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.

Genetic diversity ofPseudomonas syringaepv.actinidiae, pathogen of kiwifruit bacterial canker

“… It has been clarified that biovar 3 had been diversifying for a long time in China, and besides the pandemic lineage, which had spread worldwide, there exist diverse native strains of biovar 3 in China (McCann et al ., ). The characteristics confirmed in the pandemic lineage are shown in this table. …”

“…Moreover, it is also confirmed that the genetic diversity of these domestic biovar 1 strains is relatively large (Fig. ; Sawada et al ., ; McCann et al ., ). On the other hand, in addition to Japan, a small number of biovar 1 strains have also been detected in kiwifruit in Italy and Korea (a strain derived from Italy is indicated by the stars in Figures and ) (Mazzaglia et al ., ; Scortichini et al ., ; Cameron & Sarojini, ; Ciarroni et al ., ; McCann et al ., ).…”

“…It has been clarified that biovar 3 had been diversifying over a long period of time in China, the pandemic lineage that spread from China to various parts of the world is part of biovar 3, and there are diverse native strains in China besides the pandemic lineage (McCann et al ., ). In the biovar 3 cluster in Figure , the strains belonging to the pandemic lineage are densely assembled as a monophyletic group, whereas the Chinese native strains constitute a paraphyletic group whose variation is relatively large.…”

“…With regard to biovar 3, which has strong virulence and has become a major problem in various countries around the world, research using comparative genome analysis has been particularly intensively conducted. Based on the results, the biovar 3 strains currently distributed worldwide (hereafter referred to as ‘pandemic lineage’) were found to have been transmitted from China (Gallipoli et al ., ; Ciarroni et al ., ; McCann et al ., ; Vanneste, ). After biovar 3 strains had diversified over a long period of time in China, kiwifruit material, such as seedlings, scions and pollen, latently infected/contaminated with some strains of the pandemic lineage, have spread extensively due to exports from China that have increased rapidly in recent years, leading to the global spread of infection (pandemic) of Psa (Balestra et al ., ; Butler et al ., ; Cunty et al ., ; McCann et al ., ).…”

“…Biovar 3 is the causative agent that brought about the pandemic of kiwifruit bacterial canker disease, and because of its strong virulence (Fig. ), great damage has been reported in various parts of the world (McCann et al ., ; Vanneste, ; CABI, ). Biovar 3 was first found in central Italy in 2008, but subsequently expanded to other parts of Italy within a few years.…”