Assembly and positioning of actomyosin rings by contractility and planar cell polarity.
The actomyosin cytoskeleton is a primary force-generating mechanism in morphogenesis, thus a robust spatial control of cytoskeletal positioning is essential. In this report, we demonstrate that actomyosin contractility and planar cell polarity (PCP) interact in post-mitotic Ciona notochord cells to self-assemble and reposition actomyosin rings, which play an essential role for cell elongation. Intriguingly, rings always form at the cells' anterior edge before migrating towards the center as contractility increases, reflecting a novel dynamical property of the cortex. Our drug and genetic manipulations uncover a tug-of-war between contractility, which localizes cortical flows toward the equator and PCP, which tries to reposition them. We develop a simple model of the physical forces underlying this tug-of-war, which quantitatively reproduces our results. We thus propose a quantitative framework for dissecting the relative contribution of contractility and PCP to the self-assembly and repositioning of cytoskeletal structures, which should be applicable to other morphogenetic events.
Sars International Centre for Marine Molecular Biology, University of Bergen, Bergen, Norway.
Ivonne M
IM
Sehring
Department of Physico-Chemistry of Living Matter, Institut Curie, Paris, France.|Mathematical Institute, University of Oxford, Oxford, United Kingdom.
Pierre
P
Recho
Sars International Centre for Marine Molecular Biology, University of Bergen, Bergen, Norway.
Elsa
E
Denker
Department of Molecular, Cellular and Developmental Biology, University of California, Santa Barbara, Santa Barbara, United States.
Matthew
M
Kourakis
Sars International Centre for Marine Molecular Biology, University of Bergen, Bergen, Norway.
Birthe
B
Mathiesen
Department of Physico-Chemistry of Living Matter, Institut Curie, Paris, France.|The Gurdon Institute, University of Cambridge, Cambridge, United Kingdom.
Edouard
E
Hannezo
Ministry of Education Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao, China.|Laboratory for Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, .
Bo
B
Dong
Sars International Centre for Marine Molecular Biology, University of Bergen, Bergen, Norway.
Di
D
Jiang
D000205:Actomyosin / Q000378:metabolism*; D000818:Animals; D055592:Biophysical Phenomena; D016764:Cell Polarity; D048430:Cell Shape; D002938:Ciona intestinalis / Q000166:cytology / Q000254:growth & development / Q000502:physiology*; D009119:Muscle Contraction; D009672:Notochord / Q000166:cytology / Q000254:growth & development / Q000502:physiology*; D055503:Protein Multimerization; D021381:Protein Transport
D000205:Actomyosin
Ciona intestinalis; PCP; actomyosin ring; biophysics; cell biology; contractility; notochord; self-organization/active gels; structural biology