Pseudomonas syringae pv. actinidiae
(bacterial canker of kiwifruit)

Pictures

Picture	Title	Caption	Copyright
Title Symptoms Caption Pseudomonas syringae pv. actinidiae (bacterial canker of kiwifruit); symptoms, showing dieback. Copyright ©Joy L. Tyson	Symptoms	Pseudomonas syringae pv. actinidiae (bacterial canker of kiwifruit); symptoms, showing dieback.	©Joy L. Tyson
Title Symptoms Caption Pseudomonas syringae pv. actinidiae (bacterial canker of kiwifruit); symptoms, showing canker. Copyright ©Joy L. Tyson	Symptoms	Pseudomonas syringae pv. actinidiae (bacterial canker of kiwifruit); symptoms, showing canker.	©Joy L. Tyson
Title Symptoms Caption Pseudomonas syringae pv. actinidiae (bacterial canker of kiwifruit); symptoms, showing leafspots. Copyright ©Joy L. Tyson	Symptoms	Pseudomonas syringae pv. actinidiae (bacterial canker of kiwifruit); symptoms, showing leafspots.	©Joy L. Tyson
Title Symptoms Caption Pseudomonas syringae pv. actinidiae (bacterial canker of kiwifruit); symptoms, showing leafspots. Copyright ©Joy L. Tyson	Symptoms	Pseudomonas syringae pv. actinidiae (bacterial canker of kiwifruit); symptoms, showing leafspots.	©Joy L. Tyson
Title Symptoms Caption Pseudomonas syringae pv. actinidiae (bacterial canker of kiwifruit); symptoms, showing leafspots. Copyright ©Joy L. Tyson	Symptoms	Pseudomonas syringae pv. actinidiae (bacterial canker of kiwifruit); symptoms, showing leafspots.	©Joy L. Tyson
Title Symptoms Caption Pseudomonas syringae pv. actinidiae (bacterial canker of kiwifruit); symptoms, showing leafspots. Copyright ©Joy L. Tyson	Symptoms	Pseudomonas syringae pv. actinidiae (bacterial canker of kiwifruit); symptoms, showing leafspots.	©Joy L. Tyson
Title Symptoms Caption Pseudomonas syringae pv. actinidiae (bacterial canker of kiwifruit); symptoms, showing leafspots. Copyright ©Joy L. Tyson	Symptoms	Pseudomonas syringae pv. actinidiae (bacterial canker of kiwifruit); symptoms, showing leafspots.	©Joy L. Tyson
Title Symptoms Caption Pseudomonas syringae pv. actinidiae (bacterial canker of kiwifruit); symptoms, showing leafspots. Copyright ©Joy L. Tyson	Symptoms	Pseudomonas syringae pv. actinidiae (bacterial canker of kiwifruit); symptoms, showing leafspots.	©Joy L. Tyson
Title Symptoms Caption Pseudomonas syringae pv. actinidiae (bacterial canker of kiwifruit); symptoms, showing leafspots. Copyright ©Joy L. Tyson	Symptoms	Pseudomonas syringae pv. actinidiae (bacterial canker of kiwifruit); symptoms, showing leafspots.	©Joy L. Tyson

Identity

Preferred Scientific Name

• Pseudomonas syringae pv. actinidiae Takikawa, Serizawa, Ichikawa, Tsuyumu and Goto 1989

Preferred Common Name

• bacterial canker of kiwifruit

Summary of Invasiveness

Bacterial canker of kiwifruit, caused by Pseudomonas syringae pv. actinidiae (Psa), is a serious threat to kiwifruit production worldwide. At least four related but genetically distinct lineages of Psa are currently known, and more are likely to exist. In 2008, a particularly virulent strain emerged in Italy and spread rapidly to all main global kiwifruit production areas. This strain is variously referred to as the pandemic strain, PsaV or Biovar 3. Different Actinidia species and cultivars show varying susceptibility to Psa, and breeding resistant or tolerant kiwifruit varieties is highly important to the industry.

Like all pathovars of Pseudomonas syringae, Psa is present in infected plant material. Transfer of nursery material is a major source of long distance spread, while agronomic techniques such as pruning can contribute to spread within and between orchards. The pathogen can be dispersed in aerosols and can be carried between trees and adjacent orchards in wind-driven rain.

Psa is listed on the EPPO Alert List.

Taxonomic Tree

• Domain: Bacteria
•     Phylum: Proteobacteria
•         Class: Gammaproteobacteria
•             Order: Pseudomonadales
•                 Family: Pseudomonadaceae
•                     Genus: Pseudomonas
•                         Species: Pseudomonas syringae pv. actinidiae

Notes on Taxonomy and Nomenclature

The Pseudomonas syringae complex currently encompasses 57 different pathovars arranged into nine genomospecies, most of which are not yet formally described. Pseudomonas syringae pv. actinidiae (Psa) belongs to genomospecies 8 proposed by Gardan et al. (1999) and confirmed by Marcelletti and Scortichini (2014).

Although the global pattern of genotypic variation of Psa is unknown, several distinct populations have been characterised to date based on aggressiveness, genomic fingerprinting, 16SrDNA or ITS sequencing, multilocus sequence analysis (MLSA), production of toxins and presence of certain genes (EPPO, 2012b; Chapman et al., 2012; Vanneste et al, 2013; Cunty et al., 2014). They have been named in chronological order of detection:

Psa1: a systemic phaseolotoxin-producer described as 'moderately aggressive'. Psa1 is reported from Japan and was detected in Italy in the 1992 outbreak, but not during recent Italian epidemics.

Psa2: a systemic coronatine-producer described as 'moderately aggressive'. Psa2 is only reported from Korea. Psa1 and Psa2 have not been detected since 1998.

Psa3: a highly aggressive systemic pathogen that does not produce coronatine or phaseolotoxin. Psa3 is currently reported from Chile, China, Italy (2008-2009 outbreak) and other European countries, Japan, Korea and New Zealand. Psa3 is also referred to as PsaV or Biovar 3, and is the population responsible for the global pandemic first reported in Italy in 2008.

