Radiation-specific metabolic reprogramming drives yield-quality balance in Astragalus mongholicus: Comparative insights from gamma-ray and heavy-ion beam irradiation

• The first elucidation of gamma-ray and heavy-ion beam differential regulatory mechanisms in metabolic pathways. • Confirmed gamma-ray dose-response relationship for synchronously enhancing biomass (2 ×) and flavonoids (20.2 %). • Deciphered cytokinin-auxin signaling network mediating radiation responses. • Radiation-responsive CHS/CHI clusters drive isoflavonoid accumulation. • Established a multi-omics framework for medicinal plant mutagenesis. The inherent trade-off between biomass accumulation and secondary metabolite production remains a fundamental challenge in medicinal plant domestication. While conventional approaches predominantly focus on single-trait improvement, effective strategies for concurrent optimization remain underexplored. Here we present a pioneering comparative investigation employing gamma-ray (GR) and heavy-ion beam (HIB) irradiation (200 Gy) in Astragalus mongholicus cultivation, coupled with integrated transcriptomic and metabolomic profiling to dissect their differential impacts on agronomic traits and medicinal quality. Our findings demonstrate GR irradiation as a potent inducer of biomass enhancement, achieving a remarkable 200% increase in fresh root weight while simultaneously elevating flavonoid content by 20.2%. In comparison, HIB irradiation exerted more pronounced impacts on metabolic reprogramming and genetic regulation despite moderate growth promotion. Multi-omics analysis revealed distinct molecular mechanisms: GR preferentially activated auxin signaling pathways and phenylpropanoid biosynthesis to coordinate root development and flavonoid accumulation, whereas HIB significantly modulated amino acid metabolism and secondary metabolite biosynthesis pathways. This radiation-specific pattern provides unprecedented insights into regulation of secondary metabolic networks regulation. Our study establishes a novel paradigm for radiation-based medicinal plants improvement - GR demonstrates superior potential for biomass and primary bioactive compound enhancement, while HIB offers unique advantages in manipulating complex secondary metabolism. These findings provide a theoretical foundation for precision application of radiation technologies in agronomic strategies aimed at enhancing bioactive compound accumulation in medicinal plants by leveraging the hormesis effect, effectively addressing the persistent yield-quality paradox in pharmaceutical crop cultivation.