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The gradual establishment of complex coumarin biosynthetic pathway in Apiaceae

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  • Xin-Cheng Huang

    (Nanjing Agricultural University)

  • Huanying Tang

    (China Pharmaceutical University)

  • Xuefen Wei

    (Nanjing Agricultural University)

  • Yuedong He

    (Hunan Agricultural University)

  • Shuaiya Hu

    (Nanjing Agricultural University)

  • Jia-Yi Wu

    (Nanjing Agricultural University)

  • Dingqiao Xu

    (Shaanxi University of Chinese Medicine)

  • Fei Qiao

    (National Key Laboratory for Tropical Crop Breeding
    Chinese Academy of Tropical Agricultural Sciences)

  • Jia-Yu Xue

    (Nanjing Agricultural University)

  • Yucheng Zhao

    (China Pharmaceutical University
    China Pharmaceutical University)

Abstract

Complex coumarins (CCs) represent characteristic metabolites found in Apiaceae plants, possessing significant medical value. Their essential functional role is likely as protectants against pathogens and regulators responding to environmental stimuli. Utilizing genomes and transcriptomes from 34 Apiaceae plants, including our recently sequenced Peucedanum praeruptorum, we conduct comprehensive phylogenetic analyses to reconstruct the detailed evolutionary process of the CC biosynthetic pathway in Apiaceae. Our results show that three key enzymes – p-coumaroyl CoA 2’-hydroxylase (C2’H), C-prenyltransferase (C-PT), and cyclase – originated successively at different evolutionary nodes within Apiaceae through various means of gene duplications: ectopic and tandem duplications. Neofunctionalization endows these enzymes with novel functions necessary for CC biosynthesis, thus completing the pathway. Candidate genes are cloned for heterologous expression and subjected to in vitro enzymatic assays to test our hypothesis regarding the origins of the key enzymes, and the results precisely validate our evolutionary inferences. Among the three enzymes, C-PTs are likely the primary determinant of the structural diversity of CCs (linear/angular), due to divergent activities evolved to target different positions (C-6 or C-8) of umbelliferone. A key amino acid variation (Ala161/Thr161) is identified and proven to play a crucial role in the alteration of enzymatic activity, possibly resulting in distinct binding forms between enzymes and substrates, thereby leading to different products. In conclusion, this study provides a detailed trajectory for the establishment and evolution of the CC biosynthetic pathway in Apiaceae. It explains why only a portion, not all, of Apiaceae plants can produce CCs and reveals the mechanisms of CC structural diversity among different Apiaceae plants.

Suggested Citation

  • Xin-Cheng Huang & Huanying Tang & Xuefen Wei & Yuedong He & Shuaiya Hu & Jia-Yi Wu & Dingqiao Xu & Fei Qiao & Jia-Yu Xue & Yucheng Zhao, 2024. "The gradual establishment of complex coumarin biosynthetic pathway in Apiaceae," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-51285-x
    DOI: 10.1038/s41467-024-51285-x
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    References listed on IDEAS

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    1. Zhenhua Liu & Jitender Cheema & Marielle Vigouroux & Lionel Hill & James Reed & Pirita Paajanen & Levi Yant & Anne Osbourn, 2020. "Formation and diversification of a paradigm biosynthetic gene cluster in plants," Nature Communications, Nature, vol. 11(1), pages 1-11, December.
    2. Kathryn Tunyasuvunakool & Jonas Adler & Zachary Wu & Tim Green & Michal Zielinski & Augustin Žídek & Alex Bridgland & Andrew Cowie & Clemens Meyer & Agata Laydon & Sameer Velankar & Gerard J. Kleywegt, 2021. "Highly accurate protein structure prediction for the human proteome," Nature, Nature, vol. 596(7873), pages 590-596, August.
    3. John Jumper & Richard Evans & Alexander Pritzel & Tim Green & Michael Figurnov & Olaf Ronneberger & Kathryn Tunyasuvunakool & Russ Bates & Augustin Žídek & Anna Potapenko & Alex Bridgland & Clemens Me, 2021. "Highly accurate protein structure prediction with AlphaFold," Nature, Nature, vol. 596(7873), pages 583-589, August.
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