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: Candidatus Phytoplasma fragariae (PHYPFG)


GENERAL INFORMATION ON THE PEST

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

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?
 
Not relevant

Conclusion:
 
  • Candidate: Fruits (including hops) sector
Justification (if necessary):
 
Instead of listing 'stolbur' as strawberry lethal decline and the strawberry green petal phytoplasma, it was recommended during the RNQP Projcect part 1 to add all phytoplasma species reported from naturally infected strawberry plants. This consisted in the listing of ‘Candidatus Phytoplasma asteris’ [aster yellows phytoplasma], ‘Candidatus Phytoplasma pruni’, ‘Candidatus Phytoplasma solani’, ‘Candidatus Phytoplasma australiense’, ‘Candidatus Phytoplasma fragariae’ and the Clover phyllody phytoplasma (16Srl-C). All these phytoplasmas are associated with leaf yellowing symptoms, but just some of them are responsible for green petal symptoms (this includes the Clover phyllody phytoplasma (16Srl-C) and ‘Candidatus Phytoplasma australiense’).

In the RNQP Project Part 2, it is also recommended to list the Clover phyllody phytoplasma as 'Candidatus Phytoplasma tritici'.

In responses to the questionnaire, AT suggested 'to merge all 'Ca. Phytoplasma' species attacking Fragaria into one category (no differentiation of symptoms, testing using universal phytoplasma tests).
However, it is considered that listing individual species would not prevent measures to be based on symptoms. Testing with universal primers is also possible if all the phytoplasmas of Fragaria/Vaccinium are listed.

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):
 
Reported from Belgium (Ulmus, Acer: De Jonghe et al., 2020), Italy (Sambucus, Cornus: Filippin et al., 2008; Corylus: Gentili et al., 2022), Lithuania (Fragaria: Valiunas et al., 2006), Slovenia (Corylus: Mehle et al., 2014).

HOST PLANT N°1: Fragaria (1FRAG) 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?
 
No
 
Conclusion:
 
Evaluation continues

 
Justification (if necessary):
 
Phytoplasma is mentioned in PM4/11(2) however not 'Ca. P. fragariae'. This could be due to the limited information available in 2008, the phytoplasma was first described in 2006. When responding to the questionnaire, NL and PL supported deregulation in the EU. This was later supported by CZ (rare findings). Although being an 'environmental, local problem in fruit production', NL and PL considered that this phytoplasma was not mainly transmitted by plants for planting. NL also considered that economic impact was acceptable since strawberry was not a main host. Evaluation continues with a focus on the pathway and economic impact.

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

 
Justification:
 
Based on the first findings of ‘Ca. P. fragariae’ in the UK and the quick Pest Risk Analysis for their territories by FERA, they came to the conclusion that the pathogen is still poorly understood, and that without further knowledge of the insect vector of the pathogen, risk assessment and management decisions are subject to high levels of uncertainty (DEFRA, 2015).
Little to no information available on 'Ca. P. fragariae' in strawberry, other than the first identification and description in strawberry in 2006 (Valiunas et al., 2006). All other reports are on other crops: Acer pseudoplatanus (De Jonghe et al., 2020), Corylus avellana (Hodgetts et al., 2015; Mehle et al., 2014, Gentili et al., 2022), Cornus sanguinea (Filippin et al., 2008), Sambucus nigra (Filippin et al., 2008), Ulmus spp. (Hodgetts et al., 2014; De Jonghe et al., 2020).
If strawberry is confirmed as a host plant, it may be a dead-end host as is the case for some phytoplasmas.

5 - Economic impact:

Are there documented reports of any economic impact on the host?
 
No

Justification:
 
Limited symptom description, but no indication of how severe the impact might be (Valiunas et al., 2006).

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

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?
 
Yes

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?
 
No

Conclusion:
 
Not candidate

Justification:
 
Unclear. This may relate to the fact that the majority of Fragaria propagating material in the EPPO region is coming from in vitro cultures (minimal risk).
Originally, this phytoplasma was described in strawberry (Valiunas et al., 2006), and not reported in strawberry since (search CAB Abstracts 19/Apr/2024). Recent findings of this phytoplasma in Europe are associated with a number of other host species (De Jonghe et al., 2020; Filippin et al., 2008; Gentili et al., 2022; Hodgetts et al., 2014, 2015; Mehle et al., 2019; Loiseau et al., 2019).

Corylus avellana
In the UK ‘Ca. P. fragariae’ could induce general decline and high mortality rate on hazel (Corylus avellana) in multiple locations in the UK in 2015. The high mortality of the trees could have been a result of a susceptible genotype as the plants are all likely clones derived from the same mother plant (DEFRA, 2015).
In two plantations located in eastern Slovenia eastern, decline of some of the hazelnut trees appeared in 2012. The plantations together covered 5 ha with around 1,200 trees planted in 2002-2005 [12 to 15 years ago]. In 2018, ca. 12% of these trees had died, and an additional 12% showed decay symptoms. The dead and dying trees were scattered throughout both orchards, with no apparent pattern. ‘Ca. P. fragariae’ (16SrXII-E subgroup) and phytoplasmas of the 16SrV group appear to be the most devastating and widespread in Slovenian hazelnut plantations. ‘Ca. P. fragariae’ has also been detected in a forest trees in south-western Slovenia. All infected forest trees showed unusual dense proliferation of sprouts from roots and/or trunks (Mehle et al., 2019).
Indirect economic impact is not considered for this pest since there is no data on the role of strawberry as a particular source for hazelnut. Hazel and strawberry are generally not grown together.