Psa4 (now reclassified as Pseudomonas syringae pv. actinidifoliorum): non-systemic (i.e. associated with leaf symptoms only) and showing low aggressiveness (Chapman et al., 2012; Vanneste et al., 2013; Cunty et al., 2014). This population was also referred to as Psa LV, but was subsequently redescribed and transferred to a new pathovar, P. syringae pv. actinidifoliorum. It is reported from Australia, France, New Zealand and Spain (Cunty et al., 2014; Abelleira et al., 2015).

Analyses of sequence data from multiple isolates has supported the view that the pandemic Psa populations in Italy and other parts of Europe, New Zealand and Chile all arose independently from a single clone that has spread rapidly around the world (McCann et al., 2013). The source population is probably China (Butler et al., 2013).

Several pseudomonad pathogens have been reported for kiwifruit including Pseudomonas syringae, Pseudomonas viridiflava and Pseudomonas sp. (genomovar savastanoi; Young et al., 1997).

Description

From Takikawa et al. (1989).

P. syringae pv. actinidiae is a Gram-negative, obligate aerobe, non-sporing rod. It occurs singly or in pairs or short chains and is motile by 1-3 polar flagella. Poly-ß-hydroxybutyrate granules are not accumulated.

Colonies on nutrient agar are translucent-white, slightly raised, glistening, and round. At 27°C colonies do not exceed 1 mm after 48 hours. On King's medium B, colonies are translucent and non-fluorescent under UV light, though Cunty et al. (2014) report some strains of Psa as being fluorescent. Growth factors are not required. The pathogen is in Group Ia of the LOPAT determinative scheme of Lelliott et al. (1966) being positive for levan production and the capacity to produce a hypersensitivity reaction in tobacco, and negative in tests for oxidase and arginine dihydrolase production and pectolytic activity.

Distribution Table

The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.

History of Introduction and Spread

P. syringae pv. actinidiae was described from Japan in the 1980s (Takikawa et al., 1989). It was first detected in Korea in 1988, and had also been known from China as early as 1984/1985 (Mazzaglia et al., 2012).

Psa was first reported outside Asia in Italy in 1992 (EPPO, 1993), where it remained sporadic and with a low incidence for 15 years (EPPO, 2010a). However, economic damage and spread caused by an aggressive population started in Italy during 2007/2008 (EPPO, 2010a). This aggressive population (also known as virulent strain or pandemic clade) was shown to differ from the Japanese and Korean strains, as well as from the Italian strains isolated in the past (which were not detected during the recent Italian epidemics). The bacterial canker disease caused by the virulent strain of Psa emerged almost contemporaneously in all main areas of kiwifruit production in the world and can be regarded as a pandemic. In 2009 Psa was first detected in Turkey (EPPO, 2012c); in 2010 it was detected in France (EPPO, 2010b) and also in New Zealand (EPPO, 2010c). In 2011 it was reported from Portugal (EPPO, 2011b), Chile (EPPO, 2011c), Switzerland (EPPO, 2011e) and Spain (EPPO, 2011f) and continued to spread in Italy (EPPO, 2011d).

Hosts/Species Affected

Observations in Italy by Ballestra et al. (2008) suggested that damage is more severe on Actinidia chinensis (i.e. yellow cvs. Hort 16A, Jin Tao and Soreli) but recent observations indicate that A. deliciosa (green cultivars cv. Hayward, Summerkiwi, Tsechelidis and Greenlight) show an equivalent sensibility. However, progression of the disease is quicker in A. chinensis. In France, both yellow and green cultivars are attacked but, as in Italy, damage is more severe on yellow cultivars. Field observations in Italy and New Zealand indicate that male vines often show symptoms before female vines and are more severely affected (Balestra, pers. comm., 2011). On the basis of  field observations in Italy 'Tomuri' male vines appear to be less susceptible than 'Matua' male vines (Balestra, personal communication, 2011). P. syringae pv. actinidiae has been detected on A. arguta in France (Vanneste et al., 2014) and has also been isolated from wild A. kolomikta in Italy (Scortichini et al., 2012).

Actinidia is not a unique host for P. syringae pv. actinidiae. Liu et al. (2016) have reported Alternanthera philoxeroides, Setaria italica and Paulownia fortunei as interhosts in China.

Host Plants and Other Plants Affected

Growth Stages

Symptoms

Canes

In spring, extending canes can become water-soaked and exude a pale, translucent to dark reddish coloured ooze from lenticels of apparently healthy tissue. Small (1-3 mm) cracks form above olive-coloured, water-soaked lesions and exude gum. Lesions elongate and whole canes become necrotic.

Leaves

In spring, small, water-soaked spots form on expanding leaves. These become brown and angular with bright, chlorotic halos. On lower surfaces, translucent gum may exude from stomata.

Flowers

Most infected floral buds become brown and wither without opening. They may exude translucent gum. Sepals can become infected. Heavy flower buds may drop.

Trunks and leaders

Symptoms of canker are first observed in mid-winter when small droplets of ooze are produced. In late winter ooze increases in quantity and becomes reddish brown. When vines break dormancy, canker symptoms are revealed by gum exudation from natural openings, from cracks in the bark, and from pruning cuts. Bark in these areas is dark and dissection reveals that necrosis extends in underlying tissue beyond the externally visible discoloration. Trunks and leaders may be girdled. Prolific suckering occurs below girdling cankers (Serizawa et al., 1989; Balestra et al., 2009).

List of Symptoms/Signs

Biology and Ecology

Life-Cycle

In spring and early summer, P. syringae pv. actinidiae develops in expanding shoots and leaves. Small cankers develop on extending vines, and leaves develop angular leaf spots surrounded by chlorotic haloes. In winter and early spring, extending cankers form on trunks and branches (Serizawa et al., 1994).

