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John J. Chitambar, Primary Plant Pathologist/Nematologist, California Department of Food and Agriculture, Phone: 916-738-6693, plant.health[@]cdfa.ca.gov.
Updated on 7/10/2019 by ls
John J. Chitambar, Primary PlantPathologist/Nematologist, California Department of Food and Agriculture, plant.health[@]cdfa.ca.gov.
Updated on 7/10/2019 by ls
On September 25, 2018, Tongyan Tian, CDFA Plant Pathologist, was notified by Kai-Shu Ling, Plant Pathologist, USDA ARS, Charleston, South Carolina, of his detection of Tomato brown rugose fruit virus (ToBRFV) in a tomato plant tissue sample sent to him by a private company in California. The sample had been collected from tomato plants grown in the company’s greenhouse in Santa Barbara County. On September 13, 2018, the company had also sent an unofficial symptomatic tomato leaf sample to CDFA for diagnosis of the associated pathogen. On November 2, 2018, Tongyan Tian, CDFA, identified the associated pathogen as Tomato brown rugose fruit virus. On further investigation of the situation in California, CDFA was notified by the company that all ToBRFV-infested and symptomatic plant material had been voluntarily destroyed, thereby preventing the collection of an official sample. Nevertheless, the risk associated with the possible introduction of ToBRFV and a proposed rating for this pathogen is documented here.
Background: Tomato brown rugose fruit virus is a relatively new Tobamovirus – the genus that bears other economically important and contagious pathogens that infect Solanaceae, such as Tobacco mosaic virus (TMV) and Tomato mosaic virus (ToMV). ToBRFV was initially isolated from tomato plants grown in greenhouses in Jordan in 2015 (Salem et al., 2016). Prior to this, in 2014, an outbreak of a new disease infecting resistant tomato cultivars grown in net houses was observed in Southern Israel and was determined to be caused by the Israeli isolate of ToBRFV with high genomic sequence identity to the Jordan isolate (Luria et al., 2017). Most recently, ToBRFV was detected in tomato and chili pepper plants growing in nurseries in Yurecuaro, Michoacan, Mexico (NAPPO, 2018). There have been no previous reports of ToBRFV from the USA. The recent detection in greenhouse tomato plants in California that subsequently resulted in the destruction of all infested plants, does not verify the establishment of ToBRFV in the country (see ‘Initiating Event’).
Tobamoviruses infecting tomato are of great concern, but ToBRFV is of special concern because of its ability to overcome resistance of the TM-22 resistance gene which is genetically bred into tomato plants for resistance against Tobamoviruses (Luria et al., 2017). The Israeli isolate of ToBRFV was found to infect pepper (Capsicum annuum) plants harboring the L resistance genes, when cultivated in contaminated soil from previous grown infected tomato plants, especially in hot temperatures above 30°C (Luria et al., 2017). Disease caused by ToBRFV is infectious and local spread can occur rapidly through mechanical means (see ‘Dispersal and spread’).
Hosts: Tomato (Solanum lycopersicum) and pepper (Capsicum annuum) are the main hosts (Salem et al., 2016; Luria et al., 2017; NAPPO, 2018). Petunia (Petunia hybrida) and certain weeds like black nightshade (S. nigrum) were shown to be asymptomatic hosts in experiments (Luria et al., 2017).
Symptoms: The Jordan isolate of ToBRFV in tomato caused mild foliar symptoms and strong brown rugose symptoms on fruit thereby affecting market value of the crop. Mechanically inoculated plants exhibited a range of local and systemic symptoms (Salem et al., 2016). Symptoms caused by the Israeli isolate of ToBRFV were mild and severe mosaic of leaves with occasional narrowing of the leaves. Yellow spots on fruit affected 10-15% of the total number of fruit produced on symptomatic plants (Luria et al., 2017).
In pepper plants cultivated in ToBRFV-contaminated soil from previously grown infected tomato plants, especially in temperatures above 30°C, the hypersensitivity response included necrotic lesions on roots and stems resulting in inhibited plant growth and possibly plant collapse. Petunia and certain weeds are symptomless hosts, while eggplant and potatoes are non-hosts for the virus (Luria et al., 2017).
Dispersal and spread: ToBRFV is transmitted mechanically (plant to plant) via externally contaminated seed (over long distances), common cultural practices (worker’s hand, clothes), tools, equipment and circulating water (Salem et al., 2016). Tobamoviruses are capable of preserving infectivity in seeds and contaminated soil (Broadbent, 1976; Luria et al., 2017). Weed hosts can serve as reservoirs of inoculum for infection of the main hosts.
