Multi-omics analysis reveals the evolutionary origin of diterpenoid alkaloid biosynthesis pathways in Aconitum

doi:10.1111/jipb.13565

J Integr Plant Biol. ›› 2023, Vol. 65 ›› Issue (10): 2320-2335.DOI: 10.1111/jipb.13565

• Molecular Ecology and Evolution • Previous Articles Next Articles

Multi-omics analysis reveals the evolutionary origin of diterpenoid alkaloid biosynthesis pathways in Aconitum

Dake Zhao^1†, Ya Zhang^2†, Huanxing Ren^3,4, Yana Shi⁵, Ding Dong¹, Zonghang Li¹, Guanghong Cui⁶, Yong Shen⁷, Zongmin Mou¹, Edward J. Kennelly^8,9, Luqi Huang^5,6, Jue Ruan², Suiyun Chen^1*, Diqiu Yu^10* and Yupeng Cun^3,4*

1. School of Ecology and Environmental Science, Yunnan University, Kunming 650500, China;
2. Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen 518000, China;
3. Chongqing Key Laboratory of Translational Medical Research in Cognitive Development and Learning and Memory Disorders, Pediatric Research Institute, Ministry of Education Key Laboratory of Child Development and Disorders, National Clinical Research Center for Child Health and Disorders, China International Science and Technology Cooperation Base of Child Development and Critical Disorders, Children's Hospital of Chongqing Medical University, Chongqing 400014, China;
4. Germplasm Bank of Wild Species, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, China;
5. Faculty of Life Science and Technology, Kunming University of Science and Technology, Kunming 650500, China;
6. National Resource Center for Chinese Materia Medica, Chinese Academy of Chinese Medical Sciences, Beijing 100700, China;
7. College of Agriculture and Biotechnology, Yunnan Agricultural University, Kunming 650201, China;
8. Department of Biological Sciences, Lehman College, City University of New York, Bronx 10468, New York, USA;
9. Graduate Center, City University of New York, Bronx 10468, New York, USA;
10. State Key Laboratory for Conservation and Utilization of Bio‐resources in Yunnan, Yunnan University, Kunming 650500, China
^†These authors contributed equally to this work.
^*Correspondences: Diqiu Yu (ydq@xtbg.ac.cn); Suiyun Chen (chensuiyun@ynu.edu.cn); Yupeng Cun (cunyp@cqmu.edu.cn, Dr. Cun is fully responsible for the distributions of all materials associated with this article)

Received:2023-05-29 Accepted:2023-09-07 Online:2023-09-09 Published:2023-10-01

Abstract

Abstract: Diterpenoid alkaloids (DAs) have been often utilized in clinical practice due to their analgesic and anti-inflammatory properties. Natural DAs are prevalent in the family Ranunculaceae, notably in the Aconitum genus. Nevertheless, the evolutionary origin of the biosynthesis pathway responsible for DA production remains unknown. In this study, we successfully assembled a high-quality, pseudochromosome-level genome of the DA-rich species Aconitum vilmorinianum (A. vilmorinianum) (5.76 Gb). An A. vilmorinianum-specific whole-genome duplication event was discovered using comparative genomic analysis, which may aid in the evolution of the DA biosynthesis pathway. We identified several genes involved in DA biosynthesis via integrated genomic, transcriptomic, and metabolomic analyses. These genes included enzymes encoding target ent-kaurene oxidases and aminotransferases, which facilitated the activation of diterpenes and insertion of nitrogen atoms into diterpene skeletons, thereby mediating the transformation of diterpenes into DAs. The divergence periods of these genes in A. vilmorinianum were further assessed, and it was shown that two major types of genes were involved in the establishment of the DA biosynthesis pathway. Our integrated analysis offers fresh insights into the evolutionary origin of DAs in A. vilmorinianum as well as suggestions for engineering the biosynthetic pathways to obtain desired DAs.

Key words: Aconitum vilmorinianum, acute toxicity, biosynthetic pathway, diterpenoid alkaloid, evolutionary origin, genome assembly

Dake Zhao, Ya Zhang, Huanxing Ren, Yana Shi, Ding Dong, Zonghang Li, Guanghong Cui, Yong Shen, Zongmin Mou, Edward J. Kennelly, Luqi Huang, Jue Ruan, Suiyun Chen, Diqiu Yu and Yupeng Cun. Multi-omics analysis reveals the evolutionary origin of diterpenoid alkaloid biosynthesis pathways in Aconitum[J]. J Integr Plant Biol., 2023, 65(10): 2320-2335.

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Multi-omics analysis reveals the evolutionary origin of diterpenoid alkaloid biosynthesis pathways in Aconitum

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