| 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 solani (PHYPSO)
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 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 the clover phyllody phytoplasma. All these phytoplasma 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’).
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.
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 the clover phyllody phytoplasma. All these phytoplasma 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’).
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.
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 (2014); Bulgaria (2019); Croatia (2015); Czech Republic (2009); France (2017); Germany (2010); Greece (2019); Hungary (2011); Italy (2019); Italy/Sicilia (2020); Poland (1999); Slovakia (2000); Slovenia (2017); Spain (2014)
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, except seeds
3 - Is the pest already listed in a PM4 standard on the concerned host plant?
No
Conclusion:
Evaluation continues
Justification (if necessary):
EPPO Standard PM 4/11 Certification scheme for strawberry recommends testing for 'strawberry green petal phytoplasma', 'lethal decline', 'aster yellows phytoplasma', 'phytoplasma yellows' etc. When responding to the questionnaire, PL considered that plants for planting was not the main pathway. Evaluation continues.
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:
Over the past few decades ‘Candidatus Phytoplasma solani’, belonging to the 16SrXII-A ribosomal subgroup, has been found to be associated with a range of plant diseases in different agro-ecosystems in many European countries and all over the world. It is thought likely that it has always been present in Europe, but has only been noticed in recent years. Diseases associated include bois noir in grapevines, 'stolbur' in e.g. tomatoes potatoes, and yellowing, reddening, decline, dwarfism, leaf malformation and degeneration diseases of other wild and cultivated plants (CABI, 2017). In strawberry it was associated with a disease called strawberry decline in Northern Italy, characterized by pronounced stunting and a very poor root system (Terlizzi et al., 2006); in Serbia, it was reported as associated with a reddening disease in Vaccinium corymbosum (Starović et al., 2013).
'Ca. P. solani’ is transmitted from plant to plant by the polyphagous planthopper Hyalesthes obsoletus (Cixiidae), which has a European origin and is ubiquitous in European countries. Although it can complete its life cycle on only a small number of plant species (e.g. Convolvulus), it feeds on a much wider range. Recent studies have demonstrated the presence of additional insect vectors of this phytoplasma in Europe, such as Reptalus panzeri (Mitrović et al., 2016), R. quinquecostatus (Chuche et al., 2016), and Anaceratagallia ribauti (Riedle-Bauer et al., 2008) and several others. This scenario highlights the extreme complexity of the ecology of both ‘Ca. P. solani’ and its insect vectors, underlying the difficulty in studying the epidemiology of diseases associated with this pathogen and in developing efficient control strategies. ‘Ca. P. solani’ is also transmitted by parasitic plants.
‘Ca. P. solani’ is transmissible by grafting and vegetative propagation (CABI, 2017; EFSA Panel on Plant Health, 2014), irrespective of whether the stock or the scion is infective (CABI, 2017), and can be disseminated with propagation material. In the European Union it is listed as a harmful organism necessitating restrictions on the import of plants in the family Solanaceae (CABI, 2017).
‘Ca. P. solani’ is not thought to be transmitted in the true seed of any of its hosts, but it can be transmitted by vegetative propagation of infected host plants (EFSA, 2014).
The Fruit SEWG considered that strawberry was a dead-end host and plants for planting should not be considered as a significant pathway.
'Ca. P. solani’ is transmitted from plant to plant by the polyphagous planthopper Hyalesthes obsoletus (Cixiidae), which has a European origin and is ubiquitous in European countries. Although it can complete its life cycle on only a small number of plant species (e.g. Convolvulus), it feeds on a much wider range. Recent studies have demonstrated the presence of additional insect vectors of this phytoplasma in Europe, such as Reptalus panzeri (Mitrović et al., 2016), R. quinquecostatus (Chuche et al., 2016), and Anaceratagallia ribauti (Riedle-Bauer et al., 2008) and several others. This scenario highlights the extreme complexity of the ecology of both ‘Ca. P. solani’ and its insect vectors, underlying the difficulty in studying the epidemiology of diseases associated with this pathogen and in developing efficient control strategies. ‘Ca. P. solani’ is also transmitted by parasitic plants.
‘Ca. P. solani’ is transmissible by grafting and vegetative propagation (CABI, 2017; EFSA Panel on Plant Health, 2014), irrespective of whether the stock or the scion is infective (CABI, 2017), and can be disseminated with propagation material. In the European Union it is listed as a harmful organism necessitating restrictions on the import of plants in the family Solanaceae (CABI, 2017).
‘Ca. P. solani’ is not thought to be transmitted in the true seed of any of its hosts, but it can be transmitted by vegetative propagation of infected host plants (EFSA, 2014).
The Fruit SEWG considered that strawberry was a dead-end host and plants for planting should not be considered as a significant pathway.
5 - Economic impact:
Are there documented reports of any economic impact on the host?
