Nonagricultural reservoirs contribute to emergence and evolution of Pseudomonas syringae crop pathogens

Abstract

SummaryWhile the existence of environmental reservoirs of human pathogens is well established, less is known about the role of nonagricultural environments in emergence, evolution, and spread of crop pathogens.Here, we analyzed phylogeny, virulence genes, host range, and aggressiveness of Pseudomonas syringae strains closely related to the tomato pathogen P. syringae pv. tomato (Pto), including strains isolated from snowpack and streams.The population of Pto relatives in nonagricultural environments was estimated to be large and its diversity to be higher than that of the population of Pto and its relatives on crops. Ancestors of environmental strains, Pto, and other genetically monomorphic crop pathogens were inferred to have frequently recombined, suggesting an epidemic population structure for P. syringae. Some environmental strains have repertoires of type III-secreted effectors very similar to Pto, are almost as aggressive on tomato as Pto, but have a wider host range than typical Pto strains.We conclude that crop pathogens may have evolved through a small number of evolutionary events from a population of less aggressive ancestors with a wider host range present in nonagricultural environments.

A User's Guide to a Data Base of the Diversity of Pseudomonas syringae and Its Application to Classifying Strains in This Phylogenetic Complex

“…Genomic studies have shown that among all phylogroups, strains of phylogroup 1 have the greatest number of Type Three Effector (T3E) genes coding for virulence determinants [25], [33] (Table 3). More recently, Monteil and coworkers [34] demonstrated that strains closely related to the tomato speck pathogen P. s. pv. tomato isolated from snowpack and streams harbor the T3E genes found in epidemic strains.…”

“…Using combinations of phenotypic tests according to Table S10 could be a means to attempt to classify strains of P. syringae with the known and traditional limitations of the use of phenotypic methods. A more accurate method of identification is often needed for specific epidemics or for diseases caused by a diversity of P. syringae strains in some cases from multiple phylogroups [34], [49]–[52]. Phenotypic criteria used during the screening of strains can markedly limit the diversity revealed in ecological or epidemiological studies.…”

“…The originality of this data base is the information about strains isolated outside of agricultural contexts and from many different substrates beyond plants. It provides a broader vision of the perimeter of the P. syringae group and leads to the elaboration of new hypotheses on ecology of this group and disease emergence [32], [34]. The method we used to establish the framework for P. syringae classification is based on standard MLST, recognized as being reliable for many bacterial species and first proposed in 1998 by Maiden and colleagues [55].…”

Population-genomic insights into emergence, crop adaptation and dissemination of Pseudomonas syringae pathogens

“…aptata ( Pap ) have a broad host range, infecting various plant families (Morris et al , 2000; Berge et al , 2014). In the case of Pto , MLSA revealed the existence of closely related isolates from natural freshwater sources and recombination events between these environmental isolates, Pto and other crop pathogens (Monteil et al , 2013). The environmental lineages were found to be equipped with some of the same virulence genes as the crop pathogen Pto , in particular genes coding for type III secretion (T3S) effectors, the best studied and most important class of virulence genes in P. syringae (Lindeberg et al , 2008).…”

“…The environmental lineages were found to be equipped with some of the same virulence genes as the crop pathogen Pto , in particular genes coding for type III secretion (T3S) effectors, the best studied and most important class of virulence genes in P. syringae (Lindeberg et al , 2008). Moreover, the environmental isolates had a wider host range than Pto but were less virulent on tomato (Monteil et al , 2013). Taken together, these results are consistent with the evolution of highly virulent crop pathogens with a relatively narrow host range from a population of ancestors with a wider host range.…”