| Legend |
|---|
| Justification for qualification based on EPPO PM 4 Standards |
| Justification for disqualification |
| Additional or non-conclusive information |
| Standard text |
NAME OF THE ORGANISM: Hostuviroid impedihumuli (hop stunt viroid) (HSVD00)
GENERAL INFORMATION ON THE PEST
Name as submitted in the project specification (if different):
Hop stunt viroid
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):
Note on taxonomy: Semancik et al. (1988) reported that citrus cachexia disease was caused by a viroid. Subsequently, Diener et al. (1988) and Reanwarakorn & Semancik (1998) showed that this citrus viroid should be identified as a strain of hop stunt viroid. In 1999, Reanwarakorn and Semancik reported the correlation of Hop stunt viroid variants to cachexia and xyloporosis disease of citrus. HSVd has been detected in hop in Slovenia, not from imported material but from transmission from infected citrus fruit used as waste in hop fields (Sano, 2021).
The term cachexia variant should not be used because:
- Although only cachexia variants induce symptoms in Citrus (incl. Fortunella & Poncirus), not all laboratories can determine the variant. In addition to a PCR, it is necessary to sequence the variant or perform a quantitative PCR followed by high resolution melting analysis (Loconsole et al., 2013). Remark: populations of different isolates behave as 'quasispecies', RNA polymerase has a high error rate and there is evidence that a single nucleotide change can modulate symptoms (Serra et al., 2008).
- Other isolates from other plants that can also be infected with HSVd, such grapevines, stone fruit trees, etc., can also be transmitted to hop. The host spectrum of HSVd is very broad and isolates that are asymptomatic in one host can infect and be symptomatic in another one (Sano and Kashiwagi 2022, Marquez-Molins et al., 2021, Zhang et al., 2020).
During the RNQP Project part 1, experts considered that if measures are based on symptoms, listing the Hop stunt viroid would be sufficient.
Remarks:
- Fortunella is considered to be a synonym of Citrus by some authors. Using SSRs markers, Fortunella clusters within the genus Citrus (Barkley et al., 2006). These should be considered the same genus.
- Poncirus is considered to be a synonym of Citrus by some authors, and is categorized as such in EPPO GD. However, when using SSRs markers, Poncirus is a sister genus to Citrus (Barkley et al., 2006). In addition, one chromosomal marker can be used to distinguish Poncirus from Citrus species (Brasileiro Vidal et al., 2007). Whether to consider these as synonym or not is still a matter of debate.
The term cachexia variant should not be used because:
- Although only cachexia variants induce symptoms in Citrus (incl. Fortunella & Poncirus), not all laboratories can determine the variant. In addition to a PCR, it is necessary to sequence the variant or perform a quantitative PCR followed by high resolution melting analysis (Loconsole et al., 2013). Remark: populations of different isolates behave as 'quasispecies', RNA polymerase has a high error rate and there is evidence that a single nucleotide change can modulate symptoms (Serra et al., 2008).
- Other isolates from other plants that can also be infected with HSVd, such grapevines, stone fruit trees, etc., can also be transmitted to hop. The host spectrum of HSVd is very broad and isolates that are asymptomatic in one host can infect and be symptomatic in another one (Sano and Kashiwagi 2022, Marquez-Molins et al., 2021, Zhang et al., 2020).
During the RNQP Project part 1, experts considered that if measures are based on symptoms, listing the Hop stunt viroid would be sufficient.
Remarks:
- Fortunella is considered to be a synonym of Citrus by some authors. Using SSRs markers, Fortunella clusters within the genus Citrus (Barkley et al., 2006). These should be considered the same genus.
- Poncirus is considered to be a synonym of Citrus by some authors, and is categorized as such in EPPO GD. However, when using SSRs markers, Poncirus is a sister genus to Citrus (Barkley et al., 2006). In addition, one chromosomal marker can be used to distinguish Poncirus from Citrus species (Brasileiro Vidal et al., 2007). Whether to consider these as synonym or not is still a matter of debate.
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):
Croatia (2018); Cyprus (1972); Czech Republic (2009); France (1972); France/Corse (1994); Germany (2022); Greece (2020); Greece/Kriti (2020); Hungary (2018); Italy (2013); Italy/Sardegna (1972); Portugal (2022); Slovenia (2015); Spain (2016)
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/). HSVd has been reported in most Mediterranean countries and is among the most prevanent citrus viroids in the region (Kaponi et al., 2024). However, HSVd is generally considered absent from hop growing regions (e.g. CZ, DE and PL).