Epidemiology

Serizawa et al. (1989) noted that the damage associated with P. syringae pv. actinidiae occurs in two phases. One phase occurs in autumn/winter and involves damage to the main vine structure and overwintering canes. The other phase occurs in spring and involves the new season's growth (leaves, flowers and canes). The bacterium infects the host through stomata, hydathodes, lenticels, trychomes, leaf scars or wounds, and can progress to the roots where it overwinters (Mazzaglia et al., 2010; Renzi et al., 2012).

P. syringae pv. actinidiae is most invasive at relatively low temperatures (10-20°C; optimum 15±3°C). The optimum temperature for growth of P. syringae pv. actinidiae on new canes is 12-18°C (Serizawa and Ichikawa, 1993b). Temperatures above 20°C are less favourable to the bacterium and Serizawa and Ichikawa (1993b) observed no symptoms on plants in Japan at temperatures above 25°C. However, in France, Italy and Portugal, symptoms have been observed at temperatures above 25°C (GM Balestra, personal communication, 2011).

Like many other bacterial plant diseases, strong winds and heavy rainfall favour the disease. Strong winds during rain may both injure the plants and disperse the bacterial exudate to the wounds and/or natural openings (Serizawa et al., 1989). Winter frost and late frost ('spring frost') as well as hail also favour the occurrence of the disease.

Damage caused by P. syringae pv. actinidiae was found to increase when high populations of Pseudomonas syringae pv. syringae or P. viridiflava, two other bacterial pathogens of Actinidia sp., were present on the plants (Mazzaglia et al., 2010).

Psa is reported to colonise various plant parts epiphytically. Stefani and Giovanardi (2011) demonstrated that populations were able to survive for 21 weeks on leaves. They also isolated Psa from flowers, where colonisation was observed to be more effective than on leaves. Psa has also been isolated from asymptomatic twigs collected from symptomatic and asymptomatic plants (Gallelli et al., 2011).

Natural enemies

Means of Movement and Dispersal

Transmission

Like all pathovars of Pseudomonas syringae, P. syringae pv. actinidiae is present in infected plant material and, therefore, is usually introduced into new regions in nursery material. The pathogen can be dispersed in aerosols and can be carried between trees and adjacent orchards in wind-driven rain. As a wound-infecting pathogen, it can also be transmitted on orchard equipment such as pruning implements.

The pathways mainly involved in its transmission seem to be:

Plant material

Movement of Psa associated with imported propagative material in the nursery trade is considered the primary means for long-distance dispersal of this pathogen. Psa overwinters in infected plants and therefore propagative material can provide a pathway for Psa across short or long distances (Biosecurity Australia, 2011; EPPO, 2012b). This pathway is suspected to be responsible for the outbreaks in France (EPPO, 2010b), Spain (Cobos Suarez, personal communication, 2011, in EPPO, 2011e) and Switzerland (EPPO, 2011e).

Tissue Culture

In Italy there are indications that young plants obtained from micropropagation have been a source of infection (GM Balestra, personal communication, 2010).

Psa shows the capability to survive in detached organs, such as leaf litter and twigs, until 45 days after they fall from the plant (Scortichini et al., 2012).

Pollen

Viable Psa is associated with pollen and there is evidence that transmission of Psa can take place via infected pollen. Psa has been reisolated systemically from within plants artificially pollinated with Psa-contaminated pollen (Spinelli et al., 2015). Additionally, plants artificially pollinated with naturally Psa-contaminated pollen developed symptoms of bacterial canker, and viable Psa was recovered from these plants 2 years after pollination (Tontou et al., 2014). Nevertheless, the role of pollen in the natural spread of the disease is not yet fully understood (Biondi et al., 2013).

Natural spread, e.g., intrinsic spread, wind, water, animals (including pollinators)

Psa is non-spore forming and does not persist in the environment as well as other spore-forming bacteria. It does not become air-borne without physical assistance such as wind or rain splash. The main mode of natural spread within and between orchards is via passive transmission - bacterial exudates from kiwifruit cankers are disseminated by rain-splash and wind driven rain (Serizawa et al., 1989, Scortichini et al., 2012).

Insects, especially pollinating insects, have been shown to vector viable Psa and other P. syringae pathovars. However, their role in the transmission of disease caused by Psa is unclear. Based on preliminary studies, a stand-down period of more than 9 days before moving beehives has been recommended (Pattemore et al., 2014).

Seedborne Aspects

Incidence

There is currently no evidence that Psa infects seed, or is seed transmitted (Scortichini et al., 2012; EPPO, 2012b). Kiwifruit have small mature seeds which are extracted manually from mature and invariably healthy fruit. These factors reduce the likelihood of successful transmission or even association of pathogens such as Psa with seed (Hu et al., 1999). 

Seed Treatments

Not required. Seed from fruit for propagation obtained by aseptic excision will prevent transmission.

Impact

Under favourable conditions, P. syringae pv. actinidiae has the potential to cause severe damage to developed kiwifruit plants and to reduce yields. It is already responsible for worldwide economic loss of hundred millions of euros.

In New Zealand, 85% of gold kiwifruit (A. chinensis variety Hort16A) vines were removed between 2010 and 2014 because of the disease (SOPI, 2014). However export volumes are expected to recover as the kiwifruit industry replaces the Psa-susceptible Hort16A vines with new more tolerant varieties (SOPI, 2014).

Diagnosis

Isolates of P. syringae pv. actinidiae are very slow growing compared with other kiwifruit pathogens. P. syringae pv. actinidiae is negative in all API tests for utilization of raffinose, aesculin, xylose, arabitol, adonitol, mucate, protochatechuate and trigonelline, for production of acid from sucrose, and ice-nucleation capability. These tests discriminate P. syringae pv. actinidiae from all other known pathogens of P. syringae (Young et al., 1997). The Biolog reactions of P. syringae pv. actinidiae permit reliable identification of the pathogen (Koh, 1997).

