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Comparative metabolomics analysis of a unique yellow hawthorn (Crataegus pinnatifida) and red-skinned cultivars reveals a different polyphenol biosynthesis flux and antioxidative and antidiabetic potential

Liu Yilong,You Wenwen,Wang Ruoqi,Zeng Tao,Zhao Xiaoyong,Cao Yunlin,Zhang Wenna,Nie Zongxing,Yang Xiaochun,Li Xian

Hawthorn (Crataegus spp.) is a functional food with long medical usage and excellent health-promoting effects. In this study, comparative metabolomics analysis between the yellow hawthorn berry (Crataegus pinnatifida) and the red-skinned ones was first carried out with the peel and flesh separated to fully understand the polyphenol composition and metabolite variations. A total of 453 polyphenols was characterized, among which phenolic acids and flavonoids were abundant, and were closely relevant to the antioxidant capacity of hawthorn fruits. Polyphenol profile showed accession-specific accumulation in peel or flesh of different colored hawthorn. The unique yellow hawthorn was found to have few anthocyanins but show enhanced flux to synthesize flavones and flavonols, especially flavone C-glycosides and acylated flavonol glycosides. The specific acylation decoration includes acetylation, p-coumaroylation, and malonylation. In addition, the yellow hawthorn showed excellent α-glucosidase inhibitory effect, which might be associated with the high concentration of 8 polyphenols including 5 phenolic acids, 2 flavone C-glycosides, and an acylated flavonol glycoside, namely quercetin-7-O-(6''-malonyl)glucoside. Such acylated flavonol showed the highest correlation ship with the inhibition effect of hawthorn fruits on α-glucosidase, and was predicted to had the lowest binding energy with the enzyme by molecular docking analysis, indicating its great potential as a strong α-glucosidase inhibitors and an important antidiabetic ingredient in yellow hawthorn. Thus, acylated flavonol glycosides and C-glycosyl flavones might be chemotaxonomic markers differentiating varieties and bioactivities of yellow hawthorn from the traditional red-skinned ones. These findings complement the existing knowledge on the metabolite composition and nutritional properties of hawthorn fruits.