Damage Potential: Tobamoviruses are of main concern in tomato crops, especially when cultivated in protected environments such as greenhouses, where conditions favor rapid spread of the pathogen. The ability of ToBRFV to break resistance in tomato plants harboring the TM-22 resistance gene and, under certain conditions also pepper plants harboring the L resistance genes, makes the potential for damage a main concern. The stability and infectious nature of this Tobamovirus via mechanical transmission by workers, tools and equipment during the handling of plants, with infection most likely occurring when seedlings are thinned in nurseries or transplanted, plus transmission through contaminated seed, soil and circulating water, render a high potential for damage in tomato and pepper. Crop production and quality of ToBRFV-consumable tomato and pepper fruit can be affected thereby significantly impacting their market value.
Worldwide Distribution: Asia: Jordan (Salem et al., 2016), Israel (Luria et al., 2017); North America: Mexico (NAPPO, 2018).
Official Control: None reported.
California Distribution: Tomato brown rugose fruit virus is not present in California. The detection of ToBRFV in greenhouse tomato plants in Santa Barbara County resulted in the destruction of the plants (see ‘Initiating Event’).
California Interceptions: None reported.
The risk Tomato brown rugose fruit virus would pose to California is evaluated below.
1) Climate/Host Interaction: It is likely that Tomato brown rugose fruit virus can establish a widespread distribution in California wherever tomato and pepper plants are cultivated.
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: The main hosts of ToBRFV are tomato and pepper cultivars. Experimentally, petunia and few weeds have been proven to be asymptomatic hosts and weeds may serve as reservoirs of inoculum for subsequent infections of main cultivated hosts.
Evaluate the host range of the pest.
Score: 1
– 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: Tomato brown rugose fruit virus is a stable and readily infectious virus plant pathogen. It is easily transmitted from plant to plant by mechanical means which include common cultural practices, contaminated tools, equipment, hands, clothes, soil, and infected plants, and seed. Infections most likely occur in protected environments, where favorable conditions for pathogen spread exist, as when seedlings are thinned in nurseries or transplanted. Transmission of ToBRFV by insect vectors has not been reported.
Evaluate the natural and artificial dispersal potential of the pest.
Score: 3
– 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: ToBRFV can break resistance in tomato plants harboring the TM-22 resistance gene and under certain conditions, also pepper plants harboring the L resistance genes. The stability and infectious nature of this Tobamovirus render a high potential for damage in tomato and pepper particularly under protected environments such as greenhouses. Crop production and quality of ToBRFV consumable tomato and pepper fruit can be affected thereby significantly impacting their market value.
Evaluate the economic impact of the pest to California using the criteria below.
Economic Impact: A, B, C, D, G.
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: The natural host range is limited to tomato and pepper which are cultivated crops. Home/urban gardening of these host plants may be impacted if infected with ToBRFV. Consequently, the establishment of this resistance-breaking Tobamovirus species in California could trigger additional official or private treatment programs.
Evaluate the environmental impact of the pest on California using the criteria below.
Environmental Impact: D, 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: 3
– 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.
Add up the total score and include it here. 13
-Low = 5-8 points
-Medium = 9-12 points
–High = 13-15 points
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.
Evaluation is ‘0’. ToBRFV is not established in California.
Score: 0
–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.
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 = 13
The potential for weed plants, especially those commonly found in tomato and pepper fields in California, to serve as hosts and inoculum reservoirs of the pathogen is not known.
Based on the evidence provided above the proposed rating for Tomato brown rugose fruit virus is A.
Broadbent, L. 1976. Epidemiology and control of Tomato mosaic virus. Annual Review of Phytopathology, 14:75-96.
Luria, N. Smith, E., Reingold, V., Bekelman, I., Lapidot, M., Levin, I., Elad, N., Tam., Y., Sela, Abu-Ras, A., Ezra, N., Haberman, A., Yitzhak, L., Lachman, O. and Dombrovsky, A. 2017. A new Israeli Tobamovirus isolate infects tomato plants harboring Tm-22 resistance genes. PLoS ONE 12 (1):e0170429. doi:10.1371/journal.pone.0170429
NAPPO. 2018. Tomato Brown Rugose Fruit Virus: detected in the municipality of Yurecuaro, Michoacan. North American Plant Protection Organization (NAPPO) Phytosanitary Alert System. September 17, 2018. https://www.pestalerts.org/oprDetail.cfm?oprID=765.
Salem, N., Mansour, A., Ciuffo, M., Falk, B. W., and Turina, M. 2016. A new Tobamovirus infecting tomato crops in Jordan. Archives of Virology, 161:503-506.
John J. Chitambar, Primary Plant Pathologist/Nematologist, California Department of Food and Agriculture, 3294 Meadowview Road, Sacramento, CA 95832. Phone: 916-738-6693, plant.health[@]cdfa.ca.gov.
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Posted by ls
The risk of infestation of Citrus viroid V (CVd-V) in California is evaluated and a permanent rating is herein proposed.
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.
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.
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.
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.
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. https://doi.org/10.1094/PDIS-94-7-0922C
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. https://doi.org/10.1094/PDIS-01-18-0100-PDN
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.
John J. Chitambar, Primary Plant Pathologist/Nematologist, California Department of Food and Agriculture, 3294 Meadowview Road, Sacramento, CA 95832. Phone: 916-738-6693, plant.health[@]cdfa.ca.gov.
