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A plant genetic network for preventing dysbiosis in the phyllosphere

Author

Listed:
  • Tao Chen

    (Michigan State University
    Huazhong Agricultural University
    Michigan State University)

  • Kinya Nomura

    (Michigan State University)

  • Xiaolin Wang

    (Chinese Academy of Sciences)

  • Reza Sohrabi

    (Michigan State University
    Michigan State University)

  • Jin Xu

    (University of Florida)

  • Lingya Yao

    (Chinese Academy of Sciences)

  • Bradley C. Paasch

    (Michigan State University)

  • Li Ma

    (Michigan State University)

  • James Kremer

    (Michigan State University)

  • Yuti Cheng

    (Michigan State University
    Michigan State University)

  • Li Zhang

    (Michigan State University
    Michigan State University)

  • Nian Wang

    (University of Florida)

  • Ertao Wang

    (Chinese Academy of Sciences)

  • Xiu-Fang Xin

    (Chinese Academy of Sciences
    Chinese Academy of Sciences)

  • Sheng Yang He

    (Michigan State University
    Michigan State University
    Michigan State University)

Abstract

The aboveground parts of terrestrial plants, collectively called the phyllosphere, have a key role in the global balance of atmospheric carbon dioxide and oxygen. The phyllosphere represents one of the most abundant habitats for microbiota colonization. Whether and how plants control phyllosphere microbiota to ensure plant health is not well understood. Here we show that the Arabidopsis quadruple mutant (min7 fls2 efr cerk1; hereafter, mfec)1, simultaneously defective in pattern-triggered immunity and the MIN7 vesicle-trafficking pathway, or a constitutively activated cell death1 (cad1) mutant, carrying a S205F mutation in a membrane-attack-complex/perforin (MACPF)-domain protein, harbour altered endophytic phyllosphere microbiota and display leaf-tissue damage associated with dysbiosis. The Shannon diversity index and the relative abundance of Firmicutes were markedly reduced, whereas Proteobacteria were enriched in the mfec and cad1S205F mutants, bearing cross-kingdom resemblance to some aspects of the dysbiosis that occurs in human inflammatory bowel disease. Bacterial community transplantation experiments demonstrated a causal role of a properly assembled leaf bacterial community in phyllosphere health. Pattern-triggered immune signalling, MIN7 and CAD1 are found in major land plant lineages and are probably key components of a genetic network through which terrestrial plants control the level and nurture the diversity of endophytic phyllosphere microbiota for survival and health in a microorganism-rich environment.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:nature:v:580:y:2020:i:7805:d:10.1038_s41586-020-2185-0
    DOI: 10.1038/s41586-020-2185-0
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    Citations

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    Cited by:

    1. Adina Howe & Nejc Stopnisek & Shane K. Dooley & Fan Yang & Keara L. Grady & Ashley Shade, 2023. "Seasonal activities of the phyllosphere microbiome of perennial crops," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    2. Yayu Wang & Xiaolin Wang & Shuai Sun & Canzhi Jin & Jianmu Su & Jinpu Wei & Xinyue Luo & Jiawen Wen & Tong Wei & Sunil Kumar Sahu & Hongfeng Zou & Hongyun Chen & Zhixin Mu & Gengyun Zhang & Xin Liu & , 2022. "GWAS, MWAS and mGWAS provide insights into precision agriculture based on genotype-dependent microbial effects in foxtail millet," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    3. 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.
    4. Frederickson Entila & Xiaowei Han & Akira Mine & Paul Schulze-Lefert & Kenichi Tsuda, 2024. "Commensal lifestyle regulated by a negative feedback loop between Arabidopsis ROS and the bacterial T2SS," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    5. Kerstin Unger & Syed Ali Komail Raza & Teresa Mayer & Michael Reichelt & Johannes Stuttmann & Annika Hielscher & Ute Wittstock & Jonathan Gershenzon & Matthew T. Agler, 2024. "Glucosinolate structural diversity shapes recruitment of a metabolic network of leaf-associated bacteria," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    6. Conner J. Rogan & Yin-Yuin Pang & Sophie D. Mathews & Sydney E. Turner & Alexandra J. Weisberg & Silke Lehmann & Doris Rentsch & Jeffrey C. Anderson, 2024. "Transporter-mediated depletion of extracellular proline directly contributes to plant pattern-triggered immunity against a bacterial pathogen," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    7. Pin Su & Houxiang Kang & Qianze Peng & Wisnu Adi Wicaksono & Gabriele Berg & Zhuoxin Liu & Jiejia Ma & Deyong Zhang & Tomislav Cernava & Yong Liu, 2024. "Microbiome homeostasis on rice leaves is regulated by a precursor molecule of lignin biosynthesis," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    8. Xiaogang Li & Dele Chen & Víctor J. Carrión & Daniel Revillini & Shan Yin & Yuanhua Dong & Taolin Zhang & Xingxiang Wang & Manuel Delgado-Baquerizo, 2023. "Acidification suppresses the natural capacity of soil microbiome to fight pathogenic Fusarium infections," Nature Communications, Nature, vol. 14(1), pages 1-16, December.

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