A spatiotemporal transcriptomic atlas of porcine (Sus scrofa) female early gonadal development

Abstract The early gonads of mammals contain primordial germ cells (PGCs) and gonadal somatic cells. In females, the gonadal somatic cells promote the specification of PGCs into oogonia and their entry into meiosis, which is crucial for oogenesis. Although single-cell transcriptome sequencing technology holds significant advantages in cell type identification, its inability to resolve spatial positional information substantially hampers research on communication mechanisms between germ cells and adjacent somatic cells. Here, we utilized high-resolution spatial transcriptomic technology to dissect the spatial dynamics of various cell types during the specification of PGCs into oogonia and their entry into meiosis in porcine gonads. We clarified the spatial localization of two waves of granulosa cells in the supporting cell lineage and their roles in regulating germ cell development. Furthermore, we found that interstitial and endothelial cells were predominantly located in the medullary region of the early gonads. Notably, cell-cell communication analysis revealed the critical role of BMP signaling (BMP2, BMP4 and GDF5) in driving the specification of PGCs into oogonia and their subsequent entry into meiosis. Our study provides a spatially resolved understanding of the PGC-to-oogonia specification in vivo and offers critical resources for reconstituting oogenesis in vitro.