You must be registered and logged in to post a comment. If you have registered and have not received the registration confirmation, please contact us at plant.health[@]cdfa.ca.gov.
♦ Comments should refer to the appropriate California Pest Rating Proposal Form subsection(s) being commented on, as shown below.
Example Comment:
Consequences of Introduction: 1. Climate/Host Interaction: [Your comment that relates to “Climate/Host Interaction” here.]
♦ Posted comments will not be able to be viewed immediately.
♦ Comments may not be posted if they:
Contain inappropriate language which is not germane to the pest rating proposal;
Contains defamatory, false, inaccurate, abusive, obscene, pornographic, sexually oriented, threatening, racially offensive, discriminatory or illegal material;
Violates agency regulations prohibiting sexual harassment or other forms of discrimination;
Violates agency regulations prohibiting workplace violence, including threats.
♦ Comments may be edited prior to posting to ensure they are entirely germane.
♦ Posted comments shall be those which have been approved in content and posted to the website to be viewed, not just submitted.
Posted by ls
A pest risk assessment and rating for Grapevine pinot gris virus (GPGV) was recently requested by Joshua Kress, CDFA Pest Exclusion Branch, in response to notification received on January 24, 2018, from Foundation Plant Service (FPS), on the detection of GPGV in their Foundation grapevine plants. The risk of infestation of GPGV in California is evaluated and a permanent rating is herein proposed.
Background: Although symptoms of stunting, chlorotic mottling, and leaf deformation had been observed on V. vinifera ‘Pinot gris’, in Trentino, North Italy since 2003, it was not until 2012 that Grapevine pinot gris was first detected by deep sequencing in one symptomatic and one symptomless grapevine, Vitis vinifera cv. Pinot gris in Northern Italy. In this initial study, GPGV was associated with field symptoms of chlorotic mottling and leaf deformation, reduced yield and low quality of berries, however the plant was also associated with several other viruses and viroids. Furthermore, since GPGV was found in both symptomatic and symptomless plants from three different grape cultivars in a limited field survey, the virus could not be directly associated with the observed symptoms (Giampetruzzi et al., 2012; Glasa et al., 2014). This was further confirmed by Saldarelli et al. (2013) who reported 70% of GPGV-infected asymptomatic veins in cultivars Traminer and Pinot gris vineyards in Italy. Bianchi et al. (2015) also detected GPGV in symptomatic and asymptomatic plants over a 3-year period in a field survey of productive vineyards and scion mother plant nurseries in Italy, however, the mean quantity of the virus was significantly higher in symptomatic vines than in asymptomatic plants. Consequently, a critical level or quantity of virus could not be associated with symptom expression. Scientists in Italy determined that GPGV isolates that produce symptoms can be genetically differentiated from those that are asymptomatic (Saldarelli et al., 2015).
Grapevine pinot gris virus belongs to the genus Trichovirus in the family Betaflexiviridae. Its full-length sequence was described and shown to be phylogenetically closely related to, yet molecularly different from Grapevine berry inner necrosis virus, another Trichovirus which was found in Japan and is transmitted by eriophyid mites (Giampetruzzi et al., 2012). Since its original description in Italy, GPGV has been detected from symptomatic and asymptomatic grapevine cultivars in several countries in Europe and Asia, and few in North America, South America and Australia (see: ‘Worldwide Distribution’).
Grapevine Pinot gris virus (GPGV) was detected in California grapevine in Napa Valley and diagnosed by a testing service lab in Yolo County. An informal report of this detection was made in 2015 (Rieger, 2015) and in a ‘list of pathogens report’ submitted by a testing service lab to the CDFA. A formal first report of GPGV infecting grapevine was made in 2016 (Rwahnih et al., 2016) and marked a first detection of GPGV in the United States. In 2016, Rwahnih and other scientists at the Foundation Plant Services screened 2,014 vines, including 23 vines of Pinot gris for the possible presence and prevalence of GPGV in the collections of FPS, which are the source of all certified grapevine plants produced in California. Of all the vines tested, only one relatively rare, asymptomatic vine variety ‘Touriga Nacional” was found positive for GPGV. This vine had been imported from Portugal in 1981. The risk of GPGV spread in commercial vineyards was considered low, given the very low prevalence of the pathogen in the FPS collection, however, the need for a large-scale survey of commercial vineyards in California was emphasized, as well as, the need for research to evaluate the effect of the virus on grapevine performance and wine quality. Since cv ‘Touriga Nacional’ is rarely used in commercial vineyards, Angelini et al., (2016) molecularly surveyed 96 grapevine samples from four commercial wine grape vineyards in Napa Valley, California and reported the presence of GPGV in three cultivars, ‘Chardonnay’, ‘Cabernet Sauvignon’, and ‘Cabernet Franc’.
