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Deciphering triterpenoid saponin biosynthesis by leveraging transcriptome response to methyl jasmonate elicitation in Saponaria vaccaria

Author

Listed:
  • Xiaoyue Chen

    (University of California
    Joint BioEnergy Institute
    Lawrence Berkeley National Laboratory)

  • Graham A. Hudson

    (Joint BioEnergy Institute
    University of California)

  • Charlotte Mineo

    (University of California
    Joint BioEnergy Institute)

  • Bashar Amer

    (Joint BioEnergy Institute
    Lawrence Berkeley National Laboratory)

  • Edward E. K. Baidoo

    (Joint BioEnergy Institute
    Lawrence Berkeley National Laboratory)

  • Samantha A. Crowe

    (Joint BioEnergy Institute
    University of California
    University of California)

  • Yuzhong Liu

    (Joint BioEnergy Institute
    University of California)

  • Jay D. Keasling

    (Joint BioEnergy Institute
    University of California
    Lawrence Berkeley National Laboratory
    University of California)

  • Henrik V. Scheller

    (University of California
    Joint BioEnergy Institute
    Lawrence Berkeley National Laboratory)

Abstract

Methyl jasmonate (MeJA) is a known elicitor of plant specialized metabolism, including triterpenoid saponins. Saponaria vaccaria is an annual herb used in traditional Chinese medicine, containing large quantities of oleanane-type triterpenoid saponins with anticancer properties and structural similarities to the vaccine adjuvant QS-21. Leveraging the MeJA-elicited saponin biosynthesis, we identify multiple enzymes catalyzing the oxidation and glycosylation of triterpenoids in S. vaccaria. This exploration is aided by Pacbio full-length transcriptome sequencing and gene expression analysis. A cellulose synthase-like enzyme can not only glucuronidate triterpenoid aglycones but also alter the product profile of a cytochrome P450 monooxygenase via preference for the aldehyde intermediate. Furthermore, the discovery of a UDP-glucose 4,6-dehydratase and a UDP-4-keto-6-deoxy-glucose reductase reveals the biosynthetic pathway for the rare nucleotide sugar UDP-d-fucose, a likely sugar donor for fucosylation of plant natural products. Our work enables the production and optimization of high-value saponins in microorganisms and plants through synthetic biology approaches.

Suggested Citation

  • Xiaoyue Chen & Graham A. Hudson & Charlotte Mineo & Bashar Amer & Edward E. K. Baidoo & Samantha A. Crowe & Yuzhong Liu & Jay D. Keasling & Henrik V. Scheller, 2023. "Deciphering triterpenoid saponin biosynthesis by leveraging transcriptome response to methyl jasmonate elicitation in Saponaria vaccaria," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-42877-0
    DOI: 10.1038/s41467-023-42877-0
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    References listed on IDEAS

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    1. Soo Yeon Chung & Hikaru Seki & Yukiko Fujisawa & Yoshikazu Shimoda & Susumu Hiraga & Yuhta Nomura & Kazuki Saito & Masao Ishimoto & Toshiya Muranaka, 2020. "A cellulose synthase-derived enzyme catalyses 3-O-glucuronosylation in saponin biosynthesis," Nature Communications, Nature, vol. 11(1), pages 1-11, December.
    2. Thomas J. Simmons & Jenny C. Mortimer & Oigres D. Bernardinelli & Ann-Christin Pöppler & Steven P. Brown & Eduardo R. deAzevedo & Ray Dupree & Paul Dupree, 2016. "Folding of xylan onto cellulose fibrils in plant cell walls revealed by solid-state NMR," Nature Communications, Nature, vol. 7(1), pages 1-9, December.
    3. Karel Miettinen & Jacob Pollier & Dieter Buyst & Philipp Arendt & René Csuk & Sven Sommerwerk & Tessa Moses & Jan Mertens & Prashant D Sonawane & Laurens Pauwels & Asaph Aharoni & José Martins & David, 2017. "The ancient CYP716 family is a major contributor to the diversification of eudicot triterpenoid biosynthesis," Nature Communications, Nature, vol. 8(1), pages 1-13, April.
    4. Bryan Thines & Leron Katsir & Maeli Melotto & Yajie Niu & Ajin Mandaokar & Guanghui Liu & Kinya Nomura & Sheng Yang He & Gregg A. Howe & John Browse, 2007. "JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signalling," Nature, Nature, vol. 448(7154), pages 661-665, August.
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