Regulated Non-Quarantine Projects

Two EU funded projects for the benefit of the whole EPPO region

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Justification for qualification based on EPPO PM 4 Standards
Justification for disqualification
Additional or non-conclusive information
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NAME OF THE ORGANISM: Pseudomonas avellanae and Pseudomonas syringae pv. avellanae (PSDMAL & XXXXX)


GENERAL INFORMATION ON THE PEST

Name as submitted in the project specification (if different):
 
Pseudomonas avellanae

Pest category:
 
Bacteria


1- Identity of the pest/Level of taxonomic listing:

Is the organism clearly a single taxonomic entity and can it be adequately distinguished from other entities of the same rank?
 
Yes

Is the pest defined at the species level or lower?:
 
Yes

Can listing of the pest at a taxonomic level higher than species be supported by scientific reasons or can species be identified within the taxonomic rank which are the (main) pests of concern?
 
  • Not relevant: Fruits (including hops) sector
If necessary, please list the species:
 
-

Is it justified that the pest is listed at a taxonomic rank below species level?
 
Yes

Conclusion:
 
  • Candidate: Fruits (including hops) sector
Justification (if necessary):
 
Hazelnut (Corylus avellana) can threatened by various Pseudomonas spp. (Marcelletti & Scortichini, 2015; Turco et al., 2022):
- Pseudomonas avellanae (Pav) stains infecting hazelnut – more virulent, potentially restricted to hazelnut (Scortichini et al. 2002), has a set of three type III secretion effectors, while strains infecting Actinidia and Prunus have a WHOP island, necessary to infect woody hosts (Turco et al., 2022);
- Pseudomonas syringae infecting hazelnut contains more phytotoxins, the ice nucleation cluster, but less effectors (Turco et al., 2022)
o Pseudomonas syringae pv. avellanae (Psav) – relatively aggressive, Italy (Scortichini et al., 2013),
o Pseudomonas syringae pv. coryli (Psco) – relatively mild, in Piedmont, Campania, Latium, Sicily and Sardinia (Scortichini et al. 2002, 2005)
o Pseudomonas syringae pv. syringae (Pss) – able to induce only mild symptoms, limited to twig dieback, in Campania, Latium, Piedmont, Sardinia and Sicily (Scortichini et al., 2002; Loreti et al., 2009).
Among these, P. avellanae and P. s. pv. avellanae are considered the most dangerous pathogens for Corylus avellana (Marcelletti and Scortichini, 2015).

The disease related to these pathogens is known as bacterial canker of hazelnut, which was reported for the first time in Greece in 1976 and associated at the time to a new Pseudomonas pathovar named Pseudomonas syringae pv. avellanae (Psallidas & Panagopoulos, 1979, Psallidas 1993). The causal strains of the bacterial canker of hazelnut in Greece and Italy were originally described as Pseudomonas syringae pv. avellanae, but renamed to Pseudomonas avellanae (Janse et al. 1996). One representative strain, classified as P. avellanae and isolated in central Italy, is a genuine member of the P. syringae species complex and can be defined as P. s. pv. avellanae (Scortichini et al., 2013).

2 – Status in the EU:
 
Is this pest already a quarantine pest for the whole EU?
 
No

Presence in the EU:
 
Yes

List of countries (EPPO Global Database):
 
-

Conclusion:
 
Candidate

Justification (if necessary):
 
Pseudomonas avellanae has been reported in European countries e.g. Italy and Greece (Turco et al., 2022).
Despite the severity of P. avellanae outbreaks in central Italy and northern Greece, the spread of this disease has remained restricted to these areas (UK PRA, 2022) and its occurrence is always associated with highly acidic soils (pH < 5.0) (Scortichini et al., 2006).
However, given the existence in the literature of reports of its presence in Denmark (OISC, 2020), although still to be confirmed (UK PRA, 2022), and the role of asymptomatic plant reproductive material in the large-scale dissemination (the introduction of P. avellanae from northern to southern orchards in the Latium region of Italy by means of latently infected propagative material has been demonstrated) (Scortichini, 2002; Scortichini and Loreti, 2007), a wider distribution cannot be excluded.
The Fruit SEWG highlighted the uncertainty on presence and prevalence in other hazelnut-growing countries.

