| Legend |
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| 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 tritici {Clover phyllody phytoplasma} (PHYP03)
GENERAL INFORMATION ON THE PEST
Name as submitted in the project specification (if different):
Clover phyllody phytoplasma (strawberry green petal phytoplasmas)
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):
In 1962, Chiykowski reported that clover phyllody and strawberry green petal diseases were associated with the same pathogen. Currently, this pathogen is listed as 'Candidatus Phytoplasma tritici' (Lee et al., 2004; Zhao et al., 2021). It should be noted that green petal symptoms may also be associated with other phytoplasmas such as 'Candidatus Phytoplasma australiense' (Padovan et al., 2000) or 'Ca. P. hispanicum' (Brochu et al., 2021).
Instead of listing 'stolbur' as strawberry lethal decline and the strawberry green petal phytoplasma, it was recommended during the RNQP Project 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. All these phytoplasma are causing leaf yellowing symptoms, but just some of them are responsible for green petal symptoms (this includes the clover phyllody phytoplasma and ‘Candidatus Phytoplasma australiense’).
'Clover phyllody phytoplasma' was formerly considered as a subgroup of the Aster Yellows group: 16SrI-C. Zhao et al. (2021) described that phytoplasmas in the 16SrI-C belong to a new species 'Candidatus Phytoplasma tritici'. Arguments for this are that: the AY group is very diverse, and probably consists of more than one species, and that in China 16SrI-C is strongly linked with wheat blue dwarf and the vector Psammotettix striatus.
In responses to the questionnaire, AT suggested 'to merge all 'Ca. Phytoplasma' species infecting Fragaria into one category (no differentiation of symptoms, testing using universal phytoplasma tests). However, the Fruit SEWG maintained the recommendation to list individual species.
In the case a plant shows phytoplasma symptoms, a generic PCR test should be performed since also growth inhibitors and rickettias can be associated with similar symptoms.
Instead of listing 'stolbur' as strawberry lethal decline and the strawberry green petal phytoplasma, it was recommended during the RNQP Project 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. All these phytoplasma are causing leaf yellowing symptoms, but just some of them are responsible for green petal symptoms (this includes the clover phyllody phytoplasma and ‘Candidatus Phytoplasma australiense’).
'Clover phyllody phytoplasma' was formerly considered as a subgroup of the Aster Yellows group: 16SrI-C. Zhao et al. (2021) described that phytoplasmas in the 16SrI-C belong to a new species 'Candidatus Phytoplasma tritici'. Arguments for this are that: the AY group is very diverse, and probably consists of more than one species, and that in China 16SrI-C is strongly linked with wheat blue dwarf and the vector Psammotettix striatus.
In responses to the questionnaire, AT suggested 'to merge all 'Ca. Phytoplasma' species infecting Fragaria into one category (no differentiation of symptoms, testing using universal phytoplasma tests). However, the Fruit SEWG maintained the recommendation to list individual species.
In the case a plant shows phytoplasma symptoms, a generic PCR test should be performed since also growth inhibitors and rickettias can be associated with similar symptoms.
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):
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):
Listed in PM4/11 as Strawberry green petal 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 assess this pest/hot combination more in detail since 'Clover phyllody phytoplasma' is considered as a subgroup of the aster yellows group.
4 - Are the listed plants for planting the main* pathway for the "pest/host/intended use" combination? (*: significant compared to others):
?
Conclusion:
Justification:
Psammotettix striatus (see section on Identity) is considered as synonym for the leafhopper species P. alienus (EPPO Global Database; Holzinger, personal communication). P. alienus is widespread in Europe and also known as a vector of wheat dwarf virus. In principle, the insect species is regarded as oligophagous on grasses. However, in a study using electrical penetration graphs, Tholt et al. (2015) demonstrated that P. alienus also probes on dicotyledons. A probing/feeding activity on Fragaria seems possible (Holzinger, personal communication).
In addition, the leafhoppers Aphrodes bicincta and Euscelis lineolatus were reported to transmit the causal agent of strawberry green petal disease (Posnette & Ellenberger, 1963); however, at the time of this publication no molecular identification of the involved pathogen was feasible.
Tests in Lithuania in 2007 identified 16SrI-C phytoplasmas as causal agents of poa stunt and festuca yellows, but the insect vectors of subgroup 16SrI-C phytoplasma strains in Lithuania and neighboring countries remained unidentified (Valinjnas et al., 2007). In Canada, strawberry green petal disease induced by a 16SrI-C phytoplasma related strain is seen as linked to increasing numbers of leafhoppers in strawberry fields (Plante et al., 2021).
It remains unclear whether plants for planting should be considered as a significant pathway compared to natural spread by vectors.
In addition, the leafhoppers Aphrodes bicincta and Euscelis lineolatus were reported to transmit the causal agent of strawberry green petal disease (Posnette & Ellenberger, 1963); however, at the time of this publication no molecular identification of the involved pathogen was feasible.
Tests in Lithuania in 2007 identified 16SrI-C phytoplasmas as causal agents of poa stunt and festuca yellows, but the insect vectors of subgroup 16SrI-C phytoplasma strains in Lithuania and neighboring countries remained unidentified (Valinjnas et al., 2007). In Canada, strawberry green petal disease induced by a 16SrI-C phytoplasma related strain is seen as linked to increasing numbers of leafhoppers in strawberry fields (Plante et al., 2021).
It remains unclear whether plants for planting should be considered as a significant pathway compared to natural spread by vectors.
