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Posted by ka
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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.
Cao, M. J., Y. -Q. Yu, X. Tian, F. Y. Y. and, R. H. Li and C. Y. Zhou. 2017. First report of Citrus leaf blotch in lemon in China. Plant Disease 101: 8. https://doi.org/10.1094/PDIS-10-16-1500-PDN
Galipienso, L., L. Navarro, J. F. Ballester-Olmos, J. Pina, P. Moreno, and J. Guerri. 2000. Host range and symptomatology of a graft transmissible pathogen causing bud union crease of citrus on trifoliate rootstocks. Plant Pathology 49: 308–314.
Galipienso, L., M. C. Vives, P. Moreno, R. G. Milne, L. Navarro and J. Guerri. 2001. Partial characterization of Citrus leaf blotch virus, a new virus from Nagami kumquat. Archives of Virology 146: 357–368.
Gress, J. C., S. Smith, and I. E. Tzanetakis. 2017. First report of Citrus leaf blotch virus in peony in the U.S.A. Plant Disease 101: 637. https://doi.org/10.1094/PDIS-08-16-1218-PDN
Guardo, M., G Sorrentino, T. Marletta and A. Carusa. 2007. First report of Citrus leaf blotch on kumquat in Italy. Plant Disease 91: 104.
Guardo, M., O. Potere, M. A. Castellano, V. Savino and A. Caruso. 2009. A new herbaceous host for Citrus leaf blotch virus. Journal of Plant Pathology 91: 485-488.
Guardo, M., G. Sorrentino and A. Caruso. 2015. Characterization and incidence of Citrus leaf blotch virus in Southern Italy. 12th International Citrus Congress – International Society of Citriculture. Acta Horticulturae 1065: 825-83.
Hajeri, S., C. Ramadugu, M. Keremane, G. Vidalakis and R. Lee. 2010. Nucleotide sequence and genome organization of Dweet mottle virus and its relationship to members of the family Betaflexiviridae. Arch Virol 15: 1523-1527. DOI 10.1007/s00705-010-0758-1
Harper, S. J., K. M. Chooi and M. N. Pearson. 2008. First report of Citrus leaf blotch virus in New Zealand. Plant Disease 92: 1470. https://doi.org/10.1094/PDIS-92-10-1470C
Hernàndez-Rodríguez, L., J. M. Pérez-Castro, G. García-García, P. Luis Ramos-González, V. Zamora-Rodríguez, Xenia Ferriol-Marchena, Inés Peña-Bárzaga and L. Batista-Le Riverend. 2016. Citrus leaf blotch in Cuba: first report and partial molecular characterization. Tropical Plant Pathology 41: 147. https://doi.org/10.1007/s40858-016-0078-4
Krueger, R. R., J. A. Bash and R. F. Lee. 2005. Phytosanitary status of California citrus. International Organization of Citrus Virologists Conference Proceedings (1957-20), 16 (16): 468-472. https://escholarship.org/uc/item/3667q9qn
Krueger, R. R., J. A. Bash and R. F. Lee. 2012. Dweet mottle virus and Citrus leaf blotch virus. http://ucanr.edu/blogs/blogcore/postdetail.cfm?postnum=7112
Navarro, L., J. A. Pina, J. F. Ballester-Olmos, P. Moreno and M. Cambra. 1984. A new graft transmissible disease found in Nagami kumquat. In: Timmer L. W., and J. A. Dodds (eds) Proceedings of the 9th Conference of the International Organization of Citrus Virologists, IOCV, Riverside, pp 234–240.
Roistacher, C. N., and R. L. Blue. 1968. A psorosis-like virus causing symptoms only on ‘Dweet’ tangor. International Organization of Citrus Virologists Conference Proceedings (1957-2010), 4(4): 13-18.
Roistacher, C. N., E. M. Nauer and R. C. Wagner. 1980. Transmissibility of cachexia, Dweet mottle, psorosis and infectious variegation viruses on knife blades and its prevention. Proceedings of the 8th Conference of the International Organization of Citrus Virologists, IOCV, Riverside 1980: 225-229.
