Non-canonical cytokinesis driven by mechanical uncoupling via nematic flows and adhesion-based invagination

Cleavage - the series of rapid cell divisions that follow fertilization - marks the onset of metazoan development and represents a deeply conserved evolutionary process. Across animals, two principal modes exist: complete (holoblastic) and incomplete (meroblastic) cleavage. While holoblastic cleavage resembles conventional cytokinesis both in vitro and in vivo, the mechanisms underlying meroblastic cleavage have remained poorly understood. Using zebrafish embryos as a model, we show that meroblastic cleavage proceeds through a distinct two-step mechanism. The process begins with the assembly and contraction of a large, arc-shaped actomyosin cable. However, this contractile event alone is insufficient to complete division. A second phase, driven by cadherin-mediated membrane adhesion, is required to invaginate the furrow ridge. Strikingly, this transition depends on mechanical uncoupling of the contractile cable from the surrounding cortex. We demonstrate that such uncoupling arises from an active nematic instability, which both enhances contractility along the cable and generates actin depletion zones that relieve lateral connections. Together, these findings reveal that meroblastic cleavage is governed not by a single actomyosin-based event but by a sequential interplay between cytoskeletal contraction and cadherin-dependent adhesion, highlighting a mechanism fundamentally distinct from canonical cytokinesis.