| 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 asteris (PHYPAS)
GENERAL INFORMATION ON THE PEST
Name as submitted in the project specification (if different):
Candidatus phytoplasma asteris (Aster yellows phytoplasma)
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 blueberry witches' broom phytoplasma for Vaccinium, and 'stolbur' as strawberry lethal decline and the strawberry green petal phytoplasma for strawberry, the Fruit SEWG proposed during RNQP Project 1 to discard all names of phytoplasma listed in the EU Marketing Directive and to add all phytoplasma species reported from naturally infected Fragaria and Vaccinium plants.
This consisted for Vaccinium in the listing of ‘Candidatus Phytoplasma pruni’, ‘Candidatus Phytoplasma asteris’ (blueberry stunt phytoplasma), ‘Candidatus Phytoplasma solani’ (blueberry reddening disease), and the Cranberry false blossom phytoplasma.
For strawberry, 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 clover phyllody phytoplasma. 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 and ‘Candidatus Phytoplasma australiense’).
Consequently, ‘Candidatus Phytoplasma asteris’ was listed in the revised Marketing Directive for Fragaria and Vaccinium.
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 infecting Fragaria and Vaccinium 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.
Remark: Symptoms characteristic for phytoplasma disease in strawberry can be associated with different organisms (in Padovan et al. (2000) strawberry green petal (SGP) and strawberry lethal yellows (SLY): phytoplasma or Ricketssia sp). It is also possible that one phytoplasma may be associated with very different symptoms; factors that may account for the differences include the age of the plant at time of infection, the level of phytoplasmas inoculated at infection, and environmental factors including temperature. It is also possible that different symptoms of SGP and SLY represent disease progression (Padovan et al., 2000).
Examples:
• Strawberry green petal disease can be linked to three different phytoplasma species: ‘Ca. P. tritici' formerly 'asteris’-related strains 16SrI-C/16SrI-R (Contaldo et al, 2012; Harrison et al., 1997; Gundersen et al., 1996; Jomantiene et al., 2002), ‘Ca. P. hispanicum’-related strains 16SrXIII(A/I)I (Pérez-Lopéz & Dumonceaux, 2016; Pérez-Lopéz et al., 2017), and ‘Ca. P. australiense’-related strains 16SrXII (Padovan et al., 2000) (cited from Brochu et al., 2021).
• blueberry stunt disease is usually associated to Ca.P.asteris 16SrI-E, but also 16SrIX-E (‘Ca. P. phoenicium’-related) could be linked to blueberry stunt disease in New Jersey (Bagadia et al., 2013).
This consisted for Vaccinium in the listing of ‘Candidatus Phytoplasma pruni’, ‘Candidatus Phytoplasma asteris’ (blueberry stunt phytoplasma), ‘Candidatus Phytoplasma solani’ (blueberry reddening disease), and the Cranberry false blossom phytoplasma.
For strawberry, 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 clover phyllody phytoplasma. 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 and ‘Candidatus Phytoplasma australiense’).
Consequently, ‘Candidatus Phytoplasma asteris’ was listed in the revised Marketing Directive for Fragaria and Vaccinium.
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 infecting Fragaria and Vaccinium 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.
Remark: Symptoms characteristic for phytoplasma disease in strawberry can be associated with different organisms (in Padovan et al. (2000) strawberry green petal (SGP) and strawberry lethal yellows (SLY): phytoplasma or Ricketssia sp). It is also possible that one phytoplasma may be associated with very different symptoms; factors that may account for the differences include the age of the plant at time of infection, the level of phytoplasmas inoculated at infection, and environmental factors including temperature. It is also possible that different symptoms of SGP and SLY represent disease progression (Padovan et al., 2000).
Examples:
• Strawberry green petal disease can be linked to three different phytoplasma species: ‘Ca. P. tritici' formerly 'asteris’-related strains 16SrI-C/16SrI-R (Contaldo et al, 2012; Harrison et al., 1997; Gundersen et al., 1996; Jomantiene et al., 2002), ‘Ca. P. hispanicum’-related strains 16SrXIII(A/I)I (Pérez-Lopéz & Dumonceaux, 2016; Pérez-Lopéz et al., 2017), and ‘Ca. P. australiense’-related strains 16SrXII (Padovan et al., 2000) (cited from Brochu et al., 2021).
