Rapid assembly of a polar network architecture drives efficient actomyosin contractility

Abstract

SO_SCPLOWUMMARYC_SCPLOWActin network architecture and dynamics play a central role in cell contractility and tissue morphogenesis. Pulsed contractions driven by RhoA represent a generic mode of actomyosin contractility, but the mechanisms underlying (1) how their specific architecture emerges, and (2) how this architecture supports the contractile function of the network, remain unclear. Here, we combine quantitative microscopy, single-molecule imaging, numerical simulations and simple mathematical modelling, to explore the dynamic network architecture underlying pulsed contraction. We show that during pulsed contractions, two subpopulations of formins are recruited by RhoA from the cytoplasm and bind to the cell surface in the early C. elegans embryo: recruited formins, a functionally inactive population, and elongating formins, which actively participate in actin filaments elongation. Focusing on formin dynamics during pulses, we show that minority elongating formins precede recruited formins, a kinetic dynamics compatible with formins capturing and rapidly saturating barbed ends available for filament elongation. We then show that these elongating formins assemble a polar network of actin, with barbed ends pointing out of the pulse, pointing to a kinetic rather than mechanical control of network architecture. Finally, our numerical simulations demonstrate that this geometry favors rapid network contraction. Our results thus show that formins saturate available actin filaments barbed ends and convert a local, biochemical gradient of RhoA activity into a polar network architecture, thereby driving rapid and efficient network contractility, an important evolutionary feature in a metazoan with a rapid embryonic cell cycles. HO_SCPLOWIGHLIGHTSC_SCPLOWO_LIThe formin CYK-1 drives actin network assembly during RhoA-driven pulses C_LIO_LIThe process is extremely rapid, with a formin-based actin elongation rate higher than 1.3 m{middle dot}s-1 C_LIO_LIA barbed-end saturation mechanism allows for responsive F-actin assembly C_LIO_LIRapid and responsive F-actin elongation results in the assembly of aster-like polar actin networks C_LIO_LINumerical simulations show network polarity drives very efficient network contractility C_LI