Regulated Non-Quarantine Projects

Two EU funded projects for the benefit of the whole EPPO region

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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: Ilarvirus PNRSV (prunus necrotic ringspot virus) (PNRSV0)


GENERAL INFORMATION ON THE PEST

Name as submitted in the project specification (if different):
 
Prunus necrotic ringspot 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):
 
-

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); Belgium (2015); Bulgaria (2020); Croatia (2002); Cyprus (2002); Czech Republic (2020); Denmark (2002); France (2002); Germany (2002); Greece (2010); Hungary (2002); Italy (2002); Latvia (2010); Malta (2002); Netherlands (2022); Poland (2002); Portugal (2002); Portugal/Azores (2002); Romania (2002); Slovakia (2002); Slovenia (2017); Spain (2010); Sweden (2002)

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/).
Remark: In the 1990s, the physanitary status of the Mediterranean stone fruit industry was surveyed in Albania, Italy (Apulia), Jordan, Lebanon, Malta, Palestine, Syria, Tunisia and Turkey (East-Anatolia).
- Almond: The most common virus in almond was PNRV, the overall infection rate of almonds with this virus was 48.0% (Myrta et al. 2003).
- Apricot: PNRV infection rates of apricot plantations ranged from 5 to 12%, higher rates were found in Italy (35%) and Malta (74%) (Myrta et al. 2003).
- Peach: The PNRV infection rate in peach over all collected samples was 48.4% (Myrta et al. 2003).
- Plum: PNRV infection rates over all plum samples reached 27.1% (Myrta et al. 2003).
- Sweet & sour cherry: Overall incidence of PNRSV in sweet cherry was 5.9% (Myrta et al. 2003). In Czech republic from 2006 to 2008, the incidence of Prunus necrotic ring spot virus (and Prune dwarf virus) in commercial orchards and nurseries were analysed (1,198 sweet cherry trees and 240 sour cherry trees). Prunus necrotic ring spot virus occurred in 3.6 % of the sweet cherry samples and 20.0% of the sour cherry samples (Suchá and Svobodová 2010).

HOST PLANT N°1: Prunus armeniaca (PRNAR) 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, including seeds and pollen


3 - Is the pest already listed in a PM4 standard on the concerned host plant?
 
Yes
 
Conclusion:
 
Evaluation continues

 
Justification (if necessary):
 
Listed as 'Prunus necrotic ringspot ilarvirus (PNRSV)' in EPPO Standard PM 4-30 Certification scheme for almond, apricot, peach and plum; with testing recommended. However, in the preliminary excel file submitted by the European Commission, one country commented that the pest 'seems to be quite frequent in nursery and it has a low nuisance level on fruit plants'. As this could affect the RNQP status, a full assessment is performed. In the responses to the questionnaire, PL supported deregulation based on the pathway criteria.
Remark: The assessment performed covers the given host species as well as interspecific hybrids with other Prunus species.

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:
 
Prunus necrotic ringspot virus occurs worldwide and infects many cultivated Prunus species (Hammond, 2011), such as almond - Prunus dulcis (e.g. Mekuria et al., 2003), apricot - Prunus armenica , sweet and sour cherry, P. avium and P. cerasus (e.g. Oliver et al., 2009, Rouag et al., 2009), plum - P. domestica (e.g. Rouag et al., 2009; Jakab-Ilyefalvi et al., 2011), Japanese plum - P. salicina (e.g. Wood & Fry, 1984), and peach (e.g. Topchiiska, 1982; Uyemoto et al., 1992). PNRSV was also found in many wild Prunus spp. like black cherry (Prunus serotina) and cherry laurel (P. caroliniana) and in rose, where it is one of the causes of rose mosaic disease (Horst & Cloyd, 2007). The natural host range also includes herbaceous hosts like hops (symptomless) and cucumber, where chlorotic local lesions, systemic necrosis and severe stunting may occur (Fulton, 1995).
PNRSV is a variable virus consisting of isolates linked to various symptoms in different host species and cultivars (Howell & Mink, 1988; Moury et al., 2001; Oliver et al., 2009; Kamenova & Borisova, 2021; Chirkov et al., 2023).
Infected propagation material is an important pathway (Scott et al., 1989)
Once established PNRSV is easily spread by infected pollen - by wind, bees or thrips - and is also seed transmitted, which can lead to PNRSV-infected seedling rootstocks (e.g. Greber et al., 1991; Kryczynski et al., 1992; Amari et al., 2007; Tayal et al., 2024). Preventing mother stocks to flower prevents infection by pollen.
The Fruit SEWG concluded that plants for planting was a significant pathway.

5 - Economic impact:

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

Justification:
 
General: PNRSV can cause diseases in nurseries which reduced bud take tree growth, tree survival, and uniformity in nursery operations (Saunier, 1972; Topchiiska, 1993 – cited from Hammond, 2011), and death of buds and roots, reduced growth of fruit (10-30%) and fruit yield (20-60%), delay in fruit maturity (Saunier, 1972), diminished fruit quality, and increased susceptibility to winter injury in orchard trees (Nemeth, 1986; Scott et al, 1989; Uyemoto & Scott, 1992). Successful commercial budding can be lower in combinations where scion and rootstock carry the virus (Lang & Howell, 2001). However, PNRSV can also be symptomless in many Prunus spp. (e.g. Spiegel et al., 2004). Many of these symptoms however, were described at a time when it was more difficult to study the whole virome of plant species. New techniques revealed presence of many previously unknown viruses of which their impact on or addition to symptom development is unknown or under investigation (e.g. James et al., 2018; Koloniuk et al., 2018; Hou et al., 2020; Fontdevila Pareta et al., 2023; Khalili et al., 2023).
Prunus persica & Prunus armeniaca
Single virus infection by PNRSV significantly affected tree growth and fruit yield. A double infection with PNRSV and prune dwarf virus (PDV, another pollen dispersed ilarvirus) lead to peach stunt disease. Fruit production, trunk diameter and tree height were reduced by ca. 30, 23 and 12% respectively over 3 years (Uyemoto et al, 1992).
When peach cultivars were bud-inoculated with PNRSV, the trees developed foliar chlorotic rings and necrosis during the virus year after inoculation. Twig dieback, bark necrosis, root sprouts and trunk cankers developed during subsequent years. Symptoms on inoculated trees resembled those of the slow-decline disease prevalent in central Georgia orchards, particularly the extensive bark necrosis and longitudinal trunk cankers (Wells et al., 1986).
PNRSV affected apricot and pollen germination (by ca. 58%) and delayed germination (Amari et al., 2007). Pollen of peach can also be affected by PNRSV: infection resulted in distorted shape, reduced viability, and germination of pollen grains, but the effect was cultivar dependent (Tayal et al., 2024).
PNRSV has been observed to cause extensive economic losses to peach (Prunus persicae) and apricot (P. armaniaca) trees in Egypt. Symptoms are mostly expressed as necrotic ringspots on leaves, bud failure and poor quantity and quality of fruits (Abdel-Salam et al., 2007).
In the Mediterranean, strains of PNRSV also affected the quality of apricot fruits eliciting discoloured rings or spots, and occassionally necrotic line pattern (Myrta et al., 2003).

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?
 
No

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:
 
Candidate

Justification:
 
PNRSV infection can cause symptoms in various Prunus spp. PNRSV symptoms can vary depending on the time passed since the initial infection, species and cultivar, additional virus infection etc. Symptoms can vary between lethal infections (e.g. Lang et al., 1988) to symptomless (e.g. Pérez Sánchez et al., 2017). Due to pollen transmissibility, PNRV infected trees pose a serious risk for trees at the same production site. This became e.g. apparent in Austria in a propagation stock intended for the production of certified stone fruit material in the mid-1990s. The explosive spread of PNRV in sweet and sour cherry via pollen from single trees led to the uprooting of the plantation after a few years, despite regular ELISA testing and clearance of positive trees (Riedle-Bauer, unpublished).

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:
 
Candidate

Justification:
 
Inclusion in a certification scheme.
Propagation material plays relevant role for dissemination.
Serological and molecular detection methods available.

7- Is the quality of the data sufficient to recommend the pest to be listed as a RNQP?
 
Yes
 
Conclusion:
 
Candidate

Justification:
 
Propagation material is a relevant source of infection, the pathogen is widespread, economic damage are reported in many cases.

CONCLUSION ON THE STATUS:
 
Recommended for listing as an RNQP, based on data.


8 - Tolerance level:

Is there a need to change the Tolerance level:
 
No

Proposed Tolerance levels:
 

9 - Risk management measures:

Is there a need to change the Risk management measure:
 
No

Proposed Risk management measure:
 


REFERENCES:
  • Amari K, Burgos L, Pallas V & Sanchez-Pina MA (2007) Prunus necrotic ringspot virus early invasion and its effects on apricot pollen grain performance. Phytopathology 97, 892-899.
  • Bech K (1991) Prunus necrotic ringspot virus (PNRV) in sour cherry Symptoms, incidence in orchards and influence on fruit yield. Tidsskr. Planteavl 95 (1991), 223-232. 223
  • Chirkov S, Sheveleva A, Tsygankova S, Slobodova N, Sharko F, Petrova K & Mitrofanova I (2023) Whole genome characterization of prunus necrotic ringspot virus and prune dwarf virus infecting stone fruits in Russia. Horticulturae 9, 941. https://doi.org/10.3390/horticulturae9080941
  • Çağlayan K, Ulubas Serce C, Gazel M & Varveri C ( 2011) Prune dwarf virus. In In Virus and virus-like diseases of pome and stone fruit s (eds hadidi A, Barba M, Candresse T & Jelkmann W). American Phytopathological Society, St. Paul, Minnesota, USA. 199-205.
  • Greber RS, Klose MJ, Milne JR & Teakle DS (1991) Transmission of prunus necrotic ringspot virus using plum pollen and thrips. Annals of Applied Biology 118, 589-593.
  • Fontdevila Pareta N, Khalili M, Maachi A, Rivarez MPS, Rollin J, Salavert F, Temple C, Aranda MA, Boonham N, Botermans M, Candresse T, Fox A, Hernando Y, Kutnjak D, Marais A, Petter F, Ravnikar M, Selmi I, Tahzima R, Trontin C, Wetzel T & Massart S (2023) Managing the deluge of newly discovered plant viruses and viroids: an optimized scientific and regulatory framework for their characterization and risk analysis. Frontiers in Microbiollogy 14:1181562. doi: 10.3389/fmicb.2023.1181562
  • Fulton RW (1995) Prunus necrotic ringspot virus. In Viruses of Plants (eds Brunt A, Crabtree K, Dallwitz M, Gibbs A & Watson L). CAB International, University Press Cambridge. 1047-1049. (data collected by Fulton in 1985).
  • Hammond RW (2011) Prunus necrotic ringspot virus. In Virus and virus-like diseases of pome and stone fruit s (eds hadidi A, Barba M, Candresse T & Jelkmann W). American Phytopathological Society, St. Paul, Minnesota, USA. 207-213.
  • Horst RK & Cloyd RA (2007) Rose mosaic. In Compendium of rose diseases and pests. American Phytopathological Society, St. Paul, Minnesota, USA. 32-34.
  • Hou W, Li S and Massart S (2020) Is there a “biological desert” with the discovery of new plant viruses? A retrospective analysis for new fruit tree viruses. Frontiers in Microbiology 11:592816. doi: 10.3389/fmicb.2020.592816
  • Howell WE & Mink GI (1988) Natural spread of cherry rugose mosaic virus and two Prunus necrotic ringspot virus biotypes in a central Washington sweet cherry orchard. Plant Disease 72, 636-640.
  • Jakab-Ilyefalvi, Zs, Pamfil D & Craciun C (2011) Transmission electron microscopy of Plum pox virus, Prunus necrotic ringspot virus, Prune dwarf virus in plum (Prunus domestica, L.). Journal of Horticulture, Forestry and Biotechnology 15(1), 120- 125.
  • James D, Phelan J & Jesperson G (2018). First report of prunus virus F infecting sweet cherry (Prunus avium cv. Staccato) in Canada. Plant disease 102(7), 1468.
  • Kamenova I & Borisova A. (2021) Biological and molecular characterization of Prunus necrotic ringspot virus isolates from sweet and sour cherry. Biotechnology & Biotechnological Equipment, 35(1), 567–575. https://doi.org/10.1080/13102818.2021.1901608
  • Khalili M, Candresse T, Koloniuk I, Safarova D, Brans Y, Faure C, Delmas M, Massart S, Aranda MA, Caglayan K, Decroocq V, Drogoudi P, Glasa M, Pantelidis G, Navratil M, Latour F, Spak J, Pribylova J, Mihalik D, Palmisano F, Saponari A, Necas T, Sedlak J & Marais, A. (2023). The expanding menagerie of Prunus-infecting luteoviruses. Phytopathology 113(2), 345-354.
  • Koloniuk I, Sarkisova T, Petrzik K, Lenz O, Přibylová J, Fránová J, Špak J, Lotos L, Beta C, Katsiani A, Candresse T & Maliogka VI (2018) Variability studies of two prunus-infecting fabaviruses with the aid of High-Throughput Sequencing. Viruses 10, 204; doi:10.3390/v10040204
  • Kryczynski S, Szyndel MS, Stawiszynska A & Piskorek W (1992) The rate and the way of Prunus necrotic ringspot virus spread in sour cherry orchard and in the rootstock production. Acta Horticulturae 309, 105-110.
  • Lang GA & Howell W (2001) Lethal sensitivity of some new cherry rootstocks to pollen-borne viruses. Acta Horticulturae 557, 151-154.
  • Lang G, Howell W & Ophardt D (1998). Sweet cherry rootstock/virus interactions. Acta Horticulturae 468, 307-314. DOI: 10.17660/ActaHortic.1998.468.36
  • Lansac M, Detienne G, Bernhard R & Dunez J (1981) Analysis of nine isolates of almond mosaic. Acta Horticulturae 94, 359-366.
  • Mekuria G, Ramesh SA, Alberts E, Bertozzi T, Wirthensohn M, Collins G & Sedgley M. (2003) Comparison of ELISA and RT-PCR for the detection of Prunus necrotic ring spot virus and prune dwarf virus in almond (Prunus dulcis). Journal of virological methods 114(1), 65-69.
  • Moury B, Cardin L, Onesto JP, Candresse T & Poupet A (2001). Survey of Prunus necrotic ringspot virus in rose and its variability in rose and Prunus spp. Phytopathology 91, 84-91.
  • Myrta A, Di-Terlizzi B, Savino V & Martelli GP (2003) Virus diseases affecting the Mediterranean stone fruit industry: A decade of surveys. Option Méditerranéennes, Sér. B/n°45, 15-23.
  • Nikbakht Dehkordi A, Shiran B, Babaiyan N, Martínez-Gómez P & Rubio M (2018). Detection of Prunus necrotic ringspot virus (PNRSV) in almond and effect on pollen germination. Acta Horticulturae 1219, 357-362. DOI: 10.17660/ActaHortic.2018.1219.54
  • Nyland G, Gilmer RM & Moore JD (1976) Prunus’ ringspot virus group. Virus diseases and noninfectious disorders of stone fruits in North America, USDA Handbook 437 US government Printing Office Washington DC p 104-132.
  • Rodriguez Bonilla F & Cieniewicz E (2022) Distribution and diversity of prunus necrotic ringspot virus, prune dwarf virus, and peach latent mosaic viroid in wild Prunus spp. in South Carolina and Georgia. PhytoFrontiers 2, 363-370. https://doi.org/10.1094/PHYTOFR-02-22-0013-R.
  • Oliver JE, Freer J, Andersen RL, Cox KD, Robinson TL & Fuchs M (2009). Genetic diversity of Prunus necrotic ringspot virus isolates within a cherry orchard in New York. Plant Disease 93, 599-606.
  • Pavliuk L, Udovychenko K, Riaba I & Bublyk M (2017) Variability of some isolates of Prunus necrotic ringspot virus and Prune dwarf virus infecting sour and sweet cherry in Ukraine. Acta agriculturae Slovenica 117(1), 1–9.
  • Pérez Sánchez R, Remedios M & Gómez Sánchez MA (2017) Sour and duke cherry viruses in South-West Europe Phytopathologia Mediterranea 56(1), 62-69. DOI: 10.14601/Phytopathol_Mediterr-15326
  • Rouag N, Guechi A, Matic S & Myrta A (2008) Short communication: Viruses and viroids of stone fruits in Algeria. Journal of Plant Pathology 90(2), 391-393.
  • Saunier R (1972) Incidences d’un virus du type ringspot sur la comportment de deux cultivars du pêchers. La Pomologie Française 14, 175-185.
  • Scott SW, Barnett OW, Burrows PM (1989) Incidence of Prunus necrotic ringspot virus in selected peach orchards of South Carolina. Plant Disease 73, 913-916.
  • Spiegel S, Holand D, Tam Y, Yaakov B, Maslenin L & Rosner A (2004) Prunus necrotic ringspot virus isolates in stone fruit germplasm accessions and cultivars in Israel. Plant Pathology 144, 229-236
  • Tayal M, Ratay A, Swift N, Kaur S, Russo O, Kariyat R & Cieniewicz E (2024) Examining the effects of Prunus necrotic ringspot virus (PNRSV) and Prune dwarf virus (PDV) on peach (Prunus persica) pollen health. PhytoFrontiers™, PHYTOFR-08. https://apsjournals.apsnet.org/doi/full/10.1094/PHYTOFR-08-23-0112-R
  • Topchiiska MI (1983) Effect of Prunus necrotic ringspot virus and Prune dwarf virus on some biological properties of peach. Acta Horticulturae 130, 307-312.
  • Ulubas C & Ertunc F (2004). RT-PCR detection and molecular characterization of Prunus necrotic ringspot virus isolates occurring in Turkey. Journal of Phytopathology 152, 498-502
  • Uyemoto JK, Asai WK & Luhn CF (1992) Ilarviruses: Evidence for rapid spread and effects on vegetative growth and fruit yields of peach trees. Plant Disease 76:71-74.
  • Wells JM, Kirkpatrick HC & Parisch CL (1986) Symptomatology and incidence of Prunus necrotic ringspot virus in peach orchards in Georgia. Plant disease 70, 444-447.
  • Wood GA & Fry PR (1984) Effect of virus infection on growth and cropping of greengage and Billington plum trees. New Zealand Journal of Agricultural Research 27, 563-568.

