| Legend |
|---|
| Justification for qualification based on EPPO PM 4 Standards |
| Justification for disqualification |
| Additional or non-conclusive information |
| Standard text |
NAME OF THE ORGANISM: Apscaviroid fossulamali (apple dimple fruit viroid) (ADFVD0)
GENERAL INFORMATION ON THE PEST
Name as submitted in the project specification (if different):
Apple dimple fruit viroid
Pest category:
Viruses and viroids
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):
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):
Italy – Malus domestica (Di Serrio et al., 1996); Italy – Ficus (Chiumenti et al., 2014); Spain – Punica granatum (Ruiz-García et al., 2023). Remark: also reported from Israel in Punica granatum (Ruiz-García et al., 2023).
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?
No
Conclusion:
Evaluation continues
Justification (if necessary):
It is mentioned in EPPO Standard PM4-27 Pathogen-tested material of Malus, Pyrus and Cydonia: 'Apple dimple fruit viroid (ADFVd) belongs to the same genus as Apple scar skin viroid (ASSVd). It has been found only once near Naples (IT), and insufficient information is available on testing to include it in this scheme'. The certification scheme was published in 1999, AFDVd was first described in 1997 (Di Serrio et al 1996).
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:
The main pathway is human-assisted, likely through infected propagation material (Di Serrio et al. 2017).
When grafting ADFVd-infected material on healthy rootstocks, it took more than three years for the viroid to reach sufficiently high viroid levels to be detected [unpublished results from Naktuinbouw]. This might have an effect on symptom development and interpretation of results of shorter field experiments. It is unclear whether this slow increase in concentration of ADFVd was influenced by climate or presence of other viruses.
Plant for planting is considered to be the main pathway.
When grafting ADFVd-infected material on healthy rootstocks, it took more than three years for the viroid to reach sufficiently high viroid levels to be detected [unpublished results from Naktuinbouw]. This might have an effect on symptom development and interpretation of results of shorter field experiments. It is unclear whether this slow increase in concentration of ADFVd was influenced by climate or presence of other viruses.
Plant for planting is considered to be the main pathway.
5 - Economic impact:
Are there documented reports of any economic impact on the host?
Yes
Justification:
Symptoms of ADFVd appear on the fruit only, with no other symptoms being reported on other parts of the tree. On apples it can cause yellow rusty skin, mild fruit crinkling to roundish and depressed green spots, scattered on the fruit skin. In some cases, the spots coalesce and large discolored skin areas appear predominantly around the calyx (Malfitano et al., 2004; He et al., 2010). Apples showing the described symptoms were sporadically observed in several parts of Italy (Trentino, Alto-Adige, Campania), disease symptoms due to natural infection were reported in Starking Delicious, Royal Gala and Golden Delicious (Di Serio et al. 1998). Malfitano et al. (2004) suggest that ADFVd occurrence on apple trees is sporadic. Cultivars like Gala, Pink Lady, Braeburn, and Starkrimson showed symptoms after artificial inoculation, but other cultivars might be symptomless carriers (e.g. cultivar Golden, Golden Delicious, Smoothee, Granny Smith, Baujade, Reinette Grise du Canada) (Di Serrio et al., 2001). Reports on symptoms in various cultivars vary (see Navarro et al., 2023). Environmental factors might play a role since Golden Delicious did show symptoms when ADFVd was first discovered (Di Serio et al 1997). Apples showing symptoms have limited commercial value.
The incidence of the infection in the field, however, is low (Malfitano et al., 2004; He et al., 2010) and no natural spread from an infected tree to an adjacent tree has been reported: The viroid did not spread from infected apple trees to neighboring or distant trees in the same field during a 3-year observation period (Malfitano et al., 2004). There is no evidence for seed transmission (Malfitano et al. 2004). This all contributes to a reduced risk of outbreaks.
The incidence of the infection in the field, however, is low (Malfitano et al., 2004; He et al., 2010) and no natural spread from an infected tree to an adjacent tree has been reported: The viroid did not spread from infected apple trees to neighboring or distant trees in the same field during a 3-year observation period (Malfitano et al., 2004). There is no evidence for seed transmission (Malfitano et al. 2004). This all contributes to a reduced risk of outbreaks.
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:
No natural spread has been reported and symptoms were only seen sporadically (Malfitano et al. 2004). The 'substantially free from' requirement for quality pests would be enough.
