LAUSR

A universal feature of early oocyte differentiation is formation of the Balbiani body (Bb), a large granule of specific mRNAs, proteins, and organelles. The zebrafish Bb establishes oocyte animal-vegetal polarity by specifying the oocyte vegetal pole. The Bb has been observed for two centuries, but how it forms and is asymmetrically positioned was unknown. Using quantitative image analysis, we traced oocyte symmetry breaking to a nuclear asymmetry at the onset of meiosis called the chromosomal bouquet. The bouquet is a universal feature of meiosis where all telomeres cluster to one pole on the nuclear envelope (NE). Telomere movements and clustering on the NE facilitate chromosomal pairing and meiotic recombination. We show that Bb precursors first localize with the centrosome to the cytoplasm apposing the bouquet telomere cluster. They then aggregate around the centrosome in a specialized nuclear cleft that we identified, assembling the early Bb. We found that the bouquet nuclear events and the cytoplasmic Bb precursor localization are mechanistically coordinated bymicrotubule. Thus, the animal-vegetal axis of the oocyte is aligned to the nuclear axis of the bouquet. This symmetry breaking lays upstream to Bucky ball, the only known regulator of Bb formation. We link two universal features of oogenesis, the Bb and the chromosomal bouquet, to oocyte polarization, and propose that the centrosome forms a cellular organizer that we term the meiotic–vegetal center (MVC), coupling meiosis and oocyte patterning. We next revealed that oocytes are organized in cysts with synchronized MVCs. We discovered bouquet specific primary cilia that may synchronize and mechanically regulate cyst MVCs. Moreover, the MVC localizes near cytoplasmic bridges that connect sister cyst oocytes, suggesting its positioning by a previous mitotic division plane. These results link polarity to cyst organization. We uncovered key, functionally coordinated meiotic and cellular polarity events of the early oocyte.