HOST PLANT N°2: Prunus avium (PRNAV) 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, including seeds and pollen


3 - Is the pest already listed in a PM4 standard on the concerned host plant?
 
Yes
 
Conclusion:
 
Evaluation continues

 
Justification (if necessary):
 
Listed as 'Prunus necrotic ringspot ilarvirus (PNRSV)' in EPPO Standard PM 4-30 Certification scheme for almond, apricot, peach and plum; with testing recommended. However, in the preliminary excel file submitted by the European Commission, one country commented that the pest 'seems to be quite frequent in nursery and it has a low nuisance level on fruit plants'. As this could affect the RNQP status, a full assessment is performed. In the responses to the questionnaire, PL supported deregulation based on the pathway criteria.
Remark: The assessment performed covers the given host species as well as interspecific hybrids with other Prunus species.

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:
 
Prunus necrotic ringspot virus occurs worldwide and infects many cultivated Prunus species (Hammond, 2011), such as almond - Prunus dulcis (e.g. Mekuria et al., 2003), apricot - Prunus armenica , sweet and sour cherry, P. avium and P. cerasus (e.g. Oliver et al., 2009, Rouag et al., 2009), plum - P. domestica (e.g. Rouag et al., 2009; Jakab-Ilyefalvi et al., 2011), Japanese plum - P. salicina (e.g. Wood & Fry, 1984), and peach (e.g. Topchiiska, 1982; Uyemoto et al., 1992). PNRSV was also found in many wild Prunus spp. like black cherry (Prunus serotina) and cherry laurel (P. caroliniana) and in rose, where it is one of the causes of rose mosaic disease (Horst & Cloyd, 2007). The natural host range also includes herbaceous hosts like hops (symptomless) and cucumber, where chlorotic local lesions, systemic necrosis and severe stunting may occur (Fulton, 1995).
PNRSV is a variable virus consisting of isolates linked to various symptoms in different host species and cultivars (Howell & Mink, 1988; Moury et al., 2001; Oliver et al., 2009; Kamenova & Borisova, 2021; Chirkov et al., 2023).
Infected propagation material is an important pathway (Scott et al., 1989)
Once established PNRSV is easily spread by infected pollen - by wind, bees or thrips - and is also seed transmitted, which can lead to PNRSV-infected seedling rootstocks (e.g. Greber et al., 1991; Kryczynski et al., 1992; Amari et al., 2007; Tayal et al., 2024). Preventing mother stocks to flower prevents infection by pollen.
The Fruit SEWG concluded that plants for planting was a significant pathway.

5 - Economic impact:

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

Justification:
 
General: PNRSV can cause diseases in nurseries which reduced bud take tree growth, tree survival, and uniformity in nursery operations (Saunier, 1972; Topchiiska, 1993 – cited from Hammond, 2011), and death of buds and roots, reduced growth of fruit (10-30%) and fruit yield (20-60%), delay in fruit maturity (Saunier, 1972), diminished fruit quality, and increased susceptibility to winter injury in orchard trees (Nemeth, 1986; Scott et al, 1989; Uyemoto & Scott, 1992). Successful commercial budding can be lower in combinations where scion and rootstock carry the virus (Lang & Howell, 2001). However, PNRSV can also be symptomless in many Prunus spp. (e.g. Spiegel et al., 2004). Many of these symptoms however, were described at a time when it was more difficult to study the whole virome of plant species. New techniques revealed presence of many previously unknown viruses of which their impact on or addition to symptom development is unknown or under investigation (e.g. James et al., 2018; Koloniuk et al., 2018; Hou et al., 2020; Fontdevila Pareta et al., 2023; Khalili et al., 2023).
Prunus avium & Prunus cerasus.
PNRSV symptoms in sweet and sour cherry may vary depending on the time passed since the initial infection.
Typical PNRSV shock symptoms, i.e. leaf necrosis and shot holing, can be observed immediately after the virus enters the plant. New leaves that developed later in the season may remain symptomless. Delayed budbreak, retarded bloom, death of leaf and flower buds, slow fruit set, and reduced vigour were also early indications of the shock syndrome induced by PNRSV (Oliver et al, 2009).
From a single infected tree of P. cerasus 'Stevnsbär', the virus could spread by pollen to neighboring trees. Nearly 40% of 60 young trees planted near older trees with PNRSV were infected within three years. The first symptoms were observed five years after planting. In two older orchards the PNRSV spread from 24 to 59% of the trees within the registered area during three years, and 29 to 68% during a five year period respectively. The effect of the virus disease on fruit yield was estimated in a 16 year old orchard. After PNRSV infection fruit yield was reduced to between 25-33% of the normal yield from symptom-free trees. During the year of shock reaction the yield was usually extremely low (Bech, 1991).
Various cherry rootstocks reacted differently to PNRSV infection (tolerant to susceptible) (Lang et al., 1998; Lang & Howell, 2001).
A PNRSV infection can also be latent, especially when the disease becomes chronic (Pavliuk et al., 2021). Mixed infection of plants with PDV and PNRSV can development more severe symptoms. These two viruses are often found in combination as both are readily transmitted by pollen (Çağlayan et al., 2011). A combination of PDV and PNRSV can also be symptomless: Perez-Sanches et al (2017) found that 60-100% of the sour and duke cherry (Prunus x gondouinii) infected with PNRSV in single and combined infections were symptomless.

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?
 
Yes

Conclusion:
 
Candidate

Justification:
 
PNRSV infection can cause symptoms in various Prunus spp. PNRSV symptoms can vary depending on the time passed since the initial infection, species and cultivar, additional virus infection etc. Symptoms can vary between lethal infections (e.g. Lang et al., 1988) to symptomless (e.g. Pérez Sánchez et al., 2017). In Prunus spp., effect on fruit growth (10-30%), yield (20-60%) and a delay of maturation have been reported (Sanier, 1972; reported in EFSA 2014). However, the Fruit SEWG noted that data of economic impact on P. avium was lacking.
The Fruit SEWG considered that indirect economic impact should be considered: Due to pollen transmissibility, PNRV infected trees pose a serious risk for trees at the same production site. This became e.g. apparent in Austria in a propagation stock intended for the production of certified stone fruit material in the mid-1990s. The explosive spread of PNRV in sweet and sour cherry via pollen from single trees led to the uprooting of the plantation after a few years, despite regular ELISA testing and clearance of positive trees (Riedle-Bauer, unpublished). Also in the above mentioned Danish study including the variety 'Stevnsbär' an extremely rapid spread pf PNRV via pollen was reported (Bech, 1991). Sweet cherry and plum can flower at the same time as cherry and cause unacceptable economic impact to this species.

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:
 
Candidate

Justification:
 
Inclusion in a certification scheme.
Propagation material plays relevant role for dissemination.
Serological and molecular detection methods available.

7- Is the quality of the data sufficient to recommend the pest to be listed as a RNQP?
 
Yes
 
Conclusion:
 
Candidate

Justification:
 
Propagation material is a relevant source of infection, the pathogen is widespread, economic damage are reported in many cases.

CONCLUSION ON THE STATUS:
 
Recommended for listing as an RNQP, based on data.