USDA PCIT. 2018. USDA Phytosanitary Certificate Issuance & Tracking System. Retrieved March 15, 2018. 3:25:54 pm CDT. https://pcit.aphis.usda.gov/PExD/faces/ReportHarmOrgs.jsp.
Vives, M. C., L. Galipienso, L. Navarro, P. Moreno and J. Guerri. 2001. The nucleotide sequence and genomic organization of Citrus leaf blotch virus: Candidate type species for a new virus genus. Virology 287: 225-233.
Vives, M. C., L. Galipienso, L. Navarro, P. Moreno and J. Guerri. 2002. Citrus leaf blotch virus: a new citrus virus associated with bud union crease on trifoliate rootstocks. International Organization of Citrus Virologists Conference Proceedings (1957-2010), 15 (15): 205-212.
Vives, M. C., L. Rubio, L. Galipienso, L. Navarro, P. Moreno and J. Guerri. 2002. Low genetic variation between isolates of Citrus leaf blotch virus from different host species and different geographical origins. Journal of General Virology 83: 2587–2591.
Vives M. C., J. A. Pina, J. Juarez, L. Navarro, P. Moreno and J. Guerri. 2005. Dweet mottle disease is probably caused by Citrus leaf blotch virus. 16th Conference of the International Organization of Citrus Virologists Conference Proceedings (1957-2010), 15 (16): 251-256.
Vives, M. C., S. Martin, S. Ambros, A. Renovell, L. Navarro, J. A. Pina, P. Moreno, J. and J. Guerri. 2008a. Development of a full-genome cDNA clone of Citrus leaf blotch virus and infection of citrus plants. Molecular Plant Pathology 9:787–797.
Vives, M. C., P. Moreno, L. Navarro and J. Guerri. 2008b. Citrus leaf blotch virus. In: Rao, G. P., A. Myrta and K. Ling (eds). Characterization, Diagnosis and Management of Plant Viruses, vol. 2. Pp. 55-67. Studium Press, Houston, TX, USA.
Wang, J., D. Zhu, Y. Tan, X. Zong, H. Wei and Q. Liu. 2016. First report of Citrus leaf blotch virus in sweet cherry. Plant Disease 100:1027.
Zhu, Chen-xi, Wang, Guo-ping, Zheng, Ya-zhou, Yang, Zuo-kun, Wang, Li-ping, Xu, Wen-xing and N. Hong. 2016. RT-PCR detection and sequence analysis of coat protein gene of Citrus leaf blotch virus infecting kiwifruit trees. Acta Phytopathologica Sinica, 46 (1): 11.
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 December 15, 2017, Cucumber green mottle mosaic virus (CGMMV) was detected in a watermelon seed sample submitted by the USDA to the CDFA Plant Pathology Lab, and collected from a seed company’s storage facility outside of California. The seed crop was produced in California. The seed company had originally identified the pathogen and reported its findings to the USDA. An official identification of CGMMV was made by Tongyan Tian, CDFA plant pathologist. Subsequent investigations are currently underway. CGMMV is a Federal Actionable Pathogen regulated by USDA. Currently, both agencies consider CGMMV a quarantine pathogen that is temporary, transitional and under eradication, and therefore, not established within California or anywhere else in the United States. The current status and rating for the pathogen is reassessed here.
Background: Cucumber green mottle mosaic virus is an economically important, seed transmitted pathogen known to cause significant losses in cucurbitaceous crop production in many cucurbit growing regions globally. All cucurbits are susceptible to the virus, although some are more tolerant than others (Falk et al., 2017).
Cucumber green mottle mosaic virus was originally described from the United Kingdom in 1935. Since then, it has spread to several other regions mostly within Europe, Asia and the Middle East, most likely due to its seed-borne nature and trade of cucurbit seed from CGMMV-infected regions to non-infected regions globally. CGMMV has also been recorded in Nigeria, Africa (Falk et al., 2017) and a possible detection of CGMMV in melon was reported from Brazil, South America, however, this record has not been confirmed (Choudhury & Lin, 1982).
