Spatiotemporal organization of dynein in bulk cytoplasm promotes aster growth and positioning in large embryos

During cleavage in vertebrates, large microtubule asters grow from centrosomes in anaphase. The microtubule motor dynein pulls on these asters in bulk cytoplasm and positions centrosomes to determine cleavage geometry. However, how aster growth and pulling are coordinated remains unclear. We discovered that small metaphase asters generate a halo-like enrichment of cytoplasmic dynein at the aster periphery in medaka early embryos. In anaphase, dynein relocates from the halo to growing asters and neighboring membranous organelles, coincident with aster expansion and centrosome movement. Dynein inhibition or localized halo disruption prevents centrosome movement. Unexpectedly, dynein inhibition also suppresses aster growth and causes ectopic cytoplasmic microtubule nucleation, which leads to ectopic furrows. We propose that inactive dynein that accumulated at the metaphase aster periphery is activated in anaphase and incorporates both microtubule nucleators and organelles into growing asters to coordinately promote aster growth and pulling for efficient centrosome positioning in rapidly-dividing, large embryos.