An integrated transcriptome and metabolome approach reveals the accumulation of taste-related metabolites and gene regulatory networks during watermelon fruit development.

MAIN CONCLUSION: Accumulation patterns and gene regulatory networks of sugars and cucurbitacins and related primary and secondary metabolites during cultivated watermelon 'Cheng Lan' and wild watermelon 'PI 632,751' fruit development were identified. Metabolites are the end products of cellular regulatory processes and play important roles in fruit taste formation. However, comprehensive studies on the accumulation patterns of watermelon fruit metabolites and transcriptional regulatory networks are still scarce. In this study, 451 annotated metabolites were identified at four key fruit developmental stages in wild watermelon 'PI 632,751' and modern cultivated watermelon 'Cheng Lan'. Interestingly, 11 sugars and 25 major primary metabolites were mainly accumulated in 'Cheng Lan' during fruit development, which are considered to be the potential metabolites beneficial to the formation of watermelon taste. Cucurbitacins and the main flavonoids were mainly specifically accumulated in 'PI 632,751', not being considered to be responsible for the taste. Moreover, forty-seven genes involved in carbohydrate metabolism, glycolysis, and TCA cycle were highly expressed in 'Cheng Lan', which was positively correlated with the accumulation of major primary metabolites. Alternatively, seven UDP-glycosyltransferase genes are closely related to the glycosylation of cucurbitacins through co-expression analysis. Our findings established a global map of metabolite accumulation and gene regulation during fruit development in wild and cultivated watermelons and provided valuable information on taste formation in watermelon fruit.

Metabolome and Transcriptome Integration Reveals Insights Into Flavor Formation of 'Crimson' Watermelon Flesh During Fruit Development.

Metabolites have been reported as the main factor that influences the fruit flavor of watermelon. But the comprehensive study on the dynamics of metabolites during the development of watermelon fruit is not up-to-date. In this study, metabolome and transcriptome datasets of 'Crimson' watermelon fruit at four key developmental stages were generated. A total of 517 metabolites were detected by ultrahigh-performance liquid chromatography-electrospray ionization-tandem mass spectrometry and gas chromatography-solid-phase microextraction-mass spectrometry. Meanwhile, by K-means clustering analysis, the total differentially expressed genes were clustered in six classes. Integrating transcriptome and metabolome data revealed similar expression trends of sugars and genes involved in the glycolytic pathway, providing molecular insights into the formation of taste during fruit development. Furthermore, through coexpression analysis, we identified five differentially expressed ADH (alcohol dehydrogenase) genes (Cla97C01G013600, Cla97C05G089700, Cla97C01G001290, Cla97C05G095170, and Cla97C06G118330), which were found to be closely related to C9 alcohols/aldehydes, providing information for the formation of fruit aroma. Our findings establish a metabolic profile during watermelon fruit development and provide insights into flavor formation.

Identification of key gene networks controlling organic acid and sugar metabolism during watermelon fruit development by integrating metabolic phenotypes and gene expression profiles.

The organoleptic qualities of watermelon fruit are defined by the sugar and organic acid contents, which undergo considerable variations during development and maturation. The molecular mechanisms underlying these variations remain unclear. In this study, we used transcriptome profiles to investigate the coexpression patterns of gene networks associated with sugar and organic acid metabolism. We identified 3 gene networks/modules containing 2443 genes highly correlated with sugars and organic acids. Within these modules, based on intramodular significance and Reverse Transcription Quantitative polymerase chain reaction (RT-qPCR), we identified 7 genes involved in the metabolism of sugars and organic acids. Among these genes, Cla97C01G000640, Cla97C05G087120 and Cla97C01G018840 (r2 = 0.83 with glucose content) were identified as sugar transporters (SWEET, EDR6 and STP) and Cla97C03G064990 (r2 = 0.92 with sucrose content) was identified as a sucrose synthase from information available for other crops. Similarly, Cla97C07G128420, Cla97C03G068240 and Cla97C01G008870, having strong correlations with malic (r2 = 0.75) and citric acid (r2 = 0.85), were annotated as malate and citrate transporters (ALMT7, CS, and ICDH). The expression profiles of these 7 genes in diverse watermelon genotypes revealed consistent patterns of expression variation in various types of watermelon. These findings add significantly to our existing knowledge of sugar and organic acid metabolism in watermelon.