Citrus Viroid V

California Pest Rating  for
Citrus viroid V
Pest Rating: B


Initiating Event:  

The risk of infestation of Citrus viroid V (CVd-V) in California is evaluated and a permanent rating is herein proposed. 

History & Status:

Background: The origin of Citrus viroid V (CVd-V) is uncertain (Serra et al., 2008a).  In a study in Spain on the response of Citrus species and citrus-related genera to viroid infections, Serra and other researchers (2008a) originally detected CVd-V in Atalantia citroides, a citrus relative plant propagated on rough lemon rootstock and graft-inoculated with artificial mixtures of different viroids.  The viroid source was provided to them by a researcher at the University of California, Riverside and purified preparations were shown to be infectious in Etrog citron (Citrus medica), a classical indicator plant of citrus viroids.  Subsequently, CVd-V was considered a new species of the genus Apscaviroid in the family Pospiviroidae (Serra et al., 2008a).  Viroids are classified within two families: Pospiviroidae and Avsunviroidae.  Citrus are natural hosts of several viroid species that belong to the family Pospiviroidae.  Therefore, A. citroides was identified as an unusual viroid host since it was resistant to all previously known citrus viroids, yet capable of replicating CVd-V (Serra et al., 2008b).  Infectious assays conducted by Sierra et al. (2008) showed that CVd-V in Etrog citron exhibited mild symptoms, however, co-infections with either Citrus bent leaf viroid (CBLVd) or Citrus dwarfing viroid (CDVd, previously Citrus viroid III), also belonging to the genus Apscaviroid, showed synergistic effects in contrast to single infections of CVd-V or the other two viroids, however, titers of the viroids remained the same in singly or doubly infected plants (Serra et al., 2008a).

While the origin of CVd-V is not known, Pakistan may be one of the geographic origins of the viroid (Serra et al., 2008a, b; Parakh et al., 2017).  Serra et al. (2008a) suggested that the viroid was present, but overlooked or unnoticed, in field sources containing Hop stunt Viroid or Citrus dwarfing viroid – both of which have electrophoretic mobilities similar to CVd-V.  CVd-V has been found with some variations in its nucleotide sequence, in several countries in Africa, Asia, Europe, and North America (see ‘Worldwide Distribution).

In June 2016, the Citrus Clonal Protection Program-National Clean Plant Network (CCPP-NCPN), University of California, Riverside, California detected Citrus Viroid V in citrus budwood samples submitted by the CDFA for virus and viroid testing under the mandatory California (CA 3701) Citrus Nursery Stock Pest Cleanliness Program.  These budwood samples were taken from asymptomatic redblush grapefruit (Citrus paradisi) and variegated calamondin (C. madurensis) from a nursery in Tulare County.  This find marked the natural occurrence of CVd-V in California and corroborated the earlier report of CVd-VCA variant in the State (Dang et al., 2018; Serra et al., 2008b).

Hosts: Citrus spp.  including ‘Sanguinelli’, Salustiana’, and ‘Ricart navelina’ sweet oranges (Citrus x sinensis),  ‘Oroval’ and ‘Hernandina clementines (C. clementina), ‘Fino’ and ‘Verna’ lemons (C. limon), ‘Sevilano’ and ‘Cajel’ sour orange (C. aurantium), ‘Clausellina’ satsuma (C. unshiu), Temple mandarin (C. temple), Tahiti lime, Palestine sweet lime (C. limettioides), calamondin (C. madurensis), ‘Calabria’ bergamot (C. bergamia), ‘Orlando’ tangelo (C. paradisi x C. tangerina), ‘Page’ mandarin [(C. paradisi x C. tangerina) x C. clementina], and ‘Nagami’ kumquat (Fortunella margarita),  and Etrog citrus (Atlantia citroides) (Serra et al., 2008); ‘Shiranui’ [(C. unshiu x C. sinensis) x C. reticulata] (Ito and Ohta, 2010); ‘Moro blood’ sweet orange (Citrus x sinensis) (Bani Hashemian et al., 2013); redblush grapefruit (C. paradisi) (Dang et al., 2018).