8 - Tolerance level:

Is there a need to change the Tolerance level:
 
No

Proposed Tolerance levels:
 

9 - Risk management measures:

Is there a need to change the Risk management measure:
 
No

Proposed Risk management measure:
 


REFERENCES:
  • Amari K, Burgos L, Pallas V & Sanchez-Pina MA (2007) Prunus necrotic ringspot virus early invasion and its effects on apricot pollen grain performance. Phytopathology 97, 892-899.
  • Bech K (1991) Prunus necrotic ringspot virus (PNRV) in sour cherry Symptoms, incidence in orchards and influence on fruit yield. Tidsskr. Planteavl 95 (1991), 223-232. 223
  • Chirkov S, Sheveleva A, Tsygankova S, Slobodova N, Sharko F, Petrova K & Mitrofanova I (2023) Whole genome characterization of prunus necrotic ringspot virus and prune dwarf virus infecting stone fruits in Russia. Horticulturae 9, 941. https://doi.org/10.3390/horticulturae9080941
  • Çağlayan K, Ulubas Serce C, Gazel M & Varveri C ( 2011) Prune dwarf virus. In In Virus and virus-like diseases of pome and stone fruit s (eds hadidi A, Barba M, Candresse T & Jelkmann W). American Phytopathological Society, St. Paul, Minnesota, USA. 199-205.
  • EFSA (2014) Scientific Opinion on the pest categorization of Prunus necrotic ringspot virus. https://www.efsa.europa.eu/de/efsajournal/pub/3849#:~:text=PNRSV%20is%20a%20well%2Ddefined,in%20some%20of%20its%20hosts.
  • Fontdevila Pareta N, Khalili M, Maachi A, Rivarez MPS, Rollin J, Salavert F, Temple C, Aranda MA, Boonham N, Botermans M, Candresse T, Fox A, Hernando Y, Kutnjak D, Marais A, Petter F, Ravnikar M, Selmi I, Tahzima R, Trontin C, Wetzel T & Massart S (2023) Managing the deluge of newly discovered plant viruses and viroids: an optimized scientific and regulatory framework for their characterization and risk analysis. Frontiers in Microbiollogy 14:1181562. doi: 10.3389/fmicb.2023.1181562
  • Fulton RW (1995) Prunus necrotic ringspot virus. In Viruses of Plants (eds Brunt A, Crabtree K, Dallwitz M, Gibbs A & Watson L). CAB International, University Press Cambridge. 1047-1049. (data collected by Fulton in 1985).
  • Greber RS, Klose MJ, Milne JR & Teakle DS (1991) Transmission of prunus necrotic ringspot virus using plum pollen and thrips. Annals of Applied Biology 118, 589-593.
  • Hammond RW (2011) Prunus necrotic ringspot virus. In Virus and virus-like diseases of pome and stone fruit s (eds hadidi A, Barba M, Candresse T & Jelkmann W). American Phytopathological Society, St. Paul, Minnesota, USA. 207-213.
  • Horst RK & Cloyd RA (2007) Rose mosaic. In Compendium of rose diseases and pests. American Phytopathological Society, St. Paul, Minnesota, USA. 32-34.
  • Hou W, Li S and Massart S (2020) Is there a “biological desert” with the discovery of new plant viruses? A retrospective analysis for new fruit tree viruses. Frontiers in Microbiology 11:592816. doi: 10.3389/fmicb.2020.592816
  • Howell WE & Mink GI (1988) Natural spread of cherry rugose mosaic virus and two Prunus necrotic ringspot virus biotypes in a central Washington sweet cherry orchard. Plant Disease 72, 636-640.
  • Jakab-Ilyefalvi, Zs, Pamfil D & Craciun C (2011) Transmission electron microscopy of Plum pox virus, Prunus necrotic ringspot virus, Prune dwarf virus in plum (Prunus domestica, L.). Journal of Horticulture, Forestry and Biotechnology 15(1), 120- 125.
  • James D, Phelan J & Jesperson G (2018). First report of prunus virus F infecting sweet cherry (Prunus avium cv. Staccato) in Canada. Plant disease 102(7), 1468.
  • Kamenova I & Borisova A. (2021) Biological and molecular characterization of Prunus necrotic ringspot virus isolates from sweet and sour cherry. Biotechnology & Biotechnological Equipment, 35(1), 567–575. https://doi.org/10.1080/13102818.2021.1901608
  • Khalili M, Candresse T, Koloniuk I, Safarova D, Brans Y, Faure C, Delmas M, Massart S, Aranda MA, Caglayan K, Decroocq V, Drogoudi P, Glasa M, Pantelidis G, Navratil M, Latour F, Spak J, Pribylova J, Mihalik D, Palmisano F, Saponari A, Necas T, Sedlak J & Marais, A. (2023).
  • The expanding menagerie of Prunus-infecting luteoviruses. Phytopathology 113(2), 345-354.
  • Koloniuk I, Sarkisova T, Petrzik K, Lenz O, Přibylová J, Fránová J, Špak J, Lotos L, Beta C, Katsiani A, Candresse T & Maliogka VI (2018) Variability studies of two prunus-infecting fabaviruses with the aid of High-Throughput Sequencing. Viruses 10, 204; doi:10.3390/v10040204
  • Kryczynski S, Szyndel MS, Stawiszynska A & Piskorek W (1992) The rate and the way of Prunus necrotic ringspot virus spread in sour cherry orchard and in the rootstock production. Acta Horticulturae 309, 105-110.
  • Lang GA & Howell W (2001) Lethal sensitivity of some new cherry rootstocks to pollen-borne viruses. Acta Horticulturae 557, 151-154.
  • Lang G, Howell W & Ophardt D (1998). Sweet cherry rootstock/virus interactions. Acta Horticulturae 468, 307-314. DOI: 10.17660/ActaHortic.1998.468.36
  • Lansac M, Detienne G, Bernhard R & Dunez J (1981) Analysis of nine isolates of almond mosaic. Acta Horticulturae 94, 359-366.
  • Mekuria G, Ramesh SA, Alberts E, Bertozzi T, Wirthensohn M, Collins G & Sedgley M. (2003) Comparison of ELISA and RT-PCR for the detection of Prunus necrotic ring spot virus and prune dwarf virus in almond (Prunus dulcis). Journal of virological methods 114(1), 65-69.
  • Moury B, Cardin L, Onesto JP, Candresse T & Poupet A (2001). Survey of Prunus necrotic ringspot virus in rose and its variability in rose and Prunus spp. Phytopathology 91, 84-91.
  • Myrta A, Di-Terlizzi B, Savino V & Martelli GP (2003) Virus diseases affecting the Mediterranean stone fruit industry: A decade of surveys. Option Méditerranéennes, Sér. B/n°45, 15-23.
  • Nikbakht Dehkordi A, Shiran B, Babaiyan N, Martínez-Gómez P & Rubio M (2018). Detection of Prunus necrotic ringspot virus (PNRSV) in almond and effect on pollen germination. Acta Horticulturae 1219, 357-362. DOI: 10.17660/ActaHortic.2018.1219.54
  • Nyland G, Gilmer RM & Moore JD (1976) Prunus’ ringspot virus group. Virus diseases and noninfectious disorders of stone fruits in North America, USDA Handbook 437 US government Printing Office Washington DC p 104-132.
  • Rodriguez Bonilla F & Cieniewicz E (2022) Distribution and diversity of prunus necrotic ringspot virus, prune dwarf virus, and peach latent mosaic viroid in wild Prunus spp. in South Carolina and Georgia. PhytoFrontiers 2, 363-370. https://doi.org/10.1094/PHYTOFR-02-22-0013-R.
  • Rouag N, Guechi A, Matic S & Myrta A (2008) Short communication: Viruses and viroids of stone fruits in Algeria. Journal of Plant Pathology 90(2), 391-393.
  • Oliver JE, Freer J, Andersen RL, Cox KD, Robinson TL & Fuchs M (2009). Genetic diversity of Prunus necrotic ringspot virus isolates within a cherry orchard in New York. Plant Disease 93, 599-606.
  • Pavliuk L, Udovychenko K, Riaba I & Bublyk M (2017) Variability of some isolates of Prunus necrotic ringspot virus and Prune dwarf virus infecting sour and sweet cherry in Ukraine. Acta agriculturae Slovenica 117(1), 1–9.
  • Pérez Sánchez R, Remedios M & Gómez Sánchez MA (2017) Sour and duke cherry viruses in South-West Europe Phytopathologia Mediterranea 56(1), 62-69. DOI: 10.14601/Phytopathol_Mediterr-15326
  • Saunier R (1972) Incidences d’un virus du type ringspot sur la comportment de deux cultivars du pêchers. La Pomologie Française 14, 175-185.
  • Scott SW, Barnett OW, Burrows PM (1989) Incidence of Prunus necrotic ringspot virus in selected peach orchards of South Carolina. Plant Disease 73, 913-916.
  • Spiegel S, Holand D, Tam Y, Yaakov B, Maslenin L & Rosner A (2004) Prunus necrotic ringspot virus isolates in stone fruit germplasm accessions and cultivars in Israel. Plant Pathology 144, 229-236
  • Tayal M, Ratay A, Swift N, Kaur S, Russo O, Kariyat R & Cieniewicz E (2024) Examining the effects of Prunus necrotic ringspot virus (PNRSV) and Prune dwarf virus (PDV) on peach (Prunus persica) pollen health. PhytoFrontiers™, PHYTOFR-08. https://apsjournals.apsnet.org/doi/full/10.1094/PHYTOFR-08-23-0112-R
  • Topchiiska MI (1983) Effect of Prunus necrotic ringspot virus and Prune dwarf virus on some biological properties of peach. Acta Horticulturae 130, 307-312.
  • Ulubas C & Ertunc F (2004). RT-PCR detection and molecular characterization of Prunus necrotic ringspot virus isolates occurring in Turkey. Journal of Phytopathology 152, 498-502
  • Uyemoto JK, Asai WK & Luhn CF (1992) Ilarviruses: Evidence for rapid spread and effects on vegetative growth and fruit yields of peach trees. Plant Disease 76:71-74.
  • Wells JM, Kirkpatrick HC & Parisch CL (1986) Symptomatology and incidence of Prunus necrotic ringspot virus in peach orchards in Georgia. Plant disease 70, 444-447.
  • Wood GA & Fry PR (1984) Effect of virus infection on growth and cropping of greengage and Billington plum trees. New Zealand Journal of Agricultural Research 27, 563-568.

HOST PLANT N°3: Prunus cerasus (PRNCE) 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, including seeds and pollen


3 - Is the pest already listed in a PM4 standard on the concerned host plant?
 
Yes
 
Conclusion:
 
Evaluation continues

 
Justification (if necessary):
 
Listed as 'Prunus necrotic ringspot ilarvirus (PNRSV)' in EPPO Standard PM 4-30 Certification scheme for almond, apricot, peach and plum; with testing recommended. However, in the preliminary excel file submitted by the European Commission, one country commented that the pest 'seems to be quite frequent in nursery and it has a low nuisance level on fruit plants'. As this could affect the RNQP status, a full assessment is performed. In the responses to the questionnaire, PL supported deregulation based on the pathway criteria.
Remark: The assessment performed covers the given host species as well as interspecific hybrids with other Prunus species.

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:
 
Prunus necrotic ringspot virus occurs worldwide and infects many cultivated Prunus species (Hammond, 2011), such as almond - Prunus dulcis (e.g. Mekuria et al., 2003), apricot - Prunus armenica , sweet and sour cherry, P. avium and P. cerasus (e.g. Oliver et al., 2009, Rouag et al., 2009), plum - P. domestica (e.g. Rouag et al., 2009; Jakab-Ilyefalvi et al., 2011), Japanese plum - P. salicina (e.g. Wood & Fry, 1984), and peach (e.g. Topchiiska, 1982; Uyemoto et al., 1992). PNRSV was also found in many wild Prunus spp. like black cherry (Prunus serotina) and cherry laurel (P. caroliniana) and in rose, where it is one of the causes of rose mosaic disease (Horst & Cloyd, 2007). The natural host range also includes herbaceous hosts like hops (symptomless) and cucumber, where chlorotic local lesions, systemic necrosis and severe stunting may occur (Fulton, 1995).
PNRSV is a variable virus consisting of isolates linked to various symptoms in different host species and cultivars (Howell & Mink, 1988; Moury et al., 2001; Oliver et al., 2009; Kamenova & Borisova, 2021; Chirkov et al., 2023).
Infected propagation material is an important pathway (Scott et al., 1989)
Once established PNRSV is easily spread by infected pollen - by wind, bees or thrips - and is also seed transmitted, which can lead to PNRSV-infected seedling rootstocks (e.g. Greber et al., 1991; Kryczynski et al., 1992; Amari et al., 2007; Tayal et al., 2024). Preventing mother stocks to flower prevents infection by pollen.
The Fruit SEWG concluded that plants for planting was a significant pathway.

5 - Economic impact:

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

Justification:
 
General: PNRSV can cause diseases in nurseries which reduced bud take tree growth, tree survival, and uniformity in nursery operations (Saunier, 1972; Topchiiska, 1993 – cited from Hammond, 2011), and death of buds and roots, reduced growth of fruit (10-30%) and fruit yield (20-60%), delay in fruit maturity (Saunier, 1972), diminished fruit quality, and increased susceptibility to winter injury in orchard trees (Nemeth, 1986; Scott et al, 1989; Uyemoto & Scott, 1992). Successful commercial budding can be lower in combinations where scion and rootstock carry the virus (Lang & Howell, 2001). However, PNRSV can also be symptomless in many Prunus spp. (e.g. Spiegel et al., 2004). Many of these symptoms however, were described at a time when it was more difficult to study the whole virome of plant species. New techniques revealed presence of many previously unknown viruses of which their impact on or addition to symptom development is unknown or under investigation (e.g. James et al., 2018; Koloniuk et al., 2018; Hou et al., 2020; Fontdevila Pareta et al., 2023; Khalili et al., 2023).
Cherry Prunus avium & Prunus cerasus.
PNRSV symptoms in sweet and sour cherry may vary depending on the time passed since the initial infection.
Typical PNRSV shock symptoms, i.e. leaf necrosis and shot holing, can be observed immediately after the virus enters the plant. New leaves that developed later in the season may remain symptomless. Delayed budbreak, retarded bloom, death of leaf and flower buds, slow fruit set, and reduced vigour were also early indications of the shock syndrome induced by PNRSV (Oliver et al, 2009).
From a single infected tree of P. cerasus 'Stevnsbär', the virus could spread by pollen to neighboring trees. Nearly 40% of 60 young trees planted near older trees with PNRSV were infected within three years. The first symptoms were observed five years after planting. In two older orchards the PNRSV spread from 24 to 59% of the trees within the registered area during three years, and 29 to 68% during a five year period respectively. The effect of the virus disease on fruit yield was estimated in a 16 year old orchard. After PNRSV infection fruit yield was reduced to between 25-33% of the normal yield from symptom-free trees. During the year of shock reaction the yield was usually extremely low (Bech, 1991). In another article, it is reported that, for decades, PNRV has become an increasing problem in the traditional sour cherry-growing region of Rhineland-Palatinate. Due to the reduced productivity and fruit quality, the profitability limit can hardly be reached. The PNRV influence led to a 30% reduction in growth and a up to 57% reduction in yield (Hilsendegen, P, 1999).
Various cherry rootstocks reacted differently to PNRSV infection (tolerant to susceptible) (Lang et al., 1998; Lang & Howell, 2001).
A PNRSV infection can also be latent, especially when the disease becomes chronic (Pavliuk et al., 2021). Mixed infection of plants with PDV and PNRSV can development more severe symptoms. These two viruses are often found in combination as both are readily transmitted by pollen (Çağlayan et al., 2011). A combination of PDV and PNRSV can also be symptomless: Perez-Sanches et al (2017) found that 60-100% of the sour and duke cherry (Prunus x gondouinii) infected with PNRSV in single and combined infections were symptomless.

