| Legend |
|---|
| Justification for qualification based on EPPO PM 4 Standards |
| Justification for disqualification |
| Additional or non-conclusive information |
| Standard text |
NAME OF THE ORGANISM: Apple rubbery wood agent (ARW000)
GENERAL INFORMATION ON THE PEST
Name as submitted in the project specification (if different):
Apple rubbery wood agent (Rubbery wood)
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?
No
Is the pest defined at the species level or lower?:
No
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?
- Null: 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?
Conclusion:
- Not candidate: Fruits (including hops) sector
Justification (if necessary):
Note on taxonomy: Apple rubbery wood is a graft-transmissible disease reported from apple, pears and quince (Cropley et al., 1963; Luckwill & Crowdy, 1950). Because of its graft transmissibility, a virological cause of the disease has been assumed, although this is still not proven. Also phytoplasmas have been reported as causal agent (e.g. Bertaccini et al., 1998), but other researchers failed to detect phytoplasmas and bacteria (e.g. Menzel, 2003). Recently, Jakovljevic et al (2016) using Next Generation Sequencing based on total RNA failed to disclose a potential pathogen that could be associated with the disease. Therefore, apple rubbery wood agent still seems the most appropriate name. Field indexing using woody indexing (Jelkmann, 2004) would be needed for detection and identification.
Rott et al. (2018) described two new viruses, apple rubbery wood virus-1 and -2 (ARWV-1- Rubodvirus mali, and ARWV-2- Rubodvirus prosserense) which could be linked to material showing apple rubbery wood and/or apple flat limb symptoms (including material from Germany, Canada, USA and Japan). Since then, the viruses have been found in apple and pear: in China in pear (ARWV2, Wang et al., 2022); in Korea in apple (ARWV1, Lim et al., 2019); in Hungary in apple (ARWV2, Várallyay et al., 2022); in France in pear (ARWV2, Svanella-Dumas et al., 2019); in Italy in apple (ARWV1 and/or ARWV2) and pear (ARWV2 and ARWV1; Minutolo et al., 2023); in Belgium in apple and pear (ARWV1) (Fontdevila Pareta et al., 2022; 2023), in Switzerland in pear (ARWV1/2, Fontdevila Pareta et al., 2023). These publications focused on detection – not on symptom development - and in many samples also other viruses were detected: Tzanetakis et al. (2018) indicates that ARWV1&2 are often associated with other common viruses, making Koch's postulate challenging to demonstrate.
Due to the availability of sequence information, test development is possible and links to symptom development can be investigated in more detail. Symptom development is dependent on cultivar of the scion and the rootstock.
See also Kuhn et al., 2023.
[Remark: In the responses to the questionnaire, DE, FR, LT, NL and SI identified this entry as being of concern. DE supported the recommendation for regulation of the agent as an RNQP considering the assumption that further viruses may be associated with the disease. DE also indicated that primer sets specific for the detection of apple rubbery wood virus-1 and apple rubbery wood virus-2 (Rott et al. 2018) (and for their individual RNA segments) were currently developed by JKI and are available soon. LT supported its delisting from the EU regulation. FR, NL and SI supported the individual listing of apple rubbery wood virus 1 and 2.]
Although two viruses are associated with the symptoms, the Fruit SEWG considered that the agent had no clear identity yet and that more viruses might be involved.
Note: Canada lists Apple rubbery wood (ARW) as ARWV-1 and ARWV-2 on its list of regulated pests (https://inspection.canada.ca/en/plant-health/invasive-species/regulated-pests#a).
Rott et al. (2018) described two new viruses, apple rubbery wood virus-1 and -2 (ARWV-1- Rubodvirus mali, and ARWV-2- Rubodvirus prosserense) which could be linked to material showing apple rubbery wood and/or apple flat limb symptoms (including material from Germany, Canada, USA and Japan). Since then, the viruses have been found in apple and pear: in China in pear (ARWV2, Wang et al., 2022); in Korea in apple (ARWV1, Lim et al., 2019); in Hungary in apple (ARWV2, Várallyay et al., 2022); in France in pear (ARWV2, Svanella-Dumas et al., 2019); in Italy in apple (ARWV1 and/or ARWV2) and pear (ARWV2 and ARWV1; Minutolo et al., 2023); in Belgium in apple and pear (ARWV1) (Fontdevila Pareta et al., 2022; 2023), in Switzerland in pear (ARWV1/2, Fontdevila Pareta et al., 2023). These publications focused on detection – not on symptom development - and in many samples also other viruses were detected: Tzanetakis et al. (2018) indicates that ARWV1&2 are often associated with other common viruses, making Koch's postulate challenging to demonstrate.
