Abstract
Although the Golgi apparatus undergoes extensive disassembly during mitosis to ensure its equitable partitioning into two daughter cells, the extreme asymmetry of oocyte meiosis obviates this need, raising fundamental questions about the existence and necessity of Golgi disassembly in oocytes. Herein, we demonstrated the existence of a Golgi disassembly process during oocyte meiosis I, which peaked at germinal vesicle breakdown (GVBD) and was largely completed by metaphase II (MII). Strikingly, the vesiculation stage of Golgi disassembly exhibited a function divergent from mitosis by governing spindle cortical migration during metaphase I (MI), thereby ensuring oocyte polarity establishment. Moreover, we found that macroautophagy/autophagy negatively regulated the vesiculation stage of Golgi disassembly: its hyperactivation suppressed vesiculation, whereas its inhibition conversely accelerated this process. Mechanistically, MIA2 and SFT2D2 were identified as key downstream effectors through which autophagy controlled Golgi vesiculation. MIA2 mediated autophagy-dependent regulation of Golgi dynamics through its two LIR motifs, thereby linking autophagic signaling to Golgi remodeling. Specifically, autophagy activation downregulated MIA2, thus inhibiting the ubiquitin-dependent degradation of SFT2D2, consequently suppressing Golgi vesiculation and spindle migration during oocyte meiosis I; conversely, autophagy inhibition accelerated these processes by increasing MIA2 to promote SFT2D2 degradation. These findings elucidate the key role of autophagy in regulating Golgi disassembly, thereby providing a new organelle-based perspective on how autophagy contributes to oocyte spindle migration. Furthermore, our work identifies a novel Golgi-dependent mechanism for oocyte polarity establishment and uncovers the divergent functions of Golgi remodeling across distinct division modes.