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Multiple independent losses of the biosynthetic pathway for two tropane alkaloids in the Solanaceae family

Author

Listed:
  • Jiao Yang

    (Lanzhou University)

  • Ying Wu

    (Lanzhou University)

  • Pan Zhang

    (Lanzhou University)

  • Jianxiang Ma

    (Lanzhou University)

  • Ying Jun Yao

    (Sichuan University)

  • Yan Lin Ma

    (Lanzhou University)

  • Lei Zhang

    (North Minzu University)

  • Yongzhi Yang

    (Lanzhou University)

  • Changmin Zhao

    (Lanzhou University)

  • Jihua Wu

    (Lanzhou University)

  • Xiangwen Fang

    (Lanzhou University)

  • Jianquan Liu

    (Lanzhou University
    Sichuan University)

Abstract

Hyoscyamine and scopolamine (HS), two valuable tropane alkaloids of significant medicinal importance, are found in multiple distantly related lineages within the Solanaceae family. Here we sequence the genomes of three representative species that produce HS from these lineages, and one species that does not produce HS. Our analysis reveals a shared biosynthetic pathway responsible for HS production in the three HS-producing species. We observe a high level of gene collinearity related to HS synthesis across the family in both types of species. By introducing gain-of-function and loss-of-function mutations at key sites, we confirm the reduced/lost or re-activated functions of critical genes involved in HS synthesis in both types of species, respectively. These findings indicate independent and repeated losses of the HS biosynthesis pathway since its origin in the ancestral lineage. Our results hold promise for potential future applications in the artificial engineering of HS biosynthesis in Solanaceae crops.

Suggested Citation

  • Jiao Yang & Ying Wu & Pan Zhang & Jianxiang Ma & Ying Jun Yao & Yan Lin Ma & Lei Zhang & Yongzhi Yang & Changmin Zhao & Jihua Wu & Xiangwen Fang & Jianquan Liu, 2023. "Multiple independent losses of the biosynthetic pathway for two tropane alkaloids in the Solanaceae family," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-44246-3
    DOI: 10.1038/s41467-023-44246-3
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    1. Yu Wang & He Zhang & Hyok Chol Ri & Zeyu An & Xin Wang & Jia-Nan Zhou & Dongran Zheng & Hao Wu & Pengchao Wang & Jianfei Yang & Ding-Kun Liu & Diyang Zhang & Wen-Chieh Tsai & Zheyong Xue & Zhichao Xu , 2022. "Deletion and tandem duplications of biosynthetic genes drive the diversity of triterpenoids in Aralia elata," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    2. Prashanth Srinivasan & Christina D. Smolke, 2020. "Biosynthesis of medicinal tropane alkaloids in yeast," Nature, Nature, vol. 585(7826), pages 614-619, September.
    3. Fangyuan Zhang & Fei Qiu & Junlan Zeng & Zhichao Xu & Yueli Tang & Tengfei Zhao & Yuqin Gou & Fei Su & Shiyi Wang & Xiuli Sun & Zheyong Xue & Weixing Wang & Chunxian Yang & Lingjiang Zeng & Xiaozhong , 2023. "Revealing evolution of tropane alkaloid biosynthesis by analyzing two genomes in the Solanaceae family," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    4. Ruiqiang Li & Wei Fan & Geng Tian & Hongmei Zhu & Lin He & Jing Cai & Quanfei Huang & Qingle Cai & Bo Li & Yinqi Bai & Zhihe Zhang & Yaping Zhang & Wen Wang & Jun Li & Fuwen Wei & Heng Li & Min Jian &, 2010. "Erratum: The sequence and de novo assembly of the giant panda genome," Nature, Nature, vol. 463(7284), pages 1106-1106, February.
    5. Tian Tian & Yong-Jiang Wang & Jian-Ping Huang & Jie Li & Bingyan Xu & Yin Chen & Li Wang & Jing Yang & Yijun Yan & Sheng-Xiong Huang, 2022. "Catalytic innovation underlies independent recruitment of polyketide synthases in cocaine and hyoscyamine biosynthesis," Nature Communications, Nature, vol. 13(1), pages 1-8, December.
    6. Yu Wang & He Zhang & Hyok Chol Ri & Zeyu An & Xin Wang & Jia-Nan Zhou & Dongran Zheng & Hao Wu & Pengchao Wang & Jianfei Yang & Ding-Kun Liu & Diyang Zhang & Wen-Chieh Tsai & Zheyong Xue & Zhichao Xu , 2022. "Author Correction: Deletion and tandem duplications of biosynthetic genes drive the diversity of triterpenoids in Aralia elata," Nature Communications, Nature, vol. 13(1), pages 1-2, December.
    7. Jian-Ping Huang & Chengli Fang & Xiaoyan Ma & Li Wang & Jing Yang & Jianying Luo & Yijun Yan & Yu Zhang & Sheng-Xiong Huang, 2019. "Tropane alkaloids biosynthesis involves an unusual type III polyketide synthase and non-enzymatic condensation," Nature Communications, Nature, vol. 10(1), pages 1-8, December.
    8. Matthew A. Bedewitz & A. Daniel Jones & John C. D’Auria & Cornelius S. Barry, 2018. "Tropinone synthesis via an atypical polyketide synthase and P450-mediated cyclization," Nature Communications, Nature, vol. 9(1), pages 1-13, December.
    9. Ruiqiang Li & Wei Fan & Geng Tian & Hongmei Zhu & Lin He & Jing Cai & Quanfei Huang & Qingle Cai & Bo Li & Yinqi Bai & Zhihe Zhang & Yaping Zhang & Wen Wang & Jun Li & Fuwen Wei & Heng Li & Min Jian &, 2010. "The sequence and de novo assembly of the giant panda genome," Nature, Nature, vol. 463(7279), pages 311-317, January.
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