Grapevine pinot gris virus was recently detected in Foundation grapevine plants at FPS (see ‘Initiating Event’). Subsequently, FPS removed all source vines from the Foundation vineyard and initiated monitoring of the site with additional testing implemented to detect and destroy any further detection and contain possible spread of the pathogen (personal communication: M. Al Rwahnih, Foundation Plant Services).
Hosts: Grapevine pinot gris virus has been found in at least 28 wine and table grape varieties of Vitis vinifera and hybrids. including Pinot gris, Pinot noir, Traminer, Chardonnay, Merlot, Chardonnay, Cabernet Franc, Cabernet Sauvignon, Carmenere Glera (Prosecco), Sauvignon Blanc and Shiraz (AWRI, 2018).
Symptoms: Grapevines infected with GPGV may be symptomatic or asymptomatic. Furthermore, specific symptoms caused by GPGV have been difficult to assign as GPGV-infected grapevines were infected with other viruses. Because of this, definitive symptoms have not been attributed to GPGV alone. Symptoms putatively associated with GPGV include chlorotic mottling, leaf deformation, delayed bud-burst, stunted growth, reduced yields and low quality of berries with increased acidity (Saldarelli et al., 2015; AWRI, 2018).
Damage Potential: The complete impact of GPGV on grapevine health is currently unknown and further research is need in this area (AWRI, 2018). In Europe and Asia, GPGV and other concomitant viruses infesting grapevines have been associated with field observations of reduced yield, poor fruit set, poor quality and inner necrosis of berries (Giampetruzzi et al., 2012). In Slovenia, the disease was reported to cause considerable economic losses (Mavrič Pleško et al., 2014). Presently, the risk of spread of GPGV is considered low and the distribution of the virus has only been reported from commercial vineyards within Napa County (Al Rwahnih et al., 2016; Angelini et al., 2016).
Transmission: Grapevine Pinot gris virus is spread through movement of infected plant propagative material and by graft transmission. There is the possibility of GPGV transmission by the eriophyid mite Colomerus vitus, like the other grapevine-infecting Trichovirus, Grapevine berry inner necrosis virus, however, this has not been confirmed. Colomerus vitus commonly infests grapevine and has been reported in California.
Worldwide Distribution: Asia: China, South Korea, Georgia, Pakistan; Europe: Bosnia, Croatia, Czech Republic, France, Germany, Greece, Italy, Portugal, Romania, Serbia, Slovakia, Slovenia, Spain, Turkey, Ukraine; North America: Canada, USA (California); South America: Brazil; Oceania: Australia. (Al Rwahnih et al., 2016; Angelini et al., 2016; Beuve et al., 2015; CABI, 2018; Casati et al., 2015; EPPO, 2018; Fan et al., 2016; Gazel et al., 2016; Lou et al., 2016; Mavrič Pleško et al., 2014; Rasool et al., 2017; Reynard, et al., 2016; Rius-Garcia & Olmos, 2017; Wu et al., 2017; Xiao et al., 2016).
Official Control: None reported.
California Distribution: Napa County.
California Interceptions: There are no CDFA records of detection of GPGV in quarantine shipments of plant material intercepted in California.
The risk Grapevine Pinot gris virus would pose to California is evaluated below.
1) Climate/Host Interaction: Grapevine pinot gris virus is expected to be able to establish wherever wine and table grape varieties are cultivated in California, and therefore, is likely to establish a wide spread distribution.
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: Grapevine pinot gris virus has been found in at least 28 wine and table grape varieties of Vitis vinifera and hybrids. including Pinot gris, Pinot noir, Traminer, Chardonnay, Merlot, Chardonnay, Cabernet Franc, Cabernet Sauvignon, Carmenere Glera (Prosecco), Sauvignon Blanc and Shiraz. It’s known pest host range is evaluated as very limited.
Evaluate the host range of the pest.
Score: 1
– 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: GPGV is transmitted artificially through grafting and infested planting stock. The involvement of a vector, an eriophyid mite Colomerus vitus, although likely, has not been confirmed. The virus has high reproduction within symptomatic and asymptomatic plants. Therefore, a ‘High’ rating is given to this category.
Evaluate the natural and artificial dispersal potential of the pest.
Score: 3
– 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 economic impact of GPGV is not currently known and requires further research. This is mainly due to evidence that the virus is present in both symptomatic and symptomless grape plants, and that other viruses and viroids may be present within the same plant infested by GPGV. Nevertheless, putative symptoms of chlorotic mottling, leaf deformation, stunted growth, reduced yields and low quality of berries, have been associated with GPGV infestations. This may relate to potentially lowering crop value and yield in production. While the virus may be present in commercial vineyards of Chardonnay and Cabernet Sauvignon in California (Angelini et al., 2016), its risk of spread is considered low and its general impact on production is presently unknown. Nursery production of grapevines may be affected.
Evaluate the economic impact of the pest to California using the criteria below.
Score: A, B
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: 2
– 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: No impact to the environment is expected.
