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. A combination of high humidity and bacterial effectors, such as Pseudomonas syringae HopM1, creates an aqueous environment in the apoplast of immunodeficient Arabidopsis thaliana that allows non-pathogenic P. syringae strains to become virulent pathogens. High humidity has a profound influence on the development of numerous plant diseases in crop fields and natural ecosystems, but the molecular basis of this humidity effect is not understood. Sheng Yang He and colleagues show that plant pathogens such as Pseudomonas syringae actively establish an aqueous leaf apoplast—that is, a space between the cells and the cell walls—in a humidity-dependent manner through the secretion of conserved bacterial effectors. The effectors also cause alterations in the leaf-associated microbiota. This is a crucial step in plant infection by bacteria and the effectors involved are sufficient to transform non-pathogenic strains into virulent pathogens only under high humidity. Through elegant genetics work, the authors define immune suppression and aqueous apoplast formation as the minimal set of host processes required for bacterial pathogenesis in plant leaves.

Bacteria establish an aqueous living space in plants crucial for virulence