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Integrative omic and transgenic analyses reveal the positive effect of ultraviolet‐B irradiation on salvianolic acid biosynthesis through upregulation of SmNAC1
Ist Teil von
The Plant journal : for cell and molecular biology, 2020-11, Vol.104 (3), p.781-799
Ort / Verlag
England: Blackwell Publishing Ltd
Erscheinungsjahr
2020
Quelle
Wiley Online Library - AutoHoldings Journals
Beschreibungen/Notizen
Significance Statement
Omic approaches combined with transgenic study provide mechanistic insights into UV‐B‐induced salvianolic acid accumulation, and demonstrate that the UV‐B‐responsive SmNAC1 positively modulates salvianolic acid biosynthesis in Salvia miltiorrhiza. Our findings ultimately provide new mechanistic insights into the UV‐B‐induced SalA biosynthesis in S. miltiorrhiza and shed light on a great potential for the development of SalAs‐abundant varieties through genetic engineering.
SUMMARY
Salvianolic acids (SalAs), a group of secondary metabolites in Salvia miltiorrhiza, are widely used for treating cerebrovascular diseases. Their biosynthesis is modulated by a variety of abiotic factors, including ultraviolet‐B (UV‐B) irradiation; however, the underlying mechanisms remain largely unknown. Here, an integrated metabolomic, proteomic, and transcriptomic approach coupled with transgenic analyses was employed to dissect the mechanisms underlying UV‐B irradiation‐induced SalA biosynthesis. Results of metabolomics showed that 28 metabolites, including 12 SalAs, were elevated in leaves of UV‐B‐treated S. miltiorrhiza. Meanwhile, the contents of several phytohormones, including jasmonic acid and salicylic acid, which positively modulate the biosynthesis of SalAs, also increased in UV‐B‐treated S. miltiorrhiza. Consistently, 20 core biosynthetic enzymes and numerous transcription factors that are involved in SalA biosynthesis were elevated in treated samples as indicated by a comprehensive proteomic analysis. Correlation and gene expression analyses demonstrated that the NAC1 gene, encoding a NAC transcriptional factor, was positively involved in UV‐B‐induced SalA biosynthesis. Accordingly, overexpression and RNA interference of NAC1 increased and decreased SalA contents, respectively, through regulation of key biosynthetic enzymes. Furthermore, ChIP‐qPCR and Dual‐LUC assays showed that NAC1 could directly bind to the CATGTG and CATGTC motifs present in the promoters of the SalA biosynthesis‐related genes PAL3 and TAT3, respectively, and activate their expression. Our results collectively demonstrate that NAC1 plays a crucial role in UV‐B irradiation‐induced SalA biosynthesis. Taken together, our findings provide mechanistic insights into the UV‐B‐induced SalA biosynthesis in S. miltiorrhiza, and shed light on a great potential for the development of SalA‐abundant varieties through genetic engineering.