Origin and Evolution of the Kiwifruit Canker Pandemic

Abstract

Recurring epidemics of kiwifruit (Actinidia spp.) bleeding canker disease are caused by Pseudomonas syringae pv. actinidiae (Psa). In order to strengthen understanding of population structure, phylogeography, and evolutionary dynamics, we isolated Pseudomonas from cultivated and wild kiwifruit across six provinces in China. Based on the analysis of 80 sequenced Psa genomes, we show that China is the origin of the pandemic lineage but that strain diversity in China is confined to just a single clade. In contrast, Korea and Japan harbor strains from multiple clades. Distinct independent transmission events marked introduction of the pandemic lineage into New Zealand, Chile, Europe, Korea, and Japan. Despite high similarity within the core genome and minimal impact of within-clade recombination, we observed extensive variation even within the single clade from which the global pandemic arose.

Keywords: bacterial plant pathogen; disease emergence; genomic epidemiology; pathogen evolution; plant-microbe interactions.

Fig. 1.—

Phylogeny of Psa. RaxML Maximum likelihood tree based on 1,059,722bp nonrecombinant core genome alignment including 2,953 variant sites. FigTree was used for phylogeny visualization. All nodes displayed have bootstrap support values above 50% (50–75% in green, 76–100% in blue). Host (H) and country (C) of isolation is displayed in the first and second column, respectively. Clade designations are shown at right.

Fig. 2.—

Phylogeny of Psa-3. (A) RaxML Maximum likelihood tree based on 4,853,155bp nonrecombinant core genome alignment including 1,948 variant sites. FigTree was used for phylogeny visualization. All nodes displayed have bootstrap support values above 55% (55–80% in green, 81–100% in blue). The asterisk denotes the pandemic lineage. Integrative and conjugative element (ICE) presence; province (China) or country and year of isolation shown at right, followed by presence/absence matrix of all core and accessory genes. (B) The core and flexible genome of Psa-3. Parenthetical numbers represent the number of strains in the core, soft-core, shell, and cloud genomes. (C) Polymorphisms and recombinant regions mapped onto Psa NZ13 reference genome using CIRCOS (Krzywinski et al. 2009). Psa NZ13 CDS are displayed in the first and second ring (blue), with annotated Type 3 secretion system and effectors highlighted (red). Inner rings display polymorphisms in Psa-3 genomes ordered from most to least divergent relative to Psa NZ13. The most polymorphic region corresponds to the location of the integrative and conjugative element (ICE) in Psa NZ13.

Fig. 3.—

Psa isolation locations in East Asia. Markers correspond to location of isolation. Color corresponds to the isolate membership in each clade according to the phylogeny displayed in fig. 1. Only isolates for which the specific location of isolation is known are displayed here.