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NAME OF THE ORGANISM: Coguvirus eburi (Citrus Virus A) {Citrus impietratura agent} (CSI000)

GENERAL INFORMATION ON THE PEST

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

Citrus impietratura agent (Impietratura Cristacortis)

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?:

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?

Yes: Fruits (including hops) sector

If necessary, please list the species:

Coguvirus eburi: Citrus Virus A, CV A

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: A disease of Citrus spp. with gumming of the albedo of fruits was renamed as impietratura by Ruggieri in 1955. Since the disease is graft-transmissible a virus-like aetiology is presumed (Roistacher, 1991). However, no further characteristics on the agent causing the disease was known and therefore, Citrus impietratura agent was an appropriate name.
Pineapple sweet orange and Dweet tangor have been used as indicators for diagnostics and similar leaf symptoms are caused by inoculation with material from trees infected with cristacortis, impietratura, concave gum, or psorosis, which were difficult to separate (in fact, all these diseases were included in the psorosis complex). Nowadays, Citrus psorosis virus has been characterized and specific molecular detection methods are available. In addition, research has been carried out in order to determine the causal agents of Cristacortis and Impietratura. It appeared that these two different diseases are caused by two viruses belonging to the same genus (Coguvirus). In 2018, an Italian research group characterized the Concave gum-associated virus (CCGaV, new ICTV nomenclature: Coguvirus citri) and biologically associated it with Concave gum disease (Navarro et al., 2028a); and Citrus virus A (CV A, new ICTV nomenclature: Coguvirus eburi) but did not associate it with specific symptoms of any disease (Navarro et al., 2018b). In parallel, IVIA also worked to characterize the pathogens associated with concave gum, impietratura and cristacortis. Results indicated that CCGav (Coguvirus citri) is associated with cristacortis, and CV A (Coguvirus eburi) is associated with Impietratura and concave gum (these are two isolates of the same virus that share 97% sequence homology) (Velázquez et al., 2019). In 2021, IVIA set up a field trial to confirm the association of viral sequences with specific symptoms of the 3 diseases, but still wait for the results because symptoms take at least 5 years to appear. Recently, several papers have been published confirming these results and associating the CV A sequence with the symptoms of impietratura and concave gum (Beris et al., 2021; de Bruyn et al., 2022; Park et al.,2022).
In the responses to the questionnaire, CY and FR identified this entry as being of concern. CY supported that citrus virus A should be listed individually.
It is recommended that Coguvirus eburi (CV A - Citrus Virus A) should be listed individually.

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):

Cyprus (1993); Greece (1992); Italy (1993); Italy/Sicilia (1994); Spain (1992)

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/). It has been recorded in many Mediterranean citrus-growing areas (Moreno, 2000a).

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:

Evaluation continues

Justification (if necessary):

Although listed in PM 4/12 Standard, taxonomic entity needed to be verified (research has recently determined its taxonomic entity). A full assessment was performed.

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:

Impietratura is a graft-transmissible disease that affects mainly to fruits of sweet orange and grapefruit (Moreno, 2000a). The virus is transmitted primarily by propagation of infected material. Mechanical and vector transmission have not been demonstrated (Roistacher, 1991). It is apparently not seed -transmissible (Bar-Joseph, 1976). Transmission has been accomplished by placing pollen from infected trees under the bark of indicator plants (Vogel and Bové, 1980).

5 - Economic impact:

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

Yes

Justification:

Affected trees appear normal during most of the year but may show slight wilting, similar to water stress, during the summer. Characteristic symptoms of the disease include fruit drop, a reduction in fruit size, various patterns of skin hardening of fruits, and albedo gumming. Symptoms can vary with season and with different Citrus species and cultivars. The disease can be detected in affected fruits of susceptible varieties when the fruits are at least 1.5-2 cm diameter. A yellow halo surrounding a small, hardened area with brown glands can be seen on infected fruits; these areas can develop into yellow protuberances when the fruits enlarge. Many of the fruit drop in a short time. Affected areas may turn green during ripening. The protuberances can disappear as the fruits approach maturity and the affected areas can remain depressed (Catara et al., 1977).

