Characterization of the horse chestnut genome reveals the evolution of aescin and aesculin biosynthesis
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-specif...
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| Format: | Article |
| Language: | English |
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Nature Portfolio
2023-10-01
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| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-023-42253-y |
| _version_ | 1797557985339244544 |
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| author | 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 Shilin Chen |
| author_facet | 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 Shilin Chen |
| author_sort | Wei Sun |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-03-10T17:24:58Z |
| format | Article |
| id | doaj.art-0870f154da264ac79f6dc3d34c60e963 |
| institution | Directory Open Access Journal |
| issn | 2041-1723 |
| language | English |
| last_indexed | 2024-03-10T17:24:58Z |
| publishDate | 2023-10-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj.art-0870f154da264ac79f6dc3d34c60e9632023-11-20T10:12:23ZengNature PortfolioNature Communications2041-17232023-10-0114111510.1038/s41467-023-42253-yCharacterization of the horse chestnut genome reveals the evolution of aescin and aesculin biosynthesisWei Sun0Qinggang Yin1Huihua Wan2Ranran Gao3Chao Xiong4Chong Xie5Xiangxiao Meng6Yaolei Mi7Xiaotong Wang8Caixia Wang9Weiqiang Chen10Ziyan Xie11Zheyong Xue12Hui Yao13Peng Sun14Xuehua Xie15Zhigang Hu16David R. Nelson17Zhichao Xu18Xinxiao Sun19Shilin Chen20Key Laboratory of Beijing for Identification and Safety Evaluation of Chinese Medicine, Institute of Chinese Materia Medica, China Academy of Chinese Medical SciencesKey Laboratory of Beijing for Identification and Safety Evaluation of Chinese Medicine, Institute of Chinese Materia Medica, China Academy of Chinese Medical SciencesKey Laboratory of Beijing for Identification and Safety Evaluation of Chinese Medicine, Institute of Chinese Materia Medica, China Academy of Chinese Medical SciencesKey Laboratory of Beijing for Identification and Safety Evaluation of Chinese Medicine, Institute of Chinese Materia Medica, China Academy of Chinese Medical SciencesKey Laboratory of Beijing for Identification and Safety Evaluation of Chinese Medicine, Institute of Chinese Materia Medica, China Academy of Chinese Medical SciencesState Key Laboratory of Chemical Resource Engineering, Beijing University of Chemical TechnologyKey Laboratory of Beijing for Identification and Safety Evaluation of Chinese Medicine, Institute of Chinese Materia Medica, China Academy of Chinese Medical SciencesKey Laboratory of Beijing for Identification and Safety Evaluation of Chinese Medicine, Institute of Chinese Materia Medica, China Academy of Chinese Medical SciencesCollege of Life Science, Northeast Forestry UniversityKey Laboratory of Beijing for Identification and Safety Evaluation of Chinese Medicine, Institute of Chinese Materia Medica, China Academy of Chinese Medical SciencesKey Laboratory of Beijing for Identification and Safety Evaluation of Chinese Medicine, Institute of Chinese Materia Medica, China Academy of Chinese Medical SciencesCollege of Life Science, Northeast Forestry UniversityCollege of Life Science, Northeast Forestry UniversityKey Laboratory of Bioactive Substances and Resources Utilization of Chinese Herbal Medicine, Ministry of Education, Institute of Medicinal Plant Development, Chinese Academy of Medical Sciences and Peking Union Medical CollegeKey Laboratory of Beijing for Identification and Safety Evaluation of Chinese Medicine, Institute of Chinese Materia Medica, China Academy of Chinese Medical SciencesKey Laboratory of Beijing for Identification and Safety Evaluation of Chinese Medicine, Institute of Chinese Materia Medica, China Academy of Chinese Medical SciencesCollege of Pharmacy, Hubei University of Chinese MedicineDepartment of Microbiology, Immunology and Biochemistry, University of Tennessee Health Science CenterCollege of Life Science, Northeast Forestry UniversityState Key Laboratory of Chemical Resource Engineering, Beijing University of Chemical TechnologyKey Laboratory of Beijing for Identification and Safety Evaluation of Chinese Medicine, Institute of Chinese Materia Medica, China Academy of Chinese Medical SciencesAbstract 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.https://doi.org/10.1038/s41467-023-42253-y |
| spellingShingle | 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 Shilin Chen Characterization of the horse chestnut genome reveals the evolution of aescin and aesculin biosynthesis Nature Communications |
| title | Characterization of the horse chestnut genome reveals the evolution of aescin and aesculin biosynthesis |
| title_full | Characterization of the horse chestnut genome reveals the evolution of aescin and aesculin biosynthesis |
| title_fullStr | Characterization of the horse chestnut genome reveals the evolution of aescin and aesculin biosynthesis |
| title_full_unstemmed | Characterization of the horse chestnut genome reveals the evolution of aescin and aesculin biosynthesis |
| title_short | Characterization of the horse chestnut genome reveals the evolution of aescin and aesculin biosynthesis |
| title_sort | characterization of the horse chestnut genome reveals the evolution of aescin and aesculin biosynthesis |
| url | https://doi.org/10.1038/s41467-023-42253-y |
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