| Legend |
|---|
| Justification for qualification based on EPPO PM 4 Standards |
| Justification for disqualification |
| Additional or non-conclusive information |
| Standard text |
NAME OF THE ORGANISM: Fruit disorders: chat fruit, green crinkle, bumpy fruit of Ben Davis, rough skin, star crack, russet ring, russet wart
GENERAL INFORMATION ON THE PEST
Name as submitted in the project specification (if different):
Pest category:
1- Identity of the pest/Level of taxonomic listing:
Is the organism clearly a single taxonomic entity and can it be adequately distinguished from other entities of the same rank?
No
Is the pest defined at the species level or lower?:
No
Can listing of the pest at a taxonomic level higher than species be supported by scientific reasons or can species be identified within the taxonomic rank which are the (main) pests of concern?
- Null: Fruits (including hops) sector
If necessary, please list the species:
-
Is it justified that the pest is listed at a taxonomic rank below species level?
Not relevant
Conclusion:
- Not candidate: Fruits (including hops) sector
Justification (if necessary):
Note on taxonomy:
• 'Apple chat fruit': Adequate molecular tests are not available since aetiology of apple chat fruit agent is still unknown (CABI, 2019). Apple chat fruit disease was first observed in England in apple cv ‘Lord Lambourne’ in 1926. It is a small fruit syndrome, named “chat” apples after chats, the smallest potatoes. Fruits may remain green up until harvest or fail to develop to bright red color. It is graft transmittable, but its causal agent is still unknown (Geensen et al., 2015). It has been described as a disease caused by phytoplasmas (Nemeth, 1986), but no phytoplasmas has been detected (e.g. Geensen et al., 2015).
Apple chat fruit does not fulfill the requirement of identity and should therefore not be listed as an RNQP.
[In responses to the questionnaire, DE highlighted that it is listed on quarantine lists in Argentina, Canada and other countries. DE suggested discussing the recommendation for regulation as an RNQP of 'chat fruit']
• 'Apple green crinkle': In 2020, Li et al. conducted a series of experiments and showed that ‘green crinkle’ was caused by a variant of apple stem pitting virus (ASPV, already listed in Regulation 2019/2072 as RNQP on Malus). It can be noted that James et al. in 2013 had already considered that ‘apple green crinkle associated virus’ (AGCaV) could be a variant or strain of ASPV. Currently, authors use ‘AGCaV’ to describe their findings (e.g. Cho et al., 2016; Morelli et al., 2017; Wright et al., 2020) and APSV as a separate virus. AGCaV is not yet approved by the ICTV (7/May/2024). The Fruit SEWG concluded that there was not enough information yet on identity to recommend it for listing as an RNQP.
• 'Apple bumpy fruit of Ben Davis': The disease was described in Israel (Blodgetts et al., 1965). It was assumed to be related to apple green crinkle virus, but this has not been proven. Because of its sporadic occurrence, it is economically not important (Nemeth, 1986a). Apple bumpy fruit of Ben Davis does not fulfill the requirement of identity and should therefore not be listed as an RNQP.
• 'Apple rough skin' The disease was first described in 1955 in the Netherlands (van Katwijk, 1955). Apple cultivars Belle de Boskoop and Glorie of Holland are susceptible cultivars. Similar disease symptoms were also described in other European countries (Mulder, 1955; Nemeth, 1986b). There are several diseases of apple that express symptoms only on fruit. Some think that many of these may be caused by the same agent that causes apple green crinkle disease. The variations in symptoms are claimed to be due to differences in cultivars, climate and pathogen strain (Howell et al., 2011). Due to these differences it is difficult to ascertain whether they indeed correspond to the same disease or different diseases, cause by one specific virus or a result of a complex of viruses.
Apple rough skin does not fulfill the requirement of identity and should therefore not be listed as an RNQP.
• 'Apple star crack': See 'apple star crack agent'
• 'Apple russet ring': In 2020, Li et al. conducted a series of experiments and showed that ‘russet ring’ was caused by a variant of apple chlorotic leaf spot virus (already listed in Regulation 2019/2072 as RNQP on this host). There are several diseases of apple that express symptoms only on fruit. Some think that many of these may be caused by the same agent. The variations in symptoms are claimed to be due to differences in cultivars, climate and pathogen strain (Howell et al., 2011). Due to these differences it is difficult to ascertain whether they indeed correspond to the same disease or different diseases, cause by one specific virus or a result of a complex of viruses.