Morphological identification

P. syringae pv. actinidiae should be isolated for morphlogical identification. For symptomatic samples, non-selective growth media: PPGA (Takikawa et al., 1989), KB (King et al., 1954) and NSA (Crosse, 1959), and semi-selective media produced by modifying KB and NSA media (by adding boric acid 1.5 g/l, cycloheximide 200 mg/l and cephalexin 80 mg/l) can be used (GM Balestra, personal communication, 2011; Gallelli et al., 2011a). Populations can be characterized using phenotypic characteristics as described by Takikawa et al. (1989) and Vanneste et al. (2011).

Molecular tests

PCR primer sets have been developed for the detection of P. syringae pv. actinidiae (Sawada et al., 1997; Koh and Nou, 2002); however, these were not specific to P. syringae pv. actinidiae. Rees-George et al. (2010) have developed specific primers PsaF1/PsaR2. These primers do not allow P. syringae pv. actinidiae to be distinguished from P. syringae pv. theae, but this pest has only ever been isolated from tea plants (Scortichini et al., 2002). However, these primers are able to detect Pseudomonas syringae pv. actinidifoliorum which affects kiwifruit plants causing minor damage in New Zealand (Vanneste et al., 2013), France (Cunty et al., 2014) and Spain (Abeillera et al., 2015).

Several diagnostic methods have been developed to specifically detect P. syringae pv. actinidiae: a duplex PCR assay (Gallelli et al., 2011b) able to specifically detect all Psa biovars and distinguish them from P. syringae pv. theae and  Pseudomonas syringae pv. actinidifoliorum. A multiplex PCR assay has recently been developed to quickly indicate the origin and virulence of P. syringae pv. actinidiae strains, as well as test a large number of samples collected during surveillance and prevention activities (Balestra et al., 2013). An end-point PCR and a quantitative real-time PCR, able to detect strains belonging to the more aggressive biovar (3) were developed by Gallelli et al. (2014). A nested PCR to specifically detect the pathogen from bleeding sap (Biondi et al., 2013), a real-time PCR assay, able to detect strains of biovar 3 (Andersen et al., 2018) and a LAMP-PCR ( Ruinelli et al., 2017) have also been developed. Some inter-laboratory studies have provided a comparison of several diagnostic methods suggesting the use of the most reliable methods for screening of symptomatic and asymptomatic samples during monitoring assays and for the specific identification of the bacterium (Loreti et al., 2014; Loreti et al., 2018).

Similarities to Other Species/Conditions

P. syringae pv. actinidiae is one of several related pathogens that attack kiwifruit. There is a need to discriminate P. syringae pv. actinidiae from Pseudomonas viridiflava, Pseudomonas syringae pv. syringae, P. syringae pv. actinidifoliorum and the distinct Pseudomonas sp. of the genomovar savastanoi, pathogenic to kiwifruit, reported by Young et al. (1997). All these pathogens produce similar, if not identical, chlorotic, angular leaf lesions and infections of floral buds and flowers, but only P. syringae pv. actinidiae commonly causes the exudation of translucent gum from floral buds and the undersurfaces of leaves. Only P. syringae pv. actinidiae and P. syringae pv. syringae produce gumming, invasive, necrotic lesions which develop along canes and trunks to produce extensive cankers. The translucent gum becomes rusty brown when it is exuded from larger cankers.

Prevention and Control

Cultural Control

In countries and regions where P. syringae pv. actinidiae is not present, new plantings should be produced from nursery material from disease-free sources. In countries and regions where P. syringae pv. actinidiae is present, prophylactic measures should be implemented in orchards to prevent its spread/infection, e.g. disinfection of pruning tools between cuts or at the time of harvest, avoidance of cutting and re-growth of plants already compromised at trunk level and eliminating them completely, including the root apparatus; and avoiding grafting on plants cut after infection.

Chemical Control

Although some symptoms of the disease, such as leaf spots, may be reduced by antibacterial spray applications (Serizawa et al., 1989) economic and reliable control of the disease and prevention of vine canker is difficult. Cupric compounds are able to protect/prevent and reduce many of the risks of infection/re-infection by P. syringae pv. actinidiae if sprayed at the right concentration and the right time.

Biological Control

A natural antagonist (Bacillus amyloliquefaciens subsp. plantarum strain D747) has recently (2012) been successfully registered in the EU for use as a preventive control strategy against P. syringae pv. actinidiae.

References

Abelleira A, Ares A, Aguin O, Peñalver J, Morente MC, López MM, Sainz MJ, Mansilla JP, 2015. Detection and characterization of Pseudomonas syringae pv. actinidifoliorum in kiwifruit in Spain. Journal of Applied Microbiology, 119(6):1659-1671. http://onlinelibrary.wiley.com/journal/10.1111/(ISSN)1365-2672

Abelleira A, Ares A, Aguín O, Picoaga A, López MM, Mansilla P, 2014. Current situation and characterization of Pseudomonas syringae pv. actinidiae on kiwifruit in Galicia (northwest Spain). Plant Pathology, 63(3):691-699. http://onlinelibrary.wiley.com/doi/10.1111/ppa.12125/full

Abelleira A, López MM, Peñalver J, Aguín O, Mansilla JP, Picoaga A, García MJ, 2011. First report of bacterial canker of kiwifruit caused by Pseudomonas syringae pv. actinidiae in Spain. Plant Disease, 95(12):1583. http://apsjournals.apsnet.org/loi/pdis

Andersen, M. T., Templeton, M. D., Rees-George, J., Vanneste, J. L., Cornish, D. A., Yu, J., Cui, W., Braggins, T. J., Babu, K., Mackay, J. F., Rikkerink, E. H. A., 2018. Highly specific assays to detect isolates of Pseudomonas syringae pv. actinidiae biovar 3 and Pseudomonas syringae pv. actinidifoliorum directly from plant material. Plant Pathology, 67(5), 1220-1230. https://onlinelibrary.wiley.com/doi/abs/10.1111/ppa.12817 doi: 10.1111/ppa.12817

