Multiomics analyses of two Leonurus species illuminate leonurine biosynthesis and its evolution

Peng Li; Meng-Xiao Yan; Pan Liu; Dan-Jie Yang; Ze-Kun He; Yun Gao; Yan Jiang; Yu Kong; Xin Zhong; Sheng Wu; Jun Yang; Hong-Xia Wang; Yan-Bo Huang; Le Wang; Xiao-Ya Chen; Yong-Hong Hu; Qing Zhao; Ping Xu

doi:10.1016/j.molp.2023.11.003

Multiomics analyses of two Leonurus species illuminate leonurine biosynthesis and its evolution

Mol Plant. 2024 Jan 1;17(1):158-177. doi: 10.1016/j.molp.2023.11.003. Epub 2023 Nov 10.

Authors

Peng Li¹, Meng-Xiao Yan¹, Pan Liu¹, Dan-Jie Yang², Ze-Kun He³, Yun Gao¹, Yan Jiang¹, Yu Kong¹, Xin Zhong¹, Sheng Wu⁴, Jun Yang⁵, Hong-Xia Wang⁵, Yan-Bo Huang¹, Le Wang⁶, Xiao-Ya Chen⁵, Yong-Hong Hu¹, Qing Zhao⁵, Ping Xu⁷

Affiliations

¹ Shanghai Key Laboratory of Plant Functional Genomics and Resources, Shanghai Chenshan Botanical Garden, Shanghai Chenshan Plant Science Research Center, Chinese Academy of Sciences, Shanghai, China.
² Shanghai Key Laboratory of Plant Functional Genomics and Resources, Shanghai Chenshan Botanical Garden, Shanghai Chenshan Plant Science Research Center, Chinese Academy of Sciences, Shanghai, China; College of Life Sciences, Shanghai Normal University, Shanghai 200234, China.
³ Shanghai Key Laboratory of Plant Functional Genomics and Resources, Shanghai Chenshan Botanical Garden, Shanghai Chenshan Plant Science Research Center, Chinese Academy of Sciences, Shanghai, China; State Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences, Shanghai, China; University of the Chinese Academy of Sciences, Beijing 100049, China.
⁴ The Research Center of Chiral Drugs, Innovation Research Institute of Traditional Chinese Medicine, Shanghai University of Traditional Chinese Medicine, 1200 Cailun Road, Shanghai 201203, China.
⁵ Shanghai Key Laboratory of Plant Functional Genomics and Resources, Shanghai Chenshan Botanical Garden, Shanghai Chenshan Plant Science Research Center, Chinese Academy of Sciences, Shanghai, China; State Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences, Shanghai, China.
⁶ College of Chemistry and Chemical Engineering, Shanghai University of Engineering Science, Shanghai 201620, China.
⁷ Shanghai Key Laboratory of Plant Functional Genomics and Resources, Shanghai Chenshan Botanical Garden, Shanghai Chenshan Plant Science Research Center, Chinese Academy of Sciences, Shanghai, China; State Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences, Shanghai, China. Electronic address: xuping01@sibs.ac.cn.

PMID: 37950440
DOI: 10.1016/j.molp.2023.11.003

Abstract

The Lamiaceae family is renowned for its terpenoid-based medicinal components, but Leonurus, which has traditional medicinal uses, stands out for its alkaloid-rich composition. Leonurine, the principal active compound found in Leonurus, has demonstrated promising effects in reducing blood lipids and treating strokes. However, the biosynthetic pathway of leonurine remains largely unexplored. Here, we present the chromosome-level genome sequence assemblies of Leonurus japonicus, known for its high leonurine production, and Leonurus sibiricus, characterized by very limited leonurine production. By integrating genomics, RNA sequencing, metabolomics, and enzyme activity assay data, we constructed the leonurine biosynthesis pathway and identified the arginine decarboxylase (ADC), uridine diphosphate glucosyltransferase (UGT), and serine carboxypeptidase-like (SCPL) acyltransferase enzymes that catalyze key reactions in this pathway. Further analyses revealed that the UGT-SCPL gene cluster evolved by gene duplication in the ancestor of Leonurus and neofunctionalization of SCPL in L. japonicus, which contributed to the accumulation of leonurine specifically in L. japonicus. Collectively, our comprehensive study illuminates leonurine biosynthesis and its evolution in Leonurus.

Keywords: Lamiaceae; Leonurus japonicus; Leonurus sibiricus; alkaloids; biosynthetic pathway; evolution; gene cluster; genome sequence; leonurine.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Lamiaceae*
Leonurus* / genetics
Multiomics
Plant Extracts

Substances

leonurine
Plant Extracts