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

Due to the variable regulations around (de)registration of pesticides, your national list of registered pesticides or relevant authority should be consulted to determine which products are legally allowed for use in your country when considering chemical control. Pesticides should always be used in a lawful manner, consistent with the product's label.

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

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Distribution References

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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