title: Cortical instability drives periodic supracellular actin pattern formation in epithelial tubes.
abstract: An essential question of morphogenesis is how patterns arise without preexisting positional information, as inspired by Turing. In the past few years, cytoskeletal flows in the cell cortex have been identified as a key mechanism of molecular patterning at the subcellular level. Theoretical and in vitro studies have suggested that biological polymers such as actomyosin gels have the property to self-organize, but the applicability of this concept in an in vivo setting remains unclear. Here, we report that the regular spacing pattern of supracellular actin rings in the Drosophila tracheal tubule is governed by a self-organizing principle. We propose a simple biophysical model where pattern formation arises from the interplay of myosin contractility and actin turnover. We validate the hypotheses of the model using photobleaching experiments and report that the formation of actin rings is contractility dependent. Moreover, genetic and pharmacological perturbations of the physical properties of the actomyosin gel modify the spacing of the pattern, as the model predicted. In addition, our model posited a role of cortical friction in stabilizing the spacing pattern of actin rings. Consistently, genetic depletion of apical extracellular matrix caused strikingly dynamic movements of actin rings, mirroring our model prediction of a transition from steady to chaotic actin patterns at low cortical friction. Our results therefore demonstrate quantitatively that a hydrodynamical instability of the actin cortex can trigger regular pattern formation and drive morphogenesis in an in vivo setting.
authors.affiliation: Physicochimie Curie (Institut Curie/CNRS-UMR168/Université Pierre et Marie Curie), Institut Curie, Paris Sciences et Lettres, Centre de Recherche, 75248 Paris Cedex 05, France; Cavendish Laboratory, University of Cambridge, Cambridge CB3 0HE, United Kingdom; eh508@cam.ac.uk bodong@ouc.edu.cn.
authors.forename: Edouard
authors.initials: E
authors.lastname: Hannezo
authors.affiliation: Laboratory for Morphogenetic Signaling, RIKEN Center for Developmental Biology, Kobe, Hyogo 650-0047, Japan; Ministry of Education Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Institute of Evolution and Marine Biodiversity, Ocean University of China, Qingdao 266003, China; eh508@cam.ac.uk bodong@ouc.edu.cn.
authors.forename: Bo
authors.initials: B
authors.lastname: Dong
authors.affiliation: Physicochimie Curie (Institut Curie/CNRS-UMR168/Université Pierre et Marie Curie), Institut Curie, Paris Sciences et Lettres, Centre de Recherche, 75248 Paris Cedex 05, France; Mathematical Institute, University of Oxford, Oxford OX2 6GG, United Kingdom;
authors.forename: Pierre
authors.initials: P
authors.lastname: Recho
authors.affiliation: Physicochimie Curie (Institut Curie/CNRS-UMR168/Université Pierre et Marie Curie), Institut Curie, Paris Sciences et Lettres, Centre de Recherche, 75248 Paris Cedex 05, France; École Supérieure de Physique et de Chimie Industrielles de la Ville de Paris, 75005 Paris, France.
authors.forename: Jean-François
authors.initials: JF
authors.lastname: Joanny
authors.affiliation: Laboratory for Morphogenetic Signaling, RIKEN Center for Developmental Biology, Kobe, Hyogo 650-0047, Japan;
authors.forename: Shigeo
authors.initials: S
authors.lastname: Hayashi
mesh_terms: D000199:Actins / Q000378:metabolism*; D000818:Animals; D004330:Drosophila / Q000196:embryology; D047108:Embryonic Development; D004847:Epithelial Cells / Q000378:metabolism*; D008954:Models, Biological
chemical_list: D000199:Actins
keywords: Drosophila; actomyosin; biological tubes; biophysics; pattern formation