IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-37133-4.html
   My bibliography  Save this article

Revealing evolution of tropane alkaloid biosynthesis by analyzing two genomes in the Solanaceae family

Author

Listed:
  • Fangyuan Zhang

    (Southwest University
    Southwest University)

  • Fei Qiu

    (Southwest University
    Southwest University)

  • Junlan Zeng

    (Southwest University
    Southwest University)

  • Zhichao Xu

    (Northeast Forestry University)

  • Yueli Tang

    (Southwest University
    Southwest University)

  • Tengfei Zhao

    (Southwest University
    Southwest University)

  • Yuqin Gou

    (Southwest University
    Southwest University)

  • Fei Su

    (Southwest University
    Southwest University)

  • Shiyi Wang

    (Southwest University
    Southwest University)

  • Xiuli Sun

    (Southwest University
    Southwest University)

  • Zheyong Xue

    (Northeast Forestry University)

  • Weixing Wang

    (Southwest University)

  • Chunxian Yang

    (Southwest University
    Southwest University)

  • Lingjiang Zeng

    (Southwest University
    Southwest University)

  • Xiaozhong Lan

    (Xizang Agricultural and Animal Husbandry College)

  • Min Chen

    (Southwest University)

  • Junhui Zhou

    (China Academy of Chinese Medical Sciences)

  • Zhihua Liao

    (Southwest University
    Southwest University)

Abstract

Tropane alkaloids (TAs) are widely distributed in the Solanaceae, while some important medicinal tropane alkaloids (mTAs), such as hyoscyamine and scopolamine, are restricted to certain species/tribes in this family. Little is known about the genomic basis and evolution of TAs biosynthesis and specialization in the Solanaceae. Here, we present chromosome-level genomes of two representative mTAs-producing species: Atropa belladonna and Datura stramonium. Our results reveal that the two species employ a conserved biosynthetic pathway to produce mTAs despite being distantly related within the nightshade family. A conserved gene cluster combined with gene duplication underlies the wide distribution of TAs in this family. We also provide evidence that branching genes leading to mTAs likely have evolved in early ancestral Solanaceae species but have been lost in most of the lineages, with A. belladonna and D. stramonium being exceptions. Furthermore, we identify a cytochrome P450 that modifies hyoscyamine into norhyoscyamine. Our results provide a genomic basis for evolutionary insights into the biosynthesis of TAs in the Solanaceae and will be useful for biotechnological production of mTAs via synthetic biology approaches.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-37133-4
    DOI: 10.1038/s41467-023-37133-4
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-37133-4
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-37133-4?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Prashanth Srinivasan & Christina D. Smolke, 2020. "Biosynthesis of medicinal tropane alkaloids in yeast," Nature, Nature, vol. 585(7826), pages 614-619, September.
    2. 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.
    3. 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.
    4. Nicolas Sierro & James N.D. Battey & Sonia Ouadi & Nicolas Bakaher & Lucien Bovet & Adrian Willig & Simon Goepfert & Manuel C. Peitsch & Nikolai V. Ivanov, 2014. "The tobacco genome sequence and its comparison with those of tomato and potato," Nature Communications, Nature, vol. 5(1), pages 1-9, September.
    5. Xiaofei Yang & Shenghan Gao & Li Guo & Bo Wang & Yanyan Jia & Jian Zhou & Yizhuo Che & Peng Jia & Jiadong Lin & Tun Xu & Jianyong Sun & Kai Ye, 2021. "Three chromosome-scale Papaver genomes reveal punctuated patchwork evolution of the morphinan and noscapine biosynthesis pathway," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    6. 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.
    7. 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.
    8. Arne Kusserow & Kevin Pang & Carsten Sturm & Martina Hrouda & Jan Lentfer & Heiko A. Schmidt & Ulrich Technau & Arndt von Haeseler & Bert Hobmayer & Mark Q. Martindale & Thomas W. Holstein, 2005. "Unexpected complexity of the Wnt gene family in a sea anemone," Nature, Nature, vol. 433(7022), pages 156-160, January.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. 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.

