Pseudomonas syringae pv. actinidiae: a re-emerging, multi-faceted, pandemic pathogen

Abstract

Pseudomonas syringae pv. actinidiae is the causal agent of bacterial canker of green-fleshed kiwifruit (Actinidia deliciosa) and yellow-fleshed kiwifruit (A. chinensis). A recent, sudden, re-emerging wave of this disease has occurred, almost contemporaneously, in all of the main areas of kiwifruit production in the world, suggesting that it can be considered as a pandemic disease. Recent in-depth genetic studies performed on P. syringae pv. actinidiae strains have revealed that this pathovar is composed of four genetically different populations which, to different extents, can infect crops of the genus Actinidia worldwide. Genome comparisons of these strains have revealed that this pathovar can gain and lose the phaseolotoxin gene cluster, as well as mobile genetic elements, such as plasmids and putative prophages, and that it can modify the repertoire of the effector gene arrays. In addition, the strains currently causing worldwide severe economic losses display an extensive set of genes related to the ecological fitness of the bacterium in planta, such as copper and antibiotic resistance genes, multiple siderophore genes and genes involved in the degradation of lignin derivatives and other phenolics. This pathogen can therefore easily colonize hosts throughout the year.

Taxonomy: Bacteria; Proteobacteria, gamma subdivision; Order Pseudomonadales; Family Pseudomonadaceae; Genus Pseudomonas; Pseudomonas syringae species complex, genomospecies 8; Pathovar actinidiae.

Microbiological properties: Gram-negative, aerobic, motile, rod-shaped, polar flagella, oxidase-negative, arginine dihydrolase-negative, DNA 58.5-58.8 mol.% GC, elicits the hypersensitive response on tobacco leaves.

Host range: Primarily studied as the causal agent of bacterial canker of green-fleshed kiwifruit (Actinidia deliciosa), it has also been isolated from yellow-fleshed kiwifruit (A. chinensis). In both species, it causes severe economic losses worldwide. It has also been isolated from wild A. arguta and A. kolomikta.

Disease symptoms: In green-fleshed and yellow-fleshed kiwifruits, the symptoms include brown-black leaf spots often surrounded by a chlorotic margin, blossom necrosis, extensive twig die-back, reddening of the lenticels, extensive cankers along the main trunk and leader, and bleeding cankers on the trunk and the leader with a whitish to orange ooze.

Epidemiology: Pseudomonas syringae pv. actinidiae can effectively colonize its host plants throughout the year. Bacterial exudates can disperse a large amount of inoculum within and between orchards. In the spring, temperatures ranging from 12 to 18 °C, together with humid conditions, can greatly favour the multiplication of the bacterium, allowing it to systemically move from the leaf to the young shoots. During the summer, very high temperatures can reduce the multiplication and dispersal of the bacterium. Some agronomical techniques, as well as frost, wind, rain and hail storms, can contribute to further spreading.

Disease control: An integrated approach that takes into consideration precise scheduled spray treatments with effective and environmentally friendly bactericides and equilibrated plant nutrition, coupled with preventive measures aimed at drastically reducing the bacterial inoculum, currently seems to be the possible best solution for coexistence with the disease. The development of resistant cultivars and pollinators, effective biocontrol agents, including bacteriophages, and compounds that induce the systemic activation of plant defence mechanisms is in progress.

Useful websites: Up-to-date information on bacterial canker research progress and on the spread of the disease in New Zealand can be found at: http://www.kvh.org.nz. Daily information on the spread of the disease and on the research being performed worldwide can be found at: http://www.freshplaza.it.

Figure 1

Genealogy of Pseudomonas strains of genomospecies 8 sensu Gardan et al. (1999): P. avellanae, P. syringae pv. theae and P. s. pv. actinidiae. (A) A maximum likelihood tree resulting from the analysis of the concatenation of 171 open reading frames (ORFs). (B) An alternative genealogical hypothesis with the constraint of the common origin of the Italian P. s. pv. actinidiae strain that was rejected by the monophyly test. Psa, P. s. pv. actinidiae; J, NCPPB3739 from Japan, isolated in 1984; I, NCPPB3871 from Italy, isolated in 1992; I2, CRA‐FRU 8.43 from Italy, isolated in 2008. The National Collection of Plant Pathogenic Bacteria (NCPPB) strains are representative of past outbreaks, whereas CRA‐FRU 8.43 has been isolated in the recent pandemic. [From Marcelletti et al. (2011).]

Figure 2

Repetitive‐sequence polymerase chain reaction (PCR) (A, BOX‐PCR; B, ERIC‐PCR) fingerprint patterns for genomic DNAs of Pseudomonas syringae pv. actinidiae strains isolated in central Italy from Actinidia chinensis and A. deliciosa during 2008–2009, compared with strains of past outbreaks of bacterial canker of kiwifruit in Japan (1984) and Italy (1992). [From Ferrante and Scortichini (2010).] The arrows indicate the bands enabling the visible differentiation of the two populations.

Figure 3

Venn diagram of the type III effector gene complements of sequenced Pseudomonas syringae pv. actinidiae strains based on the comparison of the same complement of other sequenced plant pathogenic pseudomonads. The genes conserved among the three strains are indicated in the middle of the diagram. Strains of past (NCPPB3739 from Japan and NCPPB3871 from Italy) and current (CRA‐FRU 8.43) epidemics of bacterial canker display four unique different effector genes. [From Marcelletti et al. (2011).]

Figure 4

Cycle of disease of Pseudomonas syringae pv. actinidiae on Actinidia deliciosa and A. chinenis, as observed in Italy in areas characterized by a Mediterranean climate. In the middle of the panel, some agronomical techniques are indicated (i.e. winter pruning, tying of twigs, irrigation tube scraping the main young trunk) which dramatically enhance the possibility of plant colonization of the pathogen through the wounds. Frost is retained as a fundamental predisposing factor.