Symptoms:   Citrus viroid V induced mild characteristic symptoms of very small necrotic lesions and cracks, sometimes filled with gum, in the stems of the viroid indicator plant, Etrog citron.  However, CVd-V reacted synergistically when Etrog citrus was co-infected with either citrus bent leaf viroid (CBLVd) or Citrus dwarfing viroid (CDVd), and showed severe stunting and epinasty with multiple lesions in the midvein.  Plants co-infected with CBLVd and CVd-V exhibited severe stem cracking characteristic of CBLVd, but without gum exudates, whereas plant co-infected with CDVd showed necrotic lesions (Serra et al., 2008a). Symptoms induced by CVd-V alone in commercial species and varieties are presently not known since commercial trees may be co-infected with several viroids (Ito and Ohta, 2010; Serra et al., 2008a).  Citrus viroid V may be present in asymptomatic citrus plant tissue – as recently evidenced by its detection in asymptomatic budwood collected from Tulare County, California.

Damage Potential:  The effect of CVd-V in commercial citrus rootstock-scion combinations, alone and in combination with other viroids, is yet unknown, however, Serra et al. (2008b) suggested that CVd-V could reduce tree size and yield as has been reported for clementine trees grafted on trifoliate orange co-infected with several viroids. Therefore, the need for nursery planting stock free of CVd-V is important.

Transmission:  Similar to other citrus viroids, CVd-V is graft-transmitted and is spread mainly through the propagation of infested material.

Worldwide Distribution:  Africa: Oman (Serra et al., 2008), Tunisia (Hamdi et al., 2015); Asia: China, Japan, Nepal, Pakistan (Cao et al., 2013), Iran (Bani Hashemian et al., 2010), Turkey (Önelge and Yurtmen, 2012); Europe: Spain (Serra et al., 2008); North America: USA (Serra et al., 2008).

Official Control: Citrus viroid V is a disease agent of concern that is tested for in the CDFA Citrus Nursery Stock Pest Cleanliness Program (3 CCR §§ 3701, et seq.).

California Distribution Tulare County (Dang et al., 2018).

California Interceptions: None reported.

The risk Citrus viroid V would pose to California is evaluated below.

Consequences of Introduction: 

1) Climate/Host Interaction: Citrus viroid V is likely to establish within infested propagative citrus materials in all citrus-growing regions of California.

Evaluate if the pest would have suitable hosts and climate to establish in California.

Score: 3

– Low (1) Not likely to establish in California; or likely to establish in very limited areas.

– Medium (2) may be able to establish in a larger but limited part of California.

High (3) likely to establish a widespread distribution in California.

2) Known Pest Host Range: Citrus viroid V has a moderate host range that is limited to several species and varieties of Citrus.

Evaluate the host range of the pest.

Score: 2

– Low (1) has a very limited host range.

Medium (2) has a moderate host range.

– High (3) has a wide host range.

3) Pest Dispersal Potential: Citrus viroid V replicates autonomously within infested plants and is spread mainly through the propagation and movement of infested planting materials to non-infested regions.

Evaluate the natural and artificial dispersal potential of the pest.

Score: 2

– Low (1) does not have high reproductive or dispersal potential.

Medium (2) has either high reproductive or dispersal potential.

– High (3) has both high reproduction and dispersal potential.

4) Economic Impact: The effect of CVd-V in commercial citrus rootstock-scion combinations, alone and in combination with other viroids, is yet unknown, however, it has been suggested by Serra et al. (2008b) that CVd-V could reduce tree size and yield.

Evaluate the economic impact of the pest to California using the criteria below.

Score: A, B, C

A. The pest could lower crop yield.

B. The pest could lower crop value (includes increasing crop production costs).

C. The pest could trigger the loss of markets (includes quarantines).

D. The pest could negatively change normal cultural practices.

E. The pest can vector, or is vectored, by another pestiferous organism.

F. The organism is injurious or poisonous to agriculturally important animals.

G. The organism can interfere with the delivery or supply of water for agricultural uses.

Economic Impact Score: 3

– Low (1) causes 0 or 1 of these impacts.

– Medium (2) causes 2 of these impacts.

High (3) causes 3 or more of these impacts.

5) Environmental Impact: It is probable that home, urban, public garden and landscape plantings of CVd-V-infested citrus plantings may be significantly impacted by the viroid singly or in combination with other viroids.

Evaluate the environmental impact of the pest on California using the criteria below.

Environmental Impact: E

A. The pest could have a significant environmental impact such as lowering biodiversity, disrupting natural communities, or changing ecosystem processes.