What is the likely economic impact of the pest irrespective of its infestation source in the absence of phytosanitary measures? (= official measures)
 
Medium-Major

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?
 
No

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:
 
Candidate

Justification:
 
PNRSV infection can cause symptoms in various Prunus spp. PNRSV symptoms can vary depending on the time passed since the initial infection, species and cultivar, additional virus infection etc. Symptoms can vary between lethal infections (e.g. Lang et al., 1988) to symptomless (e.g. Pérez Sánchez et al., 2017). Due to pollen transmissibility, PNRV infected trees pose a serious risk for trees at the same production site. This became e.g. apparent in Austria in a propagation stock intended for the production of certified stone fruit material in the mid-1990s. The explosive spread of PNRV in sweet and sour cherry via pollen from single trees led to the uprooting of the plantation after a few years, despite regular ELISA testing and clearance of positive trees (Riedle-Bauer, unpublished).

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:
 
Candidate

Justification:
 
Inclusion in a certification scheme.
Propagation material plays relevant role for dissemination.
Serological and molecular detection methods available.

7- Is the quality of the data sufficient to recommend the pest to be listed as a RNQP?
 
Yes
 
Conclusion:
 
Candidate

Justification:
 
Propagation material is a relevant source of infection, the pathogen is widespread, economic damage are reported in many cases.

CONCLUSION ON THE STATUS:
 
Recommended for listing as an RNQP, based on data.


8 - Tolerance level:

Is there a need to change the Tolerance level:
 
No

Proposed Tolerance levels:
 

9 - Risk management measures:

Is there a need to change the Risk management measure:
 
No

Proposed Risk management measure:
 


REFERENCES:
  • Amari K, Burgos L, Pallas V & Sanchez-Pina MA (2007) Prunus necrotic ringspot virus early invasion and its effects on apricot pollen grain performance. Phytopathology 97, 892-899.
  • Bech K (1991) Prunus necrotic ringspot virus (PNRV) in sour cherry Symptoms, incidence in orchards and influence on fruit yield. Tidsskr. Planteavl 95 (1991), 223-232. 223
  • Chirkov S, Sheveleva A, Tsygankova S, Slobodova N, Sharko F, Petrova K & Mitrofanova I (2023) Whole genome characterization of prunus necrotic ringspot virus and prune dwarf virus infecting stone fruits in Russia. Horticulturae 9, 941. https://doi.org/10.3390/horticulturae9080941
  • Çağlayan K, Ulubas Serce C, Gazel M & Varveri C ( 2011) Prune dwarf virus. In In Virus and virus-like diseases of pome and stone fruit s (eds hadidi A, Barba M, Candresse T & Jelkmann W). American Phytopathological Society, St. Paul, Minnesota, USA. 199-205.
  • Greber RS, Klose MJ, Milne JR & Teakle DS (1991) Transmission of prunus necrotic ringspot virus using plum pollen and thrips. Annals of Applied Biology 118, 589-593.
  • Fontdevila Pareta N, Khalili M, Maachi A, Rivarez MPS, Rollin J, Salavert F, Temple C, Aranda MA, Boonham N, Botermans M, Candresse T, Fox A, Hernando Y, Kutnjak D, Marais A, Petter F, Ravnikar M, Selmi I, Tahzima R, Trontin C, Wetzel T & Massart S (2023) Managing the deluge of newly discovered plant viruses and viroids: an optimized scientific and regulatory framework for their characterization and risk analysis. Frontiers in Microbiollogy 14:1181562. doi: 10.3389/fmicb.2023.1181562
  • Fulton RW (1995) Prunus necrotic ringspot virus. In Viruses of Plants (eds Brunt A, Crabtree K, Dallwitz M, Gibbs A & Watson L). CAB International, University Press Cambridge. 1047-1049. (data collected by Fulton in 1985).
  • Hammond RW (2011) Prunus necrotic ringspot virus. In Virus and virus-like diseases of pome and stone fruit s (eds hadidi A, Barba M, Candresse T & Jelkmann W). American Phytopathological Society, St. Paul, Minnesota, USA. 207-213.
  • Hilsendegen P (1999) Results of the tolerance of sour cherry cultivars to prunus necrotic ringspot virus (PNRV). Erwerbsobstbau 41(6), 192-197.
  • Horst RK & Cloyd RA (2007) Rose mosaic. In Compendium of rose diseases and pests. American Phytopathological Society, St. Paul, Minnesota, USA. 32-34.
  • Hou W, Li S and Massart S (2020) Is there a “biological desert” with the discovery of new plant viruses? A retrospective analysis for new fruit tree viruses. Frontiers in Microbiology 11:592816. doi: 10.3389/fmicb.2020.592816
  • Howell WE & Mink GI (1988) Natural spread of cherry rugose mosaic virus and two Prunus necrotic ringspot virus biotypes in a central Washington sweet cherry orchard. Plant Disease 72, 636-640.
  • Jakab-Ilyefalvi, Zs, Pamfil D & Craciun C (2011) Transmission electron microscopy of Plum pox virus, Prunus necrotic ringspot virus, Prune dwarf virus in plum (Prunus domestica, L.). Journal of Horticulture, Forestry and Biotechnology 15(1), 120- 125.
  • James D, Phelan J & Jesperson G (2018). First report of prunus virus F infecting sweet cherry (Prunus avium cv. Staccato) in Canada. Plant disease 102(7), 1468.
  • Kamenova I & Borisova A. (2021) Biological and molecular characterization of Prunus necrotic ringspot virus isolates from sweet and sour cherry. Biotechnology & Biotechnological Equipment, 35(1), 567–575. https://doi.org/10.1080/13102818.2021.1901608
  • Khalili M, Candresse T, Koloniuk I, Safarova D, Brans Y, Faure C, Delmas M, Massart S, Aranda MA, Caglayan K, Decroocq V, Drogoudi P, Glasa M, Pantelidis G, Navratil M, Latour F, Spak J, Pribylova J, Mihalik D, Palmisano F, Saponari A, Necas T, Sedlak J & Marais, A. (2023). The expanding menagerie of Prunus-infecting luteoviruses. Phytopathology 113(2), 345-354.
  • Koloniuk I, Sarkisova T, Petrzik K, Lenz O, Přibylová J, Fránová J, Špak J, Lotos L, Beta C, Katsiani A, Candresse T & Maliogka VI (2018) Variability studies of two prunus-infecting fabaviruses with the aid of High-Throughput Sequencing. Viruses 10, 204; doi:10.3390/v10040204
  • Kryczynski S, Szyndel MS, Stawiszynska A & Piskorek W (1992) The rate and the way of Prunus necrotic ringspot virus spread in sour cherry orchard and in the rootstock production. Acta Horticulturae 309, 105-110.
  • Lang GA & Howell W (2001) Lethal sensitivity of some new cherry rootstocks to pollen-borne viruses. Acta Horticulturae 557, 151-154.
  • Lang G, Howell W & Ophardt D (1998). Sweet cherry rootstock/virus interactions. Acta Horticulturae 468, 307-314. DOI: 10.17660/ActaHortic.1998.468.36
  • Lansac M, Detienne G, Bernhard R & Dunez J (1981) Analysis of nine isolates of almond mosaic. Acta Horticulturae 94, 359-366.
  • Mekuria G, Ramesh SA, Alberts E, Bertozzi T, Wirthensohn M, Collins G & Sedgley M. (2003) Comparison of ELISA and RT-PCR for the detection of Prunus necrotic ring spot virus and prune dwarf virus in almond (Prunus dulcis). Journal of virological methods 114(1), 65-69.
  • Moury B, Cardin L, Onesto JP, Candresse T & Poupet A (2001). Survey of Prunus necrotic ringspot virus in rose and its variability in rose and Prunus spp. Phytopathology 91, 84-91.
  • Myrta A, Di-Terlizzi B, Savino V & Martelli GP (2003) Virus diseases affecting the Mediterranean stone fruit industry: A decade of surveys. Option Méditerranéennes, Sér. B/n°45, 15-23.
  • Nikbakht Dehkordi A, Shiran B, Babaiyan N, Martínez-Gómez P & Rubio M (2018). Detection of Prunus necrotic ringspot virus (PNRSV) in almond and effect on pollen germination. Acta Horticulturae 1219, 357-362. DOI: 10.17660/ActaHortic.2018.1219.54
  • Nyland G, Gilmer RM & Moore JD (1976) Prunus’ ringspot virus group. Virus diseases and noninfectious disorders of stone fruits in North America, USDA Handbook 437 US government Printing Office Washington DC p 104-132.
  • Rodriguez Bonilla F & Cieniewicz E (2022) Distribution and diversity of prunus necrotic ringspot virus, prune dwarf virus, and peach latent mosaic viroid in wild Prunus spp. in South Carolina and Georgia. PhytoFrontiers 2, 363-370. https://doi.org/10.1094/PHYTOFR-02-22-0013-R.
  • Rouag N, Guechi A, Matic S & Myrta A (2008) Short communication: Viruses and viroids of stone fruits in Algeria. Journal of Plant Pathology 90(2), 391-393.
  • Oliver JE, Freer J, Andersen RL, Cox KD, Robinson TL & Fuchs M (2009). Genetic diversity of Prunus necrotic ringspot virus isolates within a cherry orchard in New York. Plant Disease 93, 599-606.
  • Pavliuk L, Udovychenko K, Riaba I & Bublyk M (2017) Variability of some isolates of Prunus necrotic ringspot virus and Prune dwarf virus infecting sour and sweet cherry in Ukraine. Acta agriculturae Slovenica 117(1), 1–9.
  • Pérez Sánchez R, Remedios M & Gómez Sánchez MA (2017) Sour and duke cherry viruses in South-West Europe Phytopathologia Mediterranea 56(1), 62-69. DOI: 10.14601/Phytopathol_Mediterr-15326
  • Saunier R (1972) Incidences d’un virus du type ringspot sur la comportment de deux cultivars du pêchers. La Pomologie Française 14, 175-185.
  • Scott SW, Barnett OW, Burrows PM (1989) Incidence of Prunus necrotic ringspot virus in selected peach orchards of South Carolina. Plant Disease 73, 913-916.
  • Spiegel S, Holand D, Tam Y, Yaakov B, Maslenin L & Rosner A (2004) Prunus necrotic ringspot virus isolates in stone fruit germplasm accessions and cultivars in Israel. Plant Pathology 144, 229-236
  • Tayal M, Ratay A, Swift N, Kaur S, Russo O, Kariyat R & Cieniewicz E (2024) Examining the effects of Prunus necrotic ringspot virus (PNRSV) and Prune dwarf virus (PDV) on peach (Prunus persica) pollen health. PhytoFrontiers™, PHYTOFR-08. https://apsjournals.apsnet.org/doi/full/10.1094/PHYTOFR-08-23-0112-R
  • Topchiiska MI (1983) Effect of Prunus necrotic ringspot virus and Prune dwarf virus on some biological properties of peach. Acta Horticulturae 130, 307-312.
  • Ulubas C & Ertunc F (2004). RT-PCR detection and molecular characterization of Prunus necrotic ringspot virus isolates occurring in Turkey. Journal of Phytopathology 152, 498-502
  • Uyemoto JK, Asai WK & Luhn CF (1992) Ilarviruses: Evidence for rapid spread and effects on vegetative growth and fruit yields of peach trees. Plant Disease 76:71-74.
  • Wells JM, Kirkpatrick HC & Parisch CL (1986) Symptomatology and incidence of Prunus necrotic ringspot virus in peach orchards in Georgia. Plant disease 70, 444-447.
  • Wood GA & Fry PR (1984) Effect of virus infection on growth and cropping of greengage and Billington plum trees. New Zealand Journal of Agricultural Research 27, 563-568.

HOST PLANT N°4: Prunus domestica (PRNDO) 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, including seeds and pollen


3 - Is the pest already listed in a PM4 standard on the concerned host plant?
 
Yes
 
Conclusion:
 
Evaluation continues

 
Justification (if necessary):
 
Listed as 'Prunus necrotic ringspot ilarvirus (PNRSV)' in EPPO Standard PM 4-30 Certification scheme for almond, apricot, peach and plum; with testing recommended. However, in the preliminary excel file submitted by the European Commission, one country commented that the pest 'seems to be quite frequent in nursery and it has a low nuisance level on fruit plants'. As this could affect the RNQP status, a full assessment is performed. In the responses to the questionnaire, PL supported deregulation based on the pathway criteria.
Remark: The assessment performed covers the given host species as well as interspecific hybrids with other Prunus species.