• blueberry stunt disease is usually associated to Ca.P.asteris 16SrI-E, but also 16SrIX-E (‘Ca. P. phoenicium’-related) could be linked to blueberry stunt disease in New Jersey (Bagadia 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):
Belgium (2019); Czech Republic (2011); Denmark (2019); France (1976); Germany (1993); Hungary (2020); Italy (2010); Romania (1976); Spain (1999)
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/).
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, including seeds
3 - Is the pest already listed in a PM4 standard on the concerned host plant?
Yes
Conclusion:
Evaluation continues
Justification (if necessary):
EPPO Standard PM 4/11 Certification scheme for strawberry recommends testing for aster yellows phytoplasma. When responding to the questionnaire, PL considered that plants for planting was not the main pathway but did not provide enough supporting evidence. The Fruit SEWG recommended to re-assess the RNQP status of this pest on Fragaria.
4 - Are the listed plants for planting the main* pathway for the "pest/host/intended use" combination? (*: significant compared to others):
No
Conclusion:
Not candidate
Justification:
‘Candidatus Phytoplasma asteris’ (and related strains) appears to have a wide host range. The vast majority of strains in the aster yellows (AY, 16SrI) group infect herbaceous dicotyledonous plant hosts. However, a number of strains that belong to subgroups 16SrI-A, 16SrI-B and 16SrI-C are capable of infecting monocotyledonous plants (e.g., maize, onion, gladiolus, oat, wheat and grass). Some strains in subgroups 16SrI-A, 16SrI-B, 16SrI-D, 16SrI-E, 16SrI-F and 16SrI-Q can induce disease in woody plants (e.g., grey dogwood, sandalwood, blueberry, mulberry, peach, cherry, olive, grapevine and paulownia). For many of the plant hosts which have previously been reported to be affected by AY diseases on the basis of symptomatology and/or microscopic examinations (see McCoy et al., 1989; cited in CABI, 2011), the identity of the infecting phytoplasmas has never been determined with molecular techniques, or proved to be different from that of other established AY phytoplasma strains (Schneider et al., 1997; Marcone et al., 2000). Both strawberry (Cieslinska, 2011; Jomantiene et al., 1998; 2002: Ferriol-Marchena et al., 2013; Plante et al, 2021) and Vaccinium spp. can be infected by ‘Ca. P. asteris’ (Arocha‐Rosete et al., 2019; Brochu et al., 2022; Cieslinska, 2011; Dale & Mainland, 1981).
‘Candidatus Phytoplasma asteris’ is naturally transmitted by a wide range of leafhoppers. However, Macrosteles fascifrons [M. quadrilineatus] is reported to be the principal vector (Lee et al., 1998b, 2004; Weintraub & Beanland, 2006). In strawberry also leafhoppers Aphrodes bicincta and Euscelis lineolatus were able to transmit aster yellows (16SrI-C) to strawberry (Posnette & Ellenberger, 1963)
The phytoplasmas are seed transmitted, and there are reports of seed transmission for 'Ca. P. asteris' in several herbaceous species such as tomato, carrot, corn and others.
It may also be introduced into new areas where it may have never existed before by importing vegetative propagating materials that carry the pathogen undetected (CABI, 2011).
Strawberry is considered being a dead-end host: Although impact to the individual strawberry plant might be high (the plant may die), the phytoplasma detected in strawberry is most often the phytoplasma occurring in that specific region. The vector moves into the strawberry field infecting strawberry with phytoplasma.
Remark: definition of a dead-end host by Weintraub & Beanland (2006): Dead-end hosts are plants that can be inoculated and subsequently become infected with phytoplasma, but from which insects cannot acquire phytoplasma. Several other dead-end hosts have been identified (e.g., AY from Cyclamen persicum L.) (2). Grapevine is a dead-end host for the stolbur (Stol) phytoplasma associated with bois noir and vergilbungskrankheit grapevine yellows (GY) transmitted by the planthopper Hyalesthes obsoletus (E. Boudon-Padieu & M. Maixner, personal communication).
