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.
Highlights
Smooth components are integral to the assembly and function of human-made structures and devices
When actomyosin networks were simulated with clearances instead of Arp2/3 networks, rough boundaries persisted with low levels of myosin contractility
The overall organization of the myosin networks simulated with mechanosensitivity and Arp2/3 network growth (Fig 4D) closely resembled the myosin networks formed in the presence of Arp2/3 actin caps in wild type embryos (Fig 3A). These analyses suggest that a smooth and circular interface can form from the growth of an Arp2/3 network against a weakly contractile actomyosin network that is mechanosensitive to local activation
Summary
Smooth components are integral to the assembly and function of human-made structures and devices. Smooth structures convey important functions in living systems, but their formation relies on self-assembly and self-organization. Fuller understanding of these mechanisms will aid advanced manufacturing with smart materials for a broad range of applications; from sensors and data processing, to filters and self-cleaning surfaces, to medical devices and robotics (Begley et al, 2019; Eder et al, 2018; Holmes, 2019; Wang et al, 2020). In conventional industries, starting materials are Living and synthetic systems face a challenge: how can small and roughly distributed components form large and smooth structures that convey function? In the Drosophila wing imaginal disc, gene expression patterns define the cells of specific compartments, but non-muscle myosin II (myosin hereafter) is required to pull actin networks into straight cables integrated via cell-cell junctions to form smooth compartment boundaries that define the architecture of the mature wing (Harris, 2018; Wang and Dahmann, 2020)
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