Transcriptomic and Metabolomic Analysis Reveals the Molecular Mechanisms of the Impact on the Fruiting Body Phenotype of Lentinula edodes Under Different Light Conditions

Light quality is a pivotal environmental signal governing the morphogenesis and metabolic programming of edible fungi. This study evaluated the effects of eight light qualities—red (R), green (G), blue (B), red-green (RG), red-blue (RB), green-blue (GB), red-green-blue (RGB), and dark control (CK)—on the agronomic traits of Lentinula edodes. Among all treatments, blue light (B) emerged as the most effective regulator, yielding the highest productivity per log (228.12 g), and significantly enhancing pileus diameter (45.17 mm) and stipe thickness (29.45 mm). To elucidate the underlying molecular mechanisms, integrated transcriptomic and metabolomic analyses were performed on primordia and mature fruiting bodies. Transcriptomic profiling identified 4280 differentially expressed genes (DEGs) under blue light, which were significantly enriched in energy metabolism and structural development pathways. Metabolomic analysis revealed 45 differentially expressed metabolites (DEMs), highlighting a 7.64-fold upregulation of 9(S)-HPODE and a marked downregulation of L-arginine at the harvest stage under blue light. Multi-omics integration demonstrated that blue light orchestrates a strategic metabolic shift: it activates arginine and proline metabolism during the primordial stage, maintains linoleic acid metabolism throughout development, and triggers alanine, aspartate, and glutamate metabolism during the transition to maturity. These pathways facilitate the conversion of amino acids into energy precursors and enhance cell membrane fluidity through unsaturated fatty acid synthesis to support rapid growth. Conversely, red light treatment triggered stress-related MAPK signaling, delayed primordium formation, and redirected resources toward stipe elongation via phenylalanine accumulation, resulting in significantly lower yields. In conclusion, this study confirms that blue light is the optimal condition for L. edodes cultivation, providing a robust molecular foundation for precision light-regulation strategies to maximize yield and quality in commercial production.