Towards integrative plant pathology.

The field of plant pathology has revealed many of the mechanisms underlying the arms race, providing crucial knowledge and genetic resources for improving plant health. Although the host-microbe interaction seemingly favors rapidly evolving pathogens, it has also generated a vast evolutionary history of largely unexplored plant immunodiversity. We review studies that characterize the scope and distribution of genetic and ecological diversity in model and non-model systems with specific reference to pathogen effector diversity, plant immunodiversity in both cultivated species and their wild relatives, and diversity in the plant-associated microbiota. We show how the study of evolutionary and ecological processes can reveal patterns of genetic convergence, conservation, and diversification, and that this diversity is increasingly tractable in both experimental and translational systems. Perhaps most importantly, these patterns of diversity provide largely untapped resources that can be deployed for the rational engineering of durable resistance for sustainable agriculture.

Cooperative virulence via the collective action of secreted pathogen effectors.

Although virulence is typically attributed to single pathogenic strains, here we investigated whether effectors secreted by a population of non-virulent strains could function as public goods to enable the emergence of collective virulence. We disaggregated the 36 type III effectors of the phytopathogenic bacterium Pseudomonas syringae strain PtoDC3000 into a 'metaclone' of 36 coisogenic strains, each carrying a single effector in an effectorless background. Each coisogenic strain was individually unfit, but the metaclone was collectively as virulent as the wild-type strain on Arabidopsis thaliana, suggesting that effectors can drive the emergence of cooperation-based virulence through their public action. We show that independently evolved effector suits can equally drive this cooperative behaviour by transferring the effector alleles native to the strain PmaES4326 into the conspecific but divergent strain PtoDC3000. Finally, we transferred the disaggregated PtoDC3000 effector arsenal into Pseudomonas fluorescens and show that their cooperative action was sufficient to convert this rhizosphere-inhabiting beneficial bacterium into a phyllosphere pathogen. These results emphasize the importance of microbial community interactions and expand the ecological scale at which disease may be attributed.

Comparative genomic insights into the epidemiology and virulence of plant pathogenic pseudomonads from Turkey.

Pseudomonas is a highly diverse genus that includes species that cause disease in both plants and animals. Recently, pathogenic pseudomonads from the Pseudomonas syringae and Pseudomonas fluorescens species complexes have caused significant outbreaks in several agronomically important crops in Turkey, including tomato, citrus, artichoke and melon. We characterized 169 pathogenic Pseudomonas strains associated with recent outbreaks in Turkey via multilocus sequence analysis and whole-genome sequencing, then used comparative and evolutionary genomics to characterize putative virulence mechanisms. Most of the isolates are closely related to other plant pathogens distributed among the primary phylogroups of P. syringae, although there are significant numbers of P. fluorescens isolates, which is a species better known as a rhizosphere-inhabiting plant-growth promoter. We found that all 39 citrus blast pathogens cluster in P. syringae phylogroup 2, although strains isolated from the same host do not cluster monophyletically, with lemon, mandarin orange and sweet orange isolates all being intermixed throughout the phylogroup. In contrast, 20 tomato pith pathogens are found in two independent lineages: one in the P. syringae secondary phylogroups, and the other from the P. fluorescens species complex. These divergent pith necrosis strains lack characteristic virulence factors like the canonical tripartite type III secretion system, large effector repertoires and the ability to synthesize multiple bacterial phytotoxins, suggesting they have alternative molecular mechanisms to cause disease. These findings highlight the complex nature of host specificity among plant pathogenic pseudomonads.

The ETS-ETI cycle: evolutionary processes and metapopulation dynamics driving the diversification of pathogen effectors and host immune factors.

The natural diversity of pathogen effectors and host immune components represents a snapshot of the underlying evolutionary processes driving the host-pathogen arms race. In plants, this arms race is manifested by an ongoing cycle of disease and resistance driven by pathogenic effectors that promote disease (effector-triggered susceptibility; ETS) and plant resistance proteins that recognize effector activity to trigger immunity (effector-triggered immunity; ETI). Here we discuss how this ongoing ETS-ETI cycle has shaped the natural diversity of both plant resistance proteins and pathogen effectors. We focus on the evolutionary forces that drive the diversification of the molecules that determine the outcome of plant-pathogen interactions and introduce the concept of metapopulation dynamics (i.e., the introduction of genetic variation from conspecific organisms in different populations) as an alternative mechanism that can introduce and maintain diversity in both host and pathogen populations.