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, supported by a placental connection that facilitates 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. 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 ovarian exosomes for characterization. These findings suggest active crosstalk between developing embryos and the maternal ovary, which may underlie the observed changes. Subsequent proteomic and transcriptomic analyses revealed that these exosomes carry diverse functional cargos, including hepatocyte growth factor b (hgfb) mRNA. Ovarian cells efficiently internalize exosomes, upregulating hgfb mRNA and protein expression and secretion, which in turn reprograms gene expression and promotes angiogenesis-related placentation. Together, these results elucidate the molecular underpinnings of ovarian placentation in black rockfish and offer valuable perspectives on the oviparity-to-viviparity transition in fish evolution.