Evaluate the environmental impact of the pest on California using the criteria below.
Environmental Impact: None
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: 1
– 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.
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 GPGV to California = Medium (10).
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). Presently, Grapevine pinot gris virus has been reported only from Napa County.
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 = 9.
Several aspects of Grapevine pinot gris virus are yet not known and require further research. In general, the impact of the virus on grape production, symptoms, prevalence and distribution within California are not fully known.
Based on the evidence provided above the proposed rating for Grapevine Pinot gris virus is B.
AWRI. 2018. Grapevine pinot gris virus. Fact Sheet, Viticulture. The Australian Wine Research Institute. Updated February 2018.
Al Rwahnih, M., D. Golino, and A. Rowhani. 2016. First report of Grapevine Pinot gris virus infecting grapevine in the United States. Plant Disease (Posted online on March 4, 2016). http://dx.doi.org/10.1094/PDIS-10-15-1235-PDN.
Angelini, E., N. Bertazzon, J. Montgomery, X. Wang, A. Zinkl, J. Stamp, and A. Wei. 2016. Occurrence of Grapevine Pinot gris virus in commercial vineyards in the United States. Plant Disease (Posted online on March 23, 2016): http://dx.doi.org/10.1094/PDIS-01-16-0055-PDN.
Beuve, M., T. Candresse, M. Tannières, and O. Lemaire. 2015. First report of Grapevine Pinot gris virus (GPGV) in grapevine in France. Plant Disease 99:293. http://dx.doi.org/10.1094/PDIS-10-14-1008-PDN.
Bianchi, G. L., F. De Amicis, L. De Sabbata, N. Di Bernardo, G. Governatori, F. Nonino, G. Prete, T. Marrazzo, S. Versolatto and C. Frausin. 2015. Occurrence of Grapevine Pinot gris virus in Friuli Venezia Giulia (Italy): Field monitoring and virus quantification by real-time RT-PCR. EPPO Bulletin 45:22-32. DOI: 10.1111/epp.12196.
Casati, P., D. Maghradze, F. Ouaglino, A. Ravasio, O. Failla and P. A. Bianco. First report of Grapevine pinot gris virus in Georgia. Journal of Plant Pathology 1 (1). DOI: 10.4454/JPP.V98I1.003
EPPO. 2018. Grapevine Pinot gris virus (GPGV00). EPPO Global Database. https://gd.eppo.int/taxon/GPGV00/distribution
Fan, X. D., Y. F. Dong, Z. P. Zhang, F. Ren, G. J. Hu, Z.N. Li, and J. Zhou. 2016. First report of Grapevine Pinot gris virus in Grapevines in China. Plant Disease 100:540. http://dx.doi.org/10.1094/PDIS-08-15-0913-PDN.
Gazel, M., K. Caǧlayan, E. Elci, and L. Ozturk. 2016. First Report of Grapevine Pinot gris virus in Grapevine in Turkey. Plant Disease 100:657. http://dx.doi.org/10.1094/PDIS-05-15-0596-PDN.
Glasa, M., L. Predajňa, P. Komínek, A. Nagyová, T. Candresse and A. Olmos. 2014. Molecular characterization of divergent grapevine Pinot gris virus isolated and their detection in Slovak and Czech grapevines. Archives of Virology 159: 2103-2107.
Giampetruzzi, A., V. Roumia, R. Roberto, U. Malossinib, N. Yoshikawac, P. La Notte, F. Terlizzi, R. Credid, and P. Saldarelli. A new grapevine virus discovered by deep sequencing of virus- and viroid-derived small RNAs in cv Pinot gris. Virus Research 163:262-268.
Lou, B. H., Y. Q. Song, A. J. Chen, X. J. Bai, B. Wang, M. Z., Wang, P. Liu and J. J. He. 2016. First report of Grapevine pinot gris virus in commercial grapevines in Southern China. Journal of Plant Pathology 98: 677-697.
Mavrič Pleško, I., M. Viršček Marn, G. Seljak, and I. Žežlina. 2014. First report of Grapevine Pinot gris virus infecting grapevine in Slovenia. Plant Disease 98:1014. http://dx.doi.org/10.1094/PDIS-11-13-1137-PDN.
Rasool, S., S. Naz, A. Rowhani, D. A. Golino, N. M. Westrick, K. D. Farrar and M. Al Rwahnih. 2017. First report of Grapevine pinot gris virus infecting grapevine in Pakistan. Plant Disease 101: 1958.
Rieger, T. 2015. New grapevine virus detected in California: Grapevine Pinot Gris Virus discussed at UCD FPS meeting. http://www.winebusiness.com/news/?go=getArticle&dataid=160912.
Reynard, J. -S, S. Schumacher, W. Menzel, J. Fuchs, P. Bohnert, M. Glasa, T. Wetzel and R. Fuchs. 2016. First report of Grapevine pinot gris virus in German vineyards. Plant Disease 100: 2545.
