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Cross-kingdom synthetic microbiota supports tomato suppression of Fusarium wilt disease

Author

Listed:
  • Xin Zhou

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Jinting Wang

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Fang Liu

    (Chinese Academy of Sciences)

  • Junmin Liang

    (Chinese Academy of Sciences)

  • Peng Zhao

    (Chinese Academy of Sciences)

  • Clement K. M. Tsui

    (University of British Columbia
    Tan Tock Seng Hospital
    Nanyang Technological University
    Sidra Medicine)

  • Lei Cai

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

Abstract

The role of rhizosphere microbiota in the resistance of tomato plant against soil-borne Fusarium wilt disease (FWD) remains unclear. Here, we showed that the FWD incidence was significantly negatively correlated with the diversity of both rhizosphere bacterial and fungal communities. Using the microbiological culturomic approach, we selected 205 unique strains to construct different synthetic communities (SynComs), which were inoculated into germ-free tomato seedlings, and their roles in suppressing FWD were monitored using omics approach. Cross-kingdom (fungi and bacteria) SynComs were most effective in suppressing FWD than those of Fungal or Bacterial SynComs alone. This effect was underpinned by a combination of molecular mechanisms related to plant immunity and microbial interactions contributed by the bacterial and fungal communities. This study provides new insight into the dynamics of microbiota in pathogen suppression and host immunity interactions. Also, the formulation and manipulation of SynComs for functional complementation constitute a beneficial strategy in controlling soil-borne disease.

Suggested Citation

  • Xin Zhou & Jinting Wang & Fang Liu & Junmin Liang & Peng Zhao & Clement K. M. Tsui & Lei Cai, 2022. "Cross-kingdom synthetic microbiota supports tomato suppression of Fusarium wilt disease," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-35452-6
    DOI: 10.1038/s41467-022-35452-6
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    1. Zhong Wei & Tianjie Yang & Ville-Petri Friman & Yangchun Xu & Qirong Shen & Alexandre Jousset, 2015. "Trophic network architecture of root-associated bacterial communities determines pathogen invasion and plant health," Nature Communications, Nature, vol. 6(1), pages 1-9, December.
    2. Franciska T. Vries & Rob I. Griffiths & Mark Bailey & Hayley Craig & Mariangela Girlanda & Hyun Soon Gweon & Sara Hallin & Aurore Kaisermann & Aidan M. Keith & Marina Kretzschmar & Philippe Lemanceau , 2018. "Soil bacterial networks are less stable under drought than fungal networks," Nature Communications, Nature, vol. 9(1), pages 1-12, December.
    3. Yang Bai & Daniel B. Müller & Girish Srinivas & Ruben Garrido-Oter & Eva Potthoff & Matthias Rott & Nina Dombrowski & Philipp C. Münch & Stijn Spaepen & Mitja Remus-Emsermann & Bruno Hüttel & Alice C., 2015. "Functional overlap of the Arabidopsis leaf and root microbiota," Nature, Nature, vol. 528(7582), pages 364-369, December.
    4. Ben O. Oyserman & Stalin Sarango Flores & Thom Griffioen & Xinya Pan & Elmar Wijk & Lotte Pronk & Wouter Lokhorst & Azkia Nurfikari & Joseph N. Paulson & Mercedeh Movassagh & Nejc Stopnisek & Anne Kup, 2022. "Disentangling the genetic basis of rhizosphere microbiome assembly in tomato," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    5. Gabriel Castrillo & Paulo José Pereira Lima Teixeira & Sur Herrera Paredes & Theresa F. Law & Laura de Lorenzo & Meghan E. Feltcher & Omri M. Finkel & Natalie W. Breakfield & Piotr Mieczkowski & Corbi, 2017. "Root microbiota drive direct integration of phosphate stress and immunity," Nature, Nature, vol. 543(7646), pages 513-518, March.
    6. Tao Chen & Kinya Nomura & Xiaolin Wang & Reza Sohrabi & Jin Xu & Lingya Yao & Bradley C. Paasch & Li Ma & James Kremer & Yuti Cheng & Li Zhang & Nian Wang & Ertao Wang & Xiu-Fang Xin & Sheng Yang He, 2020. "A plant genetic network for preventing dysbiosis in the phyllosphere," Nature, Nature, vol. 580(7805), pages 653-657, April.
    7. Omri M. Finkel & Isai Salas-González & Gabriel Castrillo & Jonathan M. Conway & Theresa F. Law & Paulo José Pereira Lima Teixeira & Ellie D. Wilson & Connor R. Fitzpatrick & Corbin D. Jones & Jeffery , 2020. "A single bacterial genus maintains root growth in a complex microbiome," Nature, Nature, vol. 587(7832), pages 103-108, November.
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    1. Shikai La & Jiafan Li & Si Ma & Xingqun Liu & Lihong Gao & Yongqiang Tian, 2024. "Protective role of native root-associated bacterial consortium against root-knot nematode infection in susceptible plants," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    2. Xue Jin & Huiting Jia & Lingyi Ran & Fengzhi Wu & Junjie Liu & Klaus Schlaeppi & Francisco Dini-Andreote & Zhong Wei & Xingang Zhou, 2024. "Fusaric acid mediates the assembly of disease-suppressive rhizosphere microbiota via induced shifts in plant root exudates," Nature Communications, Nature, vol. 15(1), pages 1-15, December.

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