| Legend |
|---|
| Justification for qualification based on EPPO PM 4 Standards |
| Justification for disqualification |
| Additional or non-conclusive information |
| Standard text |
NAME OF THE ORGANISM: Candidatus Phytoplasma mali (PHYPMA)
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):
Main host plant is the Apple tree (Malus x domestica). All cultivars and rootstocks are potential host plants, including ornamentals and wild plants belonging to the genus Malus (ANSES, 2012). This justifies a listing of host plants at the genus level.
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):
Austria (2011); Belgium (2013); Bulgaria (1993); Croatia (2017); Czech Republic (2018); Finland (2013); France (2011); Germany (2011); Greece (2011); Hungary (2019); Italy (2013); Lithuania (2018); Netherlands (2022); Poland (2015); Romania (1992); Slovakia (1978); Slovenia (2018); Spain (2011)
Conclusion:
candidate
Justification (if necessary):
Data of the presence of this pest on the EU territory are available in EPPO Global Database (https://gd.eppo.int/). During the RNQP Project - part I, this pest was a candidate for the RNQP status according to the IIA2AWG
HOST PLANT N°1: Malus (1MABG) 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, except seeds
3 - Is the pest already listed in a PM4 standard on the concerned host plant?
Yes
Conclusion:
Evaluation continues
Justification (if necessary):
The assessment of the RNQP status was performed during the RNQP Project part 1. The project proposal of the RNQP Project part 2 only requested to review risk mitigation measures. Remark: Decision by the HEWG (RNQP Project part 1) to continue the evaluation in view of the problematic of vector transmission. When responding to the questionnaire (RNQP Project part 2), PL considered that plants for planting was not the main pathway but did not provide new supporting evidence.
4 - Are the listed plants for planting the main* pathway for the "pest/host/intended use" combination? (*: significant compared to others):
Yes
Conclusion:
Candidate
Justification:
Plants for planting can be an efficient pathway, when propagated from infested plants and depending on the grafting technique (Seemüller et al., 2011). Pathogen concentration and repartition in the trees is fluctuant in space and during the year. In absence of phytosanitary measures, vector transmission is the most important pathway (ANSES, 2012), with vertical transmission of the pathogen through psyllids generations (Mittelberger et al., 2017). Infection by root-bridges are possible but need short distances (<1m) between the infected Malus and the phytoplasma-free Malus to be infected. The infected trees shows altered phloem and metabolic alterations such as hormone synthesis modifications that may influence vector reproduction (Zimmermann et al., 2015 ; Siewert et al., 2014). Transfer from other host in the same place of production is very limited. The plant for planting pathway is considered to be a significant pathway compared to other pathways.
5 - Economic impact:
Are there documented reports of any economic impact on the host?
Yes
Justification:
The phytoplasma is present in the EU area and the principal factor of impact is the decrease of the fruit size (30% to 60% of mean decrease). Fruits may also have less flavour and and a rolled aspect. In case of high infestations, 30% to 90% of harvested fruits are not marketable anymore. However, impact of the disease can reduce with the time, until sometimes symptoms totally disappear. It is the case in France where its impact on the fruit production is considered as limited (ANSES, 2012). The impact is mostly affected by the local existence of reservoirs and by the size of vector populations. Where CPs does occur, its impact can be significant but shows high yearly fluctuations associated with fluctuations in the population densities of insect vectors and of wild plant reservoirs that cannot be easily controlled (Prima phacie, 2012).
What is the likely economic impact of the pest irrespective of its infestation source in the absence of phytosanitary measures? (= official measures)
Medium
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:
Crop losses in yield and quality on the affected trees, extra costs of harvesting and grading, costs of replanting could be important. While the pathogen and its vector is widely distributed in the EU area the economic losses are considered as medium or low, depending the country/area (Bertaccini et al. 2014; ANSES, 2012).
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:
Despite the presence in the EU area of both the phytoplasma and its vectors, the combination of prophylactic measures including the choice of varieties, rootstocks, the use of certified material for both, keeping pre-basic material under insect-proof conditions, removing each symptomatic tree in orchard, the targeted fight against vectors may maintain the infestation under an acceptable level (ANSES, 2012 ; PrimaFacie, 2012). Other disease management strategies focus on vector control, and recent strategies are considering strategies of biocontrol (Bulgari et al., 2014) or the use of suppressive strains (Schneider et al., 2014).