Ruiz-García, A. B., and A. Olmos. 2017. First report of Grapevine pinot gris virus in Grapevine in Spain. Plant Disease 101: 1070.
Saldarelli, P., A. Giampetruzzi, M. Morelli, U. Malossini, C. Pirolo, P. Bianchedi, and V. Gualandri. 2015. Genetic variability of Grapevine Pinot gris virus and its association with grapevine leaf mottling and deformation. Phytopathology 105:555-563. http://dx.doi.org/10.1094/PHYTO-09-14-0241-R.
Xiao, H., M. Shabanian, W. McFadden-Smith, and B. Meng. 2016. First report of Grapevine Pinot gris virus in commercial grapes in Canada. Plant Disease (Posted online on February 29, 2016). http://dx.doi.org/10.1094/PDIS-12-15-1405-PDN.
John J. Chitambar, Primary Plant Pathologist/Nematologist, California Department of Food and Agriculture, 3294 Meadowview Road, Sacramento, CA 95832. Phone: 916-262-1110, plant.health[@]cdfa.ca.gov.
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Posted by ls
On February 26, 2018, Dr. G. Vidalakis, University of California, Director, Citrus Clonal Protection Program, informed CDFA of his detection of Citrus leaf blotch virus (CLBV) from a Bearss Lime tree at a residence in Los Angeles County. Subsequently, an official sample, which comprised a total of 4 subsamples, was collected by the CDFA from the same Bearss Lime tree and sent to the CDFA Plant Pathology Laboratory for diagnosis. On February 27, 2018, Tongyan Tian, CDFA Plant Pathologist, detected Citrus leaf blotch virus from all four subsamples using RT-qPCR and further confirmed the identity of the pathogen by conventional RT-PCR and sequencing. A temporary Q rating was assigned to the pathogen. The status, risk and consequences of introduction of CLBV to California are assessed and a pest permanent pest rating is proposed herein.
Background: In 1968, Dweet mottle virus (DMV) was initially detected and reported from Riverside, California, during re-indexing of a candidate Cleopatra mandarin variety (C. reticulata) on ‘Dweet’ tangor at the University of California Riverside Citrus Variety Improvement Program, the forerunner of the present Citrus Clonal Protection Program (CCPP). The candidate mandarin variety had been introduced from Florida into the Program at Riverside. The virus produced leaf chlorotic blotching symptoms that resembled, but were distinct from, symptoms produced by psorosis virus and Citrus concave gum virus. It also produced a mild exocortis reaction in Etrog citron. The parent tree did not show symptoms of damage caused by any known virus and the trunk appeared normal without any signs of stem pitting or bark discoloration, although small fruit, twig dieback and little new growth were apparent. Since the virus produced symptoms only in ‘Dweet’, it was named Dweet mottle virus (Roistacher & Blue, 1968). However, Dweet mottle virus was not reported from any commercial citrus production sites nor was it observed to produce any economic losses and was detected only once after 1963 in the CCPP indexing program (Krueger et al., 2012).
Then in 1984, at the Citrus Variety Improvement Program in Spain, Navarro and other scientists reported a new graft transmissible disease that caused a bud-union incompatibility between ‘Nagami’ kumquat and ‘Troyer’ citrange rootstock. The ‘Nagami’ kumquat had been introduced from Corsica, France. In addition to bud-union incompatibility, the presumptive virus involved caused vein clearing in certain citrus species and stem pitting in Etrog citron. However, after shoot-tip grafting, some plants produced were compatible with Troyer, but still caused stem pitting in Etrog citron, thereby, indicating the involvement of more than one virus (Navarro et al., 1984). Galipienso et al., 2000, gave further evidence of the involvement of more than one virus by demonstrating bud union crease in certain citrus species but not others when propagated on ‘Troyer’ citrange. However, chlorotic blotching in ‘Dweet’ tangor, like those induced by DMV, and stem pitting in Etrog citron were produced by all sources of the virus. In 2001-02, the causal agent in “Nagami’ kumquat was partially purified and characterized and given the candidate name, Citrus leaf blotch virus (CLBV) (Galipienso et al., 2001; Vives et al., 2001, 2002). Furthermore, these researchers detected CLBV in different citrus varieties from Japan, New South Wales (Australia), Spain, and Florida, usually associated with abnormal bud union on citrange or citrumelo. Comparison of 14 CLBV isolates from Spain, Japan, USA, France and Australia showed low genetic diversity (Vives et al., 2002). Low rates of seed transmission were demonstrated in three citrus varieties or hybrids (Guerri et al., 2004). A few years later, Vives et al., (2005) conducted partial sequence analysis to show that Dweet mottle virus from California had over 96% sequence (high) homology with citrus leaf blotch virus from Spain and therefore, suggested that DMV may be caused by CLBV. Both viruses induce mottling in ‘Dweet’ tangor and stem pitting in ‘Etrog’ citron and that, besides CLBV, a different pathogen causing bud-union crease and vein clearing may be present in ‘Nagami’ kumquat sources but not in DMV from California source. This was further demonstrated by Vives et al., (2008a) by the development of full-genome cDNA clones of CLBV that caused systemic infection in agro-inoculated herbaceous and citrus host plants and induced chlorotic blotching in ‘Dweet’ tangor and stem pitting in Etrog citron, but not vein clearing in Pineapple sweet orange or bud union crease on trifoliate rootstocks. Then in 2010, Hajeri and other researchers at the University of California, Riverside, and the USDA ARS National Clonal Germplasm Repository for Citrus and Dates (NCGRCD), Riverside, determined the complete nucleotide sequence of DMV and with phylogenetic analysis showed that DMV is an isolate of CLBV, and not a distinct species, within the genus Citrivirus.
