; doi: https://doi.org/10.1101/2022.01.12.476069

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