Citrus fruits are widely consumed worldwide in juices or as fresh and provide a broad range of phytonutrients that are important for human health. Here, a citrus multi-omics resource is presented: comprehensive metabolic profiling of various citrus species was performed and metabolic profiles were compared among species, with a focus on the phenylpropanoid metabolic pathway. A metabolite-based genome-wide association analysis (mGWAS) of 154 pummelo accessions was performed using factored spectrally transformed linear mixed models (FaST-LMM) and efficient mixed-model association eXpedited (EMMAX), and the genetic and biochemical basis of metabolomic variation was comprehensively analysed. A metabolite-single nucleotide polymorphism-gene (metabolite-SNP-gene) interaction network was constructed for pummelo, and many candidate loci controlling the synthesis and regulation of bioactive compounds were identified; among these loci, three BAHD malonyltransferases were involved in the malonylation of flavonoid glycosides. Further investigation revealed that an R2R3-MYB transcription factor CgMYB1 positively controls the metabolism of phenylpropanoid molecules, particularly the flavonoid derivatives. This study provides valuable data resources on the metabolic regulatory networks of bioactive components in citrus, in addition to demonstrating an efficient method for metabolic pathway dissection and providing targets for future breeding work with the aim of improving nutritional value.

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