Genomic Analysis of the Kiwifruit Pathogen Pseudomonas syringae pv. actinidiae Provides Insight into the Origins of an Emergent Plant Disease

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.

Author Summary

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.