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

• Published in: Nature communications Vol. 14; no. 1; p. 6470
• Main Authors: Sun, Wei, Yin, Qinggang, Wan, Huihua, Gao, Ranran, Xiong, Chao, Xie, Chong, Meng, Xiangxiao, Mi, Yaolei, Wang, Xiaotong, Wang, Caixia, Chen, Weiqiang, Xie, Ziyan, Xue, Zheyong, Yao, Hui, Sun, Peng, Xie, Xuehua, Hu, Zhigang, Nelson, David R., Xu, Zhichao, Sun, Xinxiao, Chen, Shilin
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 13.10.2023; Nature Publishing Group; Nature Portfolio
• Subjects: 45/23; 45/91; 631/181/735; 631/208/726; 631/449/2667; 631/61/318; 82/80; 82/83; Aesculus; Angiosperms; Bioactive compounds; Biosynthesis; Chestnut; Collinearity; Coumarin; E coli; Esculin; Evolution; Gene clusters; Genes; Genomes; Humanities and Social Sciences; Metabolites; multidisciplinary; Plant species; Saponins; Science; Science (multidisciplinary)
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-023-42253-y

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. Horse chestnut ( Aesculus chinensis ) is a tree species that can produce medicinal compounds such as aescin and aesculin. Here, the authors assemble its genome, identify key genes involved in the biosynthesis of these two group of compounds, and achieve the de novo synthesis of aesculin in E. coli .