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:
 
Prunus necrotic ringspot virus occurs worldwide and infects many cultivated Prunus species (Hammond, 2011), such as almond - Prunus dulcis (e.g. Mekuria et al., 2003), apricot - Prunus armenica , sweet and sour cherry, P. avium and P. cerasus (e.g. Oliver et al., 2009, Rouag et al., 2009), plum - P. domestica (e.g. Rouag et al., 2009; Jakab-Ilyefalvi et al., 2011), Japanese plum - P. salicina (e.g. Wood & Fry, 1984), and peach (e.g. Topchiiska, 1982; Uyemoto et al., 1992). PNRSV was also found in many wild Prunus spp. like black cherry (Prunus serotina) and cherry laurel (P. caroliniana) and in rose, where it is one of the causes of rose mosaic disease (Horst & Cloyd, 2007). The natural host range also includes herbaceous hosts like hops (symptomless) and cucumber, where chlorotic local lesions, systemic necrosis and severe stunting may occur (Fulton, 1995).
PNRSV is a variable virus consisting of isolates linked to various symptoms in different host species and cultivars (Howell & Mink, 1988; Moury et al., 2001; Oliver et al., 2009; Kamenova & Borisova, 2021; Chirkov et al., 2023).
Infected propagation material is an important pathway (Scott et al., 1989)
Once established PNRSV is easily spread by infected pollen - by wind, bees or thrips - and is also seed transmitted, which can lead to PNRSV-infected seedling rootstocks (e.g. Greber et al., 1991; Kryczynski et al., 1992; Amari et al., 2007; Tayal et al., 2024). Preventing mother stocks to flower prevents infection by pollen.
The Fruit SEWG concluded that plants for planting was a significant pathway.

5 - Economic impact:

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

Justification:
 
General: PNRSV can cause diseases in nurseries which reduced bud take tree growth, tree survival, and uniformity in nursery operations (Saunier, 1972; Topchiiska, 1993 – cited from Hammond, 2011), and death of buds and roots, reduced growth of fruit (10-30%) and fruit yield (20-60%), delay in fruit maturity (Saunier, 1972), diminished fruit quality, and increased susceptibility to winter injury in orchard trees (Nemeth, 1986; Scott et al, 1989; Uyemoto & Scott, 1992). Successful commercial budding can be lower in combinations where scion and rootstock carry the virus (Lang & Howell, 2001). However, PNRSV can also be symptomless in many Prunus spp. (e.g. Spiegel et al., 2004). Many of these symptoms however, were described at a time when it was more difficult to study the whole virome of plant species. New techniques revealed presence of many previously unknown viruses of which their impact on or addition to symptom development is unknown or under investigation (e.g. James et al., 2018; Koloniuk et al., 2018; Hou et al., 2020; Fontdevila Pareta et al., 2023; Khalili et al., 2023).

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?
 
Yes

Conclusion:
 
Candidate

Justification:
 
PNRSV infection can cause symptoms in various Prunus spp. PNRSV symptoms can vary depending on the time passed since the initial infection, species and cultivar, additional virus infection etc. Symptoms can vary between lethal infections (e.g. Lang et al., 1988) to symptomless (e.g. Pérez Sánchez et al., 2017). However, the Fruit SEWG noted that data of economic impact on plum was lacking.
The Fruit SEWG considered that indirect economic impact should be considered: Due to pollen transmissibility, PNRV infected trees pose a serious risk for trees at the same production site. This became e.g. apparent in Austria in a propagation stock intended for the production of certified stone fruit material in the mid-1990s. The explosive spread of PNRV in sweet and sour cherry via pollen from single trees led to the uprooting of the plantation after a few years, despite regular ELISA testing and clearance of positive trees (Riedle-Bauer, unpublished). Sweet cherry and plum can flower at the same time as cherry and cause unacceptable economic impact to this species.

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:
 
Candidate

Justification:
 
Inclusion in a certification scheme.
Propagation material plays relevant role for dissemination.
Serological and molecular detection methods available.

7- Is the quality of the data sufficient to recommend the pest to be listed as a RNQP?
 
Yes
 
Conclusion:
 
Candidate

Justification:
 
Propagation material is a relevant source of infection, the pathogen is widespread, economic damage are reported in many cases.

CONCLUSION ON THE STATUS:
 
Recommended for listing as an RNQP, based on data.


8 - Tolerance level:

Is there a need to change the Tolerance level:
 
No

Proposed Tolerance levels:
 

9 - Risk management measures:

Is there a need to change the Risk management measure:
 
No

Proposed Risk management measure:
 


REFERENCES:
  • Amari K, Burgos L, Pallas V & Sanchez-Pina MA (2007) Prunus necrotic ringspot virus early invasion and its effects on apricot pollen grain performance. Phytopathology 97, 892-899.
  • Bech K (1991) Prunus necrotic ringspot virus (PNRV) in sour cherry Symptoms, incidence in orchards and influence on fruit yield. Tidsskr. Planteavl 95 (1991), 223-232. 223
  • Chirkov S, Sheveleva A, Tsygankova S, Slobodova N, Sharko F, Petrova K & Mitrofanova I (2023) Whole genome characterization of prunus necrotic ringspot virus and prune dwarf virus infecting stone fruits in Russia. Horticulturae 9, 941. https://doi.org/10.3390/horticulturae9080941
  • Çağlayan K, Ulubas Serce C, Gazel M & Varveri C ( 2011) Prune dwarf virus. In In Virus and virus-like diseases of pome and stone fruit s (eds hadidi A, Barba M, Candresse T & Jelkmann W). American Phytopathological Society, St. Paul, Minnesota, USA. 199-205.
  • Greber RS, Klose MJ, Milne JR & Teakle DS (1991) Transmission of prunus necrotic ringspot virus using plum pollen and thrips. Annals of Applied Biology 118, 589-593.
  • Fontdevila Pareta N, Khalili M, Maachi A, Rivarez MPS, Rollin J, Salavert F, Temple C, Aranda MA, Boonham N, Botermans M, Candresse T, Fox A, Hernando Y, Kutnjak D, Marais A, Petter F, Ravnikar M, Selmi I, Tahzima R, Trontin C, Wetzel T & Massart S (2023) Managing the deluge of newly discovered plant viruses and viroids: an optimized scientific and regulatory framework for their characterization and risk analysis. Frontiers in Microbiollogy 14:1181562. doi: 10.3389/fmicb.2023.1181562
  • Fulton RW (1995) Prunus necrotic ringspot virus. In Viruses of Plants (eds Brunt A, Crabtree K, Dallwitz M, Gibbs A & Watson L). CAB International, University Press Cambridge. 1047-1049. (data collected by Fulton in 1985).
  • Hammond RW (2011) Prunus necrotic ringspot virus. In Virus and virus-like diseases of pome and stone fruit s (eds hadidi A, Barba M, Candresse T & Jelkmann W). American Phytopathological Society, St. Paul, Minnesota, USA. 207-213.
  • Horst RK & Cloyd RA (2007) Rose mosaic. In Compendium of rose diseases and pests. American Phytopathological Society, St. Paul, Minnesota, USA. 32-34.
  • Hou W, Li S and Massart S (2020) Is there a “biological desert” with the discovery of new plant viruses? A retrospective analysis for new fruit tree viruses. Frontiers in Microbiology 11:592816. doi: 10.3389/fmicb.2020.592816
  • Howell WE & Mink GI (1988) Natural spread of cherry rugose mosaic virus and two Prunus necrotic ringspot virus biotypes in a central Washington sweet cherry orchard. Plant Disease 72, 636-640.
  • Jakab-Ilyefalvi, Zs, Pamfil D & Craciun C (2011) Transmission electron microscopy of Plum pox virus, Prunus necrotic ringspot virus, Prune dwarf virus in plum (Prunus domestica, L.). Journal of Horticulture, Forestry and Biotechnology 15(1), 120- 125.
  • James D, Phelan J & Jesperson G (2018). First report of prunus virus F infecting sweet cherry (Prunus avium cv. Staccato) in Canada. Plant disease 102(7), 1468.
  • Kamenova I & Borisova A. (2021) Biological and molecular characterization of Prunus necrotic ringspot virus isolates from sweet and sour cherry. Biotechnology & Biotechnological Equipment, 35(1), 567–575. https://doi.org/10.1080/13102818.2021.1901608
  • Khalili M, Candresse T, Koloniuk I, Safarova D, Brans Y, Faure C, Delmas M, Massart S, Aranda MA, Caglayan K, Decroocq V, Drogoudi P, Glasa M, Pantelidis G, Navratil M, Latour F, Spak J, Pribylova J, Mihalik D, Palmisano F, Saponari A, Necas T, Sedlak J & Marais, A. (2023). The expanding menagerie of Prunus-infecting luteoviruses. Phytopathology 113(2), 345-354.
  • Koloniuk I, Sarkisova T, Petrzik K, Lenz O, Přibylová J, Fránová J, Špak J, Lotos L, Beta C, Katsiani A, Candresse T & Maliogka VI (2018) Variability studies of two prunus-infecting fabaviruses with the aid of High-Throughput Sequencing. Viruses 10, 204; doi:10.3390/v10040204
  • Kryczynski S, Szyndel MS, Stawiszynska A & Piskorek W (1992) The rate and the way of Prunus necrotic ringspot virus spread in sour cherry orchard and in the rootstock production. Acta Horticulturae 309, 105-110.
  • Lang GA & Howell W (2001) Lethal sensitivity of some new cherry rootstocks to pollen-borne viruses. Acta Horticulturae 557, 151-154.
  • Lang G, Howell W & Ophardt D (1998). Sweet cherry rootstock/virus interactions. Acta Horticulturae 468, 307-314. DOI: 10.17660/ActaHortic.1998.468.36
  • Lansac M, Detienne G, Bernhard R & Dunez J (1981) Analysis of nine isolates of almond mosaic. Acta Horticulturae 94, 359-366.
  • Mekuria G, Ramesh SA, Alberts E, Bertozzi T, Wirthensohn M, Collins G & Sedgley M. (2003) Comparison of ELISA and RT-PCR for the detection of Prunus necrotic ring spot virus and prune dwarf virus in almond (Prunus dulcis). Journal of virological methods 114(1), 65-69.
  • Moury B, Cardin L, Onesto JP, Candresse T & Poupet A (2001). Survey of Prunus necrotic ringspot virus in rose and its variability in rose and Prunus spp. Phytopathology 91, 84-91.
  • Myrta A, Di-Terlizzi B, Savino V & Martelli GP (2003) Virus diseases affecting the Mediterranean stone fruit industry: A decade of surveys. Option Méditerranéennes, Sér. B/n°45, 15-23.
  • Nikbakht Dehkordi A, Shiran B, Babaiyan N, Martínez-Gómez P & Rubio M (2018). Detection of Prunus necrotic ringspot virus (PNRSV) in almond and effect on pollen germination. Acta Horticulturae 1219, 357-362. DOI: 10.17660/ActaHortic.2018.1219.54
  • Nyland G, Gilmer RM & Moore JD (1976) Prunus’ ringspot virus group. Virus diseases and noninfectious disorders of stone fruits in North America, USDA Handbook 437 US government Printing Office Washington DC p 104-132.
  • Rodriguez Bonilla F & Cieniewicz E (2022) Distribution and diversity of prunus necrotic ringspot virus, prune dwarf virus, and peach latent mosaic viroid in wild Prunus spp. in South Carolina and Georgia. PhytoFrontiers 2, 363-370. https://doi.org/10.1094/PHYTOFR-02-22-0013-R.
  • Oliver JE, Freer J, Andersen RL, Cox KD, Robinson TL & Fuchs M (2009). Genetic diversity of Prunus necrotic ringspot virus isolates within a cherry orchard in New York. Plant Disease 93, 599-606.
  • Pavliuk L, Udovychenko K, Riaba I & Bublyk M (2017) Variability of some isolates of Prunus necrotic ringspot virus and Prune dwarf virus infecting sour and sweet cherry in Ukraine. Acta agriculturae Slovenica 117(1), 1–9.
  • Pérez Sánchez R, Remedios M & Gómez Sánchez MA (2017) Sour and duke cherry viruses in South-West Europe Phytopathologia Mediterranea 56(1), 62-69. DOI: 10.14601/Phytopathol_Mediterr-15326
  • Rouag N, Guechi A, Matic S & Myrta A (2008) Short communication: Viruses and viroids of stone fruits in Algeria. Journal of Plant Pathology 90(2), 391-393.
  • Saunier R (1972) Incidences d’un virus du type ringspot sur la comportment de deux cultivars du pêchers. La Pomologie Française 14, 175-185.
  • Scott SW, Barnett OW, Burrows PM (1989) Incidence of Prunus necrotic ringspot virus in selected peach orchards of South Carolina. Plant Disease 73, 913-916.
  • Spiegel S, Holand D, Tam Y, Yaakov B, Maslenin L & Rosner A (2004) Prunus necrotic ringspot virus isolates in stone fruit germplasm accessions and cultivars in Israel. Plant Pathology 144, 229-236
  • Tayal M, Ratay A, Swift N, Kaur S, Russo O, Kariyat R & Cieniewicz E (2024) Examining the effects of Prunus necrotic ringspot virus (PNRSV) and Prune dwarf virus (PDV) on peach (Prunus persica) pollen health. PhytoFrontiers™, PHYTOFR-08. https://apsjournals.apsnet.org/doi/full/10.1094/PHYTOFR-08-23-0112-R
  • Topchiiska MI (1983) Effect of Prunus necrotic ringspot virus and Prune dwarf virus on some biological properties of peach. Acta Horticulturae 130, 307-312.
  • Ulubas C & Ertunc F (2004). RT-PCR detection and molecular characterization of Prunus necrotic ringspot virus isolates occurring in Turkey. Journal of Phytopathology 152, 498-502
  • Uyemoto JK, Asai WK & Luhn CF (1992) Ilarviruses: Evidence for rapid spread and effects on vegetative growth and fruit yields of peach trees. Plant Disease 76:71-74.
  • Wells JM, Kirkpatrick HC & Parisch CL (1986) Symptomatology and incidence of Prunus necrotic ringspot virus in peach orchards in Georgia. Plant disease 70, 444-447.
  • Wood GA & Fry PR (1984) Effect of virus infection on growth and cropping of greengage and Billington plum trees. New Zealand Journal of Agricultural Research 27, 563-568.