Impietratura is not destructive, but losses result from off-season fruit drop and the unmarketability of affected fruits of orange and grapefruit. In some cases, as many as 80% of fruits are affected, but the percentage is subject to seasonal variations (CABI, 2019: https://plantwiseplusknowledgebank.org/doi/full/10.1079/pwkb.species.16569)

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?

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:

The impact in Citrus is mainly seen in fruit production reduction and damage to fruits. Although it is not a destructive disease for the plant, it is important to consider the high impact it can have for fruit growers if control measures are not taken on the plant for planting. Because it is a pest that has been controlled for many years through certification schemes, its presence and therefore its impact has been reduced, so there is not much recent data on the economic impact on crops.

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:

Certification programs are a key tool to control the disease. The causal agent of the disease has been identified and molecular techniques for virus detection have been developed.

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

Yes

Conclusion:

Candidate

Justification:

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:

Proposed Tolerance levels:

9 - Risk management measures:

Is there a need to change the Risk management measure:

Proposed Risk management measure:

REFERENCES:

Bar-Joseph M (1976) Some effects of temperature on symptom appearance and therapy of citrus impietratura disease. In Proc. 7th Conf. IOCV. Riverside, IOCV, p 105-108.
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.
Beris D, Ioanna M, Vassilakos N, Theologidis I, Rampou A, Kektsidou O, Massart S, Varveri C (2021) Association of Citrus Virus A to Citrus Impietratura Disease Symptoms. Phytopathology 111(10), 1782–1789.
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 (2019) Citrus impietratura disease (samrah). PlantwisePlus Knowledge Bank. https://plantwiseplusknowledgebank.org/doi/full/10.1079/pwkb.species.16569
Catara A, Bassi M, Perrotta G, Magnano di San Lio G & La Ferlita C (1977) Present status of impietratura disease. In proceedings of the International Society of Citriculture 3, 946-953.
de Bruyn R, Bester R, Cook G, Steyn C, Breytenbach JHJ, Maree HJ (2022) Distribution and Genetic Diversity of Coguvirus eburi in South African Citrus and the Development of a Real-Time RT-PCR Assay for Citrus-Infecting Coguviruses. Plant disease 106(8), 2221–2227.
Minutolo M, Nicoloso V, Cinque M, Chiumenti M, Simeone GDR, Serio FD, Alioto D, Navarro B (2024). A Polyvalent Tool for Detecting Coguviruses in Multiple Hosts Allowed the Identification of a Novel Seed-Transmitted Coguvirus Infecting Brassicaceae. Phytopathology 114(4), 823–831.
Moreno P (2000a) Impietratura. In “Compendium of Citrus Diseases”. APS Press, USA, pp. 65.
Navarro B, Minutolo M, De Stradis A, Palmisano F, Alioto D & Di Serio F (2018a) The first phlebo-like virus infecting plants: a case study on the adaptation of negative-stranded RNA viruses to new hosts. Molecular plant pathology 19(5), 1075–1089.
Navarro B, Zicca S, Minutolo M, Saponari M, Alioto D and Di Serio F (2018b) A Negative-Stranded RNA Virus Infecting Citrus Trees: The Second Member of a New Genus Within the Order Bunyavirales. Front. Microbiol. 9, 2340.
Park JW, da Graça JV, Gonzalez M, Louzada ES, Alabi OJ, Kunta M (2022). First Report of Citrus Virus A in Texas Associated with Oak Leaf Patterns in Citrus sinensis. Plant disease, 106, 2005.
Roistacher CN (1991) Impietratura. In “Graft-transmissible diseases of Citrus: handbook for detection and diagnosis”. FAO, Rome, pp. 133-138.
Ruggieri G (1955) Le arance impietrate. Riv. Agrumic. 1(2), 65-69.
Velázquez K, Hervàs A, Pina JA, Moreno P, Guerri J, Navarro L, Vives MC (2019) Complete sequence of three phlebo-like viruses associated to Cristacortis, Concave gum and Impietratura diseases. XXI IOCV Conference, Riverside, California. Book of abstracts, IOCV-O2-02.
Vogel R, Bové JM (1980) Pollen transmission to citrus of the agent inducing cristacortis and psorosis young leaf symptoms. In Proc. 8th Conf IOCV. Riverside, IOCV, p 188-190.