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Metabolic reprogramming and mitochondrial dysfunction underlie β gonia arrest and niche cell dysfunction in sterile triploid oysters

Huihui Wang,Xi Lin,Chunxue Zheng,Hong Yu,Qi Li

Published 2025 in Communications Biology

ABSTRACT

Complementary to the classical view that triploid sterility results from meiotic failure, female triploid pacific oysters exhibit partial sterility also characterized by the impairment of the differentiation of germ cells, forming β gonia. However, the molecular basis underlying this sterility remains unclear, partly due to the diffuse nature of oyster gonads, which lack distinct structural boundaries, making cell-type identification challenging. Here, we integrate high-resolution spatial transcriptomics (Stereo-seq) and single-nucleus RNA sequencing (snRNA-seq) to construct a spatially resolved molecular atlas of sterile triploid oyster gonads, enabling precise characterization of β gonia transcriptional dysregulation and their disrupted interactions with niche cells. We find that β gonia exhibit germplasm mRNA downregulation, impaired ATP synthesis, and excessive mitochondrial autophagy, likely driven by the silencing of SOHLH2, a key regulator of oocyte differentiation. Additionally, triploid niche cells undergo G1 phase arrest via NOTCH-Hes1a-CCNA2 signaling, which may contribute to gonadal microenvironment disruption. We further observe disrupted metabolic partitioning between F3nβ-Niche and VCT cells, with niche cells displaying diminished steroidogenic activity and fatty acid metabolism, while VCT cells enhance lipogenesis and AMPK/PPAR signaling, forming a disrupted nutrient reservoir. Dysregulated GRN and cholesterol (LIPA/RORA) signaling further exacerbate metabolic imbalances and germ cell mitophagy. These findings establish a mechanistic framework for triploid sterility, implicating mitochondrial dysfunction, mitophagy, and niche-VCT metabolic reprogramming in germ cell arrest. Our study provides novel insights into germline-soma coordination, reproductive control strategies, and the broader implications of polyploid sterility in invertebrates. Integrative spatial and single-nucleus transcriptomics reveal mitochondrial dysfunction, mitophagy, and disrupted germ-niche signalling underlying germ cell arrest and sterility in triploid oysters.

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