SmEIL1 transcription factor inhibits tanshinone accumulation in response to ethylene signaling in Salvia miltiorrhiza

Xiujuan Li; Man Xu; Ke Zhou; Siyu Hao; Liqin Li; Leran Wang; Wei Zhou; Guoyin Kai

doi:10.3389/fpls.2024.1356922

SmEIL1 transcription factor inhibits tanshinone accumulation in response to ethylene signaling in Salvia miltiorrhiza

Front Plant Sci. 2024 Apr 2:15:1356922. doi: 10.3389/fpls.2024.1356922. eCollection 2024.

Authors

Xiujuan Li^#¹, Man Xu^#¹, Ke Zhou^#², Siyu Hao¹, Liqin Li³, Leran Wang⁴, Wei Zhou¹, Guoyin Kai¹

Affiliations

¹ Zhejiang Provincial Traditional Chinese Medicine Key Laboratory of Chinese Medicine Resource Innovation and Transformation, Zhejiang Provincial International Science and Technology Cooperation Base for Active Ingredients of Medicinal and Edible Plants and Health, School of Pharmaceutical Sciences, Zhejiang Chinese Medical University, Hangzhou, China.
² Dermatology department, Tianjin Academy of Traditional Chinese Medicine Affiliated Hospital, Tianjin, China.
³ Key Laboratory of Traditional Chinese Medicine for the Development and Clinical Transformation of Immunomodulatory Traditional Chinese Medicine in Zhejiang Province, Huzhou Central Hospital, The Fifth School of Clinical Medicine of Zhejiang Chinese Medical University, Hangzhou, China.
⁴ School of Life Sciences, Zhejiang Chinese Medical University, Hangzhou, China.

^# Contributed equally.

Abstract

Among the bioactive compounds, lipid-soluble tanshinone is present in Salvia miltiorrhiza, a medicinal plant species. While it is known that ethephon has the ability to inhibit the tanshinones biosynthesis in the S. miltiorrhiza hairy root, however the underlying regulatory mechanism remains obscure. In this study, using the transcriptome dataset of the S. miltiorrhiza hairy root induced by ethephon, an ethylene-responsive transcriptional factor EIN3-like 1 (SmEIL1) was identified. The SmEIL1 protein was found to be localized in the nuclei, and confirmed by the transient transformation observed in tobacco leaves. The overexpression of SmEIL1 was able to inhibit the tanshinones accumulation to a large degree, as well as down-regulate tanshinones biosynthetic genes including SmGGPPS1, SmHMGR1, SmHMGS1, SmCPS1, SmKSL1 and SmCYP76AH1. These are well recognized participants in the tanshinones biosynthesis pathway. Further investigation on the SmEIL1 was observed to inhibit the transcription of the CPS1 gene by the Dual-Luciferase (Dual-LUC) and yeast one-hybrid (Y1H) assays. The data in this work will be of value regarding the involvement of EILs in regulating the biosynthesis of tanshinones and lay the foundation for the metabolic engineering of bioactive ingredients in S. miltiorrhiza.

Keywords: Salvia miltiorrhiza; SmEIL1 transcription factor; ethylene; regulatory mechanism; tanshinone.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This work was supported by ‘Sannongjiufang’ Research Joint Project of Zhejiang Province (2023SNJF029), National Natural Science Foundation of China (82373979, 82204553), the Key Scientific and Technological Grant of Zhejiang for Breeding New Agricultural Varieties (2021C02074-3), National ‘Ten-thousand Talents Program’ for Leading Talents of Science and Technology Innovation in China, National Young Qihuang Scholars Training Program, Zhejiang Provincial Natural Science Foundation of China (LZ24H280002), and Research Projects of Zhejiang Chinese Medical University (2021JKZKTS011A, 2021JKZDZC06, 2020010 and YB20023).