B. The pest could directly affect threatened or endangered species.

C. The pest could impact threatened or endangered species by disrupting critical habitats.

D. The pest could trigger additional official or private treatment programs.

E. The pest significantly impacts cultural practices, home/urban gardening or ornamental plantings.

Environmental Impact Score: 2

– Low (1) causes none of the above to occur.

Medium (2) causes one of the above to occur.

– High (3) causes two or more of the above to occur.

Consequences of Introduction to California for Citrus Viroid V

Add up the total score and include it here. (Score)

-Low = 5-8 points

Medium = 9-12 points

-High = 13-15 points

Total points obtained on evaluation of consequences of introduction of CVd-V to California = 12.

6) Post Entry Distribution and Survey Information: Evaluate the known distribution in California. Only official records identified by a taxonomic expert and supported by voucher specimens deposited in natural history collections should be considered. Pest incursions that have been eradicated, are under eradication, or have been delimited with no further detections should not be included. (Score)

-Not established (0) Pest never detected in California, or known only from incursions.

Low (-1) Pest has a localized distribution in California, or is established in one suitable climate/host area (region).

-Medium (-2) Pest is widespread in California but not fully established in the endangered area, or pest established in two contiguous suitable climate/host areas.

-High (-3) Pest has fully established in the endangered area, or pest is reported in more than two contiguous or non-contiguous suitable climate/host areas.

Evaluation is Low (-1)Currently, Citrus viroid V has only been detected in a nursery in Tulare County.

Final Score:

7) The final score is the consequences of introduction score minus the post entry distribution and survey information score: (Score)

Final Score:  Score of Consequences of Introduction – Score of Post Entry Distribution and Survey Information = 11.                                                                             


The effect of CVd-V in commercial citrus rootstock-scion combinations, alone and in combination with other viroids, is yet unknown.

Conclusion and Rating Justification:

Based on the evidence provided above the proposed rating for Citrus viroid V is B.


Bani Hashemian, SM, Taheri, H, Duran-Vila, N, and Serr, P.  2010.  First report of Citrus viroid V in Moro blood sweet orange in Iran.  Plant Disease 94: 129.

Cao, M. J., Liu, Y. Q., Wang, X. F., Yang, F. Y., and Zhou, C. Y.  2010.  First report of Citrus bark cracking viroid and Citrus viroid V infecting Citrus in China.  Plant Disease 94: 922.

Dang, T., Tan, S. H., Bodaghi, S., Greer, G., Lavagi, I., Osman, F., Ramirez, B., Kress, J., Goodson, T., Weber, K., Zhang, Y. P., Vidalakis, G.  First report of Citrus Viroid V naturally infecting grapefruit and calamondin trees in California.  Plant Disease, Posted online on August 10, 2018.

Hamdi, I., Elleuch, A., Bessaies, N., Grubb, C. D., and Fakhfakh, H. 2015. First report of Citrus viroid V in North Africa. Journal of General Plant Pathology 81, 87

Ito, T., and Ohta, S.  2010.  First report of Citrus viroid V in Japan.  Journal of General Plant Pathology 76: 348-350.

Önelge, N., and Yurtmen, M. 2012. First report of Citrus viroid V in Turkey. Journal of Plant Patholology 94 (Suppl. 4), 88.

Parakh, D. B., Zhu, S., and Sano, T.  2017.  Geographical distribution of viroids in South, Southeast, and East Asia.  In: Apscaviroids Infecting Citrus Trees by Tessitori, M, Viroids and Satellites, Edited by Hadidi, A, Flores, R, Randles, JW, and Palukaitis, P, Academic Press Ltd-Elsevier Science Ltd, Pages 243-249

Serra, P., Barbosa, C. J, Daros, J. A., Flores, R., Duran-Vila, N. 2008a. Citrus viroid V: molecular characterization and synergistic interactions with other members of the genus Apscaviroid. Virology 370, 102112.

Serra, P., Eiras, M., Bani-Hashemian, S. M., Murcia, N., Kitajima, E.W., Daro`s, J. A., et al., 2008b. Citrus viroid V: occurrence, host range, diagnosis, and identification of new variants. Phytopathology 98, 11991204.

Responsible Party:

John J. Chitambar, Primary Plant Pathologist/Nematologist, California Department of Food and Agriculture, 3294 Meadowview Road, Sacramento, CA 95832. Phone: 916-738-6693,[@]


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Pest Rating: B

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