Unveiling the spatial distribution and molecular mechanisms of terpenoid biosynthesis in Salvia miltiorrhiza and S. grandifolia using multi-omics and DESI–MSI

Abstract

Salvia miltiorrhiza and S. grandifolia are rich in diterpenoids and have therapeutic effects on cardiovascular diseases. In this study, the spatial distribution of diterpenoids in both species was analyzed by a combination of metabolomics and mass spectrometry imaging techniques. The results indicated that diterpenoids in S. miltiorrhiza were mainly abietane-type norditerpenoid quinones with a furan or dihydrofuran D-ring and were mainly distributed in the periderm of the roots, e.g. cryptotanshinone and tanshinone IIA. The compounds in S. grandifolia were mainly phenolic abietane-type tricyclic diterpenoids with six- or seven-membered C-rings, and were widely distributed in the periderm, phloem, and xylem of the roots, e.g. 11-hydroxy-sugiol, 11,20-dihydroxy-sugiol, and 11,20-dihydroxy-ferruginol. In addition, the leaves of S. grandifolia were rich in tanshinone biosynthesis precursors, such as 11-hydroxy-sugiol, while those of S. miltiorrhiza were rich in phenolic acids. Genes in the upstream pathway of tanshinone biosynthesis were highly expressed in the root of S. grandifolia, and genes in the downstream pathway were highly expressed in the root of S. miltiorrhiza. Here, we describe the specific tissue distributions and mechanisms of diterpenoids in two Salvia species, which will facilitate further investigations of the biosynthesis of diterpenoids in plant synthetic biology.

Acknowledgements

This work was financially supported by Zhejiang Provincial Natural Science Foundation of China (No. LR21H280002), a Key Scientific and Technological Grant of Zhejiang for Breeding New Agricultural Varieties (No. 2021C02074), the Key project of the Central Government: Capacity Building of Sustainable Utilization of Traditional Chinese Medicine Resources (No. 2060302), and the National Natural Science Foundation of China for State Key Laboratory (No. 81973415).

Author contributions

J.X. and G.G.L. were tasked with the experimental study, data analysis, and manuscript composition; L.Z. was responsible for qRT–PCR; Y.B.H., J.Y., and J.G. for sample collection; and Z.C.Q., Z.H.L., G.L.Z., S.C.X., and X.J.S. for composition testing. Authors X.D.Z., Y.K.W., Z.S.L., and D.F.Y. were tasked with the design, preparation, and revision of the manuscript in its entirety.

Data availability

All relevant data are available within the article and its supplementary materials.

Conflict of interest

The authors declare that they have no conflicts of interest.

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