HOST PLANT N°1: Corylus avellana (CYLAV) for the Fruits (including hops) sector.


Origin of the listing:
 
Commission Implementing Directive (EU) 2014/98/EU and Commission Implementing Regulation (EU) 2019/2072

Plants for planting:
 
Plants intended for planting


3 - Is the pest already listed in a PM4 standard on the concerned host plant?
 
Yes
 
Conclusion:
 
Evaluation continues

 
Justification (if necessary):
 
Inspection for 'Pseudomonas avellanae,' is recommended in EPPO Standard PM 4-31 Certification scheme for hazelnut. Any plant found to be infected should be recorded and immediately removed. In the responses to the questionnaire, PL supported deregulation in the EU because economic impact was considered acceptable. The Fruit SEWG also wondered whether plants for planting should be considered as a significant pathway. Evaluation continues on these two criteria.

4 - Are the listed plants for planting the main* pathway for the "pest/host/intended use" combination? (*: significant compared to others):
 
?
 
Conclusion:
 
Candidate by default

 
Justification:
 
Within the species Pseudomonas avellanae at least three clusters can be identified: a cluster restricted to hazelnut (Corylus avellana) both wild and cultivated, a cluster restricted to Prunus spp. and another cluster restricted to Actinidia sp. These groups have specific traits: P. avellanae strains infecting hazelnut have a set of three type III secretion effectors, while the P. avellanae infecting Prunus and Actinidia are carrying the genomic WHOP island, necessary for woody-host plant infection (Turco et al., 2022).
Latently infected suckers used for propagation may be a main vehicle for wide-spread dispersal of the pathogen. Regenerated suckers on stumps of removed (diseased) trees have shown reinfection within 1 to 3 years. Introduction with latent infected propagative material from northern to southern orchards in the Latium region of Italy has been demonstrated (Scortichini & Tropiano, 1994). In Greece the infections could not be traced back to infected planting stock. It was mainly found in the Turkish cultivar Palaz, although there is no history of the disease in Turkey (Scortichini, 2002).
Secondary dissemination in an orchard is mainly by wind-driven rain (Martins & Scortichini, 1998). Bacterial canker also has been found in wild European hazelnut trees growing in forests adjacent to commercial orchards in Italy. The possibility of the pathogen spreading to the apparently highly susceptible wild European hazelnut population is a concern (Scortichini, 2002).
Besides the known ways of transmission, such as penetration of leaf scars during autumn through rain and wind, Pseudomonas spp. have been found to be associated with adults of the lignicolous beetle Anisandrus dispar (Coleoptera, Scolytinae), both internally and as an external contaminant, what requires further assessment concerning the possible role of insect pests of hazelnut as vectors (Nicoletti et al., 2022).
[In the responses to the questionnaire, SI commented that 'Bacteria can spread over long distances from infected trees. Planting of uninfected material seems pointless if infected trees are in vicinity'.]

The Fruit SEWG recommended that surveillance is performed (with molecular testing) in others hazelnut production areas of Europe than Italy and Greece so that the situation in those areas is clarified:
- Are the pests present at a lower level in these other areas and therefore not reported (which would support an RNQP status, plants for planting being still a significant pathway in those other areas)?,
- Are conditions in these other areas not suitable for the pests to cause symptoms (which would mean that plants for planting is not a significant pathway in the areas where it can cause economic impact i.e. in Greece and Italy)?, or
- Are the pests still absent from those other areas (which would make a quarantine pest status more appropriate than an RNQP status)?

In the meantime, the Fruit SEWG considered that there was uncertainty whether plants for planting should be considered as a significant pathway in areas where the pest is already present and highlighted the benefit of maintaining an RNQP regulation during this clarification (despite the severity of P. avellanae and P. s. pv. avellanae outbreaks in central Italy and northern Greece, which in some cases have caused hazelnut production to cease, the spread of this disease has remained restricted to these areas).