Apple russet ring does not fulfill the requirement of identity and should therefore not be listed as an RNQP.
• 'Apple russet wart': An agent that induced raised russetted warts on fruit was identified from a single orchard in the United Kingdom in the 1960s. This agent was found to be graft-transmissible to ‘Cox’s Orange Pippin’, ‘Golden Delicious’ and ‘M2’ rootstocks where it produced similar symptoms, with necrotic russet rings occasionally developing on small immature ‘Cox’s Orange’ fruit, and black necrotic spots on ‘Golden Delicious’. Other symptoms observed were similar to leaf pucker, russet ring and green crinkle diseases, but the necrotic spots on leaves of the three varieties and ‘M.2’ rootstock distinguished it from these syndromes (Posnette & Cropley, 1969). Similar symptoms had been reported across much of Europe (Németh, 1986c), but the current status of the disease is unknown.
[In responses to the questionnaire, LT suggested delisting from EU regulation of all these diseases, and NL and SI suggested considering the listing of the individual viruses identified].
At the time the symptoms were described, tools were not available to identify whether symptoms were associated with a (specific) single virus or a (specific) virus complex. The variations in symptoms were claimed to be due to differences in cultivars, climate and pathogen strain. Currently authors focus more on the HTS outcome (Hou et al., 2020). It is very difficult to make the connection between the symptoms described in the past and the current day findings with HTS.
Many of above symptoms do not fulfill the requirement of identity and should therefore not be a RNQP. If more information becomes available and specific viruses identified, these could then be reconsidered for RNQP listing.
• 'Apple chat fruit': Adequate molecular tests are not available since aetiology of apple chat fruit agent is still unknown (CABI, 2019). Apple chat fruit disease was first observed in England in apple cv ‘Lord Lambourne’ in 1926. It is a small fruit syndrome, named “chat” apples after chats, the smallest potatoes. Fruits may remain green up until harvest or fail to develop to bright red color. It is graft transmittable, but its causal agent is still unknown (Geensen et al., 2015). It has been described as a disease caused by phytoplasmas (Nemeth, 1986), but no phytoplasmas has been detected (e.g. Geensen et al., 2015).
Apple chat fruit does not fulfill the requirement of identity and should therefore not be listed as an RNQP.
[In responses to the questionnaire, DE highlighted that it is listed on quarantine lists in Argentina, Canada and other countries. DE suggested discussing the recommendation for regulation as an RNQP of 'chat fruit']
• 'Apple green crinkle': In 2020, Li et al. conducted a series of experiments and showed that ‘green crinkle’ was caused by a variant of apple stem pitting virus (ASPV, already listed in Regulation 2019/2072 as RNQP on Malus). It can be noted that James et al. in 2013 had already considered that ‘apple green crinkle associated virus’ (AGCaV) could be a variant or strain of ASPV. Currently, authors use ‘AGCaV’ to describe their findings (e.g. Cho et al., 2016; Morelli et al., 2017; Wright et al., 2020) and APSV as a separate virus. AGCaV is not yet approved by the ICTV (7/May/2024). The Fruit SEWG concluded that there was not enough information yet on identity to recommend it for listing as an RNQP.
• 'Apple bumpy fruit of Ben Davis': The disease was described in Israel (Blodgetts et al., 1965). It was assumed to be related to apple green crinkle virus, but this has not been proven. Because of its sporadic occurrence, it is economically not important (Nemeth, 1986a). Apple bumpy fruit of Ben Davis does not fulfill the requirement of identity and should therefore not be listed as an RNQP.
• 'Apple rough skin' The disease was first described in 1955 in the Netherlands (van Katwijk, 1955). Apple cultivars Belle de Boskoop and Glorie of Holland are susceptible cultivars. Similar disease symptoms were also described in other European countries (Mulder, 1955; Nemeth, 1986b). There are several diseases of apple that express symptoms only on fruit. Some think that many of these may be caused by the same agent that causes apple green crinkle disease. The variations in symptoms are claimed to be due to differences in cultivars, climate and pathogen strain (Howell et al., 2011). Due to these differences it is difficult to ascertain whether they indeed correspond to the same disease or different diseases, cause by one specific virus or a result of a complex of viruses.
Apple rough skin does not fulfill the requirement of identity and should therefore not be listed as an RNQP.
