Genome-wide identification and transcriptomic reprogramming of the hsd17b gene family during endocrine-induced sex reversal in mandarin fish (Siniperca chuatsi).

The 17β-hydroxysteroid dehydrogenase (hsd17b) gene family plays a pivotal role in sex steroid metabolism and gonadal differentiation in teleosts; however, their evolutionary dynamics and regulatory mechanisms during sex reversal in the mandarin fish (Siniperca chuatsi) remain poorly understood. In this study, we identified ten hsd17b family members in the S. chuatsi genome. Structural and phylogenetic analyses revealed the conservation of the core SDR domain across all members, alongside significant structural divergence in hsd17b4, which uniquely fused with SCP2 and PLN domains, indicating a pleiotropic role in both steroidogenesis and peroxisomal lipid metabolism. Spatiotemporal expression profiling demonstrated pronounced subfunctionalization: hsd17b4 exhibited robust testis-biased expression during spermatogenesis, whereas hsd17b1 was transiently upregulated during critical windows of ovarian differentiation. Furthermore, exogenous hormone treatments (MT, ETO, and E1) successfully induced functional sex reversal, accompanied by profound transcriptional reprogramming. Notably, ETO- and MT-induced masculinization was driven by a synergistic metabolic shift within the gonads. This process involved the significant up-regulation of the core testis-associated gene (hsd17b4), coordinated with genes facilitating cholesterol biosynthesis (hsd17b7) and estrogen inactivation (hsd17b8), effectively suppressing the female steroidogenic network (hsd17b1, hsd17b12a). Conversely, E1-induced feminization repressed male-pathway genes and promoted hsd17b1 transcription. Taken together, our findings demonstrate that the transcriptional antagonism and synergistic metabolic coordination among hsd17b members constitute the core molecular underpinning of endocrine-induced sexual plasticity. This study provides crucial molecular insights and viable targets for sex control breeding in teleost aquaculture.