Convergent Targeting of a Common Host Protein-Network by Pathogen Effectors from Three Kingdoms of Life

While conceptual principles governing plant immunity are becoming clear, its systems-level organization and the evolutionary dynamic of the host-pathogen interface are still obscure. We generated a systematic protein-protein interaction network of virulence effectors from the ascomycete pathogen Golovinomyces orontii and Arabidopsis thaliana host proteins. We combined this data set with corresponding data for the eubacterial pathogen Pseudomonas syringae and the oomycete pathogen Hyaloperonospora arabidopsidis. The resulting network identifies host proteins onto which intraspecies and interspecies pathogen effectors converge. Phenotyping of 124 Arabidopsis effector-interactor mutants revealed a correlation between intraspecies and interspecies convergence and several altered immune response phenotypes. Several effectors and the most heavily targeted host protein colocalized in subnuclear foci. Products of adaptively selected Arabidopsis genes are enriched for interactions with effector targets. Our data suggest the existence of a molecular host-pathogen interface that is conserved across Arabidopsis accessions, while evolutionary adaptation occurs in the immediate network neighborhood of effector targets. [Display omitted] •Powdery mildew fungus G. orontii virulence effectors and their host-interactors identified•Integrated network map reveals interspecies effector convergence onto shared host proteins•Mutants of convergent effector-targeted host proteins display altered infection phenotypes•Host genes under balancing selection encode indirect targets of pathogen effectors Pathogens manipulate hosts by delivering effector proteins to their cell interior. Using a network analysis approach, Weßling et al. demonstrate that effectors from evolutionarily diverse plant pathogens repeatedly target evolutionary constrained host proteins. Evolutionary adaptation is not detectable for direct targets but rather in the immediate network neighborhood of effector-targeted host-proteins.