A gelation transition enables the self-organization of bipolar metaphase spindles

The mitotic spindle is a highly dynamic bipolar structure that emerges from the self-organization of microtubules, molecular motors, and other proteins. Sustained motor-driven poleward flows of short dynamic microtubules play a key role in the bipolar organization of spindles. However, it is not understood how the local activity of motor proteins generates these large-scale coherent poleward flows. Here, we combine experiments and simulations to show that a gelation transition enables long-ranged microtubule transport causing spindles to self-organize into two oppositely polarized microtubule gels. Laser ablation experiments reveal that local active stresses generated at the spindle midplane propagate through the structure thereby driving global coherent microtubule flows. Simulations show that microtubule gels undergoing rapid turnover can exhibit long stress relaxation times, in agreement with the long-ranged flows observed in experiments. Finally, we show that either disrupting such flows or decreasing the network connectivity can lead to a microtubule polarity reversal in spindles both in the simulations and in the experiments. Thus, we uncover an unexpected connection between spindle rheology and architecture in spindle self-organization.