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Background  Fruit flesh color in watermelon ( Citrullus lanatus ) is a great index for evaluating the appearance quality and a key contributor influencing consumers’ preferences. But the molecular mechanism of this intricate trait remains largely unknown. Here, the carotenoids and transcriptome dynamics during the fruit development of cultivated watermelon with five different flesh colors were analyzed.    Results  A total of 13 carotenoids and 16,781 differentially expressed genes (DEGs), including 1295 transcription factors (TFs), were detected in five watermelon genotypes during the fruit development. The comprehensive accumulation patterns of carotenoids were closely related to flesh color. A number of potential structural genes and transcription factors were found to be associated with the carotenoid biosynthesis pathway using comparative transcriptome analysis. The differentially expressed genes were divided into six subclusters and distributed in different GO terms and metabolic pathways. Furthermore, we performed weighted gene co-expression network analysis and predicted the hub genes in six main modules determining carotenoid contents.  Cla018406  (a chaperone protein dnaJ-like protein) may be a candidate gene for β-carotene accumulation and highly expressed in orange flesh-colored fruit.  Cla007686  (a zinc finger CCCH domain-containing protein) was highly expressed in the red flesh-colored watermelon, maybe a key regulator of lycopene accumulation.  Cla003760  (membrane protein) and  Cla021635  (photosystem I reaction center subunit II) were predicted to be the hub genes and may play an essential role in yellow flesh formation.    Conclusions  The composition and contents of carotenoids in five watermelon genotypes vary greatly. A series of candidate genes were revealed through combined analysis of metabolites and transcriptome. These results provide an important data resource for dissecting candidate genes and molecular basis governing flesh color formation in watermelon fruit.    Supplementary Information  The online version contains supplementary material available at 10.1186/s12870-021-02965-z.

Transcriptome regulation of carotenoids in five flesh-colored watermelons (Citrullus lanatus)