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.

Flesh firmness of watermelon is an important quality trait for commercial fruit values, including fruit storability, transportability, and shelf life. To date, knowledge of the gene networks underlying this trait is still limited. Herein, we used weighted genes co-expression network analysis (WGCNA) based on correlation and the association of phenotypic data (cell wall contents) with significantly differentially expressed genes between two materials, a near isogeneic line “HWF” (with high average flesh firmness) and inbred line “203Z” (with low average flesh firmness), to identify the gene networks responsible for changes in fruit flesh firmness. We identified three gene modules harboring 354 genes; these gene modules demonstrated significant correlation with water-soluble pectin, cellulose, hemicellulose, and protopectin. Based on intramodular significance, eight genes involved in cell wall biosynthesis and ethylene pathway are identified as hub genes within these modules. Among these genes, two genes, Cla012351 (Cellulose synthase) and Cla004251 (Pectinesterase), were significantly correlated with cellulose (r2 = 0.83) and protopectin (r2 = 0.81); three genes, Cla004120 (ERF1), Cla009966 (Cellulose synthase), and Cla006648 (Galactosyltransferase), had a significant correlation with water-soluble pectin (r2 = 0.91), cellulose (r2 = 0.9), and protopectin (r2 = 0.92); and three genes, Cla007092 (ERF2a), Cla004119 (probable glycosyltransferase), and Cla018816 (Xyloglucan endotransglucosylase/hydrolase), were correlated with hemicellulose (r2 = 0.85), cellulose (r2 = 0.8), and protopectin (r2 = 0.8). This study generated important insights of biosynthesis of a cell wall structure and ethylene signaling transduction pathway, the mechanism controlling the flesh firmness changes in watermelon, which provide a significant source to accelerate future functional analysis in watermelon to facilitate crop improvement.

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.