In California, the seed transmissibility of citrus leaf blotch virus caused concern to the citrus nursery industry. Consequently, Kreuger et al. (2012) reported that all citrus trees at CCPP and NCGRCD were tested for the presence of the virus using RT-PCR with local DMV positives and a CLBV positive from Florida as positive controls. The virus was not detected in the tested trees. Furthermore, they failed to detect it during surveys of field trees exhibiting bud union abnormalities for the presence of specific pathogens and therefore, while the overall status of CLBV in California is presently unknown, they believe that this virus if present at all, is only at a low incidence. This is because the close identity of CLBV and DMV has likely prevented CLBV from becoming introduced into California. All introductions of new citrus germplasm are indexed into ‘Dweet’ tangor as well as other indicator species at CCPP and NCGRCD. Reaction of CLBV in ‘Dweet’ tangor would enable detection of this virus, even if the actual identity of the virus was not known at the time of indexing. Detection of positives or even misidentifications would have been eliminated by thermal therapy or shoot-tip grafting before release (Kreuger et al., 2005, 2012).
Citrus leaf blotch virus has been reported in China, Corsica (France), Cuba, Italy, Japan, New South Wales (Australia), New Zealand, Spain, Florida, Arkansas, Oregon, and California (USA). In Arkansas and Oregon, the virus was found in peony plants showing stunting and gnarled irregularities, however, since the virus was found in both symptomatic and asymptomatic material, it could not be associated with the disease and its role in peony health is currently unknown. Nonetheless, CLBV may easily move between propagation cycles via mechanical and seed transmission of clonally propagated peony plants (Gress et al., 2017).
Citrus leaf blotch virus not only causes symptomless infection in most citrus but also, is unevenly distributed within an infected plant, thereby presenting a possible challenge for its detection. In greenhouse studies, Vives et al. (2002) detected CLBV consistently in young leaves of infected ‘Nagami’ kumquat, ‘Owari’ Satsuma, Navelina and Navel oranges, however, detection in old leaves of other citrus species (Eureka lemon, Marsh grapefruit and Nules Clementine) was not consistent, particularly in Pineapple sweet orange. Detection of the virus in field trees was even less consistent, and not detected in neighbor trees showing similar symptoms possibly due to low titer or uneven distribution of the virus in the plant.
Hosts: Citrus spp., including C. sinensis, C. limon, C. unshiu, C. paradisi, Poncirus trifoliata, P. trifoliata x C. sinensis (Harper et al., 2008), C. medica (Etrog citrus), C. reticulata x C. sinensis (‘Dweet’ tangor) (Roistacher & Blue, 1968), Fortunella margarita (kumquat “Nagami’) (Navarro et al., 1984), Prunus avium cv. Red-lamp (sweet cherry) (Wang et al., 2016), Actinidia sp. (kiwifruit) (Zhu et al., 2016), Paeonia lactiflora (peony) (Gress et al., 2017). Experimental hosts include Nicotiana cavicola (Guardo et al., 2009), N. occidentalis and N. benthamiana (Vives et al., 2008b).
Symptoms: Citrus leaf blotch virus causes symptomless infection in most citrus species and cultivars (Vives et al., 2008a). However, CLBV (and the isolate, DMV) induce chlorotic blotching or mottling in ‘Dweet’ tangor and stem pitting ‘Etrog’ citron. Although CLBV does not induce bud union crease on trifoliate rootstock (Vives et al., 2008a), it has been found to be usually associated with abnormal bud union on citrange or citrumelo rootstock. A different pathogen or interaction of CLBV with a different pathogen is likely the cause of bud union crease and vein clearing symptoms (Vives et al., 2005).
Damage Potential: Citrus leaf blotch virus causes chlorotic leaf blotching in ‘Dweet’ tangor and stem pitting in Etrog citron. Although it does not induce bud union crease in several citrus species it is usually associated with bud union crease symptoms in citrange and citrumelo rootstocks and therefore, an interaction between CLBV and other agent(s) cannot be ruled out. There are no reports of yield losses due to CLBV and the virus can cause symptomless infections in most citrus species and cultivars. In California, CLBV (aka DMV) is a regulated pathogen and its distribution is unknown or at best likely to be of low incidence. CLBV (aka DMV) was not reported from any commercial citrus production sites in California nor was it observed to produce any economic losses (Krueger et al., 2012). However, in certain scion-rootstock combinations using ‘Dweet’ tangor and Etrog citron rootstocks there may be a potential for disease development due to CLBV.
