IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-40401-y.html
   My bibliography  Save this article

Functional divergence of CYP76AKs shapes the chemodiversity of abietane-type diterpenoids in genus Salvia

Author

Listed:
  • Jiadong Hu

    (Shanghai University of Traditional Chinese Medicine
    Second Affiliated Hospital of Navy Medical University)

  • Shi Qiu

    (Shanghai University of Traditional Chinese Medicine)

  • Feiyan Wang

    (Shanghai University of Traditional Chinese Medicine)

  • Qing Li

    (Second Affiliated Hospital of Navy Medical University)

  • Chun-Lei Xiang

    (Chinese Academy of Sciences)

  • Peng Di

    (Jilin Agricultural University)

  • Ziding Wu

    (Shanghai University of Traditional Chinese Medicine)

  • Rui Jiang

    (Shanghai University of Traditional Chinese Medicine)

  • Jinxing Li

    (Shanghai University of Traditional Chinese Medicine)

  • Zhen Zeng

    (Shanghai University of Traditional Chinese Medicine)

  • Jing Wang

    (Shanghai University of Traditional Chinese Medicine)

  • Xingxing Wang

    (Shanghai University of Traditional Chinese Medicine)

  • Yuchen Zhang

    (Shanghai University of Traditional Chinese Medicine)

  • Shiyuan Fang

    (Shanghai University of Traditional Chinese Medicine)

  • Yuqi Qiao

    (Shanghai University of Traditional Chinese Medicine)

  • Jie Ding

    (Shanghai Chenshan Botanical Garden)

  • Yun Jiang

    (Shanghai Chenshan Botanical Garden)

  • Zhichao Xu

    (Northeast Forestry University)

  • Junfeng Chen

    (Shanghai University of Traditional Chinese Medicine)

  • Wansheng Chen

    (Shanghai University of Traditional Chinese Medicine
    Second Affiliated Hospital of Navy Medical University)

Abstract

The genus Salvia L. (Lamiaceae) comprises myriad distinct medicinal herbs, with terpenoids as one of their major active chemical groups. Abietane-type diterpenoids (ATDs), such as tanshinones and carnosic acids, are specific to Salvia and exhibit taxonomic chemical diversity among lineages. To elucidate how ATD chemical diversity evolved, we carried out large-scale metabolic and phylogenetic analyses of 71 Salvia species, combined with enzyme function, ancestral sequence and chemical trait reconstruction, and comparative genomics experiments. This integrated approach showed that the lineage-wide ATD diversities in Salvia were induced by differences in the oxidation of the terpenoid skeleton at C-20, which was caused by the functional divergence of the cytochrome P450 subfamily CYP76AK. These findings present a unique pattern of chemical diversity in plants that was shaped by the loss of enzyme activity and associated catalytic pathways.

Suggested Citation

  • Jiadong Hu & Shi Qiu & Feiyan Wang & Qing Li & Chun-Lei Xiang & Peng Di & Ziding Wu & Rui Jiang & Jinxing Li & Zhen Zeng & Jing Wang & Xingxing Wang & Yuchen Zhang & Shiyuan Fang & Yuqi Qiao & Jie Din, 2023. "Functional divergence of CYP76AKs shapes the chemodiversity of abietane-type diterpenoids in genus Salvia," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-40401-y
    DOI: 10.1038/s41467-023-40401-y
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-40401-y
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-40401-y?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. Ulschan Scheler & Wolfgang Brandt & Andrea Porzel & Kathleen Rothe & David Manzano & Dragana Božić & Dimitra Papaefthimiou & Gerd Ulrich Balcke & Anja Henning & Swanhild Lohse & Sylvestre Marillonnet , 2016. "Elucidation of the biosynthesis of carnosic acid and its reconstitution in yeast," Nature Communications, Nature, vol. 7(1), pages 1-11, December.
    2. C. J. Paddon & P. J. Westfall & D. J. Pitera & K. Benjamin & K. Fisher & D. McPhee & M. D. Leavell & A. Tai & A. Main & D. Eng & D. R. Polichuk & K. H. Teoh & D. W. Reed & T. Treynor & J. Lenihan & H., 2013. "High-level semi-synthetic production of the potent antimalarial artemisinin," Nature, Nature, vol. 496(7446), pages 528-532, April.
    3. Jon Clardy & Christopher Walsh, 2004. "Lessons from natural molecules," Nature, Nature, vol. 432(7019), pages 829-837, December.
    4. 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.
    5. 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.
    6. Liping Zeng & Qiang Zhang & Renran Sun & Hongzhi Kong & Ning Zhang & Hong Ma, 2014. "Resolution of deep angiosperm phylogeny using conserved nuclear genes and estimates of early divergence times," Nature Communications, Nature, vol. 5(1), pages 1-12, December.
    7. Ying Ma & Guanghong Cui & Tong Chen & Xiaohui Ma & Ruishan Wang & Baolong Jin & Jian Yang & Liping Kang & Jinfu Tang & Changjiangsheng Lai & Yanan Wang & Yujun Zhao & Ye Shen & Wen Zeng & Reuben J. Pe, 2021. "Expansion within the CYP71D subfamily drives the heterocyclization of tanshinones synthesis in Salvia miltiorrhiza," Nature Communications, Nature, vol. 12(1), pages 1-11, December.
    Full references (including those not matched with items on IDEAS)