7- Is the quality of the data sufficient to recommend the pest to be listed as a RNQP?
Yes
Conclusion:
Candidate
Justification:
Epidemiological data is lacking on the presence and impact of the proliferation of the disease in all EU regions. However the impact of the pathogen on the production is documented, and the pathogen is widely dispersed throughout EU, with natural hosts present in the environment (M. sylvestris) and wide areas of production of M. communis. The psyllids vectors are aslo widely distributed in EU. Economical impact is likely to be more important on plant production, and several measures are identified to prevent the propagation of the phytoplasma with plant material : using certified/controlled material; measures against the vectors.
CONCLUSION ON THE STATUS:
Recommended for listing as an RNQP during the RNQP Project part 1, based on data.
8 - Tolerance level:
Is there a need to change the Tolerance level:
No, for tolerance levels of propagating material (Yes, for the tolerance level for basic material in the field).
Proposed Tolerance levels:
Zero tolerance approach for propagating material, based on visual examination and/or testing.
The Fruit SEWG agreed that a tolerance level in the field at 0% for basic was too strict since production of basic material is done under outdoor conditions, but did not propose a particular threshold.
The Fruit SEWG agreed that a tolerance level in the field at 0% for basic was too strict since production of basic material is done under outdoor conditions, but did not propose a particular threshold.
9 - Risk management measures:
Is there a need to change the Risk management measure:
Yes
Proposed Risk management measure:
Non-certified material (‘CAC’):
(A) Derived from mother plants which have been inspected and found free from symptoms of 'Candidatus Phytoplasma mali'. Mother plants should have been tested within the previous 3 years and found free from the pest;
AND
(B) (a) Plants produced in areas known to be free from 'Candidatus Phytoplasma mali';
or
(b) No more than 2% of plants in the production site 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 production site rogued out and destroyed immediately.
Pre-basic, Basic and Certified:
Additional measures could include
• Cultivation under insect-proof conditions (pre-basic);
• Isolation of mother plants from host plants of the pest and the vector, including uncultivated plants;
• Testing of candidate trees for mother plants;
• Mother plants in protected cultivation - retesting of all plants (pre-basic) or a representative sample (basic and certified) at least every 15 years;
• Other mother plants - testing of a representative sample (basic and certified) at least every 3 years;
• More testing in case of finding of an infection, including testing of all mother plants in the production site.
(A) Derived from mother plants which have been inspected and found free from symptoms of 'Candidatus Phytoplasma mali'. Mother plants should have been tested within the previous 3 years and found free from the pest;
AND
(B) (a) Plants produced in areas known to be free from 'Candidatus Phytoplasma mali';
or
(b) No more than 2% of plants in the production site 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 production site rogued out and destroyed immediately.
Pre-basic, Basic and Certified:
Additional measures could include
• Cultivation under insect-proof conditions (pre-basic);
• Isolation of mother plants from host plants of the pest and the vector, including uncultivated plants;
• Testing of candidate trees for mother plants;
• Mother plants in protected cultivation - retesting of all plants (pre-basic) or a representative sample (basic and certified) at least every 15 years;
• Other mother plants - testing of a representative sample (basic and certified) at least every 3 years;
• More testing in case of finding of an infection, including testing of all mother plants in the production site.
Justification (if necessary):
During the RNQP Project part 1, the following measures were recommended:
Non-certified material (‘CAC’):
(A) Derived from mother plants which have been inspected and found free from symptoms of 'Candidatus Phytoplasma mali';
AND
(B) (a) Plants produced in areas known to be free from 'Candidatus Phytoplasma mali';
or
(b) Site of production found free from 'Candidatus Phytoplasma mali' over the last complete growing season by visual inspection and any symptomatic plants in the immediate vicinity rogued out and destroyed immediately;
or
(c) No more than 2% of plants in the site of production showing symptoms during inspections at appropriate times during the last growing season, and those plants and any symptomatic plants in the immediate vicinity rogued out and destroyed immediately, and a representative sample of the remaining asymptomatic plants in the lots in which symptomatic plants were found has been tested and found free from 'Candidatus Phytoplasma mali'.
