| Legend |
|---|
| Justification for qualification based on EPPO PM 4 Standards |
| Justification for disqualification |
| Additional or non-conclusive information |
| Standard text |
NAME OF THE ORGANISM: Nepovirus avii (cherry leaf roll virus) (CLRV00)
GENERAL INFORMATION ON THE PEST
Name as submitted in the project specification (if different):
Cherry leaf roll 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):
Cherry leaf roll virus (CLRV) is a well characterized virus. It is a member of the subgroup C of the genus Nepovirus in the family Secoviridae. Complete genome sequences are available for the two genomic RNAs of CLRV. This virus can be detected by biological indexing. However, serological or molecular detection assays are preferred (EFSA PLH, 2014).
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 (1996); Croatia (2011); Czech Republic (2020); Finland (2011); France (2016); France/Corse (2016); Germany (1997); Greece (2020); Greece/Kriti (2020); Hungary (1996); Italy (2020); Netherlands (2022); Poland (2013); Portugal (1997); Romania (1986); Slovakia (2002); Spain (2011)
Conclusion:
candidate
Justification (if necessary):
CLRV is widely distributed in the EPPO region. Data of the presence of this pest on the EU territory are available in EPPO Global Database (https://gd.eppo.int/). CLRV was recorded on grapevine in Germany (Ipach et al., 2003) and Poland (Komorowska et al., 2012). It has been reported in olive trees from Croatia, Italy, Lebanon, Portugal, Spain and Turkey (Albanese et al., 2012). No systematic surveys of CLRV were performed in the EU on many of its natural woody hosts, including Actinidia spp, therefore its presence on these hosts is probably underestimated.
(Remark: In the EPPO region, CLRV is a quarantine pest for some countries e.g. Jordan, Morocco, Norway, Tunisia and Turkey. The virus had been recommended for regulation as a quarantine pest by EPPO from 1981 to 2004, see https://gd.eppo.int/taxon/CLRV00/categorization).
Detailed information
- on olive
A total of 245 olive trees representing 15 different cultivars from the FAO collection at the Centro de Investigación y Formación Agraria (CIFA), Córdoba (Spain), and other selections from different Spanish areas were tested, among other pathogens , for CLRV. One sample was found to be infected (Bertolini et al. 2006).
In an Italian study, 345 samples collected from olive fields in Italian areas in which national and local olive tree cultivars and selections are grown were tested for common viruses. The CLRV infection rate was 4.9% (Faggioli et al. 2005).
A survey on viruses infecting olive trees in Croatian Istria included a total of 62 olive trees from 15 varieties. The most frequent virus was CLRV, detected in 11.3% of tested trees both in autochthonous and in introduced varieties. Infected plants showed disease symptoms including yellowing of leaves and uneven fruit ripening (Godena et al. 2016).
(Remark: In the EPPO region, CLRV is a quarantine pest for some countries e.g. Jordan, Morocco, Norway, Tunisia and Turkey. The virus had been recommended for regulation as a quarantine pest by EPPO from 1981 to 2004, see https://gd.eppo.int/taxon/CLRV00/categorization).
Detailed information
- on olive
A total of 245 olive trees representing 15 different cultivars from the FAO collection at the Centro de Investigación y Formación Agraria (CIFA), Córdoba (Spain), and other selections from different Spanish areas were tested, among other pathogens , for CLRV. One sample was found to be infected (Bertolini et al. 2006).
In an Italian study, 345 samples collected from olive fields in Italian areas in which national and local olive tree cultivars and selections are grown were tested for common viruses. The CLRV infection rate was 4.9% (Faggioli et al. 2005).
A survey on viruses infecting olive trees in Croatian Istria included a total of 62 olive trees from 15 varieties. The most frequent virus was CLRV, detected in 11.3% of tested trees both in autochthonous and in introduced varieties. Infected plants showed disease symptoms including yellowing of leaves and uneven fruit ripening (Godena et al. 2016).
HOST PLANT N°1: Olea europaea (OLVEU) 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
3 - Is the pest already listed in a PM4 standard on the concerned host plant?
Yes
Conclusion:
Evaluation continues
Justification (if necessary):
EPPO Standard PM 4/17 Certification scheme for olive trees and rootstock recommends testing for Cherry leaf roll virus (CLRV). Full assessment of the RNQP status of CLRV was performed in 2021/2022 in the context of the revision of EPPO Standard PM 4/17. The RNQP status was considered justified by olive certification experts to prevent impact on olive yield and oil quality (to be confirmed), as well as infection of other hosts produced at the same place of production.
Although PL considered in responses to the questionnaire that plants for planting was not the main pathway, this was not supported by enough justification.
