IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-42877-0.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-42877-0
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-42877-0?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. 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.
    2. 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.
    3. 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.
    4. 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.
    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. 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.
    2. Zhen-Hui Wang & Xin-Feng Wang & Tianyuan Lu & Ming-Rui Li & Peng Jiang & Jing Zhao & Si-Tong Liu & Xue-Qi Fu & Jonathan F. Wendel & Yves Peer & Bao Liu & Lin-Feng Li, 2022. "Reshuffling of the ancestral core-eudicot genome shaped chromatin topology and epigenetic modification in Panax," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    3. Jinping Zou & Xinlin Chen & Chenxu Liu & Mingyue Guo & Mukesh Kumar Kanwar & Zhenyu Qi & Ping Yang & Guanghui Wang & Yan Bao & Diane C. Bassham & Jingquan Yu & Jie Zhou, 2023. "Autophagy promotes jasmonate-mediated defense against nematodes," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    4. Zhiyou Zong & Scott Mazurkewich & Caroline S. Pereira & Haohao Fu & Wensheng Cai & Xueguang Shao & Munir S. Skaf & Johan Larsbrink & Leila Lo Leggio, 2022. "Mechanism and biomass association of glucuronoyl esterase: an α/β hydrolase with potential in biomass conversion," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    5. Yao Xia & Rongfeng Zou & Maxime Escouboué & Liang Zhong & Chengjun Zhu & Cécile Pouzet & Xueqiang Wu & Yongjin Wang & Guohua Lv & Haibo Zhou & Pinghua Sun & Ke Ding & Laurent Deslandes & Shuguang Yuan, 2021. "Secondary-structure switch regulates the substrate binding of a YopJ family acetyltransferase," Nature Communications, Nature, vol. 12(1), pages 1-10, December.
    6. Qaseem, Mirza Faisal & Shaheen, Humaira & Wu, Ai-Min, 2021. "Cell wall hemicellulose for sustainable industrial utilization," Renewable and Sustainable Energy Reviews, Elsevier, vol. 144(C).
    7. Zi-Wei Yan & Fang-Yan Chen & Xian Zhang & Wen-Juan Cai & Chun-Yu Chen & Jie Liu & Man-Ni Wu & Ning-Jing Liu & Bin Ma & Mu-Yang Wang & Dai-Yin Chao & Cai-Ji Gao & Ying-Bo Mao, 2023. "Endocytosis-mediated entry of a caterpillar effector into plants is countered by Jasmonate," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    8. Yu Wang & He Zhang & Hyok Chol Ri & Zeyu An & Xin Wang & Jia-Nan Zhou & Dongran Zheng & Hao Wu & Pengchao Wang & Jianfei Yang & Ding-Kun Liu & Diyang Zhang & Wen-Chieh Tsai & Zheyong Xue & Zhichao Xu , 2022. "Deletion and tandem duplications of biosynthetic genes drive the diversity of triterpenoids in Aralia elata," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    9. Malitha C. Dickwella Widanage & Isha Gautam & Daipayan Sarkar & Frederic Mentink-Vigier & Josh V. Vermaas & Shi-You Ding & Andrew S. Lipton & Thierry Fontaine & Jean-Paul Latgé & Ping Wang & Tuo Wang, 2024. "Adaptative survival of Aspergillus fumigatus to echinocandins arises from cell wall remodeling beyond β−1,3-glucan synthesis inhibition," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    10. Wei Yuan & Chenjian Jiang & Qin Wang & Yubo Fang & Jin Wang & Meng Wang & Han Xiao, 2022. "Biosynthesis of mushroom-derived type II ganoderic acids by engineered yeast," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    11. Ameneh Asadi-Sardari & Esmat Mahdikhani-Moghadam & Mohammad Zaki-Aghl & Ramesh Raju Vetukuri, 2022. "Constitutive and Inducible Expression of Genes Related to Salicylic Acid and Ethylene Pathways in a Moderately Resistant Tomato Cultivar Leads to Delayed Development of Meloidogyne javanica," Agriculture, MDPI, vol. 12(12), pages 1-22, 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_s41467-023-42877-0. 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.