The pathogen was first reported from North America in 2013, from California, USA and from Alberta, Canada. A detailed account of its first and subsequent detections in California is given below (see ‘Detections in California’). The first report of CGMMV in Alberta, Canada, was of infected mini-cucumber crops grown in greenhouse. The disease had been previously found in greenhouses in Ontario, British Columbia (Ling et al., 2014; Zhang et al., 2014). In 2014, CGMMV was reported for the first time from Australia on detection of the pathogen in commercial farm-grown watermelon plants in the Northern Territory, and in 2015 and 2016 was subsequently confirmed in Queensland and Western Australia respectively (QDAF, 2017).
Biology: The virus is a species in the genus Tobamovirus (to which also belongs the well-known Tobacco mosaic virus). The species has a positive single-stranded RNA genome and coat protein, comprised in rod-shaped particles (virions). Several strains or isolates of CGMMV have been reported from different countries. All strains of the virus are extremely stable in plant sap. Infectivity is lost at 86-100 C (Type strain at 90 C) depending on viral strain. In California, although the precise source or origin of CGMMV has not been determined, research showed that the 2013 detection in Yolo County and the 2014 detections in commercial seedless watermelon production fields represented two separate introductions, as genetic analysis of those two isolates were distinct from each other (Falk et al., 2017). The California 2013 CGMMV isolate showed 95% DNA sequence identity to those isolates reported from Russia, Spain, and Israel (Tian et al., 2014), whereas, the California 2014 CGMMV isolates and the Canada CGMMV isolates showed very similar DNA sequence identity, thereby, suggesting that they may have originated from the same source (Falk et al., 2017). The Canada CGMMV isolate showed strong sequence identity to the CGMMV Asian isolates thereby, suggesting their likely Asian origin (Zhang et al., 2014; Ling et al., 2015).
Detections in California: In the USA, cucumber green mottle mosaic virus has only been detected in California, from 2013 to 2017. An up-to-date account is given of those detections and subsequent regulatory actions.
In 2013, the Cucumber green mottle mosaic virus (CGMMV) was detected in a melon field (Cucumis melo var. Saski) in Yolo County during a phytosanitary inspection for seed production. The pathogen was identified by Tongyan Tian, CDFA Plant Pathologist, and confirmed by the USDA APHIS. This detection marked the first record of the pathogen in California and in the United States (Tian et al., 2014; USDA APHIS, 2013; CDFA-PEA, 2013). Three contiguous fields planted to cucumber (2 fields) and watermelon (1 field), were also determined as positive for CGMMV. Subsequent trace back investigations revealed that the source seed for the Yolo County melon site was grown in a seed lot in Sutter County in 2012 and later, was found positive for CGMMV. The 2013 trace back also revealed that in 2012, two sites in Sutter County produced a total of 6 melon, watermelon and cucumber seed lots, of which site 1 was positive for CGMMV in all three cucurbit hosts while site 2 was negative. Those two sites are currently planted to non-hosts of CGMMV, and in 2013, volunteer cucumber plants in site 1 tested negative for CGMMV. Two foreign sources of melon and cucumber seed lots planted in the two Sutter County sites were identified as Chile and Romania: no (melon) seed remained for testing from the Chilean source and the Romanian cucumber seed tested positive for CGMMV. As for the 2013 Yolo County CGMMV positive site, County and State approved abatement measures were implemented. Eventually, wheat, a non-host, was grown at the site and in 2014, volunteer melon plants tested positive, while volunteer watermelon plants were negative. Monitoring of volunteer plants was implemented and those in the field are treated with herbicide and biodegraded. Furthermore, in 2013, approximately 120 trace forward seed lots were evaluated for risk of potential infection with CGMMV. Pathways identified as possible risk links for potential CGMMV infection were source seed, shared irrigation, proximity to a positive detection, mechanical transmission (equipment and workers), and seed processing operational steps. Trace-forward investigations revealed that 2012 Sutter County melon seeds infested with CGMMV had been shipped to Romania and Africa. Thirty-four trace forward and trace back seed lots were sampled and tested for CGMMV of which 3 were positive for the pathogen. In 2014, additional cucumber seed lots belonging to the 2013 trace forward lots in Sutter County tested negative for CGMMV.
