Article | Published:

Bacteria establish an aqueous living space in plants crucial for virulence

Nature volume 539, pages 524529 (24 November 2016) | Download Citation

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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.

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Acknowledgements

We thank He laboratory members for insightful discussions and constructive suggestions. We thank J. Kremer for help with setting up real-time disease imaging experiments and advice on 16S rRNA amplicon sequencing, K. Sugimoto for providing tomato plants (cv. Castlemart), and C. Thireault for technical help. This project was supported by funding from Gordon and Betty Moore Foundation (GBMF3037), National Institutes of Health (GM109928) and the Department of Energy (the Chemical Sciences, Geosciences, and Biosciences Division, Office of Basic Energy Sciences, Office of Science; DE–FG02–91ER20021 for infrastructural support). C.Z. acknowledges support from The Gatsby Charitable Foundation.

Author information

Author notes

    • Jian Yao

    Present address: Department of Biological Sciences, Western Michigan University, Kalamazoo, Michigan 49008, USA.

Affiliations

  1. Department of Energy, Plant Research Laboratory, Michigan State University, East Lansing, Michigan 48824, USA

    • Xiu-Fang Xin
    • , Kinya Nomura
    • , Kyaw Aung
    • , André C. Velásquez
    • , Jian Yao
    •  & Sheng Yang He
  2. Howard Hughes Medical Institute—Gordon and Betty Moore Foundation, Michigan State University, East Lansing, Michigan 48824, USA

    • Kyaw Aung
    •  & Sheng Yang He
  3. The Sainsbury Laboratory, Norwich Research Park, Norwich NR4 7UH, UK

    • Freddy Boutrot
    •  & Cyril Zipfel
  4. Department of Botany and Plant Pathology and Center for Genome Research and Biocomputing, Oregon State University, Corvallis, Oregon 97331, USA

    • Jeff H. Chang
  5. Department of Plant Biology, Michigan State University, East Lansing, Michigan 48824, USA

    • Sheng Yang He
  6. Plant Resilience Institute, Michigan State University, East Lansing, Michigan 48824, USA

    • Sheng Yang He

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Contributions

X.-F.X., K.N. and S.Y.H. designed the experiments. K.A. performed the Pst-DC3000–lux imaging experiment. A.C.V. performed biological repeats of bacterial infection experiments shown in Fig. 1a. J.Y. characterized an unpublished plant mutant line. X.-F.X. and K.N. performed all other experiments, including bacterial infections, protein blotting and generation of Arabidopsis mfec and mbbc mutant lines. F.B. and C.Z. contributed unpublished plant mutant materials. J.H.C. contributed unpublished Pst-DC3000 effector constructs. X.-F.X. and S.Y.H. wrote the manuscript with input from all co-authors.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Sheng Yang He.

Reviewer Information

Nature thanks G. Beattie, S. Lindow, J.-M. Zhou and the other anonymous reviewer(s) for their contribution to the peer review of this work.

Extended data

Supplementary information

PDF files

  1. 1.

    Supplementary Figure 1

    This file contains uncropped gel/blot images. The red boxes indicate cropped sections that are used in the Figures and Extended Data Figures. Diagram in a indicates how the two gel blots in b and c were generated.

Videos

  1. 1.

    The process of Pst DC3000 infection of Arabidopsis plants.

    Five-week-old Col-0 plants were dip-inoculated with Pst DC3000 at 1x108 cfu/ml. Plants were kept under high humidity (~95%) and the disease symptoms were recorded over 4 days. The process was sped up by 8,640-fold (24 h to 10 seconds). The recording started 7 h after inoculation and the red arrow indicates one leaf, as an example, that showed the transient appearance of water soaking.

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DOI

https://doi.org/10.1038/nature20166

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