5 - Economic impact:

Are there documented reports of any economic impact on the host?
 
Yes

Justification:
 
Bacterial canker and decline on European hazelnut (caused by P. avellaneae) was first observed in northern Greece in 1976 (Psallidas & Panagopoulos, 1979). Within a few years, young plantings of the Turkish cultivar Palaz were almost completely destroyed by the disease (Psallidas, 1987). Subsequently, the same disease, referred to locally as 'moria' was observed in plantations throughout a 20,000-ha area in the Latium region of central Italy (i.e., Viterbo province) (Scortichini & Tropiano, 1994).
Since it was first discovered, bacterial canker and decline has resulted in the mortality of more than 40,000 trees in central Italy. It continues to damage trees on approximately 1,000 ha in this area. The estimated loss per year is approximately $1.5 million, and the disease is considered a serious problem (De Castro 1999, cited in Scortichini, 2002). Since then, the inoculum pressure of the pathogen seems to have reduced (Janse & Scortichini, 2008).
Hazelnut decline through an outbreak of P. avellanae could severely damage hazelnut production and potentially make the land unsuitable for this purpose in the future. The disease could also impact the trade of hazel for hedgerows and woodlands; and affect the coppicing of woodlands (UK PRA, 2022). It can kill the whole plant within a period of a few months up to some years (Scortichini and Marchesi, 2001).

Epidemiological studies and field surveys have demonstrated differing levels of symptoms severity caused by the four pseudomonads to C. avellana. P. avellanae and P. s. pv. avellanae are the most dangerous because they can cause extensive twig wilting and dieback, canker formation along the trunk and plant death. P. s. pv. coryli and P. s. pv. syringae appear to be less aggressive and mainly cause twig dieback (Marcelletti and Scortichini, 2015).

What is the likely economic impact of the pest irrespective of its infestation source in the absence of phytosanitary measures? (= official measures)
 
Major

Is the economic impact due to the presence of the pest on the named host plant for planting, acceptable to the propagation and end user sectors concerned?
 
No

Is there unacceptable economic impact caused to other hosts (or the same host with a different intended use) produced at the same place of production due to the transfer of the pest from the named host plant for planting?
 

Conclusion:
 
Candidate

Justification:
 
Evidence of its economic impact is available in the literature. Remark: Documented reports of economic impact are also reported for P. syringae pv. avellanae (Marcelleti & Scortichini, 2015).

6 - Are there feasible and effective measures available to prevent the presence of the pest on the plants for planting at an incidence above a certain threshold (including zero) to avoid an unacceptable economic impact as regards the relevant host plants?
 
Yes
 
Conclusion:
 
Candidate

Justification:
 
There is no direct, curative control of bacterial canker.
Production of disease-free plant material and avoidance of introduction of latently infected plants are key factors in prevention of the disease (Janse & Scortichini, 2008).
When the disease is present in an area, orchards should be monitored for early disease symptoms during (early) spring and summer.
Once an orchard is infected:
- Infected plant parts should be pruned far below the infection and, in case of completely infected trees, roots and suckers should also be removed. All this material should be burned (Janse & Scortichini, 2008).
- Pruning and/or sucker removal should be avoided during humid periods. After a branch is cut, it is advisable to seal the wound with wax or Bordeaux mixture. It may take several years to eradicate the pathogen in severely damaged orchards (Janse & Scortichini, 2008).
- Sprays with copper-based compounds are not very effective, given the systemic nature of the pathogen. But when applied immediately after pruning, spring frost, hail, windy storms in early autumn, and at the beginning and middle of leaf drop, this treatment might reduce the possibility of wound colonization by the bacterium (Janse & Scortichini, 2008).
- A new approach to control P. avellanae was developed a couple of decades ago through the spray on the tree canopy of an activator of the plant defense mechanism based on pathogenesis-related proteins, namely acibenzolar-S-methyl . The compound has no direct bactericidal activity but enhances the synthesis of proteins related to the defense against microbial pathogens. The compound is to be sprayed onto the tree canopy three times, once a month, starting from the leaf sprouting (Nicoletti et al., 2022).
- Orchards having very acidic soils require lime application to increase the soil pH (Janse & Scortichini, 2008). The affected areas have highly acidic soil pH levels of <5.0 (Scortichini et al., 2006). Alongside low pH levels, a high aluminum content (>20%) can result in an increased susceptibility of hazel trees (Scortichini, 2010).
- It is also very important to control the Scolytidae by using chromotropic traps (Janse & Scortichini, 2008).

