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Justification for qualification based on EPPO PM 4 Standards
Justification for disqualification
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NAME OF THE ORGANISM: Apple flat limb agent (AFL000)

GENERAL INFORMATION ON THE PEST

Name as submitted in the project specification (if different):

Apple flat limb agent (flat limb)

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?

Is the pest defined at the species level or lower?:

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:

Not candidate: Fruits (including hops) sector

Justification (if necessary):

Note on taxonomy: Apple flat limb disease can be spread by grafting (Ronde Kristensen, 1963). The causal agent of the disease has been assumed being identical to the pathogen of apple rubbery wood (Cropley, 1963; Desvignes, 1999). Similar to apple rubbery wood disease, for some time phytoplasmas have been assumed as causal agents of the disease (Nemeth, 1986). However, unequivocal proof for both suppositions is still lacking and therefore, apple flat limb agent is the most appropriate name.

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. Due to the availability of sequence information, test development is possible and links to symptom development can be investigated in more detail.
The Fruit EWG considered that there was no proof yet that these viruses were responsible for these two diseases.

Symptom development is dependent on cultivar of the scion and the rootstock.

[In the responses to the questionnaire, no country supported the recommendation for regulation of apple flat limb disease as an RNQP. FR and LT supported its delisting from EU regulation, whereas NL and SI considered that apple rubbery wood virus 1 & 2 should be listed individually.]

2 – Status in the EU:

Is this pest already a quarantine pest for the whole EU?

Presence in the EU:

Yes

List of countries (EPPO Global Database):

Conclusion:

Justification (if necessary):

Apple flat limb agent is observed worldwide, everywhere where apple is cultivated, it has also been reported from Europe: Austria, Belgium, Bulgaria, Denmark, Finland, France, Germany, Greece, Hungary, Italy, Netherlands, Poland, Portugal, Spain, Sweden (Németh, 1986).

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 'flat limb' recommended in EPPO Standard PM4-27 Pathogen-tested material of Malus, Pyrus and Cydonia. In the preliminary excel file submitted by the European Commission, one country recommended to 'check taxonomic identity, as well as significance in today's apple cultivars (problem only in old cv. Gravensteiner?)'. It was also identified by the EPPO Secretariat as an agent needing further assessment on its taxonomy. Therefore, further evaluation was performed.

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 described pathway.

5 - Economic impact:

Are there documented reports of any economic impact on the host?

Justification:

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?

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:

Economic impact neglectable.

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.

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:

Cropley R (1963) Apple rubbery wood. In: Virus diseases of apples and pears. Technical Communication No. 30. Commonwealth Bureau of Horticulture and Plantation Crops, East Malling, Maidstone, Kent, UK (ed AF Posnette), pp 69-72.
Desvignes JC et al. (1999) Virus diseases of fruit trees (diseases caused by viruses, mycoplasmas and viroids). Centre Technique Interprofessionnel des Fruits et Légumes (Ctifl).
Fontdevila Pareta, N, Lateur M, Steyer S. Blouin AG & Massart S (2022). First reports of Apple luteovirus 1, Apple rubodvirus 1 and Apple hammerhead viroid infecting apples in Belgium. New Disease Reports 45, e12076. https://doi.org/10.1002/ndr2.12076
Fontdevila Pareta N, Gailly C, Blouin AG, Buchmann B, Buenter M, Candresse T, Dubuis N, Kutnjak D, Lateur M, Pecman A, Steyer A & Massart, S. (2024). Virome scanning of pear germplasm collections identifies a new Velarivirus and extends the geographical spread of three other pear viruses. Phytobiomes Journal (ja).
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.
Lim S, Baek D, Moon JS, Cho IS, Choi GS, Do YS, Lee DH & Lee SH (2019) First report of Apple luteovirus 1 and Apple rubbery wood virus 1 on apple tree rootstocks in Korea. Plant Disease 103(3), 591
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.
Minutolo M, Cinque M, Di Serio F, Navarro B & Alioto D (2023) Occurrence of apple rubbery wood virus 1 and apple rubbery wood virus 2 in pear and apple in Campania (southern Italy) and development of degenerate primers for the rapid detection of rubodviruses. Journal of Plant Pathology 105(2), 567-572.
Nemeth M (1986) Apple flat limb. In Virus, Mycoplasma and Rickettsia Diseases. Martinus Nijhoff Publishers, Dordrecht, The Netherlands (ed Nemeth M), pp 578-582.
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.
Ronde Kristensen H (1963) Flat limb of apple. In Virus diseases of apples and pears. Technical Communication No. 30. Commonwealth Bureau of Horticulture and Plantation Crops, East Malling, Maidstone, Kent, UK (ed AF Posnette), pp 53-58.
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.
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.