| Legend |
|---|
| Justification for qualification based on EPPO PM 4 Standards |
| Justification for disqualification |
| Additional or non-conclusive information |
| Standard text |
NAME OF THE ORGANISM: Badnavirus reterubi (Rubus yellow net virus) (RYNV00)
GENERAL INFORMATION ON THE PEST
Name as submitted in the project specification (if different):
Rubus yellow net virus
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):
Remark: Rubus yellow net virus (RYNV) belongs to genus Badnavirus. Badnavirids are found in plants as endogenous, inactive sequences, and/or in episomal (infectious and active) forms. Diaz-Lara (2016) observed that red raspberry plants, supposedly free of RYNV based on aphid or graft transmission onto R. occidentalis ‘Munger’ indicator, yielded positive results when indexed by PCR-based assays. Moreover, those plants were tested positive for RYNV by PCR even after heat therapy and meristem-tip culture for virus elimination. It was demonstrated that RYNV integrates into the red raspberry genome (Diaz-Lara et al., 2020). Later, sequence analysis revealed the presence of a diverse array of endogenous RYNV (endoRYNV) sequences that differ significantly in their structure; some lineages have nearly complete, yet non-functional genomes whereas others have rudimentary, small sequence fragments. There is a widespread presence of endoRYNVs in commercial raspberries, likely because breeding programs have been using a limited pool of germplasm that harbored endoRYNVs (Ho et al., 2024).
The virus can therefore be integrated in plant genome without symptoms, causing false positive diagnostic results.
The virus can therefore be integrated in plant genome without symptoms, causing false positive diagnostic results.
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):
RYNV has been reported in various countries of the EU: Czeck Republic (Koloniuk et al., 2023), Poland and Slovenia (Mavrič Pleško et al., 2012). The virus is likely to be more widespread in Europe, but these findings have not (yet) been published.
HOST PLANT N°1: Rubus (1RUBG) 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:
Evaluation continues
Justification (if necessary):
EPPO Standard PM 4-10 Certification scheme for Rubus recommends testing for 'Rubus yellow net virus (Badnavirus)'. In the responses to the questionnaire, NL and PL supported deregulation in the EU. NL and PL considered that plants for planting was not the main pathway. NL also considered that economic impact was acceptable and that no feasible and effective measures were available. Evaluation continues as a full assessment.
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:
Rubus yellow net virus (RYNV, Badnavirus reterubi) is a member of the genus Badnavirus in the family Caulimoviridae and is restricted to Rubus spp (Stace-Smith, 1987).
RYNV appears to infect all red raspberry cultivars and most blackberry and hybrid berry cultivars, either causing no symptoms or a faint vein netting of leaves. In R. occidentalis cv. Munger, RYNV causes uneven growth of the basal leaflets of the trifoliates and vein chlorosis that give a yellow netted appearance to the leaves. The virus is a major component of the virus complex that causes raspberry mosaic disease, which severely affects plant vigour and yield (MacFarlane et al., 2017).
The virus is readily transmitted by aphid Amphorophora agathonica (American large raspberry aphid) in Northern America, and by aphid A. idaei (European large raspberry aphid) in Europe. These vectors are common in commercial Rubus fields and are also able to transmit other viruses infecting Rubus. All instars of A. agathonica can acquire and transmit RYNV within minutes and retain this virus for several hours at 20 °C or for several days if started at low temperatures (MacFarlane et al., 2017).
In North America, RYNV spreads rapidly in areas with high populations of the large raspberry aphid and, combined with BRNV, has been reported to cause RMD (Stace-Smith, 1987). However, more recently RLMV has been found to be widespread in the Pacific Northwest of the USA and likely contributes to the RMD (Quito-Avila, 2011, MacFarlane et al., 2017).
The virus can be graft transmitted e.g. for graft indexing on e.g. R. occidentalis (Stace-Smith & Jones, 1978).
There is no evidence that RYNV is seed transmitted (Stace-Smith & Jones, 1978).
Recent studies indicate that RYNV can be integrated into the host genome. There is a widespread presence of endogenous RYNV in the genome of commercial raspberries, likely because breeding programs have been using a limited pool of germplasm that harbored endogenous RYNV, which cannot be graft transmitted and cannot be eliminated by heat treatment and meristem-tip culture (Diaz-Lara 2020; Ho et al., 2024). This has consequences for detection of RYNV by PCR and might lead to false positives.
