Integrated multi-omic analyses on yellow Flammulina filiformis cultivar reveal postharvest oxidative damage responses

Yellow cultivars of Flammulina filiformis are prone to browning, which causes significant yearly loss. This study investigated the critical factors involved and revealed that oxygen plays an essential role in the browning process. Integrated multi-omic analyses, including genome sequencing, transcriptome profiling, and 4D label-free proteome quantification, were incorporated to dissect essential genes and metabolic pathways in the process of oxidative deterioration of the mushroom. The results revealed genes encoding browning-related enzymes in the F. filiformis genome, which are involved in the metabolism of tyrosine and the biosynthesis of phenylpropanoid. Laccase 4, which is over-regulated in oxygen-treated samples compared to anaerobically treated ones by transcriptomic and proteomic analysis, and further confirmed by qRT-PCR and enzyme assays, could be a crucial polyphenol oxidase catalyzing the browning reaction. DNA damaging, proteolysis, and oxidative phosphorylation accelerate cell senescence, contribute to cell integrity damage, and trigger the biosynthesis of melanin as a defective mechanism. These findings lay the foundations for postharvest preservation and future genetic breeding of F. filiformis.