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Molecular Physiology

The ABC transporter SmABCG1 mediates tanshinones export from the peridermic cells of Salvia miltiorrhiza root

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  • 1. The SATCM Key Laboratory for New Resources & Quality Evaluation of Chinese Medicine, Institute of Chinese Materia Medica, Shanghai University of Traditional Chinese Medicine, Shanghai 201203, China
    2. Department of Pharmacy, Changzheng Hospital, Naval Medical University, Shanghai 200003, China
    3. Department of Plant Biology and Ecology, College of Life Sciences, Nankai University, Tianjin 300071, China
    4. School of Pharmacy, Naval Medical University, Shanghai 200433, China
    5. College of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou 310000, China
    6. Amway (Shanghai) Innovation & Science Co., Ltd, Shanghai 201203, China

    These authors contributed equally to this work.
    *Correspondence: Junfeng Chen (0000002928@shutcm.edu.cn); Tingzhao Li (teric.li@amway.com); Wansheng Chen (chenwansheng@shutcm.edu.cn); Ying Xiao (xiaoyingtcm@shutcm.edu.cn, Dr. Xiao is responsible for the distribution of materials integral to the findings presented in this article)

Received date: 2024-01-31

  Accepted date: 2024-10-26

  Online published: 2024-11-22

Supported by

This work was financially supported by the National Key Research and Development Program of China (2022YFC3501700), the National Natural Science Foundation of China (82304662, 82374159, 32070327, 32170402), the National Key Research and Development Program of China (2023YFC3504800), Chen-guang project of Shanghai (23CGA52), Science and Technology Development Program of Shanghai University of Traditional Chinese Medicine (23KFL051), and Shanghai Municipal Science and Technology Commission (23XD1423500).

Abstract

Plants have mechanisms to transport secondary metabolites from where they are biosynthesized to the sites where they function, or to sites such as the vacuole for detoxification. However, current research has mainly focused on metabolite biosynthesis and regulation, and little is known about their transport. Tanshinone, a class diterpenoid with medicinal properties, is biosynthesized in the periderm of Salvia miltiorrhiza roots. Here, we discovered that tanshinone can be transported out of peridermal cells and secreted into the soil environment and that the ABC transporter SmABCG1 is involved in the efflux of tanshinone ⅡA and tanshinone Ⅰ. The SmABCG1 gene is adjacent to the diterpene biosynthesis gene cluster in the S. miltiorrhiza genome. The temporal–spatial expression pattern of SmABCG1 is consistent with tanshinone accumulation profiles. SmABCG1 is located on the plasma membrane and preferentially accumulates in the peridermal cells of S. miltiorrhiza roots. Heterologous expression in Xenopus laevis oocytes demonstrated that SmABCG1 can export tanshinone ⅡA and tanshinone Ⅰ. CRISPR/Cas9-mediated mutagenesis of SmABCG1 in S. miltiorrhiza hairy roots resulted in a significant decrease in tanshinone contents in both hairy roots and the culture medium, whereas overexpression of this gene resulted in increased tanshinone contents. CYP76AH3 transcript levels increased in hairy roots overexpressing SmABCG1 and decreased in knockout lines, suggesting that SmABCG1 may affect the expression of CYP76AH3, indirectly regulating tanshinone biosynthesis. Finally, tanshinone ⅡA showed cytotoxicity to Arabidopsis roots. These findings offer new perspectives on plant diterpenoid transport and provide a new genetic tool for metabolic engineering and synthetic biology research.

Cite this article

Yajing Li, Junfeng Chen, Jingyu Zhi, Doudou Huang, Yuchen Zhang, Lei Zhang, Xinyi Duan, Pan Zhang, Shi Qiu, Jiaran Geng, Jingxian Feng, Ke Zhang, Xu Yang, Shouhong Gao, Wenwen Xia, Zheng Zhou, Yuqi Qiao, Bo Li, Qing Li, Tingzhao Li, Wansheng Chen, Ying Xiao . The ABC transporter SmABCG1 mediates tanshinones export from the peridermic cells of Salvia miltiorrhiza root[J]. Journal of Integrative Plant Biology, 2025 , 67(1) : 135 -149 . DOI: 10.1111/jipb.13806

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