Mouse pre-meiotic germline cysts contain fusome-like structure dependent on Dazl that mediates cyst fragmentation and oocyte development

Mouse female primordial germ cells undergo five synchronous, incomplete mitotic divisions, and send each resulting germline cyst into meiosis to fragment and produce 4-6 oocytes and 24-26 supportive nurse cells. How oocytes are specified, linked appropriately to nurse cells and enabled to acquire high quality organelles and cytoplasm on a massive scale remains unclear. We identified an asymmetric Golgi, ER and microtubule-associated structure, “Visham,” similar to the Drosophila fusome. Starting as the EMA granule, Visham distributes asymmetrically in cyst cells and enriches in future oocytes with Pard3, and Golgi-endosomal UPR (unfolded protein response) genes. Transient spindle remnants rich in stable acetylated microtubules link early cyst cells for part of each cell cycle. Cysts sometimes develop a gap in these microtubules beginning at the 8-cell stage that predicts programmed cyst fragmentation into six-cell cysts of similar structure. Visham persists during meiosis where it mediates Pard3-dependent polarity, Xbp1-dependent adaptive UPR, and organelle transfer to the Balbiani body. In DAZL mutants, cysts still form, but polarity and oocyte production are blocked.