Single-cell transcriptome unravels spermatogonial stem cells and dynamic heterogeneity of spermatogenesis in seasonal breeding teleost

Abstract Seasonal spermatogenesis in fish is driven by spermatogonial stem cells (SSCs), which undergo a complex cellular process to differentiate into mature sperm. In this study, we characterized spermatogenesis in the large yellow croaker ( Larimichthys crocea ), a marine fish of significant commercial value, based on a high-resolution single-cell RNA-seq atlas of testicular cells from three distinct developmental stages- juvenile, adult differentiating and regressed testes. We detailed continuous developmental trajectory of spermatogenic cells, from spermatogonia to spermatids, elucidating the molecular events involved in spermatogenesis. We uncovered dynamic heterogeneity in cellular compositions throughout the annual reproductive cycle, accompanied by strong molecular signatures within specific testicular cells. Notably, we identified a distinct population of SSCs and observed a critical metabolic transition from glycolysis to oxidative phosphorylation, enhancing our understanding of the biochemical and molecular characteristics of SSCs. Additionally, we elucidated the interactions between somatic cells and spermatogonia, illuminating the mechanisms that regulate SSCs development. Overall, this work enhances our understanding of spermatogenesis in seasonal breeding teleost and provides essential insights for the further conservation and culture of SSCs. Summary statement Our study reveals new insights into the development of spermatogonial stem cells (SSCs), potentially impacting further conservation and culture of SSCs in teleost.