The origins of crop diseases are linked to domestication of plants. Most crops were domesticated centuries – even millennia – ago, thus limiting opportunity to understand the concomitant emergence of disease. Kiwifruit (Actinidia spp.) is an exception: domestication began in the 1930s with outbreaks of canker disease caused by P. syringae pv. actinidiae (Psa) first recorded in the 1980s. Based on SNP analyses of two circularized and 34 draft genomes, we show that Psa is comprised of distinct clades exhibiting negligible within-clade diversity, consistent with disease arising by independent samplings from a source population. Three clades correspond to their geographical source of isolation; a fourth, encompassing the Psa-V lineage responsible for the 2008 outbreak, is now globally distributed. Psa has an overall clonal population structure, however, genomes carry a marked signature of within-pathovar recombination. SNP analysis of Psa-V reveals hundreds of polymorphisms; however, most reside within PPHGI-1-like conjugative elements whose evolution is unlinked to the core genome. Removal of SNPs due to recombination yields an uninformative (star-like) phylogeny consistent with diversification of Psa-V from a single clone within the last ten years. Growth assays provide evidence of cultivar specificity, with rapid systemic movement of Psa-V in Actinidia chinensis. Genomic comparisons show a dynamic genome with evidence of positive selection on type III effectors and other candidate virulence genes. Each clade has highly varied complements of accessory genes encoding effectors and toxins with evidence of gain and loss via multiple genetic routes. Genes with orthologs in vascular pathogens were found exclusively within Psa-V. Our analyses capture a pathogen in the early stages of emergence from a predicted source population associated with wild Actinidia species. In addition to candidate genes as targets for resistance breeding programs, our findings highlight the importance of the source population as a reservoir of new disease. Despite considerable scientific advances in plant protection during the last century, agricultural crops remain vulnerable to infection by pathogens. The intensive cultivation particularly of clonally propagated crop plants increases the potential for the emergence and rapid spread of new diseases. Pseudomonas syringae pv. actinidiae was first reported as a canker-causing pathogen of kiwifruit in the mid-1980s. However, a new outbreak of the disease occurred in 2008 and this strain has spread rapidly throughout growing regions of the world. In order to determine the origin, population structure and defining features of this pathogen, a large-scale sequencing project was established. This clarified the phylogenetic relationships between the different Psa isolates and identified the outbreak-specific gene sets associated with the aggressive systemic infection strategy exhibited by the virulent strain. This information is invaluable in developing robust long-term solutions for this serious disease. Given that kiwifruit production on a commercial scale is a relatively recent event, this analysis provides a unique insight into the evolution of this pathogen with its host, from its first emergence to the latest global outbreak. This understanding should aid in the mitigation of devastating outbreaks in the future.

The introduction of Pseudomonas syringae pv. actinidiae (Psa) severely damaged the New Zealand kiwifruit industry, which in 2010 was based on only two cultivars. Despite an extraordinarily quick and strong response by industry, government, and scientists to minimize the economic and social impacts, the economic consequences of this outbreak were severe. Although our understanding of Psa epidemiology and control methods increased substantively over the past six years, the kiwifruit industry largely recovered because of the introduction of a less-susceptible yellow-fleshed cultivar. The New Zealand population of Psa is clonal but has evolved rapidly since its introduction by exchanging mobile genetic elements, including integrative conjugative elements (ICEs), with the local bacterial populations. In some cases, this has led to copper resistance. It is currently believed that the center of origin of the pathogen is Japan or Korea, but biovar 3, which is responsible for the global outbreak, originated in China.

