Exosomes-mediated molecular mechanisms underlying the transformation of ovarian tissue into a functional placental analogue in black rockfish (Sebastes schlegelii)

Viviparity has independently evolved multiple times in teleosts, leading to diverse modes of maternal nutrient provisioning. In black rockfish (Sebastes schlegelii), embryos gain dry weight during gestation, with the presence of a placental connection that supports maternal-fetal nutrient transfer. Although prior studies have outlined the morphology and evolutionary convergence of the black rockfish placental analogue, its full architecture and underlying molecular mechanisms remain unresolved. Here, we show that the maternal component of the placental analogue, derived from ovarian follicular tissue, consists of a vascularized outer layer and a glandularized inner layer, organized into a sac-like structure, and at the molecular level, this transformation involves epithelial-mesenchymal interactions, angiogenesis, and immune responses. We observed exosome-like structures surrounding the placental analogue and isolated and characterized ovarian exosomes, suggesting active crosstalk between developing embryos and the maternal ovary underlying these changes. Subsequent proteomic and transcriptomic analyses revealed that they carry diverse functional cargos, including hgfb mRNA. We further showed that ovarian cells efficiently internalize exosomes, resulting in increased intracellular hgfb mRNA and subsequent Hgfb protein expression and secretion, which reprogram gene expression and promote placental development-related processes such as angiogenesis. Taken together, these findings elucidate the molecular mechanisms underlying ovarian placentation and angiogenesis during gestation in black rockfish, and are of significant theoretical relevance for understanding reproductive adaptations in fishes undergoing the evolutionary shift from oviparity to viviparity.