Regulatory network characterization of anthocyanin metabolites in purple sweetpotato via joint transcriptomics and metabolomics

INTRODUCTION: Sweet potato is an important staple food crop in the world and contains abundant secondary metabolites in its underground tuberous roots. The large accumulation of several categories of secondary metabolites result in colorful pigmentation of the roots. Anthocyanin, is a typical flavonoid compound present in purple sweet potatoes and it contributes to the antioxidant activity. METHODS: In this study, we developed joint omics research via by combing the transcriptomic and metabolomic analysis to explore the molecular mechanisms underlying the anthocyanin biosynthesis in purple sweet potato. Four experimental materials with different pigmentation phenotypes, 1143-1 (white root flesh), HS (orange root flesh), Dianziganshu No.88 (DZ88, purple root flesh), and Dianziganshu No.54 (DZ54, dark purple root flesh) were comparably studied. RESULTS AND DISCUSSION: We identified 38 differentially accumulated pigment metabolites and 1214 differentially expressed genes from a total of 418 metabolites and 50893 genes detected. There were 14 kinds of anthocyanin detected in DZ88 and DZ54, with glycosylated cyanidin and peonidin as the major components. The significantly enhanced expression levels of multiple structural genes involved in the central anthocyanin metabolic network, such as chalcone isomerase (CHI), flavanone 3-hydroxylase (F3H), dihydroflavonol 4-reductase (DFR), anthocyanidin synthase/leucocyanidin oxygenase (ANS), and glutathione S-transferase (GST) were manifested to be the primary reason why the purple sweet potatoes had a much higher accumulation of anthocyanin. Moreover, the competition or redistribution of the intermediate substrates (i.e. dihydrokaempferol and dihydroquercetin) between the downstream production of anthocyanin products and the flavonoid derivatization (i.e. quercetin and kaempferol) under the regulation of the flavonol synthesis (FLS) gene, might play a crucial role in the metabolite flux repartitioning, which further led to the discrepant pigmentary performances in the purple and non-purple materials. Furthermore, the substantial production of chlorogenic acid, another prominent high-value antioxidant, in DZ88 and DZ54 seemed to be an interrelated but independent pathway differentiated from the anthocyanin biosynthesis. Collectively, these data from the transcriptomic and metabolomic analysis of four kinds of sweet potatoes provide insight to understand the molecular mechanisms of the coloring mechanism in purple sweet potatoes.