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Abstract

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.