Due to the availability of sequence information, test development is possible and links to symptom development can be investigated in more detail. Symptom development is dependent on cultivar of the scion and the rootstock.
See also Kuhn et al., 2023.
[Remark: In the responses to the questionnaire, DE, FR, LT, NL and SI identified this entry as being of concern. DE supported the recommendation for regulation of the agent as an RNQP considering the assumption that further viruses may be associated with the disease. DE also indicated that primer sets specific for the detection of apple rubbery wood virus-1 and apple rubbery wood virus-2 (Rott et al. 2018) (and for their individual RNA segments) were currently developed by JKI and are available soon. LT supported its delisting from the EU regulation. FR, NL and SI supported the individual listing of apple rubbery wood virus 1 and 2.]
Although two viruses are associated with the symptoms, the Fruit SEWG considered that the agent had no clear identity yet and that more viruses might be involved.
Note: Canada lists Apple rubbery wood (ARW) as ARWV-1 and ARWV-2 on its list of regulated pests (https://inspection.canada.ca/en/plant-health/invasive-species/regulated-pests#a).
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 (1993); Denmark (1975); Germany (1993); Italy (1993); Netherlands (1993); Poland (1975); Sweden (1992)
Conclusion:
Justification (if necessary):
Data of the presence of this pest on the EU territory are available in EPPO Global Database (https://gd.eppo.int/). Rubbery wood seems to be present in several additional countries in the EU. Mostly reported in Malus, its presence in Pyrus is more restricted. Symptoms in Cydonia are reported in older literature, but the latter is rare and presumably mixed infections were described in these occasions.
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
3 - Is the pest already listed in a PM4 standard on the concerned host plant?
Yes
Conclusion:
Justification (if necessary):
Testing for 'rubbery wood' recommended in EPPO Standard PM4-27 Pathogen-tested material of Malus, Pyrus and Cydonia. However, the pest/host combination was further assessed in relation to taxonomy.
4 - Are the listed plants for planting the main* pathway for the "pest/host/intended use" combination? (*: significant compared to others):
Yes
Conclusion:
Justification:
Plants for planting is the only pathway described.
5 - Economic impact:
Are there documented reports of any economic impact on the host?
No
Justification:
Very little impact is described, mainly in grey literature. No impact reported in modern cultivars. Ongoing research and new information is mainly molecular (some studies mentioned by DE on symptoms in indicator plants, see below).
Remarks:
- A new paper (Seinsche et al., just before submission) includes data on novel detection primers for ARWV 1 and ARWV 2 genomic segments and their application to over 1,0000 apple samples from German commercial orchards, experimental plots, and variety collections in order to investigate distribution of these viruses across Germany. This screening provided a comprehensive overview of the infection status of ARWV 1 and 2 in Germany.
- Studies on symptom development with ARWV 1 and 2 are ongoing: a well-defined sample set for ARWD symptom expression studies comprise in total more than 20 isolates (including isolates originating from pear and apple) with ARWV 1 single infection, ARWV 2 single infection and with ARWV 1 and 2 mixed infections, selected isolates are grafted onto ‘Lord Lambourne’ indicator plants, symptom development will be monitored over the coming years.
Remarks:
- A new paper (Seinsche et al., just before submission) includes data on novel detection primers for ARWV 1 and ARWV 2 genomic segments and their application to over 1,0000 apple samples from German commercial orchards, experimental plots, and variety collections in order to investigate distribution of these viruses across Germany. This screening provided a comprehensive overview of the infection status of ARWV 1 and 2 in Germany.
- Studies on symptom development with ARWV 1 and 2 are ongoing: a well-defined sample set for ARWD symptom expression studies comprise in total more than 20 isolates (including isolates originating from pear and apple) with ARWV 1 single infection, ARWV 2 single infection and with ARWV 1 and 2 mixed infections, selected isolates are grafted onto ‘Lord Lambourne’ indicator plants, symptom development will be monitored over the coming years.
