Self-organized patterning of cell morphology via mechanosensitive feedback

Author:

Dye Natalie A123ORCID,Popović Marko456ORCID,Iyer K Venkatesan12,Fuhrmann Jana F12,Piscitello-Gómez Romina12,Eaton Suzanne12,Jülicher Frank256ORCID

Affiliation:

1. Max Planck Institute for Molecular Cell Biology and Genetics, Dresden, Germany

2. Cluster of Excellence Physics of Life, Technische Universität Dresden, Dresden, Germany

3. Mildred Scheel Nachwuchszentrum (MSNZ) P2, Medical Faculty, Technische Universität Dresden, Dresden, Germany

4. Institute of Physics, École Polytechnique Fédérale de Lausanne, Lausanne, Switzerland

5. Max Planck Institute for the Physics of Complex Systems, Dresden, Germany

6. Center for Systems Biology Dresden, Dresden, Germany

Abstract

Tissue organization is often characterized by specific patterns of cell morphology. How such patterns emerge in developing tissues is a fundamental open question. Here, we investigate the emergence of tissue-scale patterns of cell shape and mechanical tissue stress in the Drosophila wing imaginal disc during larval development. Using quantitative analysis of the cellular dynamics, we reveal a pattern of radially oriented cell rearrangements that is coupled to the buildup of tangential cell elongation. Developing a laser ablation method, we map tissue stresses and extract key parameters of tissue mechanics. We present a continuum theory showing that this pattern of cell morphology and tissue stress can arise via self-organization of a mechanical feedback that couples cell polarity to active cell rearrangements. The predictions of this model are supported by knockdown of MyoVI, a component of mechanosensitive feedback. Our work reveals a mechanism for the emergence of cellular patterns in morphogenesis.

Funder

Max-Planck-Gesellschaft

Deutsche Forschungsgemeinschaft

Swiss National Science Foundation

Simons Foundation

ELBE PhD program

Deutsche Krebshilfe

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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