7- Is the quality of the data sufficient to recommend the pest to be listed as a RNQP?
 
No
 
Conclusion:
 
Candidate by default

Justification:
 
Uncertainty on distribution in countries other than Italy and Greece (see pathway section)

CONCLUSION ON THE STATUS:
 
Recommended for listing as an RNQP by default: Insufficient data about pest distribution. The Fruit SEWG recommended that surveillance is performed (with molecular testing) in others hazelnut production areas of Europe than Italy and Greece so that the situation in those areas is clarified.


8 - Tolerance level:

Is there a need to change the Tolerance level:
 
No

Proposed Tolerance levels:
 

9 - Risk management measures:

Is there a need to change the Risk management measure:
 
Yes

Proposed Risk management measure:
 
The following measure was recommended for P. avellanae and P. s. pv. avellanae, for CAC (in addition to the substantially free from requirement for traded material):

(A) Derived from mother plants which have been inspected and found free from symptoms of P. avellanae and P. s. pv. avellanae.
AND
(B)(a) Plants for planting produced in an area known to be free from P. avellanae and P. s. pv. avellanae
or
(b) No more than 2% of the plants in the field lot showing symptoms during inspections at appropriate times during the last growing season, and those plants and any symptomatic plants in the immediate vicinity of the field lot rogued out and destroyed immediately.

For Pre-basic, Basic and Certified: a stricter tolerance level may be applicable to these categories. More systematic testing could be required.

Justification (if necessary):
 
Measures on symptomatic plants in the immediate viccinity of the field is to avoid natural spread from around the field into the field.
It is considered that to achieve the 2% level of tolerance showing symptoms during a growing season, surrounding plants of an infected/symptomatic plant would need to be rogued out and destroyed.
The Fruit SEWG also recommended that P. avellanae and P. syringae pv. avellanae are added to Annex II of Commission Implementing Directive 2014/98/EU, i.e. ‘List of RNQPs for the presence of which visual inspection, and, where applicable, sampling and testing are required […]’.

The Fruit SEWG recommended that surveillance is performed (with molecular testing) in others hazelnut production areas of Europe than Italy and Greece so that the situation in those areas is clarified. Although there is a latent phase, current measures in EU regulation are only based on visual examination. Pending clarification of the situation with surveillance, it is recommended not to require systematic testing of the mother plants for CAC material.