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. 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.
    2. 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.
    3. Radin Sadre & Thilani M. Anthony & Josh M. Grabar & Matthew A. Bedewitz & A. Daniel Jones & Cornelius S. Barry, 2022. "Metabolomics-guided discovery of cytochrome P450s involved in pseudotropine-dependent biosynthesis of modified tropane alkaloids," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    4. Junlan Zeng & Xiaoqiang Liu & Zhaoyue Dong & Fangyuan Zhang & Fei Qiu & Mingyu Zhong & Tengfei Zhao & Chunxian Yang & Lingjiang Zeng & Xiaozhong Lan & Hongbo Zhang & Junhui Zhou & Min Chen & Kexuan Ta, 2024. "Discovering a mitochondrion-localized BAHD acyltransferase involved in calystegine biosynthesis and engineering the production of 3β-tigloyloxytropane," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    5. Liye Zhang & Neahga Leonard & Rick Passaro & Mai Sy Luan & Pham Tuyen & Le Thi Ngoc Han & Nguyen Huy Cam & Larry Vogelnest & Michael Lynch & Amanda E. Fine & Nguyen Thi Thanh Nga & Nguyen Long & Benja, 2024. "Genomic adaptation to small population size and saltwater consumption in the critically endangered Cat Ba langur," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    6. Xiang Jiao & Xiaozhi Fu & Qishuang Li & Junling Bu & Xiuyu Liu & Otto Savolainen & Luqi Huang & Juan Guo & Jens Nielsen & Yun Chen, 2024. "De novo production of protoberberine and benzophenanthridine alkaloids through metabolic engineering of yeast," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    7. Xiaofei Yang & Shenghan Gao & Tun Xu & Bo Wang & Yanyan Jia & Kai Ye, 2023. "Reply to “Subgenome-aware analyses suggest a reticulate allopolyploidization origin in three Papaver genomes”," Nature Communications, Nature, vol. 14(1), pages 1-2, December.
    8. Gita Naseri, 2023. "A roadmap to establish a comprehensive platform for sustainable manufacturing of natural products in yeast," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    9. So-Hee Son & Jae-Eung Kim & Gyuri Park & Young-Joon Ko & Bong Hyun Sung & Jongcheol Seo & Seung Soo Oh & Ju Young Lee, 2022. "Metabolite trafficking enables membrane-impermeable-terpene secretion by yeast," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    10. Wenna Li & Zhao Zhou & Xianglai Li & Lin Ma & Qingyuan Guan & Guojun Zheng & Hao Liang & Yajun Yan & Xiaolin Shen & Jia Wang & Xinxiao Sun & Qipeng Yuan, 2022. "Biosynthesis of plant hemostatic dencichine in Escherichia coli," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    11. Zhijun TONG & Bingguang XIAO & Xuejun CHEN & Dunhuang FANG & Yihan ZHANG & Changjun HUANG & Yongping LI, 2018. "Construction of a genetic linkage map of cigar tobacco (Nicotiana tabacum L.) based on SSR markers and comparative studies," Czech Journal of Genetics and Plant Breeding, Czech Academy of Agricultural Sciences, vol. 54(3), pages 115-122.
    12. Bob Zimmermann & Juan D. Montenegro & Sofia M. C. Robb & Whitney J. Fropf & Lukas Weilguny & Shuonan He & Shiyuan Chen & Jessica Lovegrove-Walsh & Eric M. Hill & Cheng-Yi Chen & Katerina Ragkousi & Da, 2023. "Topological structures and syntenic conservation in sea anemone genomes," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    13. Jack Chun-Ting Liu & Ricardo De La Peña & Christian Tocol & Elizabeth S. Sattely, 2024. "Reconstitution of early paclitaxel biosynthetic network," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    14. Ruiqi Yan & Binghan Xie & Kebo Xie & Qi Liu & Songyang Sui & Shuqi Wang & Dawei Chen & Jimei Liu & Ridao Chen & Jungui Dai & Lin Yang, 2024. "Unravelling and reconstructing the biosynthetic pathway of bergenin," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    15. Abigail E. Bryson & Emily R. Lanier & Kin H. Lau & John P. Hamilton & Brieanne Vaillancourt & Davis Mathieu & Alan E. Yocca & Garret P. Miller & Patrick P. Edger & C. Robin Buell & Björn Hamberger, 2023. "Uncovering a miltiradiene biosynthetic gene cluster in the Lamiaceae reveals a dynamic evolutionary trajectory," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    16. Elizabeth Thomas & Sonia Herrero & Hayde Eng & Nafisa Gomaa & Jeff Gillikin & Roslyn Noar & Aydin Beseli & Margaret E Daub, 2020. "Engineering Cercospora disease resistance via expression of Cercospora nicotianae cercosporin-resistance genes and silencing of cercosporin production in tobacco," PLOS ONE, Public Library of Science, vol. 15(3), pages 1-19, March.
    17. Sierra M. Brooks & Celeste Marsan & Kevin B. Reed & Shuo-Fu Yuan & Dustin-Dat Nguyen & Adit Trivedi & Gokce Altin-Yavuzarslan & Nathan Ballinger & Alshakim Nelson & Hal S. Alper, 2023. "A tripartite microbial co-culture system for de novo biosynthesis of diverse plant phenylpropanoids," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    18. Theresa Catania & Yi Li & Thilo Winzer & David Harvey & Fergus Meade & Anna Caridi & Andrew Leech & Tony R. Larson & Zemin Ning & Jiyang Chang & Yves Peer & Ian A. Graham, 2022. "A functionally conserved STORR gene fusion in Papaver species that diverged 16.8 million years ago," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    19. Ren-Gang Zhang & Chaoxia Lu & Guang-Yuan Li & Jie Lv & Longxin Wang & Zhao-Xuan Wang & Zhe Chen & Dan Liu & Ye Zhao & Tian-Le Shi & Wei Zhang & Zhao-Hui Tang & Jian-Feng Mao & Yong-Peng Ma & Kai-Hua J, 2023. "Subgenome-aware analyses suggest a reticulate allopolyploidization origin in three Papaver genomes," Nature Communications, Nature, vol. 14(1), pages 1-6, December.
    20. Omar Sandoval-Ibáñez & David Rolo & Rabea Ghandour & Alexander P. Hertle & Tegan Armarego-Marriott & Arun Sampathkumar & Reimo Zoschke & Ralph Bock, 2022. "De-etiolation-induced protein 1 (DEIP1) mediates assembly of the cytochrome b6f complex in Arabidopsis," Nature Communications, Nature, vol. 13(1), pages 1-16, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-37133-4. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.