Integrative omic and transgenic analyses reveal the positive effect of ultraviolet-B irradiation on salvianolic acid biosynthesis through upregulation of SmNAC1.

Abstract

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.

• Authors: Xiaojian Yin, Hui Fan, Yan Chen, Lan-Zhu Li, Wei Song, Yuanming Fan, Wei Zhou, Gaoxiang Ma, Raphael N Alolga, Weiqiang Li, Baolong Zhang, Ping Li, Lam-Son P Tran, Xu Lu, Lian-Wen Qi
• Journal: The Plant journal : for cell and molecular biology (Plant J) Vol. 104 Issue 3 Pg. 781-799 (11 2020) ISSN: 1365-313X [Electronic] England
• PMID: 32772407 (Publication Type: Journal Article, Research Support, Non-U.S. Gov't)
• Copyright: © 2020 Society for Experimental Biology and John Wiley & Sons Ltd.

Chemical References

• Alkenes
• Enzymes
• Plant Proteins
• Polyphenols
• Transcription Factors
• salvianolic acid

Topics

• Alkenes
• Enzymes (metabolism)
• Gene Expression Regulation, Plant (radiation effects)
• Metabolomics (methods)
• Plant Leaves (metabolism, radiation effects)
• Plant Proteins (genetics, metabolism)
• Plants, Genetically Modified
• Polyphenols (biosynthesis, genetics)
• Proteomics (methods)
• RNA Interference
• Salvia miltiorrhiza (genetics, metabolism, radiation effects)
• Transcription Factors (genetics, metabolism)
• Ultraviolet Rays
• Up-Regulation