REFERENCES:
  • De Castro P (1999) Disposizioni a favore delle colture corilicole colpite dalla moria del nocciolo. Legge della Repubblica Italiana n°307, del 17 Agosto 1999. Gazzetta Ufficiale n° 210.
  • Janse JD, Rossi P, Angelucci L, Storcichini M, Derks JHJ, Akkermans ADL, De Vrijer R & Psallidas PG (1996) Reclassification of Pseudomonas syringae pv. avellanae as Pseudomonas avellanae (spec. nov, the Bacterium Causing Canker of Hazelnut (Corylus avellana L.). Systematic and applied microbiology 19(4), 589-595.
  • Janse JD & Scortichini M (2008) Pseudomonas avellanae (Psallidas) Janse et al., Bacterial canker of hazelnut (Corylus avellana). Factsheet COST. http://www.moseslab.csb.utoronto.ca/alan/P_avellanae_FactSheet.pdf.
  • Loreti S, Gallelli A, De Simone D & Bosco A (2009) Detection of Pseudomonas avellanae and the bacterial microflora of hazelnut affected by ‘Moria’ in central Italy. Journal of Plant Pathology 91 (2), 365-373.
  • Marcelletti S & Scortichini M (2015). Comparative genomic analyses of multiple Pseudomonas strains infecting Corylus avellana trees reveal the occurrence of two genetic clusters with both common and distinctive virulence and fitness traits. PLoS One 10(7), e0131112.
  • Martins JMS & Scortichini M (1998). Spatio-temporal spread of a bacterial disease in a hazelnut orchard. Pages 82-88 in: Actas 2a Reuniao bienal de Sociedade Portuguesa de Fitopatologia, Oeiras, Portugal
  • Nicoletti R, Petriccione M, Curci M & Scortichini M (2022) Hazelnut-associated bacteria and their implications in crop management. Horticulturae 8, 1195. https://doi.org/10.3390/horticulturae8121195
  • OISC JA (2020) Hazelnut Bacterial Canker Pseudomonas avellanae: Pest Risk Assessment. Oregon Invasive Species Council. https://www.oregoninvasivespeciescouncil.org/invasive-species-resources/blog/2020/8/26/hazelnut-bacterial-canker-pseudomonas-avellanae-risk-assessment
  • Psallidas PG (1993). Pseudomonas syringae pv. avellanae pathovar nov., the bacterium causing canker disease on Corylus avellana. Plant Pathology 42, 358–363.
  • Psallidas PG & Panagopoulos CG (1979). A bacterial canker of Corylus avellana in Greece. Journal of Phytopathology 94, 103–111.
  • Scortichini M (2002) Bacterial canker and decline of European hazelnut. Plant Disease 86(7), 704-709.
  • Scortichini M (2010) Epidemiology and predisposing factors of some major bacterial diseases of stone and nut fruit tree species. Journal of Plant Pathology 92.
  • Scortichini M & Tropiano FG (1994) Severe outbreak of Pseudomonas syringae pv. avellanae on hazelnut in Italy. Journal of Phytopathology 140, 65-70.
  • Scortichini M & Loreti S (2007) Occurrence of an endophytic, potentially pathogenic strain of Pseudomonas syringae in symptomless wild trees of Corylus avellana. Journal of Phytopathology 89, 431-434.
  • Scortichini M & Marchesi U (2001) Sensitive and specific detection of Pseudomonas using primers based on 16S rRNA gene sequences. Journal of Phytopathology 149, 527-532.
  • Scortichini M, Marchesi U, Rossi MP & Di Prospero P (2002) Bacteria associated with hazelnut (Corylus avellana L.) decline are of two groups: Pseudomonas avellanae and strains resembling P. syringae pv. syringae. Applied and Environmental Microbiology 68, 476–484.
  • Scortichini M, Rossi MP, Loreti S, Bosco A, Fiori M, Jackson RW, Stead DE, Aspin A, Marchesi U, Zini M & Janse JD (2005) Pseudomonas syringae pv. coryli, the causal agent of bacterial twig dieback of Corylus avellana. Phytopathology 95, 1316–1324.
  • Scortichini M, Natalini E & Marchesi U (2006) Evidence for separate origins of the two Pseudomonas avellanae lineages. Plant Pathology 55, 451-457.
  • Scortichini M, Marcelletti S, Ferrante P & Firrao G (2013). A genomic redefinition of Pseudomonas avellanae species. PLoS One, 8, 75794.
  • Turco S, Zuppante L, Drais MI & Mazzaglia A (2022) Dressing like a pathogen: Comparative analysis of different Pseudomonas genomospecies wearing different features to infect Corylus avellana. Journal of Phytopathology 170, 504-516. DOI: 10.1111/jph.13101
  • UK PRA (2022) Rapid Pest Risk Analysis (PRA) for Pseudomonas avellanae - United Kingdom (2022-04-30).