Remark: ADFVd has also been found in pomegranate (Punica granatum) (Spain) and fig (Ficus carica) (e.g. in Italy). In pomegranate ADFVd was found in fruits showing bright yellow rings, however there were no internal symptoms in those fruits or leaf symptoms on the plants bearing them (Ruiz-García et al 2022). In fig the viroid was found in low concentrations and was no link to obvious symptoms was mentioned (Chiumenti et al., 2014). However, these AFDVd sequences deviate from the sequences found in Malus (Ruiz-García et al 2022).
Remark: ADFVd has also been found in pomegranate (Punica granatum) (Spain) and fig (Ficus carica) (e.g. in Italy). In pomegranate ADFVd was found in fruits showing bright yellow rings, however there were no internal symptoms in those fruits or leaf symptoms on the plants bearing them (Ruiz-García et al 2022). In fig the viroid was found in low concentrations and was no link to obvious symptoms was mentioned (Chiumenti et al., 2014). However, these AFDVd sequences deviate from the sequences found in Malus (Ruiz-García et al 2022).
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:
Inclusion in a certification scheme can prevent introduction and spread of the pathogen in the propagation process. However, test protocol (PCR protocol) would have to be evaluated/developed. RT PCR testing of plants in early steps of certification scheme would likely be effective (as there is no natural spread) (Di Serio et al. 2002). However, there are no commercially available tests, no validated diagnostic protocols.
7- Is the quality of the data sufficient to recommend the pest to be listed as a RNQP?
No
Conclusion:
Justification:
Occurrence rare and precise data on economic damage too few.
CONCLUSION ON THE STATUS:
Disqualified: occurrence rare and precise data on economic damage too few
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:
- Chiumenti M, Torchetti EM, Di Serio F, Minafra A (2014) Identification and characterization of a viroid resembling apple dimple fruit viroid in fig (Ficus carica L.) by next generation sequencing of small RNAs. Virus Research 188, 54–59.
- Di Serio F, Aparicio F, Alioto D, Ragozzino A & Flores R (1996). Identification and molecular properties of a 306 nucleotide viroid associated with apple dimple fruit disease. Journal of General Virology 77: 2833-2837.
- Di Serio F, Alioto D, Ragozzino A, Giunchedi L & Flores R (1998) Identification of apple dimple fruit viroid in different commercial varieties of apple grown in Italy. Acta Horticulturae 472: 595-601.
- Di Serio F, Malfitano M, Alioto D, Ragozzino A, Desvignes JC & Flores R (2001) Apple dimple fruit viroid: Fulfillment of Koch’s postulates and symptom characteristics. Plant Disease 85, 179-182.
- Di Serio, Malfitano M, Alioto D, Ragozzino A & Flores R (2002) apple dimple fruit viroid sequence variability and its specific detection by multiplex fluorescent RT-PCR in the presence of apple scar skin viroid. Journal of Plant Pathology (2002), 84 (1), 27-34.
- Di Serio F, Malfitano M, Alioto D, Ragozzino A & Flores R (2011) Chapter 10: Apple dimple fruit viroid. In Virus and Virus-Like Diseases of Pome and Stone Fruits (eds Hadidi A, Barba M, Candresse T & Jelkmann W), pp. 49-52. American Phytopathological Society, St Paul, Minnesota USA.
- Di Serio, F., Torchetti, E.M., Flores, R., Sano, T. (2017) Other Apscaviroids in infecting pome fruit trees. In Viroids and satellites (eds Hadidi A, Flore R, Randles JW, Palukaitis P). Academic Press London UK. pp. 229-241
- EPPO (1999) Pathogen-tested material of Malus, Pyrus and Cydonia. EPPO Bulletin 29, 239-252.
- He Y, Isono S, Kawaguchi-Ito Y, Taneda A, Kondo K, Iijima A, Tanaka K & Sano T (2010) Characterization of a new apple dimple fruit viroid variant that causes yellow dimple fruit formation in “Fuji” apple trees. J. Gen. Plant Pathol. 76, 324–330. https://doi. org/10.1007/s10327-010-0258-x.
- Malfitano M, Alioto D, Ragozzino A, Flores R & Di Serio F (2004) Experimental evidence that apple dimple fruit viroid does not spread naturally. Acta Horticulturae 657, 357-360.
- Navarro B, Ambrós S, Di Serio F & Hernández C (2023) On the early identification and characterization of pear blister cankerviroid, apple dimple fruit viroid, peach latent mosaic viroid and chrysanthemum chlorotic mottle viroid. Virus Research 2023, 323. https://doi.org/10.1016/j.virusres.2022.199012.
- Ruiz-García AB, Olmos A, Marais A, Faure C & Candresse T (2023) Natural infection of pomegranate (Punica granatum) by apple dimple fruit viroid. Cells 12, 49. https://doi.org/10.3390/cells12010049.