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Article|25 Jul 2022|OPEN
The genome of Dioscorea zingiberensis sheds light on the biosynthesis, origin and evolution of the medicinally important diosgenin saponins
Yi Li1 , Chao Tan1 , Zihao Li1 , Jingzhe Guo1 , Song Li1 , Xin Chen1 , Chen Wang1 , Xiaokang Dai1 , Huan Yang1 , Wei Song1 , Lixiu Hou1 , Jiali Xu1 , Ziyu Tong1 , Anran Xu1 , Xincheng Yuan1 , Weipeng Wang1 , Qingyong Yang2 , Lingling Chen3 , Zongyi Sun4 , Kai Wang4 , Bo Pan5 , Jianghua Chen6 , Yinghua Bao7 , Faguang Liu7 , Xiaoquan Qi8 , David R. Gang9 , Jun Wen10 and Jiaru Li,1 ,
1State Key Laboratory of Hybrid Rice, College of Life Sciences, Wuhan University, Wuhan, 430072, China
2Hubei Key Laboratory of Agricultural Bioinformatics, College of Informatics, Huazhong Agricultural University, Wuhan, 430070, China
3College of Life Science and Technology, Guangxi University, Nanning, 530004, China
4Grandomics Biosciences, Beijing 102200, China
5Center for Integrative Conservation, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Menglun, 666303, China
6CAS Key Laboratory of Tropical Plant Resources and Sustainable Use, CAS Center for Excellence in Molecular Plant Sciences, Xishuangbanna Tropical Botanical Garden, Kunming, 650223, China
7Henry Fok College of Biology and Agriculture, Shaoguan University, Shaoguan, 512005, China
8Key Laboratory of Plant Molecular Physiology, Institute of Botany, Chinese Academy of Sciences, Beijing, 100093, China
9Institute of Biological Chemistry, Washington State University, Pullman, WA, 99164, USA
10Department of Botany, National Museum of Natural History, Smithsonian Institution, Washington, DC, 20013-7012, USA
*Corresponding author. E-mail: jrli@whu.edu.cn

Horticulture Research 9,
Article number: uhac165 (2022)
doi: https://doi.org/10.1093/hr/uhac165
Views: 76

Received: 11 Mar 2022
Accepted: 18 Jul 2022
Published online: 25 Jul 2022

Abstract

Diosgenin saponins isolated from Dioscorea species such as D. zingiberensis exhibit a broad spectrum of pharmacological activities. Diosgenin, the aglycone of diosgenin saponins, is an important starting material for the production of steroidal drugs. However, how plants produce diosgenin saponins and the origin and evolution of the diosgenin saponin biosynthetic pathway remain a mystery. Here we report a high-quality, 629-Mb genome of Dzingiberensis anchored on 10 chromosomes with 30 322 protein-coding genes. We reveal that diosgenin is synthesized in leaves (‘source’), then converted into diosgenin saponins, and finally transported to rhizomes (‘sink’) for storage in plants. By evaluating the distribution and evolutionary patterns of diosgenin saponins in Dioscorea species, we find that diosgenin saponin-containing may be an ancestral trait in Dioscorea and is selectively retained. The results of comparative genomic analysis indicate that tandem duplication coupled with a whole-genome duplication event provided key evolutionary resources for the diosgenin saponin biosynthetic pathway in the Dzingiberensis genome. Furthermore, comparative transcriptome and metabolite analysis among 13 Dioscorea species suggests that specific gene expression patterns of pathway genes promote the differential evolution of the diosgenin saponin biosynthetic pathway in Dioscorea species. Our study provides important insights and valuable resources for further understanding the biosynthesis, evolution, and utilization of plant specialized metabolites such as diosgenin saponins.