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.

Origin of the Outbreak in France of Pseudomonas syringae pv. actinidiae Biovar 3, the Causal Agent of Bacterial Canker of Kiwifruit, Revealed by a Multilocus Variable-Number Tandem-Repeat Analysis

“…actinidiae biovar 3 in France and in Italy share the same origin. The recent outbreaks in Chile, Europe, and New Zealand could have three different origins (32). In the present study, we did not find any common haplotype for syringae pv.…”

“…Various genomic analyses have concluded that P. syringae pv. actinidiae biovar 3 remains a highly monomorphic pathogen at the genomic level (30)(31)(32).…”

“…This could support the hypothesis that the common ancestor of P. syringae pv. actinidiae biovar 3 strains could originate from China, which is the diversification area for kiwifruit as well (30)(31)(32)44).…”

“…actinidiae biovar 3 strains responsible for the current worldwide outbreaks are monophyletic, genomic analyses based on the accessory genome revealed diversity within these strains (30)(31)(32). P. syringae pv.…”

“…Examining the composition of genomic islands in P. syringae pv. actinidiae, such as integrative and conjugative element (ICE)-carrying genes involved in pathogenicity, revealed that strains isolated in Europe are very similar to each other and that epidemics in Europe may have a different source population than epidemics in New Zealand or Chile (30)(31)(32).…”