A Node Organization Generates Tension And Promotes Stability In The Fission Yeast Contractile Ring

During cytokinesis in fungi, amoeba, and animals, cells divide into two using the tension generated by a contractile actomyosin ring. Tension is generated by myosin-II that pulls on actin filaments, but how these forces are marshalled to generate tension is unclear. Recently super-resolution microscopy (FPALM) showed that myosin-II and formin-capped barbed-ends of actin filaments colocalize in membrane-anchored protein complexes called nodes in fission yeast rings (Laplante et al., 2016). Using this information, a mathematical model showed there exists two contra-rotating families of nodes. Actomyosin forces operate both within and between families, and both contribute equally to ring tension. Anchoring ensures that nodes aggregate slowly such that turnover can prevent instabilities. We incorporated this nodes ultrastructure in a mathematical model of the fission yeast ring that uses a coarse-grained, continuous representation of the nodes, and is constrained by the ample experimental data about the fission yeast ring. We find there are two classes of node, stochastically determined by the polarity of the actin filaments associated with the node: nodes that move clockwise, or nodes that move counterclockwise around the ring, due to myosin-II pulling forces. Thus, two node families contra-rotate with respect to one another. This agrees with the bidirectional motion measured in FPALM. We find that opposite-polarity nodes are pulled towards one another, and this sliding filament mechanism generates 50% of ring tension. Pulling forces between same-polarity nodes contributes another 50% and involves no relative motion. The predicted ring tension agrees with experiment (390 pN), with a best-fit force per Myo2 head of ∼1 pN, close to previous measurements. Without turnover, a catastrophic intrinsic contractile instability occurs. Small density fluctuations are amplified and fracture the ring. Restoring turnover reduced instabilities as turnover is faster than aggregation.