Pre-basic, Basic and Certified:
Additional measures could include
• Cultivation under insect-proof conditions (pre-basic);
• Isolation of mother plants from host plants of the pest and the vector, including uncultivated plants;
• Testing of candidate trees for mother plants;
• Mother plants in protected cultivation - retesting of all plants (pre-basic) or a representative sample (basic and certified) at least every 15 years;
• Other mother plants - testing of a representative sample (basic and certified) at least every 5 years;
• More testing in case of finding of an infection, including testing of all mother plants in the production site;
In RNQP Project part 1, a 2% threshold was also applicable to ‘Candidatus Phytoplasma pyri’ in the recommendation by the Fruit SEWG. However, in 2021, EU regulation for ‘Ca. P. Pyri’, option B)c) was replaced 2021 by:
(B)(c) the plants in the site of production and any plants in the immediate vicinity, which have shown symptoms of Candidatus Phytoplasma pyri during visual inspections at appropriate times during the last three growing seasons, have been rogued out and destroyed immediately.
During the RNQP Project part 2, the Fruit SEWG highlighted that there are three different vectors for pear decline. For ‘Ca. P. mali’, the risk of transmission is considered lower than for pear decline, but the situation is variable depending on the countries. On a scientific point of view, it is considered that 2% is already high since only based on symptoms. Symptomatology depends on drought and environmental factors. Technically, the Fruit SEWG considered that the 2% threshold was still justified for Ca. P. mali. Decision should be taken by the risk manager on a cost/benefit analysis, considering how this measure affects nursery growers.
During the RNQP Project part 1, the SEWG considered that visual examination of the mother plant was sufficient (no support for testing of the mother plants, as symptoms on mother plants are considered to be easily seen). Later, during the RNQP Project part 1, the coreHEWGplus discussed the ratio cost/benefit of a more systematic testing of CAC mother plants: This would allow detection of asymptomatic plants. However, this was counterbalanced by the difficulty of testing (testing would be more reliable, but not practical) and by the risk of reinfestation in case of high vector pressure. No consensus was reached within the core-HEWGplus on the added value of such a more systematic testing, in the context of the RNQP status.
During the RNQP Project part 2, the Fruit SEWG considered that measures without any testing of the CAC mother plants are too weak, but this testing is not very practical when using different sources of material depending on the years.
Remark: when testing the mother plants, the roots should be tested.
During the RNQP Project part 2, the following information was collected on resistant rootstocks (Petruschke, pers. comm., 2024):
there are promising tolerant rootstock for extensive production but not for intensive production on small trees. Although there is no trial data from larger cultivation trials, a lot of information is already available for D2212 Malia (R). Experience shows that
- it has very good properties as a rootstock for container trees, robust and very long-lived
- according to the test protocols in the basic stock (meanwhile several 1000 PCR's), apples on D 2212 remain phytoplasma-free, and if there is an infection via the scion variety, it disappears the following year
- D 2212 is stable, produces early and promotes fruit size, ideal for medium-sized tree shapes
- tolerates very high temperatures (ideal for thermotherapy)
- for very vigorous cider apple varieties (Brettacher, Kaiser Wilhelm), can also be trained to produce tall stems, but is actually more of a rootstock for half-stems. Also suitable as a spindle for low-growing varieties (Ananasrenette).
- Resistance to black bark blight (Diplodia spp.) is currently being tested.
- Resistance to the soil-borne fungus Athelia rolfsii has been proven.
Concerning other apple proliferation-resistant apple rootstocks, a joint project of the JKI, RLP Agroscience, Neustadt and the San Michele experimental station resulted in many new crosses, which were tested in a federal trial in Germany. However, all trials have been canceled. None of the new rootstocks was an alternative to the standard rootstock M 9.
Following a comment received from Germany, the Fruit SEWG also discussed during RNQP Project part 2 whether by derogation, when infestation occurs on 'Ca. P. mali'-resistant rootstocks (e.g. D2212), plants should be exempted from the requirement to be destructed.
The Fruit SEWG commented that if testing the mother plants every 3 years under outdoor conditions, since symptoms should not appear during the first years, resistant rootstocks can be used under option (B)(b) and there is limited risk that symptoms would be observed in the first years. Developing an option (d) for resistant rootstocks may not be necessary.
