First genome report of Oudemansiella apalosarca and comparative transcriptomics on fruiting body formation under different light conditions

Oudemansiella apalosarca, a newly identified edible fungus, exhibits industrial cultivation potential because of its short production cycle and lack of a casing layer. However, the absence of genomic data has hampered its development and varietal enhancement. This study reports the first genome sequence of O. apalosarca, comprising 53.13 Mb across 27 scaffolds and 14,650 protein-coding genes, with superior scaffold N50 and BUSCO values compared to those of other Oudemansiella genomes. Phylogenetic analysis of single-copy orthologous proteins from 25 fungal genomes revealed close relations to O. raphanipes and Mucidula mucidula, with significant protein collinearity within the Physalacriaceae family. Cultivation in complete darkness yielded pure white, small-cap, and long-stipe fruiting bodies, indicating industrial advantages. Differential transcriptome analysis of the cap and stipe under varying light conditions identified key genes and pathways regulating phenotypic changes. Kyoto Encyclopedia of Genes and Genomes (KEGG) assessment and gene set enrichment analysis (GSEA) revealed significant negative regulation of DNA replication pathway genes in the cap, with the downregulation of 10 cell cycle and mismatch repair genes. Genes related to cell wall formation and carbon metabolism were upregulated, thus promoting stipe elongation. The tyrosine metabolism pathway influenced cap coloration, with tyrosinase identified as a multicopy gene. Phylogenetic analysis revealed diverse evolutionary origins. Key tyrosinase-related genes A6_A10477 and A6_A09603 were overexpressed in the light, revealing their role in melanin formation. In summary, this study provides genomic resources for O. apalosarca breeding improvement and elucidates light-induced regulatory mechanisms in its development, thereby providing theoretical and technical support for industrial applications.