Follicle development is a critical process in mammalian reproduction, with significant implications for ovarian reserve and fertility. is a known key factor regulating the initiation of meiosis; however, oocyte-like cells still appear in -deficient mice. Nevertheless, the underlying mechanism remains unclear and requires further investigation. Therefore, we used single-cell RNA sequencing to construct a comprehensive transcriptional atlas of ovarian cells from both wild-type and -deficient mice at embryonic stages E14.5 and E16.5. With stringent quality control, we obtained a total of 14,755 single cells of six major cell types. A further fine-scale analysis of the germ cell clusters revealed notable heterogeneity between wild-type and -deficient mice. Compared to the wild-type mice, the deficiency in led to the downregulation of meiosis-related genes (e.g., , and ), and the upregulation of apoptosis-related genes (e.g., , , and ), thereby hindering the meiotic process. Notably, we observed that, following deficiency, the expression levels of and remained elevated at this stage. Furthermore, an RNA interference analysis confirmed the potential role of these genes as regulatory factors in the formation of primordial follicle-like cells. Additionally, deficiency disrupted the signaling between germ cells and pregranulosa cells that is mediated by Mdk-Sdc1, leading to the abnormal expression of the PI3K/AKT signaling pathway. Together, these results shed light on the molecular processes governing germ cell differentiation and folliculogenesis, emphasizing the complex role of in ovarian function.