Evaluation continues because the Fruit SEWG of the RNQP Project part 2 decided to revise the assessment of the RNQP status, in particular in relation to the economic impact.
Although PL considered in responses to the questionnaire that plants for planting was not the main pathway, this was not supported by enough justification.
Evaluation continues because the Fruit SEWG of the RNQP Project part 2 decided to revise the assessment of the RNQP status, in particular in relation to the economic impact.
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:
CLRV has a wide natural host range, which includes a number of woody or herbaceous hosts (e.g. plants of genera: Betula, Celtis, Cornus, Fagus, Juglans, Ligustrum, Olea, Populus, Ulmus, Rubus, Sambucus and Rheum. Its experimental host range includes plants from more than 36 families (Albanese et al., 2012; EFSA PLH, 2014)).
CLRV is transmitted through the vegetative multiplication of infected host plants. In addition, CLRV is seed- and pollen-transmitted at variable rates in many of its natural hosts. In at least some natural hosts, pollen transmission is both vertical (resulting in infected seeds and, upon germination, seedlings) and horizontal (resulting in infection of the pollinated mother plant) (EFSA PLH, 2014). In olive plants, its transmission by means of pollen has not been demonstrated, but has been ascertained by seeds at the rate of 41% (Albanese et al., 2012). However, a population genetics study of CLRV isolates has shown that transfer between different host species is likely to be rare, possibly as a consequence of the need for pollen germination and ovule fertilisation for transmission. As a consequence, the fact that CLRV may have high prevalence in some hosts in a given region does not necessarily imply that all potential host plants (e.g. olive plants) are at a high risk of infection in this region (EFSA PLH, 2014).
CLRV can be transmitted by mechanical inoculation in experimental hosts (EFSA PLH, 2014).
Despite early reports suggesting that CLRV, like other nepoviruses, might be transmitted by soil-inhabiting nematodes, more recent studies have ruled out this possibility (EFSA PLH, 2014).
Plants for planting is considered to be the main pathway in olive plants for planting.
CLRV is transmitted through the vegetative multiplication of infected host plants. In addition, CLRV is seed- and pollen-transmitted at variable rates in many of its natural hosts. In at least some natural hosts, pollen transmission is both vertical (resulting in infected seeds and, upon germination, seedlings) and horizontal (resulting in infection of the pollinated mother plant) (EFSA PLH, 2014). In olive plants, its transmission by means of pollen has not been demonstrated, but has been ascertained by seeds at the rate of 41% (Albanese et al., 2012). However, a population genetics study of CLRV isolates has shown that transfer between different host species is likely to be rare, possibly as a consequence of the need for pollen germination and ovule fertilisation for transmission. As a consequence, the fact that CLRV may have high prevalence in some hosts in a given region does not necessarily imply that all potential host plants (e.g. olive plants) are at a high risk of infection in this region (EFSA PLH, 2014).
CLRV can be transmitted by mechanical inoculation in experimental hosts (EFSA PLH, 2014).
Despite early reports suggesting that CLRV, like other nepoviruses, might be transmitted by soil-inhabiting nematodes, more recent studies have ruled out this possibility (EFSA PLH, 2014).
Plants for planting is considered to be the main pathway in olive plants for planting.
5 - Economic impact:
Are there documented reports of any economic impact on the host?
Yes
Justification:
Infection with CLRV is generally asymptomatic in olive (Albanese et al., 2012; EFSA PLH, 2014) or may show yellowing of leaves and uneven fruit ripening (Godena et al., 2016).
However, it has been shown that infected olives had lower oil yield and maturity index. Oils from infected fruits had significant lower value of K232 and K270 and very elevated total phenols content. The quality of the virgin olive oils obtained from the infected Frantoio fruits resulted depauperated in terms of richness in o-diphenols (especially in the 2nd harvest). The decrease in the oleic/linoleic ratio and the lower level of o-diphenols also suggest a possible lowering of the oxidative stability during the oil storage (Godena et al., 2012).
The Fruit SEWG highlighted that this study only shows possible impact on one variety over two, over two years. The virus is asymptomatic.
However, it has been shown that infected olives had lower oil yield and maturity index. Oils from infected fruits had significant lower value of K232 and K270 and very elevated total phenols content. The quality of the virgin olive oils obtained from the infected Frantoio fruits resulted depauperated in terms of richness in o-diphenols (especially in the 2nd harvest). The decrease in the oleic/linoleic ratio and the lower level of o-diphenols also suggest a possible lowering of the oxidative stability during the oil storage (Godena et al., 2012).
The Fruit SEWG highlighted that this study only shows possible impact on one variety over two, over two years. The virus is asymptomatic.