[In the responses to the questionnaire, NL indicated that it can only be transmitted by aphids or grafting and PL considered that the virus was 'Transmitted by aphids that are widespread'.]
The Fruit SEWG supported that plants for planting could still be considered as a significant pathway under protected cultivation.
RYNV appears to infect all red raspberry cultivars and most blackberry and hybrid berry cultivars, either causing no symptoms or a faint vein netting of leaves. In R. occidentalis cv. Munger, RYNV causes uneven growth of the basal leaflets of the trifoliates and vein chlorosis that give a yellow netted appearance to the leaves. The virus is a major component of the virus complex that causes raspberry mosaic disease, which severely affects plant vigour and yield (MacFarlane et al., 2017).
The virus is readily transmitted by aphid Amphorophora agathonica (American large raspberry aphid) in Northern America, and by aphid A. idaei (European large raspberry aphid) in Europe. These vectors are common in commercial Rubus fields and are also able to transmit other viruses infecting Rubus. All instars of A. agathonica can acquire and transmit RYNV within minutes and retain this virus for several hours at 20 °C or for several days if started at low temperatures (MacFarlane et al., 2017).
In North America, RYNV spreads rapidly in areas with high populations of the large raspberry aphid and, combined with BRNV, has been reported to cause RMD (Stace-Smith, 1987). However, more recently RLMV has been found to be widespread in the Pacific Northwest of the USA and likely contributes to the RMD (Quito-Avila, 2011, MacFarlane et al., 2017).
The virus can be graft transmitted e.g. for graft indexing on e.g. R. occidentalis (Stace-Smith & Jones, 1978).
There is no evidence that RYNV is seed transmitted (Stace-Smith & Jones, 1978).
Recent studies indicate that RYNV can be integrated into the host genome. There is a widespread presence of endogenous RYNV in the genome of commercial raspberries, likely because breeding programs have been using a limited pool of germplasm that harbored endogenous RYNV, which cannot be graft transmitted and cannot be eliminated by heat treatment and meristem-tip culture (Diaz-Lara 2020; Ho et al., 2024). This has consequences for detection of RYNV by PCR and might lead to false positives.
[In the responses to the questionnaire, NL indicated that it can only be transmitted by aphids or grafting and PL considered that the virus was 'Transmitted by aphids that are widespread'.]
The Fruit SEWG supported that plants for planting could still be considered as a significant pathway under protected cultivation.
5 - Economic impact:
Are there documented reports of any economic impact on the host?
Yes
Justification:
RYNV is a major component of the complex that causes raspberry mosaic disease, which severely affects plant vigour and yield. In North America, RYNV spreads rapidly in areas with high populations of the large raspberry aphid and, combined with BRNV and/or RLMV, has been reported to cause RMD (Stace-Smith, 1987; Martin et al., 2013; MacFarlane et al., 2017). On its own the virus does not seem to cause significant symptoms: either causing no symptoms or a faint vein netting of leaves. In R. occidentalis cv. Munger, RYNV causes uneven growth of the basal leaflets of the trifoliates and vein chlorosis that give a yellow netted appearance to the leaves (Martin et al., 2013). In R. occidentalis cv. Munger, which is also used as indicator plant, RYNV causes uneven growth of the basal leaflets of the trifoliates and vein chlorosis that give a yellow netted appearance to the leaves (Martin et al., 2013).
Cultivated blackberries are considered to be tolerant. However, yield and fruit quality effects probably do occur. As more molecular tools become available to identify and differentiate the viruses that are found in raspberry cultivations, it is likely that the accepted definitions of what viruses cause which diseases will be modified (MacFarlane et al., 2017).
Cultivated blackberries are considered to be tolerant. However, yield and fruit quality effects probably do occur. As more molecular tools become available to identify and differentiate the viruses that are found in raspberry cultivations, it is likely that the accepted definitions of what viruses cause which diseases will be modified (MacFarlane et al., 2017).
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:
As part of a virus complex, RYNV is a factor in raspberry vein-banding mosaic disease.
Wild and cultivated blackberries may be infected with any or all of the RMD component viruses but do not exhibit disease symptoms and are generally considered to be tolerant. It is unknown how common this virus is in the natural environment in e.g. blackberry.
Decisions about where to plant, how much area to plant, and how long to retain a Rubus field are relevant in control of raspberry mosaic disease. The more isolated the planting can be from cultivated or wild Rubus spp. infected with RMD complex, the longer the plating is likely to escape damage. Larger plantings have a lower proportion of plants infected by incoming winged viruliferous aphids.
