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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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.
Extended data figures
Extended data tables
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.
About this article
Nature Reviews Microbiology (2018)