What is the likely economic impact of the pest irrespective of its infestation source in the absence of phytosanitary measures? (= official measures)
Minor to 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?
Yes? (to be further studied)
Is there unacceptable economic impact caused to other hosts (or the same host with a different intended use) produced at the same place of production due to the transfer of the pest from the named host plant for planting?
No
Conclusion:
Not candidate
Justification:
There are data available pointing out that CLRV may have an impact on olive yield and oil quality (Godena et al., 2012). The expert working group for the revision of EPPO Standard PM 4/17 considered that additional studies would be needed to confirm the results from this study on a larger scale as well as in other olive varieties. The Fruit SEWG of the RNQP Project part 2 highlighted that the pest is asymptomatic in olive. Possible economic impact would need to be further studied.
Economic impact on other hosts: CLRV causes foliar symptoms generally in the form of chlorotic mosaic, chlorotic or yellow ring patterns or ringspots, yellow vein netting and yellow spotting in many of its hosts. Albanese et al. (2012) also refers to delayed leaf development, dieback of branches or whole trees for some of the hosts.
As examples, CLRV can cause decline in American elm; tree decline or death in cherry, in particular in situations of co-infection with Prunus necrotic ringspot virus and Prune dwarf virus; decline and death of European walnut (Juglans regia) scions grafted onto Northern California black walnut (J. hindsii), ‘Paradox’ hybrids (J. hindsii × J. regia), Chinese wingnut (Pterocarya stenoptera) or other sensitive Juglans spp. rootstocks, in what is known as the ‘black line’ or ‘brown line’ disease. Although CLRV remains symptomless or causes only foliar symptoms in many cultivars of J. regia, it causes tissue necrosis (resulting in a black or brown line of necrotic tissues) at the scion/rootstock junction of susceptible graft combinations, eventually girdling and killing the tree. This problem can be avoided by using non-susceptible rootstocks, such as J. regia, but these may be of lower agricultural interest. In its regulated Rubus spp. hosts, CLRV also causes severe disease symptoms in at least some circumstances. The reported symptoms include leaf patterning and plant death in blackberry and leaf size reduction, deformation and chlorotic mottling or ringspotting and stunting of fruiting canes in raspberry. Affected plants produce less fruit. However, the precise contribution of CLRV to these severe symptoms remains to be precisely established. It is possible that these symptoms were caused by CLRV alone or in combination with co-infecting viruses, resulting in synergistic effects and increased symptomatology. It is also possible that these symptoms were caused by an unrelated agent, which was not identified during these early efforts. Overall, although there are elements to suggest that CLRV can cause severe symptoms in its regulated Rubus spp. hosts, this conclusion is affected by strong uncertainties (EFSA PHL, 2014).
The expert working group for the revision of EPPO Standard PM 4/17 considered that other crops (e.g. Juglans, Rubus) could be impacted because of host plants for planting produced at the same place of production than olive (as is the case in Italian nurseries) and infected there by mechanical infection. The Fruit SEWG of the RNQP Project part 2 recommended not to consider indirect economic impact since interspecies infection is reported not to occur. Mechanical infection between different species is improbable since disinfection would prevent indirect economic impact.
The expert working group for the revision of EPPO Standard PM 4/17 considered that controlling CLRV in olive plant production could help preventing impact on olive yield and oil quality (to be confirmed). The Fruit SEWG of the RNQP Project part 2 considered that the only study available was not enough to justify a listing as an RNQP. Also, despite being two well-known traditional varieties of olive, these two varieties are not so used for the olive production in terms of quantity at global level.
Economic impact on other hosts: CLRV causes foliar symptoms generally in the form of chlorotic mosaic, chlorotic or yellow ring patterns or ringspots, yellow vein netting and yellow spotting in many of its hosts. Albanese et al. (2012) also refers to delayed leaf development, dieback of branches or whole trees for some of the hosts.