Remark: The Fruit SEWG recommended that the RNQP status of 'Candidatus Phytoplasma fragariae' on hazelnut is further considered in the future.

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?
 
 
Conclusion:
 

Justification:
 
Testing is possible (e.g. real time PCR)

7- Is the quality of the data sufficient to recommend the pest to be listed as a RNQP?
 
 
Conclusion:
 

Justification:
 

CONCLUSION ON THE STATUS:
 
Disqualified: uncertainty on the host status and no economic impact reported. The RNQP status of 'Ca. P. fragariae' should be considered for hazelnut.


8 - Tolerance level:

Is there a need to change the Tolerance level:
 
Yes

Proposed Tolerance levels:
 
Delisting

9 - Risk management measures:

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

Proposed Risk management measure:
 
Delisting


REFERENCES:
  • Bertaccini A (2019). The phytoplasma classification between ‘Candidatus species’ provisional status and ribosomal grouping system Phytopathogenic Mollicutes 9(1), 1-2.
  • Cheng M, Dong J, Zhang L, Laski PJ, Zhang Z and McBeath JH (2012). Molecular characterization of “stolbur” group subgroup E (16SrXII-E) phytoplasma associated with potatoes in China. Plant Disease 96(9): 1372.
  • De Jonghe K, Goedefroit T, Deeren AM, Fauche F, Steyer S (2020) A phytoplasma survey reveals the presence of ‘Candidatus Phytoplasma fragariae’ in Ulmus spp. and Acer pseudoplatanus in Belgium. Forest Pathology 50(5), e12635, 6 pages. e12635https://doi.org/10.1111/efp.12635.
  • DEFRA (2015). Rapid Pest Risk Analysis (PRA) for: ‘Candidatus Phytoplasma fragariae’. Online publication: https://planthealthportal.defra.gov.uk/pests-and-diseases/uk-plant-health-risk-register/downloadExternalPra.cfm?id=4089.
  • Filippin L, Angelini E, Borgo M (2008) First identification of a phytoplasma infecting Cornus sanguinea and Sambucus nigra. Plant Pathology 57(6), 1175. https://doi.org/10.1111/j.1365-3059.2008.01914
  • Gentili A, Donati L, Bertin S, Manglli A & Ferretti L (2022) First report of ‘Candidatus Phytoplasma fragariae’ infecting hazelnut in Italy. Plant Disease 106(8), 2254. https://doi.org/10.1094/PDIS-11-21-2566-PDN
  • Hodgetts J, Flint LJ & Fox A (2014) First report of 'Candidatus Phytoplasma ulmi' (16SrV-A) associated with Ulmus cultivar Morfeo (elm) in the United Kingdom. New Disease Reports 32, 26. https://doi.org/10.5197/j.2044-0588.2015.032.026
  • Hodgetts J, Flint LJ, Davey C, Forde S, Jackson L, Harju V, Skelton A & Fox A (2015). Identification of ‘Candidatus Phytoplasma fragariae' (16Sr XII-E) infecting Corylus avellana (hazel) in the United Kingdom. New Disease Reports, 32, 3. https://doi.org/10.5197/j.2044-0588.2015.032.003
  • Loiseau M, Massot M, Cousseau-Suhard P, Foissac X, Piou D & Robin C (2019) Are phytoplasmas associated with dieback symptoms of Fraxinus in France? Phytopathogenic Mollicutes 9(1), 53-54. doi: 10.5958/2249-4677.2019.00027.6
  • Martini M, Mesaglio A, Savian F, Loschi A, Loi N, Ermacora P (2018). Identification of ‘Candidatus Phytoplasma fragariae’ (16SrXII-E) infecting Cornus sanguinea in Friuli Venezia Giulia (north-eastern Italy). Bois Noir 5th Workshop, Slovenia 18-19 September 2018. Conference paper
  • Mehle N, Jakoš N, Mešl M, Miklavc J, Matko B, Rot M, Rus AF, Brus R & Dermastia M (2019) Phytoplasmas associated with declining of hazelnut (Corylus avellana) in Slovenia. European Journal of Plant Pathology 155, 1117–1132. https://doi.org/10.1007/s10658-019-01839-3.
  • Valiunas D, Staniulis J, Davis RE (2006). ‘Candidatus Phytoplasma fragariae’, a novel phytoplasma taxon discovered in yellows diseased strawberry, Fragaria ananassa. International Journal of Systematic and Evolutionary Microbiology 56(Pt 1):277-81. DOI: 10.1099/ijs.0.63935-0