Integrated transcriptome and metabolome analysis provide insights into the mechanism of saponin biosynthesis and its role in alleviating cadmium-induced oxidative damage in Ophiopogon japonicum

Qian Zhao; Jie Wang; Qing Li; Jiarong Zhang; Ruijun Hou; Zhihui Wang; Qian Zhu; Yifeng Zhou; Yue Chen; Jun Huang

doi:10.1016/j.plaphy.2024.108634

Integrated transcriptome and metabolome analysis provide insights into the mechanism of saponin biosynthesis and its role in alleviating cadmium-induced oxidative damage in Ophiopogon japonicum

Plant Physiol Biochem. 2024 Apr 17:210:108634. doi: 10.1016/j.plaphy.2024.108634. Online ahead of print.

Authors

Qian Zhao¹, Jie Wang¹, Qing Li¹, Jiarong Zhang¹, Ruijun Hou¹, Zhihui Wang¹, Qian Zhu¹, Yifeng Zhou¹, Yue Chen², Jun Huang³

Affiliations

¹ Zhejiang University of Science and Technology, Hangzhou, China.
² Horticulture Research Institute, Zhejiang Academy of Agricultural Sciences, Hangzhou, China.
³ Zhejiang University of Science and Technology, Hangzhou, China. Electronic address: hjunlzr@163.com.

PMID: 38642440
DOI: 10.1016/j.plaphy.2024.108634

Abstract

Zhe-Maidong, a cultivar of Ophiopogon japonicus is a prominent traditional herbal medicine rich in saponins. This study explored the mechanism of saponin biosynthesis and its role in alleviating Cd-induced oxidative damage in the Zhe-Maidong cultivar using three experimental groups undergoing Cd stress. In the Cd-contaminated soil treatment, total saponins were 1.68 times higher than those in the control. The saponin content in the Cd-2 and Cd-3 treatments was approximately twice as high as that in the Cd-CK treatment. These findings revealed that Cd stress leads to total saponin accumulation. Metabolomic analysis identified the accumulated saponins, primarily several monoterpenoids, diterpenoids, and triterpenoids. The increased saponins exhibited an antioxidant ability to prevent the accumulation of Cd-induced reactive oxygen species (ROS). Subsequent saponin application experiments provided strong evidence that saponin played a crucial role in promoting superoxide dismutase (SOD) activity and reducing ROS accumulation. Transcriptome analysis revealed vital genes for saponin synthesis under Cd stress, including SE, two SSs, and six CYP450s, positively correlated with differentially expressed metabolite (DEM) levels in the saponin metabolic pathway. Additionally, the TF-gene regulatory network demonstrated that bHLH1, bHLH3, mTERF, and AUX/IAA transcript factors are crucial regulators of hub genes involved in saponin synthesis. These findings significantly contribute to our understanding of the regulatory network of saponin synthesis and its role in reducing oxidative damage in O. japonicum when exposed to Cd stress.

Keywords: Antioxidant; Cadmium stress; Ophiopogon japonicus; Saponin; Superoxide dismutase.