Combined transcriptome and metabolome analysis reveals the mechanism of fruit quality formation in different watermelon (Citrullus lanatus) cultivars

• Metabolites and gene expression of four watermelon cultivars were analyzed. • Differentially expressed genes and differential metabolites affecting fruit flesh sugar and acid content were identified. • Metabolic networks affecting watermelon flesh color formation were identified. • Most DEGs and DAMs associated with anthocyanin synthesis were higher in JC (‘Jingcai No.1’) than in other cultivars. Fruit characteristics (flesh color, sweetness, flavor, etc.) of watermelon are largely the result of human selection. In this study, we combined the metabolome and transcriptome to investigate differentially expressed genes and differential metabolites related to sugar-acid and flesh color in four commercial watermelon cultivars. Fifty-eight genes and nine metabolites were identified in the organic acid and sugar metabolism pathways. Six of these metabolites were significantly up-regulated in ‘Jingcai No.1’ (JC), including sucrose, fructose, cellobiose, oxaloacetate, succinate, and malate. The expression of sucrose synthase 2 ( SUS2 ), sucrose-phosphate synthase ( SPS1 ), fructose bisphosphate aldolase ( FBA2 ), glyceraldehyde 3-phosphate dehydrogenase( GAPN ), trehalose-phosphate phosphatase ( TPPJ ), trehalose-phosphate synthase ( TPS1 ), 1,4-alpha-glucan-branching ( SBE1 ) and SBE3 , which are involved in sugar and acid metabolism, was also significantly higher than that of the other three cultivars. A total of 55 genes and 102 metabolites were identified in the pathway related to flesh color formation (carotenoid synthesis, phenylpropanoid synthesis, flavonoid synthesis). The abundance of genes and metabolites associated with sugar and acid metabolism and color formation were generally lower in ‘Jingmei 2k’ (EK) and ‘L600’ (LB) than in JC and ‘Chaoyue’ (CY). In summary, the omics analysis of the four watermelon cultivars revealed significant differences in metabolic genes and metabolites involved in sugar-acid biosynthesis and flesh color formation, which provides new ideas for improving the quality and commercial value of watermelon fruits through genetic engineering.