Integrative analysis of multiple metabolomes and transcriptome revealed color expression mechanism in red skin root syndrome of Panax ginseng

Abstract

Red skin root syndrome causes reduction of both production and quality of Panax ginseng (ginseng). However, its development process and key metabolites are still unknown. Multiple metabolomes including non-targeted metabolome, and anthocyanins-targeted and carotenoids-targeted metabolomes were performed on field grown red skin and healthy ginseng. The detected metabolites were analyzed in combination with previous transcriptome results. The total metabolite profiles revealed that primary metabolites especially citrate was decreased, but secondary metabolites mainly involved in phenylpropanoid pathway were increased in red skin ginseng compared to those in healthy ginseng. Targeted metabolome found that each gram of fresh red skin ginseng sample contained 8 μg β-carotene, 0.56 μg α-carotene, 0.017 μg rutin, 0.248 μg chalcone, and some anthocyanins including 0.023 μg cyanidin and 0.037 μg quercetin 3-O-glucoside, albeit in low concentrations but higher than those in healthy ginseng. Furthermore, integrative metabolome and transcriptome analysis revealed that changes of metabolites related to anthocyanins synthesis were correlated with the related gene expression patterns. Additionally, jasmonate (JA) and its precursor 12-oxophytodienoic acid increased their concentrations dramatically in red skin ginseng, suggesting the possible role of JA or JA signaling pathway in regulating red skin syndrome. Consistently, the expressions of 17 MYB transcription factors were differentially regulated in red skin ginseng. JA related cis-elements are widely distributed at their promoters. Taken together, our study revealed reduction of primary metabolism but increase of secondary metabolism in red skin ginseng. MYB transcription factors of JA signal pathway were supposed to mediate accumulation of anthocyanins and carotenoids that contributed to the development of red skin ginseng.