Pseudomonas syringae pv. actinidiae, the causal agent of canker in kiwifruit (Actinidia spp.) vines, was first detected in Japan in 1984, followed by detections in Korea and Italy in the early 1990s. Isolates causing more severe disease symptoms have recently been detected in several countries with a wide global distribution, including Italy, New Zealand, and China. In order to characterize P. syringae pv. actinidiae populations globally, a representative set of 40 isolates from New Zealand, Italy, Japan, South Korea, Australia, and Chile were selected for extensive genetic analysis. Multilocus sequence analysis (MLSA) of housekeeping, type III effector and phytotoxin genes was used to elucidate the phylogenetic relationships between P. syringae pv. actinidiae isolates worldwide. Four additional isolates, including one from China, for which shotgun sequence of the whole genome was available, were included in phylogenetic analyses. It is shown that at least four P. syringae pv. actinidiae MLSA groups are present globally, and that marker sets with differing evolutionary trajectories (conserved housekeeping and rapidly evolving effector genes) readily differentiate all four groups. The MLSA group designated here as Psa3 is the strain causing secondary symptoms such as formation of cankers, production of exudates, and cane and shoot dieback on some kiwifruit orchards in Italy and New Zealand. It is shown that isolates from Chile also belong to this MLSA group. MLSA group Psa4, detected in isolates collected in New Zealand and Australia, has not been previously described. P. syringae pv. actinidiae has an extensive global distribution yet the isolates causing widespread losses to the kiwifruit industry can all be traced to a single MLSA group, Psa3.

Pseudomonas syringae pv. actinidiae, the causal agent of bacterial canker of kiwifruit, was detected for the first time in New Zealand in November 2010. Only in Bay of Plenty, one of the four regions where this pathogen had been detected, did symptoms evolve beyond leaf spots, resulting in cane die-back, wilting of canes, and canker, sometimes leading to death of the vine. Molecular analysis (cts haplotype and BOX-polymerase chain reaction [PCR] electrophoretic pattern) of strains isolated from different regions of New Zealand revealed that two biovars could be distinguished. They have been called biovar 3 and biovar 4 to differentiate them from strains from Japan (biovar 1) or Korea (biovar 2), which have a different cts haplotype or a different BOX-PCR pattern. Biovars 3 and 4 displayed different degrees of virulence, as measured by their ability to cause leaf spots on young, potted kiwifruit plants. Biovar 3, which has also been present in Italy since 2008 and in France, was found in the Bay of Plenty, where cane diebacks were observed. In contrast, no symptoms other than leaf spots have been observed in orchards where strains of biovar 4 have been isolated. We report the distribution and the disease progression of biovars 3 and 4 in New Zealand.

Nonhost environmental reservoirs of pathogens play key roles in their evolutionary ecology and in particular in the evolution of pathogenicity. In light of recent reports of the plant pathogen Pseudomonas syringae in pristine waters outside agricultural regions and its dissemination via the water cycle, we have examined the genetic and phenotypic diversity, population structure, and biogeography of P. syringae from headwaters of rivers on three continents and their phylogenetic relationship to strains from crops. A collection of 236 strains from 11 sites in the United States, in France, and in New Zealand was characterized for genetic diversity based on housekeeping gene sequences and for phenotypic diversity based on measures of pathogenicity and ice nucleation activity. Phylogenetic analyses revealed several new genetic clades from water. The genetic structure of P. syringae populations was not influenced by geographic location or water chemistry, whereas the phenotypic structure was affected by these parameters. Comparison with strains from crops revealed that the metapopulation of P. syringae is structured into three genetic ecotypes: a crop-specific type, a water-specific type, and an abundant ecotype found in both habitats. Aggressiveness of strains was significantly and positively correlated with ice nucleation activity. Furthermore, the ubiquitous genotypes were the most aggressive, on average. The abundance and diversity in water relative to crops suggest that adaptation to the freshwater habitat has played a nonnegligible role in the evolutionary history of P. syringae . We discuss how adaptation to the water cycle is linked to the epidemiological success of this plant pathogen. IMPORTANCE Many pathogens have life cycles that involve survival and multiplication in nonhost environmental habitats. For human pathogens, numerous studies have revealed how adaptation to environmental habitats is linked to the evolution of their pathogenicity and emergence of pathogens. For plant pathogens, the link between adaptation to nonhost habitats and pathogenicity has not been explored. Here we have examined the genetic and phenotypic diversity of the plant pathogen Pseudomonas syringae in headwaters of rivers on three continents and compared it to that of strains from crops. This model pathogen was chosen because it is widely abundant in habitats associated with the water cycle and in particular in pristine waters outside agricultural regions. This work reveals that there is considerable exchange of populations between freshwater and agricultural habitats and that those in the former contribute considerably to the diversification of P. syringae .