HOST PLANT N°5: Prunus dulcis (PRNDU) 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, including seeds and pollen


3 - Is the pest already listed in a PM4 standard on the concerned host plant?
 
Yes
 
Conclusion:
 
Evaluation continues

 
Justification (if necessary):
 
Listed as 'Prunus necrotic ringspot ilarvirus (PNRSV)' in EPPO Standard PM 4-30 Certification scheme for almond, apricot, peach and plum; with testing recommended. However, in the preliminary excel file submitted by the European Commission, one country commented that the pest 'seems to be quite frequent in nursery and it has a low nuisance level on fruit plants'. As this could affect the RNQP status, a full assessment is performed. In the responses to the questionnaire, PL supported deregulation based on the pathway criteria.
Remark: The assessment performed covers the given host species as well as interspecific hybrids with other Prunus species.

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:
 
Prunus necrotic ringspot virus occurs worldwide and infects many cultivated Prunus species (Hammond, 2011), such as almond - Prunus dulcis (e.g. Mekuria et al., 2003), apricot - Prunus armenica , sweet and sour cherry, P. avium and P. cerasus (e.g. Oliver et al., 2009, Rouag et al., 2009), plum - P. domestica (e.g. Rouag et al., 2009; Jakab-Ilyefalvi et al., 2011), Japanese plum - P. salicina (e.g. Wood & Fry, 1984), and peach (e.g. Topchiiska, 1982; Uyemoto et al., 1992). PNRSV was also found in many wild Prunus spp. like black cherry (Prunus serotina) and cherry laurel (P. caroliniana) and in rose, where it is one of the causes of rose mosaic disease (Horst & Cloyd, 2007). The natural host range also includes herbaceous hosts like hops (symptomless) and cucumber, where chlorotic local lesions, systemic necrosis and severe stunting may occur (Fulton, 1995).
PNRSV is a variable virus consisting of isolates linked to various symptoms in different host species and cultivars (Howell & Mink, 1988; Moury et al., 2001; Oliver et al., 2009; Kamenova & Borisova, 2021; Chirkov et al., 2023).
Infected propagation material is an important pathway (Scott et al., 1989).
Once established PNRSV is easily spread by infected pollen - by wind, bees or thrips - and is also seed transmitted, which can lead to PNRSV-infected seedling rootstocks (e.g. Greber et al., 1991; Kryczynski et al., 1992; Amari et al., 2007; Tayal et al., 2024). Preventing mother stocks to flower prevents infection by pollen.
The Fruit SEWG concluded that plants for planting was a significant pathway.

5 - Economic impact:

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

Justification:
 
General: PNRSV can cause diseases in nurseries which reduced bud take tree growth, tree survival, and uniformity in nursery operations (Saunier, 1972; Topchiiska, 1993 – cited from Hammond, 2011), and death of buds and roots, reduced growth of fruit (10-30%) and fruit yield (20-60%), delay in fruit maturity (Saunier, 1972), diminished fruit quality, and increased susceptibility to winter injury in orchard trees (Nemeth, 1986; Scott et al, 1989; Uyemoto & Scott, 1992). Successful commercial budding can be lower in combinations where scion and rootstock carry the virus (Lang & Howell, 2001). However, PNRSV can also be symptomless in many Prunus spp. (e.g. Spiegel et al., 2004). Many of these symptoms however, were described at a time when it was more difficult to study the whole virome of plant species. New techniques revealed presence of many previously unknown viruses of which their impact on or addition to symptom development is unknown or under investigation (e.g. James et al., 2018; Koloniuk et al., 2018; Hou et al., 2020; Fontdevila Pareta et al., 2023; Khalili et al., 2023).
Prunus dulcis: In almond, PNRV can cause weakness, overall decline and reduced yield which finally lead to reduced quality and quantity of the product and annually cause great losses. Infected almond trees may develop sudden necrosis, chlorotic and necrotic leaf spots, leaf mosaic, ring spot and line patterns (Nyland et al., 1976; Lansac et al., 1980; reviewed in Nikbakht Dehkordi et al., 2018).
Infection with PNRSV can reduce the germination of pollen of almond (Nikbakht Dehkordi et al., 2018).
Several authors raise the concern that co-occurrence of PNRV with other viruses could greatly aggravate the damage (e.g. reviewed in Tayal et al., 2024).

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?
 
No

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:
 
Candidate

Justification:
 
PNRSV infection can cause symptoms in various Prunus spp. PNRSV symptoms can vary depending on the time passed since the initial infection, species and cultivar, additional virus infection etc. Symptoms can vary between lethal infections (e.g. Lang et al., 1988) to symptomless (e.g. Pérez Sánchez et al., 2017). Due to pollen transmissibility, PNRV infected trees pose a serious risk for trees at the same production site. This became e.g. apparent in Austria in a propagation stock intended for the production of certified stone fruit material in the mid-1990s. The explosive spread of PNRV in sweet and sour cherry via pollen from single trees led to the uprooting of the plantation after a few years, despite regular ELISA testing and clearance of positive trees (Riedle-Bauer, unpublished).

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:
 
Candidate

Justification:
 
Inclusion in a certification scheme.
Propagation material plays relevant role for dissemination.
Serological and molecular detection methods available.

7- Is the quality of the data sufficient to recommend the pest to be listed as a RNQP?
 
Yes
 
Conclusion:
 
Candidate

Justification:
 
Propagation material is a relevant source of infection, the pathogen is widespread, economic damage are reported in many cases.

CONCLUSION ON THE STATUS:
 
Recommended for listing as an RNQP, based on data.


8 - Tolerance level:

Is there a need to change the Tolerance level:
 
No

Proposed Tolerance levels:
 

9 - Risk management measures:

Is there a need to change the Risk management measure:
 
No

Proposed Risk management measure:
 


REFERENCES:
  • Amari K, Burgos L, Pallas V & Sanchez-Pina MA (2007) Prunus necrotic ringspot virus early invasion and its effects on apricot pollen grain performance. Phytopathology 97, 892-899.
  • Bech K (1991) Prunus necrotic ringspot virus (PNRV) in sour cherry Symptoms, incidence in orchards and influence on fruit yield. Tidsskr. Planteavl 95 (1991), 223-232. 223
  • Chirkov S, Sheveleva A, Tsygankova S, Slobodova N, Sharko F, Petrova K & Mitrofanova I (2023) Whole genome characterization of prunus necrotic ringspot virus and prune dwarf virus infecting stone fruits in Russia. Horticulturae 9, 941. https://doi.org/10.3390/horticulturae9080941
  • Çağlayan K, Ulubas Serce C, Gazel M & Varveri C ( 2011) Prune dwarf virus. In In Virus and virus-like diseases of pome and stone fruit s (eds hadidi A, Barba M, Candresse T & Jelkmann W). American Phytopathological Society, St. Paul, Minnesota, USA. 199-205.
  • Greber RS, Klose MJ, Milne JR & Teakle DS (1991) Transmission of prunus necrotic ringspot virus using plum pollen and thrips. Annals of Applied Biology 118, 589-593.
  • Fontdevila Pareta N, Khalili M, Maachi A, Rivarez MPS, Rollin J, Salavert F, Temple C, Aranda MA, Boonham N, Botermans M, Candresse T, Fox A, Hernando Y, Kutnjak D, Marais A, Petter F, Ravnikar M, Selmi I, Tahzima R, Trontin C, Wetzel T & Massart S (2023) Managing the deluge of newly discovered plant viruses and viroids: an optimized scientific and regulatory framework for their characterization and risk analysis. Frontiers in Microbiollogy 14:1181562. doi: 10.3389/fmicb.2023.1181562
  • Fulton RW (1995) Prunus necrotic ringspot virus. In Viruses of Plants (eds Brunt A, Crabtree K, Dallwitz M, Gibbs A & Watson L). CAB International, University Press Cambridge. 1047-1049. (data collected by Fulton in 1985).
  • Hammond RW (2011) Prunus necrotic ringspot virus. In Virus and virus-like diseases of pome and stone fruit s (eds hadidi A, Barba M, Candresse T & Jelkmann W). American Phytopathological Society, St. Paul, Minnesota, USA. 207-213.
  • Horst RK & Cloyd RA (2007) Rose mosaic. In Compendium of rose diseases and pests. American Phytopathological Society, St. Paul, Minnesota, USA. 32-34.
  • Hou W, Li S and Massart S (2020) Is there a “biological desert” with the discovery of new plant viruses? A retrospective analysis for new fruit tree viruses. Frontiers in Microbiology 11:592816. doi: 10.3389/fmicb.2020.592816
  • Howell WE & Mink GI (1988) Natural spread of cherry rugose mosaic virus and two Prunus necrotic ringspot virus biotypes in a central Washington sweet cherry orchard. Plant Disease 72, 636-640.
  • Jakab-Ilyefalvi, Zs, Pamfil D & Craciun C (2011) Transmission electron microscopy of Plum pox virus, Prunus necrotic ringspot virus, Prune dwarf virus in plum (Prunus domestica, L.). Journal of Horticulture, Forestry and Biotechnology 15(1), 120- 125.
  • James D, Phelan J & Jesperson G (2018). First report of prunus virus F infecting sweet cherry (Prunus avium cv. Staccato) in Canada. Plant disease 102(7), 1468.
  • Kamenova I & Borisova A. (2021) Biological and molecular characterization of Prunus necrotic ringspot virus isolates from sweet and sour cherry. Biotechnology & Biotechnological Equipment, 35(1), 567–575. https://doi.org/10.1080/13102818.2021.1901608
  • Khalili M, Candresse T, Koloniuk I, Safarova D, Brans Y, Faure C, Delmas M, Massart S, Aranda MA, Caglayan K, Decroocq V, Drogoudi P, Glasa M, Pantelidis G, Navratil M, Latour F, Spak J, Pribylova J, Mihalik D, Palmisano F, Saponari A, Necas T, Sedlak J & Marais, A. (2023). The expanding menagerie of Prunus-infecting luteoviruses. Phytopathology 113(2), 345-354.
  • Koloniuk I, Sarkisova T, Petrzik K, Lenz O, Přibylová J, Fránová J, Špak J, Lotos L, Beta C, Katsiani A, Candresse T & Maliogka VI (2018) Variability studies of two prunus-infecting fabaviruses with the aid of High-Throughput Sequencing. Viruses 10, 204; doi:10.3390/v10040204
  • Kryczynski S, Szyndel MS, Stawiszynska A & Piskorek W (1992) The rate and the way of Prunus necrotic ringspot virus spread in sour cherry orchard and in the rootstock production. Acta Horticulturae 309, 105-110.
  • Lang GA & Howell W (2001) Lethal sensitivity of some new cherry rootstocks to pollen-borne viruses. Acta Horticulturae 557, 151-154.
  • Lang G, Howell W & Ophardt D (1998). Sweet cherry rootstock/virus interactions. Acta Horticulturae 468, 307-314. DOI: 10.17660/ActaHortic.1998.468.36
  • Lansac M, Detienne G, Bernhard R & Dunez J (1981) Analysis of nine isolates of almond mosaic. Acta Horticulturae 94, 359-366.
  • Mekuria G, Ramesh SA, Alberts E, Bertozzi T, Wirthensohn M, Collins G & Sedgley M. (2003) Comparison of ELISA and RT-PCR for the detection of Prunus necrotic ring spot virus and prune dwarf virus in almond (Prunus dulcis). Journal of virological methods 114(1), 65-69.
  • Myrta A, Di-Terlizzi B, Savino V & Martelli GP (2003) Virus diseases affecting the Mediterranean stone fruit industry: A decade of surveys. Option Méditerranéennes, Sér. B/n°45, 15-23.
  • Moury B, Cardin L, Onesto JP, Candresse T & Poupet A (2001). Survey of Prunus necrotic ringspot virus in rose and its variability in rose and Prunus spp. Phytopathology 91, 84-91.
  • Nikbakht Dehkordi A, Shiran B, Babaiyan N, Martínez-Gómez P & Rubio M (2018). Detection of Prunus necrotic ringspot virus (PNRSV) in almond and effect on pollen germination. Acta Horticulturae 1219, 357-362. DOI: 10.17660/ActaHortic.2018.1219.54
  • Nyland G, Gilmer RM & Moore JD (1976) Prunus’ ringspot virus group. Virus diseases and noninfectious disorders of stone fruits in North America, USDA Handbook 437 US government Printing Office Washington DC p 104-132.
  • Rodriguez Bonilla F & Cieniewicz E (2022) Distribution and diversity of prunus necrotic ringspot virus, prune dwarf virus, and peach latent mosaic viroid in wild Prunus spp. in South Carolina and Georgia. PhytoFrontiers 2, 363-370. https://doi.org/10.1094/PHYTOFR-02-22-0013-R.
  • Rouag N, Guechi A, Matic S & Myrta A (2008) Short communication: Viruses and viroids of stone fruits in Algeria. Journal of Plant Pathology 90(2), 391-393.
  • Oliver JE, Freer J, Andersen RL, Cox KD, Robinson TL & Fuchs M (2009). Genetic diversity of Prunus necrotic ringspot virus isolates within a cherry orchard in New York. Plant Disease 93, 599-606.
  • Pavliuk L, Udovychenko K, Riaba I & Bublyk M (2017) Variability of some isolates of Prunus necrotic ringspot virus and Prune dwarf virus infecting sour and sweet cherry in Ukraine. Acta agriculturae Slovenica 117(1), 1–9.
  • Pérez Sánchez R, Remedios M & Gómez Sánchez MA (2017) Sour and duke cherry viruses in South-West Europe Phytopathologia Mediterranea 56(1), 62-69. DOI: 10.14601/Phytopathol_Mediterr-15326
  • Saunier R (1972) Incidences d’un virus du type ringspot sur la comportment de deux cultivars du pêchers. La Pomologie Française 14, 175-185.
  • Scott SW, Barnett OW, Burrows PM (1989) Incidence of Prunus necrotic ringspot virus in selected peach orchards of South Carolina. Plant Disease 73, 913-916.
  • Spiegel S, Holand D, Tam Y, Yaakov B, Maslenin L & Rosner A (2004) Prunus necrotic ringspot virus isolates in stone fruit germplasm accessions and cultivars in Israel. Plant Pathology 144, 229-236
  • Tayal M, Ratay A, Swift N, Kaur S, Russo O, Kariyat R & Cieniewicz E (2024) Examining the effects of Prunus necrotic ringspot virus (PNRSV) and Prune dwarf virus (PDV) on peach (Prunus persica) pollen health. PhytoFrontiers™, PHYTOFR-08. https://apsjournals.apsnet.org/doi/full/10.1094/PHYTOFR-08-23-0112-R
  • Topchiiska MI (1983) Effect of Prunus necrotic ringspot virus and Prune dwarf virus on some biological properties of peach. Acta Horticulturae 130, 307-312.
  • Ulubas C & Ertunc F (2004). RT-PCR detection and molecular characterization of Prunus necrotic ringspot virus isolates occurring in Turkey. Journal of Phytopathology 152, 498-502
  • Uyemoto JK, Asai WK & Luhn CF (1992) Ilarviruses: Evidence for rapid spread and effects on vegetative growth and fruit yields of peach trees. Plant Disease 76:71-74.
  • Wells JM, Kirkpatrick HC & Parisch CL (1986) Symptomatology and incidence of Prunus necrotic ringspot virus in peach orchards in Georgia. Plant disease 70, 444-447.
  • Wood GA & Fry PR (1984) Effect of virus infection on growth and cropping of greengage and Billington plum trees. New Zealand Journal of Agricultural Research 27, 563-568.

