Distinct muscle stem cell fates governing hyperplasia and hypertrophy muscle growth in fish

BackgroundIn vertebrates, skeletal muscle grows postnatally through different strategies. While mammals predominantly rely on fiber hypertrophy after birth, many teleost fish retain the unique ability to generate new fibers via hyperplasia well into juvenile stages. The molecular mechanisms governing the transition between hyperplastic-hypertrophic and hypertrophic growth modes in fish muscle remain poorly understood. ResultsWe generated a single-cell transcriptomic atlas of muscle-derived cells from juvenile Oncorhynchus mykiss (rainbow trout) at five growth stages. Fifteen tissue resident cell populations were identified, including eight myogenic subpopulations spanning from quiescent stem cells to terminally differentiating myocytes. Two distinct transcriptional trajectories were uncovered thanks to RNA velocity analysis: one present only during hyperplastic growth and another maintained throughout growth, indicating specialization of satellite cells toward hyperplasia or hypertrophy. Comparative analyses with human single-cell atlases indicate that subpopulations specifically related to hyperplasia and hypertrophy are conserved, depending on stage (fetal or adult). Strikingly, we identified a population of pax7+/pdgfr+ cells, indicating plasticity toward fibroblastic lineage and associating these cells with hypertrophic growth. Furthermore, both intrinsic changes in muscle stem cells and extrinsic remodeling of the extracellular matrix accompanied the decline of hyperplasia, highlighting dynamic crosstalk between myogenic and mesenchymal compartments. ConclusionsOur findings reveal the existence of two transcriptionally distinct muscle stem cell fates that underlie hyperplastic versus hypertrophic growth in fish. The identification of a tissue-resident pax7+/pdgfr+ subpopulation provides new insights into muscle stem cell plasticity and niche remodeling. This work establishes a comparative framework to explore the regulation of postnatal muscle growth across vertebrates.