In 2014, during August and September, CGMMV was detected in watermelon plant samples collected from seven watermelon production fields in Fresno, Kern, and San Joaquin Counties. The CDFA did a trace-back to the seed lots that were linked to the CGMMV-positive fields, but found those seed lots to be negative for the pathogen. Subsequently, the seeds were traced back to the transplant nursery and CDFA theorized that the seed lots were cross contaminated at the transplant nursery. The CGMMV-positive watermelon fields were placed on a regulatory hold (quarantine) and an abatement order was issued to growers requiring; non-host planting, equipment sanitation, other bio-security measures, and monitoring for the virus for a period of two years (Schnabel, 2017).
In 2016, during February, a seed company reported its detection of CGMMV in imported melon seed. Consequently, the seed company voluntarily destroyed the seed lots by deep burial at a local landfill. Later, in June 2016, a seed company reported its detection of CGMMV in seed produced in Sutter County The field had already been disked and planted with rice at the time of the report. Nevertheless, cucurbit volunteers from the field and adjacent fields were sampled by the County and tested negative for the virus by CDFA. The field continues to be monitored and planted to a non-host crop. The CGMMV-positive seeds which were stored at a facility outside of California, were seized by the USDA and destroyed by incineration. Then, in October 2016, a seed company reported its detection of CGMMV in watermelon seed produced in Yolo County. At the time of testing and reporting, the section of the field that produced the positive detection, was already fallow. The seed company has maintained the field as fallow and will continue to notify CDFA of any volunteers, which if present, will be sampled in spring of 2018 by CDFA. Also, the seed was voluntarily destroyed and appropriate sanitation and biosecurity measures have been implemented by the seed company (Schnabel, 2017).
In 2017, during March, a seed company reported its detection of CGMMV in watermelon seeds produced in Colusa County. The field had already been disked and was fallow at the time of the report. However, cucurbit volunteers and broadleaf weeds, present at the field site, were sampled and tested negative for the pathogen. The grower continues to use appropriate best management practices including, sanitation and biosecurity measures. The CGMMV-positive seeds which were stored outside of California, were seized by the USDA and destroyed by incineration. In October, a seed company reported its detection of CGMMV in a watermelon seed lot produced in Sutter County. The production field was fallow at the time of the report and any plant material recovered from the field tested negative for CGMMV. The field will be monitored next season and the grower will be implementing sanitary and biosecurity measures. The seed lot was seized and destroyed. Also, at that time, CGMMV was detected in Opo squash (Lagenaria siceraria) plants grown in a small farm in Fresno County. Fresno County issued a regulatory hold on the field as well as an abatement notice. No host crops will be grown at the site for the next two years. The associated seeds were collected for destruction by the County. In November, two different seed companies provided a total of four separate reports of the detection of CGMMV in watermelon seeds. The positive seed lots were produced in Sutter, Colusa, and Glenn Counties. Trace-investigations are currently underway for each detection. The fields were sampled and have tested negative for CGMMV. The fields will be monitored and sanitation and biosecurity measures will be implemented. Currently, the seed lots are on hold pending voluntary destruction (Schnabel, 2017).
Plant infection: CGMMV gains entrance into a plant through wounds, infects a few cells, moves from cell to cell (through plasmodesmata) colonizing the plant tissues and reaches the phloem where it travels systemically and infects the entire plant.
