Emergence of a smooth interface from growth of a dendritic network against a mechanosensitive contractile material

Elife. 2021 Aug 23:10:e66929. doi: 10.7554/eLife.66929.

Abstract

Structures and machines require smoothening of raw materials. Self-organized smoothening guides cell and tissue morphogenesis and is relevant to advanced manufacturing. Across the syncytial Drosophila embryo surface, smooth interfaces form between expanding Arp2/3-based actin caps and surrounding actomyosin networks, demarcating the circumferences of nascent dome-like compartments used for pseudocleavage. We found that forming a smooth and circular boundary of the surrounding actomyosin domain requires Arp2/3 in vivo. To dissect the physical basis of this requirement, we reconstituted the interacting networks using node-based models. In simulations of actomyosin networks with local clearances in place of Arp2/3 domains, rough boundaries persisted when myosin contractility was low. With addition of expanding Arp2/3 network domains, myosin domain boundaries failed to smoothen, but accumulated myosin nodes and tension. After incorporating actomyosin mechanosensitivity, Arp2/3 network growth locally induced a surrounding contractile actomyosin ring that smoothened the interface between the cytoskeletal domains, an effect also evident in vivo. In this way, a smooth structure can emerge from the lateral interaction of irregular active materials.

Keywords: Arp2/3; D. melanogaster; actomyosin; cell biology; cell cortex; drosophila embryo pseudo-cleavage; mechanosensitivity; pattern formation; physics of living systems.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actins / genetics
  • Actins / metabolism*
  • Actomyosin / metabolism
  • Animals
  • Cytokinesis / physiology
  • Cytoskeleton / genetics
  • Cytoskeleton / metabolism*
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism*
  • Drosophila melanogaster / enzymology*
  • Drosophila melanogaster / genetics
  • Drosophila melanogaster / metabolism
  • Embryo, Nonmammalian / physiology*
  • Gene Expression Regulation, Developmental

Substances

  • Actins
  • Arp2 protein, Drosophila
  • Arp3 protein, Drosophila
  • Drosophila Proteins
  • Actomyosin

Grants and funding

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