Non-certified material (‘CAC’):
(A) Derived from mother plants which have been inspected and found free from symptoms of 'Candidatus Phytoplasma mali';
AND
(B) (a) Plants produced in areas known to be free from 'Candidatus Phytoplasma mali';
or
(b) Site of production found free from 'Candidatus Phytoplasma mali' over the last complete growing season by visual inspection and any symptomatic plants in the immediate vicinity rogued out and destroyed immediately;
or
(c) No more than 2% of plants in the site of production showing symptoms during inspections at appropriate times during the last growing season, and those plants and any symptomatic plants in the immediate vicinity rogued out and destroyed immediately, and a representative sample of the remaining asymptomatic plants in the lots in which symptomatic plants were found has been tested and found free from 'Candidatus Phytoplasma mali'.
Pre-basic, Basic and Certified:
Additional measures could include
• Cultivation under insect-proof conditions (pre-basic);
• Isolation of mother plants from host plants of the pest and the vector, including uncultivated plants;
• Testing of candidate trees for mother plants;
• Mother plants in protected cultivation - retesting of all plants (pre-basic) or a representative sample (basic and certified) at least every 15 years;
• Other mother plants - testing of a representative sample (basic and certified) at least every 5 years;
• More testing in case of finding of an infection, including testing of all mother plants in the production site;
In RNQP Project part 1, a 2% threshold was also applicable to ‘Candidatus Phytoplasma pyri’ in the recommendation by the Fruit SEWG. However, in 2021, EU regulation for ‘Ca. P. Pyri’, option B)c) was replaced 2021 by:
(B)(c) the plants in the site of production and any plants in the immediate vicinity, which have shown symptoms of Candidatus Phytoplasma pyri during visual inspections at appropriate times during the last three growing seasons, have been rogued out and destroyed immediately.
During the RNQP Project part 2, the Fruit SEWG highlighted that there are three different vectors for pear decline. For ‘Ca. P. mali’, the risk of transmission is considered lower than for pear decline, but the situation is variable depending on the countries. On a scientific point of view, it is considered that 2% is already high since only based on symptoms. Symptomatology depends on drought and environmental factors. Technically, the Fruit SEWG considered that the 2% threshold was still justified for Ca. P. mali. Decision should be taken by the risk manager on a cost/benefit analysis, considering how this measure affects nursery growers.
During the RNQP Project part 1, the SEWG considered that visual examination of the mother plant was sufficient (no support for testing of the mother plants, as symptoms on mother plants are considered to be easily seen). Later, during the RNQP Project part 1, the coreHEWGplus discussed the ratio cost/benefit of a more systematic testing of CAC mother plants: This would allow detection of asymptomatic plants. However, this was counterbalanced by the difficulty of testing (testing would be more reliable, but not practical) and by the risk of reinfestation in case of high vector pressure. No consensus was reached within the core-HEWGplus on the added value of such a more systematic testing, in the context of the RNQP status.
During the RNQP Project part 2, the Fruit SEWG considered that measures without any testing of the CAC mother plants are too weak, but this testing is not very practical when using different sources of material depending on the years.
Remark: when testing the mother plants, the roots should be tested.
During the RNQP Project part 2, the following information was collected on resistant rootstocks (Petruschke, pers. comm., 2024):
there are promising tolerant rootstock for extensive production but not for intensive production on small trees. Although there is no trial data from larger cultivation trials, a lot of information is already available for D2212 Malia (R). Experience shows that
- it has very good properties as a rootstock for container trees, robust and very long-lived
- according to the test protocols in the basic stock (meanwhile several 1000 PCR's), apples on D 2212 remain phytoplasma-free, and if there is an infection via the scion variety, it disappears the following year
- D 2212 is stable, produces early and promotes fruit size, ideal for medium-sized tree shapes
- tolerates very high temperatures (ideal for thermotherapy)
- for very vigorous cider apple varieties (Brettacher, Kaiser Wilhelm), can also be trained to produce tall stems, but is actually more of a rootstock for half-stems. Also suitable as a spindle for low-growing varieties (Ananasrenette).
- Resistance to black bark blight (Diplodia spp.) is currently being tested.