Hosts: All cucurbit species are susceptible to CGMMV. Main hosts include, Citrullus lanatus (watermelon), Cucumis melo (melon), C. sativus (cucumber), C. anguria (burr gherkin), Gladiolus hybrids (sword lily), Lagenaria siceraria (bottle gourd), Momordica charantia (bitter gourd), Cucurbita moschata (butternut squash), C. pepo (zucchini and button squash), C. maxima (squash), Luffa acutangula (angled luffa), L. cylindrical (smooth luffa), Benincasa hispida (winter melon), Cucumis metuliferus (horned melon), C. myriocarpus (prickly paddy melon), Citrullus colocynthis (bitter paddy melon), Trichosanthes cucumerina (snake gourd) (CABI, 2017; Falk et al., 2017). [Cech (1980) reported that the CGMMV caused apricot bare twig and unfruitfulness disease syndrome in Prunus armeniaca (apricot) only when co-infected with strawberry latent ringspot virus.]
Several experimental hosts have been tested and susceptible hosts are in three families namely, Chenopodiaceae, Cucurbitaceae and Solanaceae. CGMMV-indicator plant species include Chenopodium album ssp. amaranticolor, Datura stramonium, and Nicotiana benthamiana. Weeds species may be potential alternate hosts, however, currently, the role of alternate host plants in CGMMV epidemiology is not known (Falk, 2017). Potential CGMMV weed hosts include: Amaranthus retroflexus (red root or American pigweed), Chenopodium album (lambsquarter), Heliotropium europium (Helitrope), Portulaca oleracea (pigweed), Solanum nigrum (nightshade) and Cucumis myriocarpus (paddy melon) (Falk et al., 2017).
Symptoms: Plant symptoms may vary mainly depending on virus strain, host plant species/cultivar, plant part, time of plant growth, and environmental conditions. In general, plant symptoms may include leaf mosaic, mottling, distortion, vein clearing, and stunted growth; infected fruit can be mottled, discolored, distorted, internally discolored and deteriorated. Root systems may be reduced.
Some Asian cultivars of cucumber only show yield losses without showing leaf symptoms. In cucumber, the type strain causes leaf mottling, blistering and distortion, and stunted growth. Symptoms appear 7-14 days after infection. Usually no symptoms are produced on fruit, however, certain strains cause fruit mottling and distortion. On the other hand, the watermelon strain can cause slight leaf mottling and dwarfing in watermelons and necrotic lesions develop on the peduncle. Virus infection at fruit set or soon after can result in serious internal discoloration and decomposition in the fruit.
No symptoms are produced in CGMMV infected squirting cucumber (Ecballium elaterium) (CABI, 2017) – a plant native to Europe, North Africa and parts of Asia, grown sometimes for its ornamental and medicinal value. Not present in California (acc. to USDA Natural Resources Conservation Services). It is thought that infected weed species may be asymptomatic – however, this has yet to be proven.
Seed set or appearance is not affected by CGMMV and therefore, infected seed are indistinguishable from non-infected ones (Reingold et al., 2015, 2016).
Plant symptoms due to CGMMV are similar to those of other viruses in cucurbitaceous species. Therefore, it is difficult to definitively identify the virus solely by the symptoms its causes in host plants. For a definitive identification, serological, molecular and/or electron microscopy tests are needed.
Damage Potential: In commercial field or greenhouse environments, losses up to 100% can occur, although 40-80% losses are common (Falk et al., 2017). Yield losses of approximately 15% in Cucurbitaceous vegetable crops are reported (Shang et al., 2011). In Japan, considerable economic losses in watermelon have occurred. Severe symptoms in fruit including, fruit pulp deterioration, low sugar accumulation and flavor, and distortion make fruit unmarketable and non-consumable (CABI, 2017). In India 75%, 80% and 100% losses are reported in watermelon, muskmelon, and bottle gourd respectively. 5-16 % losses occur in cucumber yields and fruit quality. Increased costs in production of clean planting sites and stock can be expected. Furthermore, since the pathogen is seedborne in cucurbits, it could negatively impact export of cucurbit seeds.
