Anchoring of actin to the plasma membrane enables tension production in the fission yeast cytokinetic ring

The cytokinetic ring generates tensile force that drives cell division, but how tension emerges from the relatively disordered ring organization remains unclear. Long ago a muscle-like sliding filament mechanism was proposed, but evidence for sarcomeric order is lacking. Here we present quantitative evidence that in fission yeast ring tension originates from barbed-end anchoring of actin filaments to the plasma membrane, providing resistance to myosin forces which enables filaments to develop tension. The role of anchoring was highlighted by experiments on isolated fission yeast rings, where sections of ring unanchored from the membrane and shortened ~30-fold faster than normal [Mishra M., et al. (2013) Nat Cell Biol 15(7):853-859]. The dramatically elevated constriction rates are unexplained. Here we present a molecularly explicit simulation of constricting partially anchored rings as studied in these experiments. Simulations accurately reproduced the experimental constriction rates, and showed that following anchor release a segment becomes tensionless and shortens via a novel non-contractile reeling-in mechanism at about the load-free myosin-II velocity. The ends are reeled in by barbed-end-anchored actin filaments in adjacent segments. Other actin anchoring schemes failed to constrict rings. Our results quantitatively support a specific organization and anchoring scheme that generates tension in the cytokinetic ring.