- Resistance to the soil-borne fungus Athelia rolfsii has been proven.
Concerning other apple proliferation-resistant apple rootstocks, a joint project of the JKI, RLP Agroscience, Neustadt and the San Michele experimental station resulted in many new crosses, which were tested in a federal trial in Germany. However, all trials have been canceled. None of the new rootstocks was an alternative to the standard rootstock M 9.
Following a comment received from Germany, the Fruit SEWG also discussed during RNQP Project part 2 whether by derogation, when infestation occurs on 'Ca. P. mali'-resistant rootstocks (e.g. D2212), plants should be exempted from the requirement to be destructed.
The Fruit SEWG commented that if testing the mother plants every 3 years under outdoor conditions, since symptoms should not appear during the first years, resistant rootstocks can be used under option (B)(b) and there is limited risk that symptoms would be observed in the first years. Developing an option (d) for resistant rootstocks may not be necessary.
REFERENCES:
- ANSES (2012) Rapport d'expertise collective. Groupe de travail "ARP phytoplasmes des arbres fruitiers". Available at https://www.anses.fr/fr/system/files/SVEG2011sa0137Ra.pdf;
- Baric S, Öttl S & Dalla Via J (2010) Infection rates of natural psyllid populations with ‘Candidatus Phytoplasma mali’in South Tyrol (Northern Italy). In Proceedings of the 21st International Conference on Virus and other Graft Transmissible Diseases of Fruit Crops July 5-10, 2009, Neustadt, Germany (pp. 189-192). Julius Kühn-Inst. Bundesforschungsinst. für Kulturpflanzen.
- Bertaccini A, Duduk B, Paltrinieri S & Contaldo N (2014) Phytoplasmas and phytoplasma diseases: a severe threat to agriculture. American Journal of Plant Sciences, 2014;
- Bulgari D, Casati P, Quaglino F & Bianco P A (2014) Isolation of potential biocontrol agents of ‘Candidatus Phytoplasma mali’. Phytoplasmas and phytoplasma disease management: how to reduce their economic impact. International Phytoplasmologist Working Group. Food and Agriculture COST Action FA0807, 226. Available at: http://www.cost.eu/download/FAP_FA0807;
- Corretto E, Trenti M, Štarhová Serbina L, Howie JM, Dittmer J, Kerschbamer C, Candian V, Tedeschi R, Janik K & Schuler H (2023) Multiple factors driving the acquisition efficiency of apple proliferation phytoplasma in Cacopsylla melanoneura. Journal of Pest Science. https://doi.org/10.1007/s10340-023-01699-1
- EU COM (2016) Recommendation of the Working Group on the Annexes of the Council Directive 2000/29/EC – Section II – Listing of Harmful Organisms as regards the future listing of Candidatus Phytoplasma mali [Apple Proliferation Mycoplasm];
- Janik K (2020) Apple Proliferation Nothern Italy & Germany—A Joint Review.
- Jarausch B, Fuchs A, Schwind N, Krczal G & Jarausch W (2007) Cacopsylla picta as most important vector for ‘Candidatus Phytoplasma mali’ in Germany and neighbouring regions.
- Mittelberger C, Obkircher L, Oettl S, Oppedisano T, Pedrazzoli F, Panassiti B, Kerschbamer C, Anfora G & Janik K (2017) The insect vector Cacopsylla picta vertically transmits the bacterium ‘Candidatus Phytoplasma mali’ to its progeny. Plant Pathology.
- Prima phacie (2012) Pest risk assessment for the European Community plant health: A comparative approach with case studies. External scientific report by group of authors: http://www.efsa.europa.eu/fr/supporting/doc/319e.pdf;
- Schneider B, Sule S, Jelkmann W & Seemüller E (2014) Suppression of aggressive strains of ‘Candidatus phytoplasma mali’by mild strains in Catharanthus roseus and Nicotiana occidentalis and indication of similar action in apple trees. Phytopathology, 104, 453-461;
- Seemüller E, Carraro L, Jarausch W & Schneider B (2011) Apple proliferation phytoplasma. In: Virus and Virus-Like Disease of Pome and Stone Fruits. Edited by Hadidi A, Barba M, Candresse T and Jelkman W, p. 67-73;