Transmission: Citrus leaf blotch virus is transmitted in citrus by grafting and seed. CLBV dispersal occurs primarily by propagation of infected buds. Low rates of seed transmission in at least three citrus species and hybrid, ‘Troyer’ citrange (Citrus sinensis x Poncirus trifoliata), ‘Nagami’ kumquat (Fortunella margarita) and sour orange (C. aurantium), has been demonstrated (Guerri et al., 2004). Also, CLBV has been mechanically transmitted to Nicotiana cavicola (Guardo et al., 2009), by sap inoculation to N. occidentalis and N. benthamiana (Vives et al., 2008b), and transmitted from citrus to citrus by contaminated knife blades (Roistacher et al., 1980). The virus is not transmitted by vectors (Galipienso et al., 2000).
Worldwide Distribution: Asia: China, Japan; Europe: Italy, Spain; North America: USA, Cuba; Oceania: New South Wales (Australia), New Zealand (Cao et al., 2017; Gress et al., 2017; Guardo et al., 2007; Harper et al., 2008; Hernández-Rodríguez, 2016; Navarro et al., 1984; Roistacher & Blue, 1968; Vives et al., 2002; Wang et al., 2016).
Official Control: Citrus leaf blotch virus is on the ‘Harmful Organism’ list for Uruguay (USDA PCIT, 2018). CLBV (aka DMV) is a regulated pathogen in California’s mandatory Citrus Nursery Stock Pest Cleanliness Program (CCR, Title 3, Division 4, Chapter 4, Subchapter 6, Section 3701).
California Distribution: The distribution in California is unknown. If at all present, it is likely to be only at a low incidence (Kreuger et al., 2005, 2012. See: ‘Background’).
California Interceptions: No official interceptions have been reported.
The risk Citrus leaf blotch virus would pose to California is evaluated below.
1) Climate/Host Interaction: Although the distribution of Citrus leaf blotch virus in California, is presently unknown and is likely to be only at a low incidence (Kreuger et al., 2012), if not regulated, it may be possible for the pathogen to have a widespread establishment in symptomatic and non-symptomatic infected citrus varieties in commercial citrus-growing regions of the State.
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: The natural host range is limited primarily to Citrus Other hosts include sweet cherry and kiwifruit reported from China and peony reported from Arkansas and Oregon. Experimental hosts include, Nicotiana cavicola, N. occidentalis and N. benthamiana.
Evaluate the host range of the pest.
Score: 1
– 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 leaf blotch virus has high reproduction within its plant host, although unevenly distributed within infected plants. It is transmitted by grafting, seed, and mechanically. Its ability for long distance spread through infected seed render it a high rating for dispersal.
Evaluate the natural and artificial dispersal potential of the pest.
Score: 3
– 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: Citrus leaf blotch virus is a regulated pathogen under California’s mandatory Citrus Nursery Stock Pest Cleanliness Program. Under this program any citrus stock found positive for the pathogen would be eliminated before release for commercial planting. This pathogen causes chlorotic leaf blotching in ‘Dweet’ tangor and stem pitting in Etrog citron. Although it does not induce bud union crease in several citrus species, it is usually associated with bud union crease symptoms in citrange and citrumelo rootstocks and therefore, an interaction between CLBV and other agent(s) cannot be ruled out. There are no reports of yield losses due to CLBV and the virus can cause symptomless infections in most citrus species and cultivars. Researchers have stated that CLBV has not been reported from commercial citrus production sites in California nor was it observed to cause any economic losses. If citrus stock were not regulated, it is likely that in certain scion-rootstock combinations using ‘Dweet’ tangor and Etrog citron rootstocks there may be a potential for disease development due to CLBV. In such a case, it is estimated that CLBV could lower crop yield and value and trigger the loss of markets.
Evaluate the economic impact of the pest to California using the criteria below.
Economic Impact: 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: No environmental impact is expected, however, if not regulated, CLBV may impact home/urban plantings of citrus host plants.
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.
Add up the total score and include it here. (Score)
-Low = 5-8 points
–Medium = 9-12 points
-High = 13-15 points
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)
Evaluation is (0). While the distribution of CLBV in California is currently not known, there is no evidence that it is established within the State.
–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.
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 = 12
The in-state distribution of CLBV is not currently known. Also, the impact of infection related to crop damage and losses is not known.
Based on the evidence provided above the proposed rating for Citrus leaf blotch virus is B.
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John J. Chitambar, Primary Plant Pathologist/Nematologist, California Department of Food and Agriculture, 3294 Meadowview Road, Sacramento, CA 95832. Phone: 916-262-1110, plant.health[@]cdfa.ca.gov.
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