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Justification for qualification based on EPPO PM 4 Standards
Justification for disqualification
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NAME OF THE ORGANISM: Citrivirus citri (Citrus leaf blotch virus) (CLBV00)

GENERAL INFORMATION ON THE PEST

Name as submitted in the project specification (if different):

Citrus leaf blotch 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):

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?

Presence in the EU:

Yes

List of countries (EPPO Global Database):

Conclusion:

Candidate

Justification (if necessary):

The pest is reported in the EU e.g. Spain (Galipienso et al., 2004) and Italy (Guardo et al., 2007).

HOST PLANT N°1: Citrus (Fortunella) (1FOLG) 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?

Conclusion:

Evaluation continues

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:

Plants for planting is the main pathway. Seed transmission has been reported, although at very low rate (Guerri et al., 2004). Vector transmission has not been demonstrated.

5 - Economic impact:

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

Justification:

There are no data about economic impact. No significant damage has been reported in commercial plantations.

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?

Yes

Is there unacceptable economic impact caused to other hosts (or the same host with a different intended use) produced at the same place of production due to the transfer of the pest from the named host plant for planting?

Conclusion:

Not candidate

Justification:

When CLBV was first characterized, it was associated to bud union crease symptom on Nagami kumquat grafted on citrange rootstocks (Navarro et al.,1984 ) but in 2008, the development of a full-genome cDNA clone of CLBV allowed to demonstrate that this virus only induce minor symptoms (leaf blotching in Dweet tangor and stem pitting in Etrog citron) (Vives et al., 2008). In the original isolate in which CLBV was found, the presence of a new Cytorabdovirus was found and this could be associated with the bud union crease symptom on citrange rootstocks (Vives Garcia MC (IVIA), pers. comm., 2024). In addition, CLBV has also been found affecting Actinidia (Liu et al., 2019; Peng et al., 2020), Malus (Li et al., 2020), Morus alba (Xuan et al., 2020), Nandina domestica (Kamitani et al., 2021), Prunus avium (Wang et al., 2016) and Viburnum lentago (Kim et al., 2023), but there are not a clear association with symptomatology since in most cases CLBV has been found together with other viruses.

CLBV infects all the tested citrus species and varieties, but only causes symptoms in tangor Dweet and citron Etrog (Renovell, 2010). Some isolates also induce transient nerve chlorosis in several species or hybrids of sweet orange, pineapple, Citrus macrophylla or Troyer and Carrizo citranges, and poor union on different varieties propagated on trifoliate rootstocks (Poncirus trifoliata, citranges or citrumelos), both in the greenhouse and in field. However, these latter symptoms have not been shown to be actually caused by CLBV and could have involved a different agent (SEF, 2023). The economic importance of this virus is unknown (Renovell, 2010).

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: economic importance of this virus is unknown.

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:

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.
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.
Galipienso L, Vives MC, Navarro L, Moreno P & Guerri J (2004) Detection of Citrus Leaf Blotch Virus Using Digoxigenin-Labeled cDNA Probes and RT–PCR. European Journal of Plant Pathology 110, 175–181.
Guardo M, Sorrentino G, Marletta T & Caruso A (2007) First Report of Citrus leaf blotch virus on Kumquat in Italy. Plant Disease 91(8),1054.
Guerri J, Pina JA, Vives MC, Navarro L & Moreno P (2004) Seed Transmission of Citrus leaf botch virus: Implications in Quarantine and Certification Programs. Plant Disease 88(8),906.
Kamitani M, Nagano AJ & Okuno T (2021) Characterization of citrus leaf blotch virus from Nandina domestica ‘Otafukunanten’. Journal of General Plant Pathology 87, 113-116.
Kim MH, Byun HS, Kwak HR, Kwon SJ & Seo JK (2023) First report of citrus leaf blotch virus infecting Viburnum lentago in South Korea. Plant Disease 107(8), 2568-2569.
Li HF, Zhao Q, Gray SM & Xu Y (2020) Viral small RNA-based screening of Malus spp. reveals citrus leaf blotch virus infection of Kaido crab apple in China. Plant Disease 104(12), 3272-3272.
Liu H, Song S, Wu W, Mi W, Shen C, Bai B, Wu Y (2019) Distribution and molecular characterization of Citrus leaf blotch virus from Actinidia in Shaanxi province, China. European Journal of Plant Pathology 154, 855-862.
Navarro L, Pina JA, Ballester-Olmos JF, Moreno P & Cambra M (1984) A new graft transmissible disease found in Nagami kumquat. In: Timmer LW, Dodds JA (eds) Proceedings of the 9th Conference of the International Organisation of Citrus Virologists, IOCV, Riverside, pp 234–240.
Peng Q, Qiu L, Yang T & Ning J (2020) A multiple reverse transcription PCR assay for simultaneous detection of four main viruses in kiwifruit. European Journal of Plant Pathology 156(4), 1207–1212.
Renovell A (2010) El virus del manchado foliar de los círicos: caracterización del promotor del RNA subgenómico del gen de la proteína de la cápsida y del supresor del silenciamiento de RNA. PhD. Universidad Politécnica de Valencia.
SEF (2023) Citrus leaf blotch virus (CLBV) Virus del manchado foliar de los cítricos. In “Patógenos de plantas descritos en España”. Sociedad Española de Fitopatología. https://sef.es/patogeno/phytophthora-cinnamomi-rands (accessed: 08/20/2024).
Vives MC, Martín S, Ambrós S, Renovell A, Navarro L, Pina JA, Moreno P & Guerri J (2008) Development of a full-genome cDNA clone of Citrus leaf blotch virus and infection of citrus plants. Mol Plant Pathol. 9(6),787-97.
Wang J, Zhu D, Tan Y, Zong X, Wei H & Liu Q (2016) First report of Citrus leaf blotch virus in sweet cherry. Plant Disease 100(5), 1027.
Xuan Z, Xie J, Yu H, Zhang S, Li R & Cao M (2020) Mulberry (Morus alba) is a new natural host of Citrus leaf blotch virus in China. Plant Disease 105(3), p 716.