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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
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    as
    1. 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.
    2. 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.
    3. 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.
    4. 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.
    5. Jon Clardy & Christopher Walsh, 2004. "Lessons from natural molecules," Nature, Nature, vol. 432(7019), pages 829-837, December.
    6. 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.
    7. 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.
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