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Bacteria establish an aqueous living space in plants crucial for virulence

Author

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  • Xiu-Fang Xin

    (Plant Research Laboratory, Michigan State University)

  • Kinya Nomura

    (Plant Research Laboratory, Michigan State University)

  • Kyaw Aung

    (Plant Research Laboratory, Michigan State University
    Howard Hughes Medical Institute—Gordon and Betty Moore Foundation, Michigan State University)

  • André C. Velásquez

    (Plant Research Laboratory, Michigan State University)

  • Jian Yao

    (Plant Research Laboratory, Michigan State University
    †Present address: Department of Biological Sciences, Western Michigan University, Kalamazoo, Michigan 49008, USA.)

  • Freddy Boutrot

    (The Sainsbury Laboratory, Norwich Research Park)

  • Jeff H. Chang

    (Oregon State University)

  • Cyril Zipfel

    (The Sainsbury Laboratory, Norwich Research Park)

  • Sheng Yang He

    (Plant Research Laboratory, Michigan State University
    Howard Hughes Medical Institute—Gordon and Betty Moore Foundation, Michigan State University
    Michigan State University
    Plant Resilience Institute, Michigan State University)

Abstract

High humidity has a strong influence on the development of numerous diseases affecting the above-ground parts of plants (the phyllosphere) in crop fields and natural ecosystems, but the molecular basis of this humidity effect is not understood. Previous studies have emphasized immune suppression as a key step in bacterial pathogenesis. Here we show that humidity-dependent, pathogen-driven establishment of an aqueous intercellular space (apoplast) is another important step in bacterial infection of the phyllosphere. Bacterial effectors, such as Pseudomonas syringae HopM1, induce establishment of the aqueous apoplast and are sufficient to transform non-pathogenic P. syringae strains into virulent pathogens in immunodeficient Arabidopsis thaliana under high humidity. Arabidopsis quadruple mutants simultaneously defective in a host target (AtMIN7) of HopM1 and in pattern-triggered immunity could not only be used to reconstitute the basic features of bacterial infection, but also exhibited humidity-dependent dyshomeostasis of the endophytic commensal bacterial community in the phyllosphere. These results highlight a new conceptual framework for understanding diverse phyllosphere–bacterial interactions.

Suggested Citation

  • Xiu-Fang Xin & Kinya Nomura & Kyaw Aung & André C. Velásquez & Jian Yao & Freddy Boutrot & Jeff H. Chang & Cyril Zipfel & Sheng Yang He, 2016. "Bacteria establish an aqueous living space in plants crucial for virulence," Nature, Nature, vol. 539(7630), pages 524-529, November.
  • Handle: RePEc:nat:nature:v:539:y:2016:i:7630:d:10.1038_nature20166
    DOI: 10.1038/nature20166
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    Cited by:

    1. Jiahui Liu & Xiaoyun Wu & Yue Fang & Ye Liu & Esther Oreofe Bello & Yong Li & Ruyi Xiong & Yinzi Li & Zheng Qing Fu & Aiming Wang & Xiaofei Cheng, 2023. "A plant RNA virus inhibits NPR1 sumoylation and subverts NPR1-mediated plant immunity," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    2. Gaële Lajeunesse & Charles Roussin-Léveillée & Sophie Boutin & Élodie Fortin & Isabelle Laforest-Lapointe & Peter Moffett, 2023. "Light prevents pathogen-induced aqueous microenvironments via potentiation of salicylic acid signaling," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    3. 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.
    4. Mamoru Matsumura & Mika Nomoto & Tomotaka Itaya & Yuri Aratani & Mizuki Iwamoto & Takakazu Matsuura & Yuki Hayashi & Tsuyoshi Mori & Michael J. Skelly & Yoshiharu Y. Yamamoto & Toshinori Kinoshita & I, 2022. "Mechanosensory trichome cells evoke a mechanical stimuli–induced immune response in Arabidopsis thaliana," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    5. Yunpeng Liu & Huihui Zhang & Jing Wang & Wenting Gao & Xiting Sun & Qin Xiong & Xia Shu & Youzhi Miao & Qirong Shen & Weibing Xun & Ruifu Zhang, 2024. "Nonpathogenic Pseudomonas syringae derivatives and its metabolites trigger the plant “cry for help” response to assemble disease suppressing and growth promoting rhizomicrobiome," Nature Communications, Nature, vol. 15(1), pages 1-14, December.

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