HOST PLANT N°6: Prunus persica (PRNPS) 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, including seeds and pollen


3 - Is the pest already listed in a PM4 standard on the concerned host plant?
 
Yes
 
Conclusion:
 
Evaluation continues

 
Justification (if necessary):
 
Listed as 'Prunus necrotic ringspot ilarvirus (PNRSV)' in EPPO Standard PM 4-30 Certification scheme for almond, apricot, peach and plum; with testing recommended. However, in the preliminary excel file submitted by the European Commission, one country commented that the pest 'seems to be quite frequent in nursery and it has a low nuisance level on fruit plants'. As this could affect the RNQP status, a full assessment is performed. In the responses to the questionnaire, PL supported deregulation based on the pathway criteria.
Remark: The assessment performed covers the given host species as well as interspecific hybrids with other Prunus species.

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:
 
Prunus necrotic ringspot virus occurs worldwide and infects many cultivated Prunus species (Hammond, 2011), such as almond - Prunus dulcis (e.g. Mekuria et al., 2003), apricot - Prunus armenica , sweet and sour cherry, P. avium and P. cerasus (e.g. Oliver et al., 2009, Rouag et al., 2009), plum - P. domestica (e.g. Rouag et al., 2009; Jakab-Ilyefalvi et al., 2011), Japanese plum - P. salicina (e.g. Wood & Fry, 1984), and peach (e.g. Topchiiska, 1982; Uyemoto et al., 1992). PNRSV was also found in many wild Prunus spp. like black cherry (Prunus serotina) and cherry laurel (P. caroliniana) and in rose, where it is one of the causes of rose mosaic disease (Horst & Cloyd, 2007). The natural host range also includes herbaceous hosts like hops (symptomless) and cucumber, where chlorotic local lesions, systemic necrosis and severe stunting may occur (Fulton, 1995).
PNRSV is a variable virus consisting of isolates linked to various symptoms in different host species and cultivars (Howell & Mink, 1988; Moury et al., 2001; Oliver et al., 2009; Kamenova & Borisova, 2021; Chirkov et al., 2023).
Infected propagation material is an important pathway (Scott et al., 1989)
Once established PNRSV is easily spread by infected pollen - by wind, bees or thrips - and is also seed transmitted, which can lead to PNRSV-infected seedling rootstocks (e.g. Greber et al., 1991; Kryczynski et al., 1992; Amari et al., 2007; Tayal et al., 2024). Preventing mother stocks to flower prevents infection by pollen.
The Fruit SEWG concluded that plants for planting was a significant pathway.

5 - Economic impact:

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

Justification:
 
General: PNRSV can cause diseases in nurseries which reduced bud take tree growth, tree survival, and uniformity in nursery operations (Saunier, 1972; Topchiiska, 1993 – cited from Hammond, 2011), and death of buds and roots, reduced growth of fruit (10-30%) and fruit yield (20-60%), delay in fruit maturity (Saunier, 1972), diminished fruit quality, and increased susceptibility to winter injury in orchard trees (Nemeth, 1986; Scott et al, 1989; Uyemoto & Scott, 1992). Successful commercial budding can be lower in combinations where scion and rootstock carry the virus (Lang & Howell, 2001). Many of these symptoms however, were described at a time when it was more difficult to study the whole virome of plant species. New techniques revealed presence of many previously unknown viruses of which their impact on or addition to symptom development is unknown or under investigation (e.g. James et al., 2018; Koloniuk et al., 2018; Hou et al., 2020; Fontdevila Pareta et al., 2023; Khalili et al., 2023).
Prunus persica & Prunus armeniaca
Single virus infection by PNRSV significantly affected tree growth and fruit yield (Uyemoto et al, 1992). When peach cultivars were bud-inoculated with PNRSV, the trees developed foliar chlorotic rings and necrosis during the virus year after inoculation. Twig dieback, bark necrosis, root sprouts and trunk cankers developed during subsequent years. Symptoms on inoculated trees resembled those of the slow-decline disease prevalent in central Georgia orchards, particularly the extensive bark necrosis and longitudinal trunk cankers (Wells et al., 1986).
PNRSV affected apricot and pollen germination (by ca. 58%) and delayed germination (Amari et al., 2007). Pollen of peach can also be affected by PNRSV: infection resulted in distorted shape, reduced viability, and germination of pollen grains, but the effect was cultivar dependent (Tayal et al., 2024).
PNRSV has been observed to cause extensive economic losses to peach (Prunus persicae) and apricot (P. armaniaca) trees in Egypt. Symptoms are mostly expressed as necrotic ringspots on leaves, bud failure and poor quantity and quality of fruits (Abdel-Salam et al., 2007).
In peach, PNRSV, together with prune dwarf virus (PDV, another pollen dispersed ilarvirus), causes synergistic effects on growth reduction and yield losses. The resulting disease, peach stunt (PSD) is a frequently reported disease in the Mediterranean area (Myrta et al. 2003). Typical symptoms of PSD include stunting, shortening of internodes, reduction in fruit yield and vegetative growth, defoliation of leaves, rosetting, leaf chlorosis, gummosis, bark splitting, delay in bud break, as well as an increase in water sprouts production. Mixed infection could be more harmful than individual infections as PSD was associated with an 80% mortality in stone fruits in Morocco (Srhiri et al.1998; for review see Tayal et al. 2024). Uyemoto et al. (1992) reported that a double infection with PNRSV and PDV leading to peach stunt disease reduced fruit production, trunk diameter and tree height by ca. 30, 23 and 12% respectively over 3 years. In another publication, peach trees infected with PDV and PNRV were reported to display bark splitting and increased watersprout (sucker) production. Fruit yields were reduced by up to 60% in trees infected with both PNRSV and PDV (Scott et al., 2001).

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?
 
No

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:
 
Candidate

Justification:
 
PNRSV infection can cause symptoms in various Prunus spp. PNRSV symptoms can vary depending on the time passed since the initial infection, species and cultivar, additional virus infection etc. Symptoms can vary between lethal infections (e.g. Lang et al., 1988) to symptomless (e.g. Pérez Sánchez et al., 2017). Due to pollen transmissibility, PNRV infected trees pose a serious risk for trees at the same production site. This became e.g. apparent in Austria in a propagation stock intended for the production of certified stone fruit material in the mid-1990s. The explosive spread of PNRV in sweet and sour cherry via pollen from single trees led to the uprooting of the plantation after a few years, despite regular ELISA testing and clearance of positive trees (Riedle-Bauer, unpublished).

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:
 
Candidate

Justification:
 
Inclusion in a certification scheme.
Propagation material plays relevant role for dissemination.
Serological and molecular detection methods available.

7- Is the quality of the data sufficient to recommend the pest to be listed as a RNQP?
 
Yes
 
Conclusion:
 
Candidate

Justification:
 
Propagation material is a relevant source of infection, the pathogen is widespread, economic damage are reported in many cases.

CONCLUSION ON THE STATUS:
 
Recommended for listing as an RNQP, based on data.


8 - Tolerance level:

Is there a need to change the Tolerance level:
 
No

Proposed Tolerance levels:
 

9 - Risk management measures:

Is there a need to change the Risk management measure:
 
No

Proposed Risk management measure:
 