Balestra GM, Mazzaglia A, Quattrucci A, Renzi M, Rossetti A, 2009. Current status of bacterial canker spread on kiwifruit in Italy. Australasian Plant Disease Notes, 4(1):34-36. http://www.publish.csiro.au/nid/208.htm

Balestra GM, Mazzaglia A, Spinelli R, Graziani S, Quattrucci A, Rossetti A, 2008. Kiwifruit bacterial canker on Actinidia chinensis. (Cancro batterico su Actinidia chinensis.) L' Informatore Agrario, 38:75-76

Balestra GM, Renzi M, Mazzaglia A, 2010. First report of bacterial canker of Actinidia deliciosa caused by Pseudomonas syringae pv. actinidiae in Portugal. New Disease Reports, 22:Article 10. http://www.ndrs.org.uk/article.php?id=22010

Balestra GM, Renzi M, Mazzaglia A, 2011. First report of Pseudomonas syringae pv. actinidiae on kiwifruit plants in Spain. New Disease Reports, 24:Article 10. http://www.ndrs.org.uk/article.php?id=024010

Balestra GM, Renzi M, Mazzaglia A, 2011. Occurrence of bacterial canker caused by Pseudomonas syringae pv. actinidiae in kiwifruit plants of cv. Tsechelidis. Journal of Plant Pathology, 93(4, Supplement):S4.86. http://sipav.org/main/jpp/index.php/jpp/issue/view/118

Balestra GM, Taratufolo MC, Vinatzer BA, Mazzaglia A, 2013. A Multiplex PCR Assay for Detection of Pseudomonas syringae pv. actinidiae and Differentiation of Populations with Different Geographic Origin. Plant Disease, 97(4):472-478

Balestra, G. M., Buriani, G., Cellini, A., Donati, I., Mazzaglia, A., Spinelli, F., 2018. First report of Pseudomonas syringae pv. actinidiae on Kiwifruit pollen from Argentina. Plant Disease, 102(1), 237. http://apsjournals.apsnet.org/loi/pdis doi: 10.1094/PDIS-04-17-0510-PDN

Bastas KK, Karakaya A, 2012. First report of bacterial canker of kiwifruit caused by Pseudomonas syringae pv. actinidiae in Turkey. Plant Disease, 96(3):452. http://apsjournals.apsnet.org/loi/pdis

Biondi E, Galeone A, Kuzmanovic N, Ardizzi S, Lucchese C, Bertaccini A, 2013. Pseudomonas syringae pv. actinidiae detection in kiwifruit plant tissue and bleeding sap. Annals of Applied Biology, 162(1):60-70. http://onlinelibrary.wiley.com/journal/10.1111/(ISSN)1744-7348

Biosecurity Australia, 2011. Final pest risk analysis report for Pseudomonas syringae pv. actinidiae associated with Actinidia (kiwifruit) propagative material. Canberra, Australia: Department of Agriculture, Fisheries and Forestry

Butler MI, Stockwell PA, Black MA, Day RC, Lamont IL, Poulter RTM, 2013. Pseudomonas syringae pv. actinidiae from recent outbreaks of kiwifruit bacterial canker belong to different clones that originated in China. PLoS ONE, 8(2):e57464. http://www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0057464

CABI/EPPO, 2012. Pseudomonas syringae pv. actinidiae. [Distribution map]. Distribution Maps of Plant Diseases, No.April. Wallingford, UK: CABI, Map 1043 (Edition 2)

CABI/EPPO, 2016. Pseudomonas syringae pv. actinidiae. [Distribution map]. Distribution Maps of Plant Diseases, No.October. Wallingford, UK: CABI, Map 1043 (Edition 3)

Cainelli C, Ferrante P, Scortichini M, 2016. Records of Pseudomonas syringae pv. Actinidiae on actinidia spp. in Trentino (north-east Italy). Journal of Plant Pathology, 98(3):689. http://www.sipav.org/main/jpp/index.php/jpp/article/view/3751/2392

Chapman JR, Taylor RK, Weir BS, Romberg MK, Vanneste JL, Luck J, Alexander BJR, 2012. Phylogenetic relationships among global populations of Pseudomonas syringae pv. actinidiae. Phytopathology, 102(11):1034-1044. http://apsjournals.apsnet.org/loi/phyto

CROSSE, J. E. , 1959. Bacterial canker of stone-fruits. IV. Investigation of a method for measuring the inoculum potential of Cherry trees. Annals of Applied Biology, 47(2), 306-317 pp. doi: 10.1111/j.1744-7348.1959.tb02546.x

Cunty A, Poliakoff F, Rivoal C, Cesbron S, Fischer-Le Saux M, Lemaire C, Jacques MA, Manceau C, Vanneste JL, 2014. Characterisation of Pseudomonas syringae pv. actinidiae (Psa) isolated from France and assignment of Psa biovar 4 to a de novo pathovar: Pseudomonas syringae pv. actinidifoliorum pv. nov. Plant Pathology, 64(3):582-596

Dai, Y., Chen, Y., Gan, L., Lan, C., Gao, M., Yang, X., 2019. First report of bacterial canker of kiwifruit caused by Pseudomonas syringae pv. actinidiae in Fujian Province, China. Plant Disease, 103(1), 143. http://apsjournals.apsnet.org/loi/pdis doi: 10.1094/PDIS-04-18-0618-PDN

Dreo T, Pirc M, Ravnikar M, Zezlina I, Poliakoff F, Rivoal C, Nice F, Cunty A, 2014. First report of Pseudomonas syringae pv. actinidiae, the causal agent of bacterial canker of kiwifruit in Slovenia. Plant Disease, 98(11):1578. http://apsjournals.apsnet.org/loi/pdis

EPPO, 1993. Pseudomonas syringae pv. actinidiae infecting kiwifruit in the EC (IT). EPPO Reporting Service, 1993/103. Paris, France: European and Mediterranean Plant Protection Organization