Transmission: CGMMV is contagious and is transmitted by mechanical contact with contaminated sources. It can spread through foliage contact, when plants are handled during cultivation or through grafting, when infected rootstocks are used in watermelon or cucumber cultivation. It can survive on plant pruning equipment, clothing, hands, and machinery and be spread by agricultural practices and mechanical means (Reingold et al., 2016; USDA, 2017). It can be transmitted from infected plant debris in soil to uninfected plants via roots. The virus is very stable in the sap of infected plants and therefore, is able to remain active in plant debris in soil long after the death of host plant cells. Also, it is spread through untreated irrigation water and in recirculated greenhouse water. All of these can serve as sources of inoculum. The virus is also transmitted by pollen and seed of CGMMV-infected cucurbit plants (Liu et al., 2014) both on and within the seed coat (Hollings, et al., 1975). However, research has shown that the rate of CGMMV infection of seedlings developing from cucurbit seeds containing the pathogen, is typically 1-5% or less, under greenhouse conditions, thereby, indicating that cucurbit seeds may contain infectious CGMMV, but the virus is not always transmitted to developing seedlings (Falk, 2017). On the other hand, high seed-transmission rates of 76% from CGMMV-infected cucumber plants, have been reported (Liu et al., 2014).
Movement of infected seed appears to be the primary means for long-distance spread, whereas, the virus is spread locally through contact, infested crop residues, and irrigation water.
CGMMV is not spread from plant to plant by specific insect or nematode vectors. Experimentally, the cucumber leaf beetle Raphidopalpa fevicollis was shown to be a probable vector of CGMMV to test plants, whereas, the green peach aphid (Myzus persicae), the cotton aphid (Aphis gossypii) or cucumber leaf beetles (Aulacophora femoralis) did not transmit the virus (Rao & Varma, 1984).
Experimentally, CGMMV has been transmitted by dodder species (Hollings et al., 1975).
CGMMV was detected in cow dung manure and studies have demonstrated the ability of the virus to pass through the alimentary system of rodents without losing biological activity.
Worldwide Distribution: Asia: China, India, Iran, Israel, Japan, Republic of Korea, Lebanon, Myanmar, Pakistan, Saudi Arabia, Sri Lanka, Syria, Taiwan, Thailand, Turkey;
Africa: Nigeria; North America: Canada, USA (California: temporary, transitional, and under eradication); Europe: Austria, Bulgaria, Czechoslovakia (former), Denmark, Finland, Germany, Greece, Hungary, Latvia, Lithuania, Moldova, Netherlands, Norway, Romania, Russian Federation, Spain, Sweden, Ukraine, United Kingdom and Yugoslavia (former); Oceania: Australia (CABI, 2017; Ling & Li, 2013; Tesoriero et al., 2016).
An unconfirmed record of CGMMV is from Brazil, South America (CABI, 2017)
Official Control: Currently, the following countries include CGMMV on their ‘Harmful Organism’ lists: Chiles, China, Colombia, Ecuador, Georgia, Guatemala, Honduras, Indonesia, Japan, New Zealand, Nicaragua, Panama, Paraguay, Peru, Syrian Arab Republic, Thailand, and Timor-Leste (USDA PCIT, 2017).
In the USA, CGMMV is a Federal Actionable Pathogen of quarantine concern and is considered temporary, transitional and under eradication. Currently, CGMMV is an A-rated, quarantine actionable pathogen in California.
California Distribution: CGMMV is not established in California.
California Interceptions: There are no state reports of CGMMV detections in plant materials intercepted within or at points of entry in California.
The risk Cucumber green mottle mosaic virus would pose to California is evaluated below.
1) Climate/Host Interaction: Since its first detection in 2013, there have been repeated incidences of field detections that directly indicate that CGMMV is likely to establish a widespread distribution in all cucurbit-growing regions within 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: CGMMV has a moderate range of cucurbitaceous host plants which are commonly grown mostly in the warmest areas of California, such as the San Joaquin Valley, the Sacramento, Valley and the low desert valleys.
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: CGMMV is capable of high reproduction and widespread dispersal mainly as it is highly contagious and is easily transmitted through mechanical, plant and human contact, irrigation water and water in contact with infected crop debris. It can be widely dispersed over long distance through infected seed, and is highly stable and remains active in infected plant debris in soil.