REFERENCES:
  • Amari K, Burgos L, Pallas V & Sanchez-Pina MA (2007) Prunus necrotic ringspot virus early invasion and its effects on apricot pollen grain performance. Phytopathology 97, 892-899.
  • Bech K (1991) Prunus necrotic ringspot virus (PNRV) in sour cherry Symptoms, incidence in orchards and influence on fruit yield. Tidsskr. Planteavl 95 (1991), 223-232. 223
  • Chirkov S, Sheveleva A, Tsygankova S, Slobodova N, Sharko F, Petrova K & Mitrofanova I (2023) Whole genome characterization of prunus necrotic ringspot virus and prune dwarf virus infecting stone fruits in Russia. Horticulturae 9, 941. https://doi.org/10.3390/horticulturae9080941
  • Çağlayan K, Ulubas Serce C, Gazel M & Varveri C ( 2011) Prune dwarf virus. In In Virus and virus-like diseases of pome and stone fruit s (eds hadidi A, Barba M, Candresse T & Jelkmann W). American Phytopathological Society, St. Paul, Minnesota, USA. 199-205.
  • Greber RS, Klose MJ, Milne JR & Teakle DS (1991) Transmission of prunus necrotic ringspot virus using plum pollen and thrips. Annals of Applied Biology 118, 589-593.
  • Fontdevila Pareta N, Khalili M, Maachi A, Rivarez MPS, Rollin J, Salavert F, Temple C, Aranda MA, Boonham N, Botermans M, Candresse T, Fox A, Hernando Y, Kutnjak D, Marais A, Petter F, Ravnikar M, Selmi I, Tahzima R, Trontin C, Wetzel T & Massart S (2023) Managing the deluge of newly discovered plant viruses and viroids: an optimized scientific and regulatory framework for their characterization and risk analysis. Frontiers in Microbiollogy 14:1181562. doi: 10.3389/fmicb.2023.1181562
  • Fulton RW (1995) Prunus necrotic ringspot virus. In Viruses of Plants (eds Brunt A, Crabtree K, Dallwitz M, Gibbs A & Watson L). CAB International, University Press Cambridge. 1047-1049. (data collected by Fulton in 1985).
  • Hammond RW (2011) Prunus necrotic ringspot virus. In Virus and virus-like diseases of pome and stone fruit s (eds hadidi A, Barba M, Candresse T & Jelkmann W). American Phytopathological Society, St. Paul, Minnesota, USA. 207-213.
  • Horst RK & Cloyd RA (2007) Rose mosaic. In Compendium of rose diseases and pests. American Phytopathological Society, St. Paul, Minnesota, USA. 32-34.
  • Hou W, Li S and Massart S (2020) Is there a “biological desert” with the discovery of new plant viruses? A retrospective analysis for new fruit tree viruses. Frontiers in Microbiology 11:592816. doi: 10.3389/fmicb.2020.592816
  • Howell WE & Mink GI (1988) Natural spread of cherry rugose mosaic virus and two Prunus necrotic ringspot virus biotypes in a central Washington sweet cherry orchard. Plant Disease 72, 636-640.
  • Jakab-Ilyefalvi, Zs, Pamfil D & Craciun C (2011) Transmission electron microscopy of Plum pox virus, Prunus necrotic ringspot virus, Prune dwarf virus in plum (Prunus domestica, L.). Journal of Horticulture, Forestry and Biotechnology 15(1), 120- 125.
  • James D, Phelan J & Jesperson G (2018). First report of prunus virus F infecting sweet cherry (Prunus avium cv. Staccato) in Canada. Plant disease 102(7), 1468.
  • Kamenova I & Borisova A. (2021) Biological and molecular characterization of Prunus necrotic ringspot virus isolates from sweet and sour cherry. Biotechnology & Biotechnological Equipment, 35(1), 567–575. https://doi.org/10.1080/13102818.2021.1901608
  • Khalili M, Candresse T, Koloniuk I, Safarova D, Brans Y, Faure C, Delmas M, Massart S, Aranda MA, Caglayan K, Decroocq V, Drogoudi P, Glasa M, Pantelidis G, Navratil M, Latour F, Spak J, Pribylova J, Mihalik D, Palmisano F, Saponari A, Necas T, Sedlak J & Marais, A. (2023). The expanding menagerie of Prunus-infecting luteoviruses. Phytopathology 113(2), 345-354.
  • Koloniuk I, Sarkisova T, Petrzik K, Lenz O, Přibylová J, Fránová J, Špak J, Lotos L, Beta C, Katsiani A, Candresse T & Maliogka VI (2018) Variability studies of two prunus-infecting fabaviruses with the aid of High-Throughput Sequencing. Viruses 10, 204; doi:10.3390/v10040204
  • Kryczynski S, Szyndel MS, Stawiszynska A & Piskorek W (1992) The rate and the way of Prunus necrotic ringspot virus spread in sour cherry orchard and in the rootstock production. Acta Horticulturae 309, 105-110.
  • Lang GA & Howell W (2001) Lethal sensitivity of some new cherry rootstocks to pollen-borne viruses. Acta Horticulturae 557, 151-154.
  • Lang G, Howell W & Ophardt D (1998). Sweet cherry rootstock/virus interactions. Acta Horticulturae 468, 307-314. DOI: 10.17660/ActaHortic.1998.468.36
  • Lansac M, Detienne G, Bernhard R & Dunez J (1981) Analysis of nine isolates of almond mosaic. Acta Horticulturae 94, 359-366.
  • Mekuria G, Ramesh SA, Alberts E, Bertozzi T, Wirthensohn M, Collins G & Sedgley M. (2003) Comparison of ELISA and RT-PCR for the detection of Prunus necrotic ring spot virus and prune dwarf virus in almond (Prunus dulcis). Journal of virological methods 114(1), 65-69.
  • Moury B, Cardin L, Onesto JP, Candresse T & Poupet A (2001). Survey of Prunus necrotic ringspot virus in rose and its variability in rose and Prunus spp. Phytopathology 91, 84-91.
  • Myrta A, Di-Terlizzi B, Savino V & Martelli GP (2003) Virus diseases affecting the Mediterranean stone fruit industry: A decade of surveys. Option Méditerranéennes, Sér. B/n°45, 15-23.
  • Nikbakht Dehkordi A, Shiran B, Babaiyan N, Martínez-Gómez P & Rubio M (2018). Detection of Prunus necrotic ringspot virus (PNRSV) in almond and effect on pollen germination. Acta Horticulturae 1219, 357-362. DOI: 10.17660/ActaHortic.2018.1219.54
  • Nyland G, Gilmer RM & Moore JD (1976) Prunus’ ringspot virus group. Virus diseases and noninfectious disorders of stone fruits in North America, USDA Handbook 437 US government Printing Office Washington DC p 104-132.
  • Rodriguez Bonilla F & Cieniewicz E (2022) Distribution and diversity of prunus necrotic ringspot virus, prune dwarf virus, and peach latent mosaic viroid in wild Prunus spp. in South Carolina and Georgia. PhytoFrontiers 2, 363-370. https://doi.org/10.1094/PHYTOFR-02-22-0013-R.
  • Oliver JE, Freer J, Andersen RL, Cox KD, Robinson TL & Fuchs M (2009). Genetic diversity of Prunus necrotic ringspot virus isolates within a cherry orchard in New York. Plant Disease 93, 599-606.
  • Pavliuk L, Udovychenko K, Riaba I & Bublyk M (2017) Variability of some isolates of Prunus necrotic ringspot virus and Prune dwarf virus infecting sour and sweet cherry in Ukraine. Acta agriculturae Slovenica 117(1), 1–9.
  • Pérez Sánchez R, Remedios M & Gómez Sánchez MA (2017) Sour and duke cherry viruses in South-West Europe Phytopathologia Mediterranea 56(1), 62-69. DOI: 10.14601/Phytopathol_Mediterr-15326
  • Rouag N, Guechi A, Matic S & Myrta A (2008) Short communication: Viruses and viroids of stone fruits in Algeria. Journal of Plant Pathology 90(2), 391-393.
  • Saunier R (1972) Incidences d’un virus du type ringspot sur la comportment de deux cultivars du pêchers. La Pomologie Française 14, 175-185.
  • Scott SW, Barnett OW, Burrows PM (1989) Incidence of Prunus necrotic ringspot virus in selected peach orchards of South Carolina. Plant Disease 73, 913-916.
  • Scott SW, Zimmerman MT, Yilmaz S, Zehr EI & Bachman E (2001) The interaction between Prunus necrotic ringspot virus and Prune dwarf virus in peach stunt disease. Acta Horticulturae 550, 229-236. https://doi.org/10.17660/ActaHortic.2001.550.32.
  • Spiegel S, Holand D, Tam Y, Yaakov B, Maslenin L & Rosner A (2004) Prunus necrotic ringspot virus isolates in stone fruit germplasm accessions and cultivars in Israel. Plant Pathology 144, 229-236
  • Tayal M, Ratay A, Swift N, Kaur S, Russo O, Kariyat R & Cieniewicz E (2024) Examining the effects of Prunus necrotic ringspot virus (PNRSV) and Prune dwarf virus (PDV) on peach (Prunus persica) pollen health. PhytoFrontiers™, PHYTOFR-08. https://apsjournals.apsnet.org/doi/full/10.1094/PHYTOFR-08-23-0112-R
  • Topchiiska MI (1983) Effect of Prunus necrotic ringspot virus and Prune dwarf virus on some biological properties of peach. Acta Horticulturae 130, 307-312.
  • Ulubas C & Ertunc F (2004). RT-PCR detection and molecular characterization of Prunus necrotic ringspot virus isolates occurring in Turkey. Journal of Phytopathology 152, 498-502
  • Uyemoto JK, Asai WK & Luhn CF (1992) Ilarviruses: Evidence for rapid spread and effects on vegetative growth and fruit yields of peach trees. Plant Disease 76:71-74.
  • Wells JM, Kirkpatrick HC & Parisch CL (1986) Symptomatology and incidence of Prunus necrotic ringspot virus in peach orchards in Georgia. Plant disease 70, 444-447.
  • Wood GA & Fry PR (1984) Effect of virus infection on growth and cropping of greengage and Billington plum trees. New Zealand Journal of Agricultural Research 27, 563-568.

HOST PLANT N°7: Prunus salicina (PRNSC) 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, including seeds and pollen


3 - Is the pest already listed in a PM4 standard on the concerned host plant?
 
Yes
 
Conclusion:
 
Evaluation continues

 
Justification (if necessary):
 
Listed as 'Prunus necrotic ringspot ilarvirus (PNRSV)' in EPPO Standard PM 4-30 Certification scheme for almond, apricot, peach and plum; with testing recommended. However, in the preliminary excel file submitted by the European Commission, one country commented that the pest 'seems to be quite frequent in nursery and it has a low nuisance level on fruit plants'. As this could affect the RNQP status, a full assessment is performed. In the responses to the questionnaire, PL supported deregulation based on the pathway criteria.
Remark: The assessment performed covers the given host species as well as interspecific hybrids with other Prunus species.

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:
 
Prunus necrotic ringspot virus occurs worldwide and infects many cultivated Prunus species (Hammond, 2011), such as almond - Prunus dulcis (e.g. Mekuria et al., 2003), apricot - Prunus armenica , sweet and sour cherry, P. avium and P. cerasus (e.g. Oliver et al., 2009, Rouag et al., 2009), plum - P. domestica (e.g. Rouag et al., 2009; Jakab-Ilyefalvi et al., 2011), Japanese plum - P. salicina (e.g. Wood & Fry, 1984), and peach (e.g. Topchiiska, 1982; Uyemoto et al., 1992). PNRSV was also found in many wild Prunus spp. like black cherry (Prunus serotina) and cherry laurel (P. caroliniana) and in rose, where it is one of the causes of rose mosaic disease (Horst & Cloyd, 2007). The natural host range also includes herbaceous hosts like hops (symptomless) and cucumber, where chlorotic local lesions, systemic necrosis and severe stunting may occur (Fulton, 1995).
PNRSV is a variable virus consisting of isolates linked to various symptoms in different host species and cultivars (Howell & Mink, 1988; Moury et al., 2001; Oliver et al., 2009; Kamenova & Borisova, 2021; Chirkov et al., 2023).
Infected propagation material is an important pathway (Scott et al., 1989)
Once established PNRSV is easily spread by infected pollen - by wind, bees or thrips - and is also seed transmitted, which can lead to PNRSV-infected seedling rootstocks (e.g. Greber et al., 1991; Kryczynski et al., 1992; Amari et al., 2007; Tayal et al., 2024). Preventing mother stocks to flower prevents infection by pollen.
The Fruit SEWG concluded that plants for planting was a significant pathway.

5 - Economic impact:

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

Justification:
 
General: PNRSV can cause diseases in nurseries which reduced bud take tree growth, tree survival, and uniformity in nursery operations (Saunier, 1972; Topchiiska, 1993 – cited from Hammond, 2011), and death of buds and roots, reduced growth of fruit (10-30%) and fruit yield (20-60%), delay in fruit maturity (Saunier, 1972), diminished fruit quality, and increased susceptibility to winter injury in orchard trees (Nemeth, 1986; Scott et al, 1989; Uyemoto & Scott, 1992). Successful commercial budding can be lower in combinations where scion and rootstock carry the virus (Lang & Howell, 2001). However, PNRSV can also be symptomless in many Prunus spp. (e.g. Spiegel et al., 2004). Many of these symptoms however, were described at a time when it was more difficult to study the whole virome of plant species. New techniques revealed presence of many previously unknown viruses of which their impact on or addition to symptom development is unknown or under investigation (e.g. James et al., 2018; Koloniuk et al., 2018; Hou et al., 2020; Fontdevila Pareta et al., 2023; Khalili et al., 2023).

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?
 
Yes

Conclusion:
 
Candidate

Justification:
 
PNRSV infection can cause symptoms in various Prunus spp. PNRSV symptoms can vary depending on the time passed since the initial infection, species and cultivar, additional virus infection etc. Symptoms can vary between lethal infections (e.g. Lang et al., 1988) to symptomless (e.g. Pérez Sánchez et al., 2017). However, the Fruit SEWG noted that data of economic impact on plum was lacking.
The Fruit SEWG considered that indirect economic impact should be considered: Due to pollen transmissibility, PNRV infected trees pose a serious risk for trees at the same production site. This became e.g. apparent in Austria in a propagation stock intended for the production of certified stone fruit material in the mid-1990s. The explosive spread of PNRV in sweet and sour cherry via pollen from single trees led to the uprooting of the plantation after a few years, despite regular ELISA testing and clearance of positive trees (Riedle-Bauer, unpublished). Sweet cherry and plum can flower at the same time as cherry and cause unacceptable economic impact to this species.

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:
 
Candidate

Justification:
 
Inclusion in a certification scheme.
Propagation material plays relevant role for dissemination.
Serological and molecular detection methods available.

7- Is the quality of the data sufficient to recommend the pest to be listed as a RNQP?
 
Yes
 
Conclusion:
 
Candidate

Justification:
 
Propagation material is a relevant source of infection, the pathogen is widespread, economic damage are reported in many cases.

CONCLUSION ON THE STATUS:
 
Recommended for listing as an RNQP, based on data.


8 - Tolerance level:

Is there a need to change the Tolerance level:
 
No

Proposed Tolerance levels:
 

9 - Risk management measures:

Is there a need to change the Risk management measure:
 
No

Proposed Risk management measure:
 


REFERENCES:
  • Amari K, Burgos L, Pallas V & Sanchez-Pina MA (2007) Prunus necrotic ringspot virus early invasion and its effects on apricot pollen grain performance. Phytopathology 97, 892-899.
  • Bech K (1991) Prunus necrotic ringspot virus (PNRV) in sour cherry Symptoms, incidence in orchards and influence on fruit yield. Tidsskr. Planteavl 95 (1991), 223-232. 223
  • Chirkov S, Sheveleva A, Tsygankova S, Slobodova N, Sharko F, Petrova K & Mitrofanova I (2023) Whole genome characterization of prunus necrotic ringspot virus and prune dwarf virus infecting stone fruits in Russia. Horticulturae 9, 941. https://doi.org/10.3390/horticulturae9080941
  • Çağlayan K, Ulubas Serce C, Gazel M & Varveri C ( 2011) Prune dwarf virus. In In Virus and virus-like diseases of pome and stone fruit s (eds hadidi A, Barba M, Candresse T & Jelkmann W). American Phytopathological Society, St. Paul, Minnesota, USA. 199-205.
  • Greber RS, Klose MJ, Milne JR & Teakle DS (1991) Transmission of prunus necrotic ringspot virus using plum pollen and thrips. Annals of Applied Biology 118, 589-593.
  • Fontdevila Pareta N, Khalili M, Maachi A, Rivarez MPS, Rollin J, Salavert F, Temple C, Aranda MA, Boonham N, Botermans M, Candresse T, Fox A, Hernando Y, Kutnjak D, Marais A, Petter F, Ravnikar M, Selmi I, Tahzima R, Trontin C, Wetzel T & Massart S (2023) Managing the deluge of newly discovered plant viruses and viroids: an optimized scientific and regulatory framework for their characterization and risk analysis. Frontiers in Microbiollogy 14:1181562. doi: 10.3389/fmicb.2023.1181562
  • Fulton RW (1995) Prunus necrotic ringspot virus. In Viruses of Plants (eds Brunt A, Crabtree K, Dallwitz M, Gibbs A & Watson L). CAB International, University Press Cambridge. 1047-1049. (data collected by Fulton in 1985).
  • Hammond RW (2011) Prunus necrotic ringspot virus. In Virus and virus-like diseases of pome and stone fruit s (eds hadidi A, Barba M, Candresse T & Jelkmann W). American Phytopathological Society, St. Paul, Minnesota, USA. 207-213.
  • Horst RK & Cloyd RA (2007) Rose mosaic. In Compendium of rose diseases and pests. American Phytopathological Society, St. Paul, Minnesota, USA. 32-34.
  • Hou W, Li S and Massart S (2020) Is there a “biological desert” with the discovery of new plant viruses? A retrospective analysis for new fruit tree viruses. Frontiers in Microbiology 11:592816. doi: 10.3389/fmicb.2020.592816
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