EPPO, 2010. First record of Pseudomonas syringae pv. actinidiae in France. EPPO Reporting Service, 2010/188. Paris, France: European and Mediterranean Plant Protection Organization

EPPO, 2010. First report of Pseudomonas syringae pv. actinidiae in New Zealand. EPPO Reporting Service, 2010/216. Paris, France: European and Mediterranean Plant Protection Organization

EPPO, 2010. Situation of Pseudomonas syringae pv. actinidiae in Italy. EPPO Reporting Service, 2010/144. Paris, France: European and Mediterranean Plant Protection Organization

EPPO, 2011. EPPO Reporting Service. EPPO Reporting Service. Paris, France: EPPO. http://archives.eppo.org/EPPOReporting/Reporting_Archives.htm

EPPO, 2011. First report of Pseudomonas syringae pv. actinidiae in Chile. EPPO Reporting Service, 2011/055. Paris, France: European and Mediterranean Plant Protection Organization

EPPO, 2011. First report of Pseudomonas syringae pv. actinidiae in Portugal. EPPO Reporting Service, 2011/054. Paris, France: European and Mediterranean Plant Protection Organization

EPPO, 2011. First report of Pseudomonas syringae pv. actinidiae in Spain. EPPO Reporting Service, 2011/188. Paris, France: European and Mediterranean Plant Protection Organization

EPPO, 2011. First report of Pseudomonas syringae pv. actinidiae in Switzerland. EPPO Reporting Service, 2011/168. Paris, France: European and Mediterranean Plant Protection Organization

EPPO, 2011. Pseudomonas syringae pv. actinidiae found in Calabria, Campania, and Friuli-Venezia Giulia regions (IT). EPPO Reporting Service, 2011/131. Paris, France: European and Mediterranean Plant Protection Organization

EPPO, 2012. EPPO Reporting Service. EPPO Reporting Service. Paris, France: EPPO. http://archives.eppo.org/EPPOReporting/Reporting_Archives.htm

EPPO, 2012. Final pest risk analysis for Pseudomonas syringae pv. actinidiae. Paris, France: European and Mediterranean Plant Protection Organization. http://www.atlasplantpathogenicbacteria.it/PSA%20PRA.pdf

EPPO, 2012. First report of Pseudomonas syringae pv. actinidiae in Turkey. EPPO Reporting Service, 2012/001. Paris, France: European and Mediterranean Plant Protection Organization

EPPO, 2014. PQR database. Paris, France: European and Mediterranean Plant Protection Organization. http://www.eppo.int/DATABASES/pqr/pqr.htm

Everett KR, Taylor RK, Romberg MK, Rees-George J, Fullerton RA, Vanneste JL, Manning MA, 2011. First report of Pseudomonas syringae pv. actinidiae causing kiwifruit bacterial canker in New Zealand. Australasian Plant Disease Notes, 6(1):67-71. http://www.springerlink.com/content/21624v144402rlm0/fulltext.html

Gallelli A, Talocci S, L'Aurora A, Loreti S, 2011. Detection of Pseudomonas syringae pv. actinidiae, causal agent of bacterial canker of kiwifruit, from symptomless fruits and twigs, and from pollen. Phytopathologia Mediterranea, 50(3):462-472. http://www.fupress.com/pm/

Gallelli, A., L'Aurora, A., Loreti, S., 2011. Gene sequence analysis for the molecular detection of Pseudomonas syringae pv. actinidiae: developing diagnostic protocols. Journal of Plant Pathology, 93(2), 425-435. http://sipav.org/main/jpp/index.php/jpp/article/view/1198

Gallelli, A., Talocci, S., Pilotti, M., Loreti, S., 2014. Real-time and qualitative PCR for detecting Pseudomonas syringae pv. actinidiae isolates causing recent outbreaks of kiwifruit bacterial canker. Plant Pathology, 63(2), 264-276. http://onlinelibrary.wiley.com/doi/10.1111/ppa.12082/full doi: 10.1111/ppa.12082

Gardan L, Shafik H, Belouin S, Broch R, Grimont F, Grimont PAD, 1999. DNA relatedness among the pathovars of Pseudomonas syringae and description of Pseudomonas tremae sp. nov. and Pseudomonas cannabina sp. nov. (ex Sutic and Dowson 1959). International Journal of Systematic Bacteriology, 49(2):469-478; 30 ref

Gardan L, Shafik HL, Grimont PAD, 1997. DNA relatedness among pathovars of P. syringae and related bacteria. In: Pseudomonas syringae Pathovars and Related Pathogens. In: Proceedings of the 5th International Working Group on Pseudomonas syringae pathovars and related pathogens, September 1995, Berlin, pp. 445-448. Dordrecht, Netherlands: Kluyver Academic Publications, 445-448

Holeva MC, Glynos PE, Karafla CD, 2015. First report of bacterial canker of kiwifruit caused by Pseudomonas syringae pv. actinidiae in Greece. Plant Disease, 99(5):723. http://apsjournals.apsnet.org/loi/pdis

Hu FP, Young JM, Jones DS, 1999. Evidence that bacterial blight of kiwifruit, caused by a Pseudomonas sp., was introduced into New Zealand from China. Journal of Phytopathology, 147(2):89-97

IPPC, 2011. Detection of the Asian strain of bacterial canker of kiwifruit in Victoria, Australia. IPPC Official Pest Report, No. AUS-45/1, No. AUS-45/1. Rome, Italy: FAO. https://www.ippc.int/

IPPC, 2016. Information on Pest Status in the Republic of Lithuania in 2015. IPPC Official Pest Report, No. LTU-01/2. Rome, Italy: FAO. https://www.ippc.int/

King, E. O., Raney, M. K., Ward, D. E., 1954. Two simple media for the demonstration of pyocianin and fluorescin. Journal of Laboratory and Clinical Medicine, 44, 301–307.

