|MONTEIL, CAROLINE - Swansea University|
|YAHARA, KOJI - National Institute Of Infectious Diseases|
|STUDHOLME, DAVID - University Of Exeter|
|MAGEIROS, LEONARDIS - Swansea University|
|MERIC, GUILLAUME - Swansea University|
|MORRIS, CINDY - Inra, Génétique Animale Et Biologie Intégrative , Jouy-En-josas, France|
|VINATZER, BORIS - Virginia Tech|
|SHEPPARD, SAMUEL - Swansea University|
Submitted to: PLoS Pathogens
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/13/2016
Publication Date: 10/21/2016
Citation: Swingle, B.M., Monteil, C.L., Yahara, K., Studholme, D.J., Mageiros, L., Meric, G., Morris, C.E., Vinatzer, B.A., Sheppard, S.K. 2016. Population genomic insights into the emergence, crop-adaptation and dissemination of Pseudomonas syringae pathogens. PLoS Pathogens. 2(10):e000089.
Interpretive Summary: Just as with human diseases, new crop diseases emerge without warning and sometimes spread rapidly around the globe causing devastation. Where these pathogens originally came from is often unknown. The bacterial species Pseudomonas syringae consists of a group of genetically diverse bacteria including strains that are devastating crop pathogens as well as strains isolated from wild plants and components of the water cycle, such as clouds, rain and fresh water. The existence of these environmental strains that are closely related to crop pathogens suggests that crop pathogenic P. syringae possibly emerged from a diverse P. syringae population that pre-existed in the environment even before the dawn of agriculture. Here we found evidence for this hypothesis by sequencing and comparing the genomes of crop pathogenic and environmental strains; we inferred their evolutionary relationships, and identified genes with putative key roles in emergence of crop disease.
Technical Abstract: Although pathogen strains that cause disease outbreaks are often well characterized, relatively little is known about the reservoir populations from which they emerge. Genomic comparison of outbreak strains with isolates of reservoir populations can give new insight into mechanisms of disease emergence. Pseudomonas syringae sensu lato is an ideal model to study disease emergence because it is a genetically diverse group of bacteria that comprises crop pathogens as well as closely related environmental isolates found in wild plants and in components of the water cycle. Here, we compared genome sequences of 45 P. syringae crop pathogen outbreak strains with 69 closely related environmental isolates. Phylogenetic reconstruction revealed that crop pathogens emerged many times independently from environmental populations. Population structure analysis showed that crop pathogens and environmental populations have not separated from each other suggesting that emergence events occurred recently. Unexpectedly, differences in gene content between environmental populations and outbreaks strains were minimal with most known virulence genes present in both. However, a genome-wide association study identified a small group of genes, including the type III effector genes hopQ1 and hopD1, to be associated with crop pathogens, but not with environmental populations, suggesting that these two effectors may play an important role in crop disease. Intriguingly, analysis of recombination across the whole genome revealed that a gene predicted to confer antibiotic resistance has been frequently exchanged among lineages and thus may contribute to pathogen fitness. Finally, the finding that isolates from diseased crops and from components of the water cycle collected during a crop disease epidemic form a single population provides the strongest evidence yet that precipitation may be a so far overlooked inoculation source of disease epidemics caused by P. syringae.