• 'Apple star crack': See 'apple star crack agent'
• 'Apple russet ring': In 2020, Li et al. conducted a series of experiments and showed that ‘russet ring’ was caused by a variant of apple chlorotic leaf spot virus (already listed in Regulation 2019/2072 as RNQP on this host). There are several diseases of apple that express symptoms only on fruit. Some think that many of these may be caused by the same agent. The variations in symptoms are claimed to be due to differences in cultivars, climate and pathogen strain (Howell et al., 2011). Due to these differences it is difficult to ascertain whether they indeed correspond to the same disease or different diseases, cause by one specific virus or a result of a complex of viruses.
Apple russet ring does not fulfill the requirement of identity and should therefore not be listed as an RNQP.
• 'Apple russet wart': An agent that induced raised russetted warts on fruit was identified from a single orchard in the United Kingdom in the 1960s. This agent was found to be graft-transmissible to ‘Cox’s Orange Pippin’, ‘Golden Delicious’ and ‘M2’ rootstocks where it produced similar symptoms, with necrotic russet rings occasionally developing on small immature ‘Cox’s Orange’ fruit, and black necrotic spots on ‘Golden Delicious’. Other symptoms observed were similar to leaf pucker, russet ring and green crinkle diseases, but the necrotic spots on leaves of the three varieties and ‘M.2’ rootstock distinguished it from these syndromes (Posnette & Cropley, 1969). Similar symptoms had been reported across much of Europe (Németh, 1986c), but the current status of the disease is unknown.
[In responses to the questionnaire, LT suggested delisting from EU regulation of all these diseases, and NL and SI suggested considering the listing of the individual viruses identified].
At the time the symptoms were described, tools were not available to identify whether symptoms were associated with a (specific) single virus or a (specific) virus complex. The variations in symptoms were claimed to be due to differences in cultivars, climate and pathogen strain. Currently authors focus more on the HTS outcome (Hou et al., 2020). It is very difficult to make the connection between the symptoms described in the past and the current day findings with HTS.
Many of above symptoms do not fulfill the requirement of identity and should therefore not be a RNQP. If more information becomes available and specific viruses identified, these could then be reconsidered for RNQP listing.
2 – Status in the EU:
Is this pest already a quarantine pest for the whole EU?
No
Presence in the EU:
List of countries (EPPO Global Database):
-
Conclusion:
Justification (if necessary):
HOST PLANT N°1: Malus (1MABG) for the Fruits (including hops) sector.
Origin of the listing:
Commission Implementing Directive (EU) 2014/98/EU and Commission Implementing Regulation (EU) 2019/2072
Plants for planting:
Plants intended for planting
3 - Is the pest already listed in a PM4 standard on the concerned host plant?
Yes
Conclusion:
Justification (if necessary):
Testing for 'Fruit disorders: chat fruit, green crinkle, bumpy fruit of Ben Davis, rough skin, star crack, russet ring, russet wart' recommended in EPPO Standard PM 4-27 Pathogen-tested material of Malus, Pyrus and Cydonia, for Pyrus and Cydonia. However, since these pests are not listed at species level (fruit disorders), it was suggested to perform a review of the knowledge available on these disorders.
In responses to the questionnaire, DE questioned the economic impact of 'chat fruit', which is listed as a
In responses to the questionnaire, DE questioned the economic impact of 'chat fruit', which is listed as a
4 - Are the listed plants for planting the main* pathway for the "pest/host/intended use" combination? (*: significant compared to others):
Conclusion:
Justification:
5 - Economic impact:
Are there documented reports of any economic impact on the host?
Justification:
What is the likely economic impact of the pest irrespective of its infestation source in the absence of phytosanitary measures? (= official measures)
Is the economic impact due to the presence of the pest on the named host plant for planting, acceptable to the propagation and end user sectors concerned?
Is there unacceptable economic impact caused to other hosts (or the same host with a different intended use) produced at the same place of production due to the transfer of the pest from the named host plant for planting?
Conclusion:
Justification:
6 - Are there feasible and effective measures available to prevent the presence of the pest on the plants for planting at an incidence above a certain threshold (including zero) to avoid an unacceptable economic impact as regards the relevant host plants?
Conclusion:
Justification:
7- Is the quality of the data sufficient to recommend the pest to be listed as a RNQP?