Koh YoungJin, 1997. A database for identification of Pseudomonas syringae pv. actinidiae, the pathogen of kiwifruit bacterial canker, using Biolog program. Korean Journal of Plant Pathology, 13(2):125-128; 8 ref

Lelliott RA, Billing E, Hayward AC, 1966. A determinative scheme for the fluorescent plant pathogenic pseudomonads. Journal of Applied Bacteriology, 29:470-489

Li L, Zhong C, Li D, Huang H, 2013. Diversity of Pseudomonas syringae pv. actinidiae causing bacterial canker of kiwifruit in China. In: PSA 2013: First International Symposium on Bacterial Canker of Kiwifruit (Psa), 19-22 November 2013, Tauranga, New Zealand

Liu P, Xue S, He R, Hu J, Wang X, Jia B, 2016. Pseudomonas syringae pv. actinidiae isolated from non-kiwifruit plant species in China. European Journal of Plant Pathology. http://link.springer.com/article/10.1007/s10658-016-0863-4/fulltext.html

Loreti, S., Cunty, A., Pucci, N., et al., 2018. Performance of diagnostic tests for the detection and identification of Pseudomonas syringae pv.actinidiae (Psa) from woody samples. Eur J Plant Pathol, 152: 657. https://doi.org/10.1007/s10658-018-1509-5

Loreti, S., Pucci, N., Gallelli, A., Minardi, P., Ardizzi, S., Balestra, G. M., Mazzaglia, A., Taratufolo, M. C., 2014. The Italian inter-laboratory study on the detection of Pseudomonas syringae pv. actinide. Phytopathologia Mediterranea, 53(1), 159-167. http://www.fupress.com/pm/

Marcelletti S, Scortichini M, 2014. Definition of plant-pathogenic Pseudomonas genomospecies of the Pseudomonas syringae complex through multiple comparative approaches. Phytopathology, 104(12):1274-1282. http://apsjournals.apsnet.org/loi/phyto

Mazzaglia A, Renzi M, Balestra GM, 2011. Comparison and utilization of different PCR-based approaches for molecular typing of Pseudomonas syringae pv. actinidiae strains from Italy. Canadian Journal of Plant Pathology, 33(1):8-18. http://www.informaworld.com/smpp/content~db=all~content=a932232999~frm=titlelink

Mazzaglia A, Renzi M, Taratufolo MC, Gallipoli L, Bernardino R, Ricci L, Quattrucci A, Rossetti A, Balestra GM, 2010. Kiwifruit bacterial canker in italy: the current situation. (Cancro Batterico dell'Actinidia in Italia: il punto della situazione.) Rivista di Ortoflorofrutticoltura, 9:66-76

Mazzaglia A, Studholme DJ, Taratufolo MC, Cai RM, Almeida NF, Goodman T, Guttman DS, Vinatzer BA, Balestra GM, 2012. Pseudomonas syringae pv. actinidiae (PSA) isolates from recent bacterial canker of kiwifruit outbreaks belong to the same genetic lineage. PLoS ONE, 7(5):e36518. http://www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0036518

McCann HC, Rikkerink EHA, Bertels F, Fiers M, Lu A, Rees-George J, Andersen MT, Gleave AP, Haubold B, Wohlers MW, Guttman DS, Wang PW, Straub C, Vanneste J, Rainey PB, Templeton MD, 2013. Genomic analysis of the kiwifruit pathogen Pseudomonas syringae pv. actinidiae provides insight into the origins of an emergent plant disease. PLoS Pathogens, 9(7):e1003503. http://www.plospathogens.org/article/info%3Adoi%2F10.1371%2Fjournal.ppat.1003503

Meparishvili G, Gorgiladze L, Sikharulidze Z, Muradashvili M, Koiava L, Dumbadze R, Jabnidze N, 2016. First report of bacterial canker of kiwifruit caused by Pseudomonas syringae pv. actinidiae in Georgia. Plant Disease, 100(2):517. http://apsjournals.apsnet.org/loi/pdis

New Zealand MAF Biosecurity, 2010. MAF confirms positive test for kiwifruit vine bacteria Psa. MAF Biosecurity New Zealand. http://www.maf.govt.nz/mafnet/press/2010/positive-test-for-kiwifruit-vine-bacteria-Psa.htm

Pattemore DE, Goodwin RM, McBrydie HM, Hoyte SM, Vanneste JL, 2014. Evidence of the role of honey bees (Apis mellifera) as vectors of the bacterial plant pathogen Pseudomonas syringae. Australasian Plant Pathology, 43(5):571-575. http://rd.springer.com/article/10.1007/s13313-014-0306-7

Rees-George J, Vanneste JL, Cornish DA, Pushparajah IPS, Yu J, Templeton MD, Everett KR, 2010. Detection of Pseudomonas syringae pv. actinidiae using polymerase chain reaction (PCR) primers based on the 16S-23S rDNA intertranscribed spacer region and comparison with PCR primers based on other gene regions. Plant Pathology, 59(3):453-464. http://www.blackwell-synergy.com/loi/ppa

Renzi M, Copini P, Taddei AR, Rossetti A, Gallipoli L, Mazzaglia A, Balestra GM, 2012. Bacterial canker on Kiwifruit in Italy: anatomical changes in the wood and in the primary infection sites. Phytopathology, 102(9):827-840. http://apsjournals.apsnet.org/loi/phyto

Ruinelli, M., Schneeberger, P. H. H., Ferrante, P., Bühlmann, A., Scortichini, M., Vanneste, J. L., Duffy, B., Pothier, J. F., 2017. Comparative genomics-informed design of two LAMP assays for detection of the kiwifruit pathogen Pseudomonas syringae pv. actinidiae and discrimination of isolates belonging to the pandemic biovar 3. Plant Pathology, 66(1), 140-149. http://onlinelibrary.wiley.com/doi/10.1111/ppa.12551/full doi: 10.1111/ppa.12551

Sawada H, Takeuchi T, Matsuda I, 1997. Comparative analysis of Pseudomonas syringae pv. actinidiae and pv. phaseolicola based on phaseolotoxin-resistant ornithine carbamoyltransferase gene (argK) and 16S-23S rRNA intergenic spacer sequences. Applied and Environmental Microbiology, 63(1):282-288