As examples, CLRV can cause decline in American elm; tree decline or death in cherry, in particular in situations of co-infection with Prunus necrotic ringspot virus and Prune dwarf virus; decline and death of European walnut (Juglans regia) scions grafted onto Northern California black walnut (J. hindsii), ‘Paradox’ hybrids (J. hindsii × J. regia), Chinese wingnut (Pterocarya stenoptera) or other sensitive Juglans spp. rootstocks, in what is known as the ‘black line’ or ‘brown line’ disease. Although CLRV remains symptomless or causes only foliar symptoms in many cultivars of J. regia, it causes tissue necrosis (resulting in a black or brown line of necrotic tissues) at the scion/rootstock junction of susceptible graft combinations, eventually girdling and killing the tree. This problem can be avoided by using non-susceptible rootstocks, such as J. regia, but these may be of lower agricultural interest. In its regulated Rubus spp. hosts, CLRV also causes severe disease symptoms in at least some circumstances. The reported symptoms include leaf patterning and plant death in blackberry and leaf size reduction, deformation and chlorotic mottling or ringspotting and stunting of fruiting canes in raspberry. Affected plants produce less fruit. However, the precise contribution of CLRV to these severe symptoms remains to be precisely established. It is possible that these symptoms were caused by CLRV alone or in combination with co-infecting viruses, resulting in synergistic effects and increased symptomatology. It is also possible that these symptoms were caused by an unrelated agent, which was not identified during these early efforts. Overall, although there are elements to suggest that CLRV can cause severe symptoms in its regulated Rubus spp. hosts, this conclusion is affected by strong uncertainties (EFSA PHL, 2014).
The expert working group for the revision of EPPO Standard PM 4/17 considered that other crops (e.g. Juglans, Rubus) could be impacted because of host plants for planting produced at the same place of production than olive (as is the case in Italian nurseries) and infected there by mechanical infection. The Fruit SEWG of the RNQP Project part 2 recommended not to consider indirect economic impact since interspecies infection is reported not to occur. Mechanical infection between different species is improbable since disinfection would prevent indirect economic impact.
The expert working group for the revision of EPPO Standard PM 4/17 considered that controlling CLRV in olive plant production could help preventing impact on olive yield and oil quality (to be confirmed). The Fruit SEWG of the RNQP Project part 2 considered that the only study available was not enough to justify a listing as an RNQP. Also, despite being two well-known traditional varieties of olive, these two varieties are not so used for the olive production in terms of quantity at global level.
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:
Justification:
Inclusion in a certification scheme: Experts considered that testing only when producing the nuclear stock was sufficient (regular testing for the maintenance of the nuclear stock was not considered necessary).
Thermotherapy has also been shown to be at least partially effective for the elimination of CLRV and to allow the production of healthy plants from contaminated stocks (EFSA PLH, 2014).
Thermotherapy has also been shown to be at least partially effective for the elimination of CLRV and to allow the production of healthy plants from contaminated stocks (EFSA PLH, 2014).
7- Is the quality of the data sufficient to recommend the pest to be listed as a RNQP?
No
Conclusion:
Justification:
There are uncertainties about the efficiency of pollen-transmission of CLRV in many of its hosts. There are also important uncertainties about the impact of CLRV in olive varieties as well as for many other hosts.
CONCLUSION ON THE STATUS:
Disqualified: asymptomatic in olive. Potential economic impact on olive oil needs to be further studied.
8 - Tolerance level:
Is there a need to change the Tolerance level:
Yes
Proposed Tolerance levels:
Delisting
9 - Risk management measures:
Is there a need to change the Risk management measure:
Yes
Proposed Risk management measure:
Delisting
REFERENCES:
- Albanese G, Saponari M & Faggioli F (2012) Olive Germplasm – The Olive Cultivation, Table Olive and Olive Oil Industry in Italy. Chapter 6. Phytosanitary certification. Available at http://dx.doi.org/10.5772/51722
- Bertolini E, Olmos A, López MM, Cambra M (2003) Multiplex Nested Reverse Transcription-Polymerase Chain Reaction in a Single Tube for Sensitive and Simultaneous Detection of Four RNA Viruses and Pseudomonas savastanoi pv. savastanoi in Olive Trees. Phytopathology 93(3):286-92. doi: 10.1094/PHYTO.2003.93.3.286. PMID: 18944338.
- EFSA PLH (2014) EFSA Panel on Plant Health (PLH). Scientific opinion on the risk to plant health posed by Cherry leafroll virus. EFSA Journal 2014;12(10):3848, 23 pp. doi:10.2903/j.efsa.2014.384
- Faggioli F, Feretti L, Albanese G, Sciarrino R, Pasquini G, Lumia V & Barba M (2005) Distribution of olive tree viruses in Italy as revealed by one-step-PCR. J. Plant Pathol. 87 (1), 49–55.
- Godena S, Bendini A, Giambanelli E, Cerretani L, Ðermic D & Dermic E (2012) Cherry leafroll virus: Impact on olive fruit and virgin olive oil quality, European Journal of Lipid Science and Technology 114, 535–541.
- Godena S, Faggioli F, Luigi M, Saponari M, Loconsole G, Voncina D & Đermic E (2016) Incidence of viruses on autochtonous and introduced olive varieties in Croatian Istria detected by three diagnostic techniques. Journal of Plant Pathology 98 (3), 657-660