Yes
Justification:
‘Candidatus Phytoplasma solani’ is associated with a disease in strawberry which is characterized by pronounced stunting and a very poor root system. Older leaves of diseased plants rolled upward and displayed a marked premature purple discoloration; new leaves showed size reduction, shortened petioles, chlorosis, and were generally cupped. When some of these plants were potted and kept in greenhouse conditions, they exhibited typical floral abnormalities as virescent and phylloid petals the following spring. Flowers were fully or partly sterile, producing small and deformed fruits; new foliage was dwarfed, asymmetrical, and pale green with chlorotic margins. Later, the affected plants expressed a quick decline consisting of growth cessation, bronzing of mature leaves, wilting, and death (Terlizzi et al., 2006). When infected plant material was replanted, the plants showed stunting, yellowing and poor establishment (Hodgetts et al., 2015).
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?
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?
Conclusion:
Justification:
In other hosts, 'Candidatus Phytoplasma solani' infects grapevine ('bois noir' disease), producing leaf yellows (in whiteberried cultivars) or leaf reddening (in red-berried cultivars), downwards leaf rolling, irregular ripening of wood, growth reduction and shriveling and drying up of berries and bunches. Young grapevine plants can die following infection, while older plants tend to recover (Belli et al., 2010). In potato, 'Ca. P. solani' is associated with red discoloration of the top leaves, shortened internodes, early senescence and finally, plant wilting and death (Holeva et al. , 2014; Mitrovic et al., 2016). Early infection of tomato plants induces the development of numerous axillary buds. The flowers of infected plants are abnormally straight, they are sterile and have altered morphological development (CABI, 2020). Other crops can become infected due to vector dispersal. 'Ca. P. solani’ is naturally dispersed over fairly long distances by its planthopper vectors (EFSA, 2014; CABI, 2020).
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:
Justification:
healthy propagation material, control of vector
7- Is the quality of the data sufficient to recommend the pest to be listed as a RNQP?
Yes
Conclusion:
Justification:
CONCLUSION ON THE STATUS:
Disqualified: plants for planting is not a significant pathway (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:
- CABI (2017) Candidatus Phytoplasma solani (stolbur phytoplasma) https://doi.org/10.1079/cabicompendium.108243 (accessed 30/May/2024).
- Chuche J, Danet JL, Salar P, Foissac X & Thiéry D (2016). Transmission of 'Candidatus Phytoplasma solani' by Reptalus quinquecostatus (Hemiptera: Cixiidae). Annals of Applied Biology 169(2), 214-223. http://onlinelibrary.wiley.com/journal/10.1111/(ISSN)1744-7348
- EFSA (2014) Scientific opinion on the pest categorisation of 'Candidatus Phytoplasma solani'. EFSA Journal, 12(12), 3924. http://www.efsa.europa.eu/en/efsajournal/doc/3924.pdf.
- Hodgetts J, Flint LJ, Daly M, Harju VA, Skelton AL, Fox A, 2015. Identification of 'Candidatus Phytoplasma solani' (16Sr XII-A) infecting strawberry plants in the United Kingdom. New Disease Reports 31, 5. http://www.ndrs.org.uk/article.php?id=031005
- Mitrovic M, Jakovljevic M, Jovic J, Krstic O, Kosovac A, Trivellone V, Jermini M, Toševski I & Cvrkovic T (2016). 'Candidatus Phytoplasma solani' genotypes associated with potato stolbur in Serbia and the role of Hyalesthes obsoletus and Reptalus panzeri (Hemiptera, Cixiidae) as natural vectors. European Journal of Plant Pathology 144(3), 619-630.
- Quaglino F, Zhao Yan, Casati P, Bulgari D, Bianco PA, Wei Wei & Davis RE (2013) 'Candidatus Phytoplasma solani', a novel taxon associated with stolbur- and bois noir-related diseases of plants. International Journal of Systematic and Evolutionary Microbiology 63(8). 2879-2894.
- Riedle-Bauer M, Sára A & Regner F (2008) Transmission of a stolbur phytoplasma by the agalliinae leafhopper Anaceratagallia ribauti (Hemiptera, Auchenorrhyncha, Cicadellidae). Journal of Phytopathology 156(11/12) 687-690.
- Starović M, Kojic S, Kuzmanovic ST, Stojanovic SD, Pavlovic S & Josic D (2013) First report of blueberry reddening disease in Serbia associated with 16SrXII-A (stolbur) phytoplasma. Plant Disease 97(12), 1563.
- Terlizzi F, Babini AR & Credi R (2006) First report of stolbur phytoplasma (16SrXII-A) on strawberry in Northern Italy. Plant Disease 90(6), 831.
- Valiunas D, Alminaite A, Jomantiene R, Davis RE & Maas JL (2004) Possible cause of European blueberry disease is related to North American milkweed yellows phytoplasma. Journal of Plant Pathology 86(2):135-140.