Integrative analysis of transcriptomic and metabolomic profiles reveals new insights into the molecular foundation of fruit quality formation in Citrullus lanatus (Thunb.) Matsum. & Nakai

Abstract In this study, an integrated transcriptome and metabolome analysis was used to explore the molecular foundation of fruit quality in two parent lines of Citrullus lanatus with distinct flesh characteristics, including ‘14-1’ (sweet, red, and soft) and ‘W600’ (bitter, light yellow, and firm), as well as the corresponding F1 population (bitter, light yellow, and firm). Numerous differentially expressed genes (DEGs) were identified in the fruit samples: 3766 DEGs for ‘14-1’ vs. ‘W600’, 2767 for ‘14-1’ vs. F1, and 1178 for F1 vs. ‘W600’ at the transition stage; and 4221 for ‘14-1’ vs. ‘W600’, 2447 for ‘14-1’ vs. F1, and 446 for F1 vs. ‘W600’ at the maturity stage. Weighted gene co-expression network analysis (WGCNA) revealed that a gene module including 1111 DEGs was closely associated with flesh taste and color, and another gene module including 1575 DEGs contributed significantly to flesh texture. The metabolomic results showed that there were 447 differential metabolites (DMs) for ‘14-1’ vs. ‘W600’ fruits, 394 for ‘14-1’ vs. F1, and 298 for F1 vs. ‘W600’ at the maturity stage. Combining WGNCA and metabolomic results, several DEGs and DMs were further identified as hub players in fruit quality formation: 6 DEGs with 4 DMs for flesh sweetness; 6 DEGs with 13 DMs for bitterness; 9 DEGs with 10 DMs for flesh color; and 9 DEGs with 4 DMs for flesh texture. Altogether, these observations not only expand our knowledge of the molecular basis of fruit quality in watermelon, but also provide potential targets for future watermelon improvement.