The Fruit SEWG rated the economic impact as Minor (single infection with this virus). Since the effect of co-infection with other particular viruses was not considered clear enough, the SEWG assessed the economic impact of the virus on its own, which is considered acceptable.
Wild and cultivated blackberries may be infected with any or all of the RMD component viruses but do not exhibit disease symptoms and are generally considered to be tolerant. It is unknown how common this virus is in the natural environment in e.g. blackberry.
Decisions about where to plant, how much area to plant, and how long to retain a Rubus field are relevant in control of raspberry mosaic disease. The more isolated the planting can be from cultivated or wild Rubus spp. infected with RMD complex, the longer the plating is likely to escape damage. Larger plantings have a lower proportion of plants infected by incoming winged viruliferous aphids.
The Fruit SEWG rated the economic impact as Minor (single infection with this virus). Since the effect of co-infection with other particular viruses was not considered clear enough, the SEWG assessed the economic impact of the virus on its own, which is considered acceptable.
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:
RYNV indexed material, however, since RYNV can be integrated in the genome of Rubus spp., diagnostics is more complicated.
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: economic impact on its own considered acceptable. No clear relation of co-infection with other particular viruses. Plants for planting is not considered to be a significant pathway compared to natural spread by aphids under outdoor conditions.
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:
- Cieślińska M (2021) First report of raspberry leaf mottle virus infecting raspberry in Poland. Plant Disease 105 (3), 714-714. DOI:10.1094/PDIS-08-20-1767-PDN.
- Diaz-Lara A (2016) Identification of endogenous and exogenous pararetroviruses in red raspberry (Rubus idaeus L.) and blueberry (Vaccinium corymbosum L.). PhD thesis. Oregon State University, Corvallis, USA.
- Diaz-Lara A, Mosier NJ, Stevens K, Keller KE & Martin RR (2020) Evidence of Rubus Yellow Net Virus Integration into the red raspberry genome. Cytogenet Genome Research 160(6), 329-334. doi: 10.1159/000509845. Epub 2020 Jul 18. PMID: 32683370.
- Ho T, Broome JC, Buhler JP, O'Donovan W, TianT, Diaz-Lara A, Martin RR & Tzanetakis IE (2024) Integration of Rubus yellow net virus in the raspberry genome: A story centuries in the making. Virology 591, 109991. https://doi.org/10.1016/j.virol.2024.109991
- Jones AT, McGavin WJ, Geering ADW & Lockhart BEL (2006) Identification of Rubus yellow net virus as a distinct badnavirus and its detection by PCR in Rubus species and in aphids. Annals of Applied Biology 141(1), 1-10. https://doi.org/10.1111/j.1744-7348.2002.tb00189.x
- Koloniuk I, Fránová J, Přibylová J, Sarkisova T, Špak J, Tan JL, Sedlák J, Holub J, Skalík J, Blystad DR, Sapkota B & Hamborg Z (2023) Molecular characterization of a novel Enamovirus infecting raspberry. Viruses 15(12), 2281. https://doi.org/10.3390/v15122281
- MacFarlane SA, Tzanetakis IE, Halgren AB & Martin RR (2017) Raspberry mosaic disease. In Compendium of raspberry and blackberry diseases and pest, 2nd edition (eds Martin RR, Ellis MA, Williamson B & Williams RN). American Phytopathological Society, St Paul MN, USA. Pages 75-78.
- Martin RR, MacFarlane S, Sabanadzovic S, Quito D, Poudel B & Tzanetaki IE (2013). Viruses and Virus Diseases of Rubus. Plant Disease 97(2), 168-182. https://doi.org/10.1094/PDIS-04-12-0362-FE.
- Mavrič Pleško I, Marn MV & Koron D (2012) Studies of Rubus viruses in Slovenia. Petria 22(3), 351.
- Quito-Avila DF (2011) Impact of raspberry bushy dwarf virus, raspberry leaf mottle virus, and raspberry latent virus on plant growth and fruit crumbliness in red raspberry (Rubus idaeus L.) ‘Meeker’. PhD Thesis. Oregon State University, Corvallis, USA.
- Stace-Smith R (1987) Virus and virus-like diseases of Rubus (Raspberry and Blackberry). In Virus Diseases of Small Fruits (ed Converse RH). U.S. Government Printing Office, Washington, D.C.
- Stace-Smith R & Jones AT (1978) Rubus yellow net virus, No 188. In Description Plant Viruses. https://www.dpvw