What is the likely economic impact of the pest irrespective of its infestation source in the absence of phytosanitary measures? (= official measures)
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:
Lack of information on pathogenicity and impact.
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:
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: agent with no clear identity. Lack of information on pathogenicity and impact.
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:
- Bertaccini A, Vibio M, Franova-Honetslegrova J & Janeckova M (1998) Molecular detection of phytoplasmas in apple with rubbery wood symptoms. Acta Horticulturae 472, 693-700.
- Cropley R, Wolfswinkel LD & Posnette AF (1963) The identification of some viruses infecting apple, pear and quince. Proceedings 5th European Symposium Fruit Tree Virus Diseases, in Phytpathologia mediterranea 2, 132-136.
- Jakovljevic V, Otten P, Berwarth C & Jelkmann W (2016) Analysis of the apple rubbery wood disease by next generation sequencing of total RNA. European Journal of Plant Pathology, European Journal of Plant Pathology, 1-10..
- Jelkmann W (2004) Detection of virus and virus-like diseases of fruit trees: laboratory assays, bioassays and indicators. Acta Horticulturae 657, 575-596.
- Kuhn JH, Abe J, Adkins S, Alkhovsky SV, Avšič-Županc T, Ayllón MA et al. (2023) Annual (2023) taxonomic update of RNA-directed RNA polymerase-encoding negative-sense RNA viruses (realm Riboviria: kingdom Orthornavirae: phylum Negarnaviricota). In: The Journal of general virology 104 (8). DOI: 10.1099/jgv.0.001864.
- Luckwill LC & Crowdy SH (1950) Virus diseases of fruit trees II. Observations on rubbery wood, chat fruit, and mosaic in Apples. Progress Report. Report. Long Ashton Research Station 1949, pp 68-79.
- Menzel W (2003) Entwicklung, Optimierung und Erprobung von Nachweisverfahren von Viren an Apfel und Untersuchungen zur Ätiologie des Erregers der Gummiholzkrankheit (ARW). Dissertation, 193 pp., University of Hannover.
- Rott ME, Kesanakurti P, Berwarth C, Rast H, Boyes I, Phelan J & Jelkmann W (2018) Discovery of Negative-Sense RNA Viruses in Trees Infected with Apple Rubbery Wood Disease by Next-Generation Sequencing Plant Disease, 102:7, 1254-1263.
- Seinsche C, Berwarth C, Brodbeck M, Zikeli K, Vondran A, Kleemann L, Thomas S & Jelkmann W (just before submission) Development of Novel Detection Primers and Screening for Apple Rubbery Wood Virus 1 and 2 in Germany.
- Svanella-Dumas L, Marais A, Depasse F, Faure C, Lefebre M, Brans Y, Castaing J, Latour F, Brechti A & Candresse T (2019) First Report of Citrus Virus A (CiVA) Infecting Pear (Pyrus communis) in France. Plant Disease. Disease notes. Available at https://doi.org/10.1094/PDIS-01-19-0028-PDN.
- Tzanetakis IE, Aknadibossian V, Špak J, Constable F, Harper SJ, Hammond J, ... & Škorić D (2024) Streamlining Global Germplasm Exchange: Integrating Scientific Rigor and Common Sense to Exclude Phantom Agents from Regulation. Plant disease, PDIS-04
- Várallyay E, Přibylová J, Galbacs ZN, Jahan A, Varga T, Špak J, Lenz O, Fránová J, Sedlák J & Koloniuk I (2022) Detection of Apple Hammerhead Viroid, Apple Luteovirus 1 and Citrus Concave Gum-Associated Virus in Apple Propagation Materials and Orchards in the Czech Republic and Hungary. Viruses 14 (11), 2347. DOI: 10.3390/v14112347.
- Wang Y, Wang GP, Hong N, Wang YX, Yang ZK, Guo JS, Zhang Z, Li L, Li YJ, Li QY, Xu L & Qi LY (2019) First Report of Apple Rubbery Wood Virus 2 Infecting Pear (Pyrus spp.) in China. Plant disease. Disease notes. Available at https://doi.org/10.1094/PDIS-07-19-1451-PDN.