‘Candidatus Phytoplasma asteris’ is naturally transmitted by a wide range of leafhoppers. However, Macrosteles fascifrons [M. quadrilineatus] is reported to be the principal vector (Lee et al., 1998b, 2004; Weintraub & Beanland, 2006). In strawberry also leafhoppers Aphrodes bicincta and Euscelis lineolatus were able to transmit aster yellows (16SrI-C) to strawberry (Posnette & Ellenberger, 1963)
The phytoplasmas are seed transmitted, and there are reports of seed transmission for 'Ca. P. asteris' in several herbaceous species such as tomato, carrot, corn and others.
It may also be introduced into new areas where it may have never existed before by importing vegetative propagating materials that carry the pathogen undetected (CABI, 2011).
Strawberry is considered being a dead-end host: Although impact to the individual strawberry plant might be high (the plant may die), the phytoplasma detected in strawberry is most often the phytoplasma occurring in that specific region. The vector moves into the strawberry field infecting strawberry with phytoplasma.
Remark: definition of a dead-end host by Weintraub & Beanland (2006): Dead-end hosts are plants that can be inoculated and subsequently become infected with phytoplasma, but from which insects cannot acquire phytoplasma. Several other dead-end hosts have been identified (e.g., AY from Cyclamen persicum L.) (2). Grapevine is a dead-end host for the stolbur (Stol) phytoplasma associated with bois noir and vergilbungskrankheit grapevine yellows (GY) transmitted by the planthopper Hyalesthes obsoletus (E. Boudon-Padieu & M. Maixner, personal communication).
5 - Economic impact:
Are there documented reports of any economic impact on the host?
Justification:
The incidence of aster yellows in strawberry is normally low, although it may occasionally reach as high as 20%. Infected plants produce no marketable fruit and usually die within two month after symptoms appear (Chiykowski, 1987).
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?
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:
Justification:
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:
Remark: Removal of plants for planting showing symptoms might have some effect, but in relation to the activity of vectors it will only partly help.
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: plants for planting is not considered as a significant pathway compared to natural dispersal. Strawberry is a dead-end host.
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:
- Arocha‐Rosete Y, Lambert L, Joly‐Séguin V, Michelutti R, Schilder A & Bertaccini A (2019) Surveys reveal a complex association of phytoplasmas and viruses with the blueberry stunt disease on Canadian blueberry farms. Annals of Applied Biology 174(2), 142-152.
- Bagadia PG, Polashock J, Bottner-Parke, KD, Zhao Y, Davis RE & Lee IM (2013) Characterization and molecular differentiation of 16SrI-E and 16SrIX-E phytoplasmas associated with blueberry stunt disease in New Jersey. Molecular and Cellular Probes 27(2), 90-97.
- Brochu AS, Rodríguez-Martínez D, Goulet C & Pérez-López E (2021) Strawberry green petal disease: a diagnostic guide. Plant Health Progress 22(4), 591-595.
- Brochu AS, Methot A, Breton AM, Lacroix C, Légaré JP & Pérez‐López E (2022) First report of a ‘Candidatus Phytoplasma asteris’ strain affecting lingonberry (Vaccinium vitis‐idaea) and causing lingonberry stunt phytoplasma disease. New Disease Reports 45(1), 12058.
- CABI (2011) ‘Candidatus Phytoplasma asteris’ (yellow disease phytoplasmas). CABI Compendium 7642. https://doi.org/10.1079/cabicompendium.7642 (Assessed 16/Sep/2024).
- Chiykowski LN (1987) Aster Yellows in strawberry. In Virus Disease of Small Fruits (ed Converse RH). US Department of Agriculture, Agricultural Research Service Handbook No. 631. pp. 31-34
- Cieslinska M (2011) Viruses and phytoplasmas of small fruit plants maintained in collection of Institute of Horticulture in Skierniewice, Poland. IOBC/WPRS Bulletin 70, 69-74.
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