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Characterization of the horse chestnut genome reveals the evolution of aescin and aesculin biosynthesis

Wei Sun, Qinggang Yin, Huihua Wan, Ranran Gao, Chao Xiong, Chong Xie, Xiangxiao Meng, Yaolei Mi, Xiaotong Wang, Caixia Wang, Weiqiang Chen, Ziyan Xie, Zheyong Xue, Hui Yao, Peng Sun, Xuehua Xie, Zhigang Hu, David R. Nelson, Zhichao Xu (), Xinxiao Sun () and Shilin Chen ()
Additional contact information
Wei Sun: China Academy of Chinese Medical Sciences
Qinggang Yin: China Academy of Chinese Medical Sciences
Huihua Wan: China Academy of Chinese Medical Sciences
Ranran Gao: China Academy of Chinese Medical Sciences
Chao Xiong: China Academy of Chinese Medical Sciences
Chong Xie: Beijing University of Chemical Technology
Xiangxiao Meng: China Academy of Chinese Medical Sciences
Yaolei Mi: China Academy of Chinese Medical Sciences
Xiaotong Wang: Northeast Forestry University
Caixia Wang: China Academy of Chinese Medical Sciences
Weiqiang Chen: China Academy of Chinese Medical Sciences
Ziyan Xie: Northeast Forestry University
Zheyong Xue: Northeast Forestry University
Hui Yao: Chinese Academy of Medical Sciences and Peking Union Medical College
Peng Sun: China Academy of Chinese Medical Sciences
Xuehua Xie: China Academy of Chinese Medical Sciences
Zhigang Hu: Hubei University of Chinese Medicine
David R. Nelson: University of Tennessee Health Science Center
Zhichao Xu: Northeast Forestry University
Xinxiao Sun: Beijing University of Chemical Technology
Shilin Chen: China Academy of Chinese Medical Sciences

Nature Communications, 2023, vol. 14, issue 1, 1-15

Abstract: Abstract Horse chestnut (Aesculus chinensis) is an important medicinal tree that contains various bioactive compounds, such as aescin, barrigenol-type triterpenoid saponins (BAT), and aesculin, a glycosylated coumarin. Herein, we report a 470.02 Mb genome assembly and characterize an Aesculus-specific whole-genome duplication event, which leads to the formation and duplication of two triterpenoid biosynthesis-related gene clusters (BGCs). We also show that AcOCS6, AcCYP716A278, AcCYP716A275, and AcCSL1 genes within these two BGCs along with a seed-specific expressed AcBAHD6 are responsible for the formation of aescin. Furthermore, we identify seven Aesculus-originated coumarin glycoside biosynthetic genes and achieve the de novo synthesis of aesculin in E. coli. Collinearity analysis shows that the collinear BGC segments can be traced back to early-diverging angiosperms, and the essential gene-encoding enzymes necessary for BAT biosynthesis are recruited before the splitting of Aesculus, Acer, and Xanthoceras. These findings provide insight on the evolution of gene clusters associated with medicinal tree metabolites.

Date: 2023
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DOI: 10.1038/s41467-023-42253-y

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