A Centrosome Organizing Center Couples Oocyte Polarization with Meiosis and Coordinates Cellular Mechanisms of Early Oogenesis

Widely in animals and plants, gamete polarization lays the foundations for early embryonic development. Vertebrate oocyte polarity has been observed for two centuries, but how it is generated was unknown. Universal to differentiating oocytes is formation of the Balbiani body (Bb), a large phase-separated aggregate of specific mRNP granules. The zebrafish Bb establishes the oocyte animal-vegetal polarity and is essential for embryonic development, but how it forms and positioned was unknown. We traced oocyte symmetry breaking to a nuclear asymmetry at the onset of meiosis called the chromosomal bouquet. The bouquet is a universal meiotic feature, where telomeres associate with Sun/KASH proteins on the nuclear envelope (NE), connecting to cytoplasmic microtubules that emanate from the centrosome. Telomeres then rotate to facilitate chromosomal pairing and recombination, and cluster to the NE pole apposing the centrosome. We found that Bb granules first localize to the bouquet centrosome and required microtubules that mechanistically coupled their localization with bouquet formation. Granule nucleation around the centrosome assembled the mature phase-separated Bb requiring the intrinsically disordered protein Bucky ball, demonstrating phase-separation mechanisms in oocyte polarization. Thus, the bouquet centrosome functions as a cellular organizer that we termed the Centrosome Organizing Center (COC), coupling meiosis and oocyte patterning. Upstream, the COC localized adjacent to a cytoplasmic bridge from preceding cytokinesis, aligning oocyte polarity to precursor mitotic division plane. We further identified a novel primary cilium that connects to the COC, likely regulating bouquet mechanics. We uncovered a cellular organizer that integrates multiple functionally coordinated events in oogenesis.