Transcriptomic analysis and functional validation reveal key genes involved in metabolism of sucrose, organic acids, phenolics, and carotenoids of fresh-cut melon during storage

• Transcriptomic and bioinformatic analysis revealed key genes involved in quality changes of melon affected by cut-wounding. • Twenty-eight TFs were speculated for regulating the quality of fresh-cut melon. • Overexpression of MELO3C003622 promoted the conversion of sucrose to hexose. • MELO3C007576 and MELO3C026740 positively regulated citric acid and total phenolics contents, respectively. • MELO3C002090 of fresh-cut melon negatively regulated carotenoid metabolism. In this study, transcriptomic and bioinformatic analyses were used to investigate the molecular mechanisms underlying the quality changes in melon fruit (cv. Xizhoumi-17) caused by cut-wounding. Cutting of melon accelerated sucrose decomposition, promoted hexose phosphorylation, and increased the contents of citric acid and malic acid, which were associated with altered expression of CmAI1, CmNI3, CmHXK1, CmCS1, CmMDH1/3 , and CmIDH1 in fresh-cut melon. In addition, four phenylalanine ammonia-lyase genes, three cinnamate-4-hydroxylase genes, one 4-coumarate-CoA ligase gene, one cinnamoyl-CoA reductase gene, and one cinnamyl alcohol dehydrogenase gene were identified as key regulatory genes for phenolic biosynthesis, as well as one geranylgeranyl pyrophosphate synthase gene, one phytoene synthase gene, one lycopene beta-cyclase gene, and two 9-cis epoxycarotenoid dioxygenase genes for carotenoid metabolism. Moreover, combining bioinformatics analysis, nine CmERFs , thirteen CmWRKYs , two CmNACs , two CmMYBs , and two CmbHLHs were identified as putative transcription factors involved in regulating the quality of fresh-cut melon during storage. The results of subcellular localization, dual-luciferase assays, and transient gene expression assays indicated that the nucleus-localized CmWRKY MELO3C003622 activated the CmNI3 promoter, accelerating sucrose decomposition and hexose accumulation, and the nucleus-localized CmWRKYs (MELO3C007576, and MELO3C026740) and CmMYB MELO3C002090 correspondingly increased or decreased the contents of citric acid, total phenolics, or total carotenoids by regulating key genes. These findings indicate that cut-wounding alters the metabolic pathways of melon, and affects the flavor of fresh-cut melon during storage. This genetic information provides a valuable foundation for further improving the quality of fresh-cut melon.