    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. 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.
    2. Yifeng Zhang & Jie Gao & Lin Ma & Lichan Tu & Tianyuan Hu & Xiaoyi Wu & Ping Su & Yujun Zhao & Yuan Liu & Dan Li & Jiawei Zhou & Yan Yin & Yuru Tong & Huan Zhao & Yun Lu & Jiadian Wang & Wei Gao & Luq, 2023. "Tandemly duplicated CYP82Ds catalyze 14-hydroxylation in triptolide biosynthesis and precursor production in Saccharomyces cerevisiae," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    3. Nikolaj Lervad Hansen & Louise Kjaerulff & Quinn Kalby Heck & Victor Forman & Dan Staerk & Birger Lindberg Møller & Johan Andersen-Ranberg, 2022. "Tripterygium wilfordii cytochrome P450s catalyze the methyl shift and epoxidations in the biosynthesis of triptonide," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    4. Ashty S. Karim & Dylan M. Brown & Chloé M. Archuleta & Sharisse Grannan & Ludmilla Aristilde & Yogesh Goyal & Josh N. Leonard & Niall M. Mangan & Arthur Prindle & Gabriel J. Rocklin & Keith J. Tyo & L, 2024. "Deconstructing synthetic biology across scales: a conceptual approach for training synthetic biologists," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    5. Leixia Chu & Xiaoxia Luo & Taoting Zhu & Yingying Cao & Lili Zhang & Zixin Deng & Jiangtao Gao, 2022. "Harnessing phosphonate antibiotics argolaphos biosynthesis enables a synthetic biology-based green synthesis of glyphosate," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    6. Jianxiang Ma & Pengchuan Sun & Dandan Wang & Zhenyue Wang & Jiao Yang & Ying Li & Wenjie Mu & Renping Xu & Ying Wu & Congcong Dong & Nawal Shrestha & Jianquan Liu & Yongzhi Yang, 2021. "The Chloranthus sessilifolius genome provides insight into early diversification of angiosperms," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    7. 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.
    8. 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.
    9. Xing Guo & Dongming Fang & Sunil Kumar Sahu & Shuai Yang & Xuanmin Guang & Ryan Folk & Stephen A. Smith & Andre S. Chanderbali & Sisi Chen & Min Liu & Ting Yang & Shouzhou Zhang & Xin Liu & Xun Xu & P, 2021. "Chloranthus genome provides insights into the early diversification of angiosperms," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    10. Shan Yang & Ruibing Chen & Xuan Cao & Guodong Wang & Yongjin J. Zhou, 2024. "De novo biosynthesis of the hops bioactive flavonoid xanthohumol in yeast," Nature Communications, Nature, vol. 15(1), pages 1-10, December.
    11. 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.
    12. Anna Zimmermann & Julian E. Prieto-Vivas & Charlotte Cautereels & Anton Gorkovskiy & Jan Steensels & Yves Peer & Kevin J. Verstrepen, 2023. "A Cas3-base editing tool for targetable in vivo mutagenesis," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    13. Jiangyong Gu & Yuanshen Gui & Lirong Chen & Gu Yuan & Hui-Zhe Lu & Xiaojie Xu, 2013. "Use of Natural Products as Chemical Library for Drug Discovery and Network Pharmacology," PLOS ONE, Public Library of Science, vol. 8(4), pages 1-10, April.
    14. Xixian Chen & Rehka T & Jérémy Esque & Congqiang Zhang & Sudha Shukal & Chin Chin Lim & Leonard Ong & Derek Smith & Isabelle André, 2022. "Total enzymatic synthesis of cis-α-irone from a simple carbon source," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    15. Zhong Li & Lilan Zhang & Kangwei Xu & Yuanyuan Jiang & Jieke Du & Xingwang Zhang & Ling-Hong Meng & Qile Wu & Lei Du & Xiaoju Li & Yuechan Hu & Zhenzhen Xie & Xukai Jiang & Ya-Jie Tang & Ruibo Wu & Re, 2023. "Molecular insights into the catalytic promiscuity of a bacterial diterpene synthase," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    16. Quanli Liu & Yi Liu & Gang Li & Otto Savolainen & Yun Chen & Jens Nielsen, 2021. "De novo biosynthesis of bioactive isoflavonoids by engineered yeast cell factories," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    17. 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.
    18. 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.
    19. 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 & Xu, 2023. "Characterization of the horse chestnut genome reveals the evolution of aescin and aesculin biosynthesis," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    20. Shuangjia Zheng & Tao Zeng & Chengtao Li & Binghong Chen & Connor W. Coley & Yuedong Yang & Ruibo Wu, 2022. "Deep learning driven biosynthetic pathways navigation for natural products with BioNavi-NP," Nature Communications, Nature, vol. 13(1), pages 1-9, 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_s41467-023-40401-y. 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.