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: CGMMV is capable of significantly lowering crop yield and value thereby, increasing crop production costs. It can result in the loss of markets through the imposition of quarantines by domestic and international trade partners, change in cultural practices, including adoption of a non-host crop period in infested and treated fields for 3-5 or more years, and alteration of delivery and distribution of irrigation water to and from infested fields. Furthermore, significant losses in seed and transplant production can result due to a CGMMV infestation.
Evaluate the economic impact of the pest to California using the criteria below.
Economic Impact: A, B, C, 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: Detection and establishment of CGMMV would significantly impact existing cultural practices, as well as those followed for home/urban gardening and ornamental production. Subsequently, it could result in the implementation of additional and costly official and home/urban 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. (Score)
-Low = 5-8 points
-Medium = 9-12 points
–High = 13-15 points
Total points obtained on evaluation of consequences of introduction to California = 14 (High)
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 ‘Not Established (0)’: Similar and subsequent to its original detection in 2013, all incidences of Cucumber green mottle mosaic virus detections (detailed above in ‘Detections in California’) have resulted in eradicative actions. The viral pathogen is, therefore, not considered as established in California and continues to be ‘transient, temporary and under eradication’.
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 = 14.
Currently, the precise origin or source of CGMMV introduction into the USA is not known for certain.
Based on the evidence provided above the proposed rating for Cucumber green mottle mosaic virus continues as A.
Abatement Notice. 2013. ( ) Seed Company, Cucumber green mottle mosaic virus (CGMMV) Acidovorax avenae subsp. citrulli (BFB) abatement notice. County of Yolo, John Young Agricultural Commissioner.
CABI 2017. Cucumber green mottle mosaic virus (white break mosaic) datasheet. Crop Protection Compendium. http://www.cabi.org/cpc/datasheet/16951
CDFA-PEA. 2013. Cucumber green mottle mosaic virus and Bacterial fruit blotch detection in California. Pest Exclusion Advisory no. 29-2013. California Department of Food and Agriculture, November 27, 2013.
Choudhury, M. M., and M. T. Lin. 1982. ‘Ocorrência de viroses em plantas de melão e abobrinha na região do sub-médio São Francisco’, EMBRAPA Pesquisa am Andamento, vol. 14, no. 4, pp. 1–2.
Falk, B. W., T. L. Pitman, B. Aegerter, and K-S. Ling. 2017. Recovery Plan for Cucumber green mottle mosaic virus. Plant Diseases That Threaten U. S. Agriculture Identified and Prepared for Under the National Plant Disease Recovery System. USDA ARS. https://www.ars.usda.gov/office-of-pest-management-policy/npdrs/ Last modified 3/7/2017.
Hollings M, Y. Komuro, and H. Tochihara. 1975. Descriptions of Plant Viruses No. 154. Wellesbourne, UK: AAB, 4 pp.
Ling, K. S., and R. Li. 2014. First report of cucumber green mottle mosaic virus infecting greenhouse cucumber in Canada. Plant Disease 98 (5): 701.
Liu, H. W., L. X. Luo, J. Q. Li, P. F. Liu, X. Y. Chen, and J. J. Hao. 2014. Pollen and seed transmission on Cucumber green mottle mosaic virus in cucumber. (Published online 17 April 2013.) Plant Pathology (2014) 63, 62-77.
Lovig, E. 2014. Email communication from E. Lovig, CDFA, to A. Morris and J. Chitambar, CDFA. Subject: Cucumber green mottle mosaic virus (CGMMV) and Bacterial fruit blotch (BFB) detections in California. Dated April 29, 2014.
NPAG. 2013. Cucumber green mottle mosaic virus (CGMMV). New Pest Advisory Group, Plant Epidemiology and risk Analysis Laboratory, Center for Plant Health Science & Technology, USDA-APHIS. NPAG Report 20130819.docx, August 19, 2013: 1-9.
QDAF. 2017. Cucumber green mottle mosaic virus. The State of Queensland Department of Agriculture and Fisheries, Queensland Government. https://www.daf.qld.gov.au/plants/health-pests-diseases/a-z-significant/cucumber-green-mottle-mosaic-virus# Last updated 01 March, 2017.