Scortichini M, 1994. Occurrence of Pseudomonas syringae pv. actinidiae on kiwifruit in Italy. Plant Pathology, 43(6):1035-1038

Scortichini M, Marcelletti S, Ferrante P, Petriccione M, Firrao G, 2012. Pseudomonas syringae pv. actinidiae: a re-emerging, multi-faceted, pandemic pathogen. Molecular Plant Pathology, 13(7):631-640. http://onlinelibrary.wiley.com/journal/10.1111/(ISSN)1364-3703

Serizawa S, Ichikawa T, 1993. Epidemiology of bacterial canker of kiwifruit. 2. The most suitable times and environments for infection on new canes. Annals of the Phytopathological Society of Japan, 59(4):460-468

Serizawa S, Ichikawa T, 1993. Epidemiology of bacterial canker of kiwifruit. 4. Optimum temperature for disease development on new canes. Annals of the Phytopathological Society of Japan, 59(6):694-701

Serizawa S, Ichikawa T, Suzuki H, 1994. Epidemiology of bacterial canker of kiwifruit. 5. Effect of infection in fall to early winter on the disease development in branches and trunk after winter. Annals of the Phytopathological Society of Japan, 60(2):237-244

Serizawa S, Ichikawa T, Takikawa Y, Tsuyumu S, Goto M, 1989. Occurrence of bacterial canker of kiwifruit in Japan: description of symptoms, isolation of the pathogen and screening of bactericides. Annals of the Phytopathological Society of Japan, 55(4):427-436

Shim HH, Koh YJ, Jae-Seoun J, Jung JS, 2003. Identification and characterization of coronatine-producing Pseudomonas syringae pv. actinidiae. Journal of Microbiology and Biotechnology, 13:110-118

SOPI, 2014. Situation and Outlook for Primary Industries 2014. Wellington, New Zealand: Ministry for Primary Industries. https://www.mpi.govt.nz/about-mpi/corporate-publications/

SOPI, 2016. Situation and Outlook for Primary Industries 2016. Wellington, New Zealand: Ministry for Primary Industries. https://www.mpi.govt.nz/about-mpi/corporate-publications/

Spinelli F, Donati I, Cellini A, Buriani G, Fiorentini L, Rocchi L, Giacomuzzi V, Mauri S, Tosi L, Tacconi G, Kay C, Vanneste J, Costa G, 2015. Pollen-mediated dispertion [sic] of Pseudomonas syringae pv. actinidiae. In: 1st International Symposium on bacterial canker of kiwifruit (Psa), Mt Maunganui, New Zealand, 19-22 November 2013. Acta Horticulturae, No. 1095. Leuven, Belgium: International Society for Horticultural Science (ISHS)

Stefani E, Giovanardi D, 2011. Dissemination of Pseudomonas syringae pv. actinidiae through pollen and its epiphytic life on leaves and fruits. Phytopathologia Mediterranea, 50(3):489-496. http://www.fupress.com/pm/

Takikawa Y, Serizawa S, Ichikawa T, Tsuyumu S, Goto M, 1989. Pseudomonas syringae pv. actinidip pv. nov.: the causal bacterium of canker of kiwifruit in Japan. Annals of the Phytopathological Society of Japan, 55(4):437-444

Tontou R, Giovanardi D, Stefani E, 2014. Pollen as a possible pathway for the dissemination of Pseudomonas syringae pv. actinide and bacterial canker of kiwifruit. Phytopathologia Mediterranea, 53(2):333-339. http://www.fupress.com/pm/

Ushiyama K, Kita N, Suyama K, Aono N, Ogawa J, Fujii H, 1992. Bacterial canker disease of wild actinidia plants as the infection source of outbreak of bacterial canker of kiwifruit caused by Pseudomonas syringae pv. actinidiae. Annals of the Phytopathological Society of Japan, 58(3):426-430

Ushiyama K, Suyama K, Kita N, Aono N, Fujii H, 1992. Isolation of kiwifruit canker pathogen, Pseudomonas syringae pv. actinidiae, from leaf spot of tara vine (Actinidia arguta Planch.). Annals of the Phytopathological Society of Japan, 58(3):476-479

Vanneste JL, Cornish DA, Yu J, Stokes CA, 2014. First report of Pseudomonas syringae pv. actinidiae the causal agent of bacterial canker of kiwifruit on Actinidia arguta vines in New Zealand. Plant Disease, 98(3):418. http://apsjournals.apsnet.org/doi/abs/10.1094/PDIS-06-13-0667-PDN

Vanneste JL, Poliakoff F, Audusseau C, Cornish DA, Paillard S, Rivoal C, Yu J, 2011. First report of Pseudomonas syringae pv. actinidiae, the causal agent of bacterial canker of kiwifruit in France. Plant Disease, 95(10):1311. http://apsjournals.apsnet.org/loi/pdis

Vanneste JL, Yu J, Cornish DA, Tanner DJ, Windner R, Chapman JR, Taylor RK, Mackay JF, Dowlut S, 2013. Identification, virulence, and distribution of two biovars of Pseudomonas syringae pv. actinidiae in New Zealand. Plant Disease, 97(6):708-719. http://apsjournals.apsnet.org/loi/pdis

Young JM, Gardan L, Ren XZ, Hu FP, 1997. Genomic and phenotypic characterization of the bacterium causing blight of kiwifruit in New Zealand. Plant Pathology, 46(6):857-864; 21 ref

Contributors

08/01/18 Review of Diagnosis section by:

Stefania Loreti, Consiglio per la ricerca in agricoltura e l'analisi dell'economia agraria, Centro di ricerca Difesa e Certificazione, Sede di Roma, Rome, Italy.

20/12/16 Reviewed by:

Jocelyn A Berry, Policy and Risk Directorate, Ministry for Primary Industries, Wellington, New Zealand.

Distribution Maps