The coordination of spindle-positioning forces during the asymmetric division of the Caenorhabditis elegans zygote

In Caenorhabditis elegans zygote, astral microtubules generate forces essential to position the mitotic spindle, by pushing against and pulling from the cortex. Measuring microtubule dynamics there, we revealed the presence of two populations, corresponding to pulling and pushing events. It offers a unique opportunity to study, under physiological conditions, the variations of both spindle-positioning forces along space and time. We propose a threefold control of pulling force, by polarity, spindle position and mitotic progression. We showed that the sole anteroposterior asymmetry in dynein on-rate, encoding pulling force imbalance, is sufficient to cause posterior spindle displacement. The positional regulation, reflecting the number of microtubule contacts in the posterior-most region, reinforces this imbalance only in late anaphase. Furthermore, we exhibited the first direct proof that dynein processivity increases along mitosis. It reflects the temporal control of pulling forces, which strengthens at anaphase onset following mitotic progression and independently from chromatid separation. In contrast, the pushing force remains constant and symmetric and contributes to maintaining the spindle at the cell centre during metaphase.

Automated summary

In C. elegans zygote, astral microtubules play a crucial role in generating forces to position the mitotic spindle by pushing against and pulling from the cortex. Two populations of microtubule dynamics, corresponding to pulling and pushing events, were identified. A threefold control of pulling force was proposed, with anteroposterior asymmetry in dynein on-rate being a key factor in posterior spindle displacement. Dynein processivity increases along mitosis, reflecting the temporal control of pulling forces, strengthening at anaphase onset independently from chromatid separation, while pushing force remains constant and symmetric during metaphase to maintain spindle position.