5 - Economic impact:
Are there documented reports of any economic impact on the host?
Yes
Justification:
The disease is characterized by small and red-leaves, the infected plants bear abnormal fruits and frequently show diagnostic symptoms of virescence on flowers (reviewed in Franova Honetslegrova et al., 1996; Contaldo et al., 2012; Plante et al., 2021). In studies in Czech Republic during 1991-1995, strawberry with strawberry green petal symptoms was very rare, indicating a low incidence of this phytoplasma in strawberry in the Czech Republic. The authors concluded that this may be the positive consequence of long term use of meristem derived strawberry seedlings by Czech Republic growers (Franova Honetslegrova, et al. 1996).
What is the likely economic impact of the pest irrespective of its infestation source in the absence of phytosanitary measures? (= official measures)
Minor
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:
Green petal: Economic impact is generally minor.
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?
No
Conclusion:
Not candidate
Justification:
Lack of knowledge on epidemic disease cycle.
7- Is the quality of the data sufficient to recommend the pest to be listed as a RNQP?
No
Conclusion:
Justification:
Role of propagation material as a pathway is unclear, presumably low due to in vitro propagation of strawberry. The epidemic disease cycle is unclear, likely at least some spread by insect vectors.
CONCLUSION ON THE STATUS:
Disqualified: unclear whether plants for planting should be considered as a significant pathway. Economic impact is acceptable.
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:
- 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.
- CABI (2011) ‘Candidatus Phytoplasma asteris’ (yellow disease phytoplasmas). CABI Compendium 7642. https://doi.org/10.1079/cabicompendium.7642 (Assessed 16/Sep/2024).
- Chiykowski LN (1962) Clover phyllody and strawberry green petal diseases, caused by the same virus in eastern Canada. Canadian Journal of Botany 40(12), 1615-1617.
- 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
- Contaldo N, Mejia JF, Paltrinieri S, Calari A & Bertaccini A (2012) Identification and GroEL gene characterization of green petal phytoplasma infecting strawberry in Italy. Phytopathogenic Mollicutes 2(2), 59-62.
- Franova-HonetŜlegrová JF, Vibio M & Bertaccinc A (1996) Electron microscopy and molecular identification of phytoplasmas associated with strawberry green petals in the Czech Republic. European Journal of Plant Pathology 102, 831–835. https://doi.org/10.1007/BF01877052.
- Harrison NA, Legard DE, DiBonito R & Richardson PA (1997) Detection and differentiation of phytoplasmas associated with diseases of strawberry in Florida. Plant Disease 81(2), 230-230.
- Lee IM, Gundersen-Rindal DE, Davis RE, Bottner KD, Marcone C & Seemüller E (2004) ‘Candidatus Phytoplasma asteris’, a novel phytoplasma taxon associated with aster yellows and related diseases. International journal of systematic and evolutionary microbiology 54(4), 1037-1048.
- Padovan A, Gibb K & Persley D (2000) Association of `Candidatus Phytoplasma australiense' with green petal and lethal yellows diseases in strawberry. Plant Pathology 49, 362-369.
- Pérez-López E & Dumonceaux TJ (2016). Detection and identification of the heterogeneous novel subgroup 16SrXIII-(A/I) I phytoplasma associated with strawberry green petal disease and Mexican periwinkle virescence. International Journal of Systematic and Evolutionary Microbiology 66(11), 4406-4415.
- Pérez-López E, Rodríguez-Martínez D, Olivier CY, Luna-Rodríguez M & Dumonceaux TJ (2017). Molecular diagnostic assays based on cpn60 UT sequences reveal the geographic distribution of subgroup 16SrXIII-(A/I) I phytoplasma in Mexico. Scientific Reports 7(1), 950.
- Plante N, Brochu AS, Goulet C, Thibault P, Fournier V & Pérez‐López E (2021) First evidence of the occurrence of a putative new subgroup of ‘Candidatus Phytoplasma asteris’(16SrI) associated with strawberry green petal disease in Quebec, Canada. New Disease Reports 44(1), 12038.
- Posnette AF & Ellenberger CE (1963) Further studies of green petal and other leafhopper-transmitted viruses infecting strawberry and clover. Annals of Applied Biology 51, 69-83.
- Schneider B, Marcone C, Kampmann M, Ragozzino A, Lederer W, Cousin MT & Seemüller E (1997) Characterization and classification of phytoplasmas from wild and cultivated plants by RFLP and sequence analysis of ribosomal DNA. European Journal of Plant Pathology 103(8), 675-686.
- Tholt G, Samu F & Kiss B (2015) Feeding behaviour of a virus-vector leafhopper on host and non-host plants characterised by electrical penetration graphs. Entomologia experimentalis et applicata 155, 123-136.
- Valinjnas D., Urbanavlýieno L, Jomantieno R & Davis RE (2007) Molecular detection, classification, and phylogenetic analysis of subgroup 16SrI-C phytoplasmas detected in diseased Poa and Festuca in Lithuania. Biologija 18 (2), 63-66.
- Weintraub PG & Beanland L (2006). Insect vectors of phytoplasmas. Annual review of Entomology 51(1), 91-111.
- Zhao Y, Wei W, Davis RE, Lee IM & Bottner-Parker KD (2021) The agent associated with blue dwarf disease in wheat represents a new phytoplasma taxon, 'Candidatus Phytoplasma tritici'. International Journal of Systematic and Evolutionary Microbiology 71(1). doi: 10.1099/ijsem.0.004604.