Conclusion:
Justification:
CONCLUSION ON THE STATUS:
Disqualified: no clear taxonomy or phantom agents
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:
- Behl MK, Parakh DB & Khurana SMP (1998) Bumpy fruit and other viroid and viroid-like diseases of apple in HP, India. Acta Horticulturae 472, 627-630.
- Blodgett EC, Fleisher Z & Pappo Sh (1965) A survey on virus diseases of deciduous fruit trees in Israel. Zašt. Bilja 16, 503-508.
- CABI (Centre for Agricultural Bioscience International) (2019) Online. Datasheets Apple chat fruit disease (apple chat fruit). CABI compendium. CABI, Wallingford, UK. Available from https://www.cabidigitallibrary.org/doi/full/10.1079/cabicompendium.6076;
- Cho IS, Igori D, Lim S, Choi GS, Hammond J, Lim HS & Moon JS (2016) Deep sequencing analysis of apple infecting viruses in Korea. The plant pathology journal 32(5), 441.
- 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 Microbiology 14, 1181562.
- Geensen B, Maas FM, Meekes ETM, Konings JAM & Jongedijk GP (2015) Effect of apple chat fruit infection on fruit size and yield of cultivars Elstar and Jonagold [abstract]. 23rd International conference on virus and other graft-transmissible diseases of fruit crops, 7-12 June, 2015, Marioka, Japan.
- James D, Varga A, Jesperson GD, Navratil M, Safarova D, Constable F, Horner M, Eastwell K & Jelkmann W (2013) Identification and complete genome analysis of a virus variant or putative new foveavirus associated with apple green crinkle disease. Archives of Virology, 158, 1877-1887.
- Hou W, Li S & Massart S (2020) Is there a “Biological Desert” with the discovery of new plant viruses? A retrospective analysis for new fruit tree viruses. Frontiers of Microbiology 11, 2953. doi: 10.3389/fmicb.2020.592816
- Howell WE, Thompson D & Scott S (2011) Virus-like disorders of fruit trees with undetermined etiology. ). In Virus and Virus-Like Diseases of Pome and Stone Fruits (eds Hadidi A, Barba M, Candresse T & Jelkmann W). American Phytopathological Society, St Paul, MN, USA. pop 259-265.
- Li C, Yaegashi H, Kishigami R, Kawakubo A, Yamagishi N, Ito T.& Yoshikawa N (2020) Apple russet ring and apple green crinkle diseases: Fulfillment of Koch’s postulates by virome analysis, amplification of full-length cDNA of viral genomes, in vitro transcription of infectious viral RNAs, and reproduction of symptoms on fruits of apple trees inoculated with viral RNAs. Frontiers in Microbiology 11, 1627.
- Morelli M, Giampetruzzi A, Laghezza L, Catalano L, Savino VN & Saldarelli P (2017) Identification and characterization of an isolate of apple green crinkle associated virus involved in a severe disease of quince (Cydonia oblonga, Mill.). Archives of Virology 162(1), 299-306.
- Mulder D (1955) Ruwschillige vruchten en een bladsymptoom bij appel [Rough skin disease of the apple and a leaf symptom]. Tijdschrift over Plantenziekten (European Journal of Plant Pathology) 61(1), 11-14.
- Nemeth M (1986a) Apple bumpy fruit of Ben Davis. In Virus, Mycoplasma and Rickettsia Diseases (ed Nemeth M). Martinus Nijhoff Publishers, Dordrecht, The Netherlands, pp 154-155.
- Nemeth M (1986b) Apple rough skin. In Virus, Mycoplasma and Rickettsia Diseases (ed Nemeth M). Martinus Nijhoff Publishers, Dordrecht, The Netherlands, pp 180-181.
- Nemeth M (1986b) Apple russet wart. In Virus, Mycoplasma and Rickettsia Diseases (ed Nemeth M). Martinus Nijhoff Publishers, Dordrecht, The Netherlands, pp 184-186.
- Posnette AF & Cropley R (1969) Apple russet wart. Technical Communication - Commonwealth Bureau of Horticulture and Plantation Crops. 30 Suppl. No 3, 44a-44d.
- Van Katwijk W (1955) Ruwschilligheid bij appels, een virusziekte [Rough skin of apples]. Tijdschrift over Plantenziekten (European Journal of Plant Pathology) 61(1), 4-6.
- Wright AA, Cross AR & Harper SJ (2020) A bushel of viruses: Identification of seventeen novel putative viruses by RNA-seq in six apple trees. PLoS One 15(1), e0227669.