HOST PLANT N°1: Citrus (1CIDG) 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:
Qualified
Justification (if necessary):
Listed in Standard PM 4/12 on Citrus as 'Citrus cachexia-xyloporosis viroid'. The name in the Standard PM 4/12 list should be revised and changed to HSVd.
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?
Yes
Justification:
Affected trees show an estimated yield reduction between 20 and 76% (Belabess et al., 2021, CABI: https://plantwiseplusknowledgebank.org/doi/10.1079/pwkb.species.27694).
What is the likely economic impact of the pest irrespective of its infestation source in the absence of phytosanitary measures? (= official measures)
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:
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:
Recommended for listing as an RNQP, based on EPPO PM4 Standards.
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:
- Barkley NA, Roose ML, Krueger RR, Federici CT (2006) Assessing genetic diversity and population structure in a citrus germplasm collection utilizing simple sequence repeat markers (SSRs). Theor Apple Genet. 112(8), 1519-31.
- Belabess Z, Radouane N, Sagouti T, Tahiri A, Lahlali R. (2021). A Current Overview of Two Viroids Prevailing in Citrus Orchards: Citrus Exocortis Viroid and Hop Stunt Viroid. IntechOpen.
- Brasileiro-Vidal AC, Dos Santos-Serejo JA, Soares Filho Wdos S, Guerra M. (2007) A simple chromosomal marker can reliably distinguishes Poncirus from Citrus species. Genética 129(3), 273-9.
- CABI: Hop stunt viroid https://plantwiseplusknowledgebank.org/doi/10.1079/pwkb.species.27694
- Davis T J, Gómez M I, Harper S J, Twomey M (2021) The Economic Impact of Hop Stunt Viroid and Certified Clean Planting Materials. HortScience, 56(12), 1471-1475.
- DEFRA (2013) Rapid pest risk analysis for Hop stunt viroid. Available from https://pra.eppo.int/pra/8f3eb6fc-06d3-412a-8306-c679d641da95
- Diener TO, Smith DR, Hammond RH, Albanese G, Rosa R & la Davino M (1988) Citrus B viroid identification as a strain of hop stunt viroid. Plant Disease 72(8), 691-693.
- Federici CT (2006) Assessing genetic diversity and population structure in a citrus germplasm collection utilizing simple sequence repeat markers (SSRs). Theor Apple Genet. 112(8), 1519-31.
- Kaponi M, Kyriakopoulou PE, Hadidi A (2024) Viroids of the Mediterranean Basin. Viruses 16(4), 612.
- Loconsole G, Onelge N, Yokomi RK, Kubaa RA, Savino V, Saponari M (2013) Rapid differentiation of citrus Hop stunt viroid variants by real-time RT-PCR and high resolution melting analysis. Mol Cell Probes 27(5-6), 221-9.
- Marquez-Molins J, Gomez G, Pallas V (2021) Hop stunt viroid: A polyphagous pathogenic RNA that has shed light on viroid-host interactions. Mol Plant Pathol 22(2), 153-162.
- Reanwarakorn K & Semancik JS (1998) Regulation of pathogenicity in hop stunt viroid-related group II citrus viroids. Journal of General Virology 79(12), 3163-3171.
- Reanwarakorn K & Semancik JS (1999) Correlation of Hop stunt viroid variants to cachexia and xyloporosis diseases of citrus. Phytopathology 89(7), 568-574.
- Sano T (2021) Progress in 50 years of viroid research-Molecular structure, pathogenicity, and host adaptation. Proc Jpn Acad Ser B Phys Biol Sci 97(7), 371-401.
- Sano T, Kashiwagi A (2022) Host selection-producing variations in the genome of hop stunt viroid. Virus Res 2;311,198706.
- Semancik JS, Roistacher CN, Rivera-Bustamante R & Duran-Vila N (1988) Citrus cachexia viroid, a new viroid of citrus: relationship to viroids of the exocortis disease complex. Journal of General Virology 69(12), 3059-3068.
- Serra P, Gago S, Duran-Vila N (2008) A single nucleotide change in Hop stunt viroid modulates citrus cachexia symptoms. Virus Res 138(1-2), 130-4.
- Zhang Z, Xia C, Matsuda T, Taneda A, Murosaki F, Hou W, Owens RA, Li S, Sano T (2020) Effects of Host-Adaptive Mutations on Hop Stunt Viroid Pathogenicity and Small RNA Biogenesis. Int J Mol Sci 6;21(19), 7383.