Shang, J., Y. Xie, X. Zhou, Y. Qian, and J. Wu. 2011. Monoclonal antibody-based serological methods for detection of Cucumber green mottle mosaic virus. Virology Journal 8:228.
Schnabel, D. 2017. Email from D. Schnabel, CDFA, to S. Brown and J. Chitambar, CDFA. Subject: CGMMV. Dated December 11, 2017, 7:16 am.
Reingold V., E. Lachman, A. Koren, and A. Dombrovsky. 2015. Seed disinfection treatments do not sufficiently eliminate the infectivity of Cucumber green mottle mosaic virus (CGMMV) on cucurbit seeds. Plant Pathology 64: 245-255.
Reingold V., E. Lachman, O. Beelausov, A. Koren, N. Mor, and A. Dombrovsky. 2016. Epidemiological study of Cucumber green mottle mosaic virus in greenhouses enables reduction of disease damage in cucurbit production. Annals of Applied Biology 168:29-40.
Technical Working Group Responses: Cucumber green mottle mosaic virus. October 28, 2013. United States Department of Agriculture, Animal and Plant Health Inspection Service, Plant Protection and Quarantine.
Tian, T., K. Posis, C. J. Maroon-Lango, V. Mavrodieva, S. Haymes, T. L. Pitman, and B. W. Falk. 2014. First report of Cucumber green mottle mosaic virus in melon in the United States. Plant Disease 98:1163.
USDA APHIS. July 25, 2013. Email communication from K. J. Handy, CAPS Database Manager, USDA APHIS PPQ, PDEP to R. A. Bailey (and other APHIS members) Director, PHPPS, CDFA. Subject: FW: confirmed id: Cucumber green mottle mosaic virus (CGMMV) detection in melon in CA – new US record.
USDA PCIT. 2017. USDA Phytosanitary Certificate Issuance & Tracking System. December 14, 2017, 3:49:31 pm CDT. https://pcit.aphis.usda.gov/PExD/faces/ReportHarmOrgs.jsp
Zhang, J. W., K-S. Ling, and R. Cramer. 2014. New Cucumber threat studied. https://www.greenhousecanada.com/inputs/crop-protection/march-april-2014-4021
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 March 21, 2016, two samples of diseased Lilium sp. (lily) plants exhibiting leaf spots, were collected from a nursery in San Luis Obispo County, during a regulatory nursery inspection by San Luis Obispo County Agricultural officials, and sent to the CDFA Plant Pathology Laboratory for analysis. Tongyan Tian, CDFA plant pathologist, identified two pathogens associated with the sample, namely, Freesia mosaic virus (FreMV) and Freesia sneak virus (FreSV). Freesia mosaic virus was assigned a temporary Q rating by the CDFA, whereas FreSV already has a permanent B rating. Subsequently, all infected propagative plant material was destroyed. The risk of infestation of FreMV in California is evaluated and a permanent rating is proposed here.
History & Status:
Background: Freesia mosaic virus is a plant virus belonging to the genus Potyvirus in the family Potyviridae, and is vectored by the potato aphid, Macrosiphum euphoribae and green peach aphid, Myzus persicae. Freesia mosaic virus (FreMV) was originally reported from Freesia refracta, in Lisse, the Netherlands, by Van Koot et al. in 1954 (Brunt, et al., 1996 onwards; Van Koot et al., 1954). This pathogen, along with few other plant virus pathogens, has been reported to naturally infect freesia plants (Van Koot et al., 1954; Bouwen, 1994). In the Netherlands, Freesia mosaic virus was frequently found in field samples of freesia plants with and without symptoms of freesia leaf necrosis disease and, more or less frequently in double infections with Freesia sneak virus in the same plants (Vaira et al., 2006; Meekes & Verbeek, 2011). Freesia leaf necrosis disease has been reported in Europe since the 1970s and double infections of FreMv and FreSV in freesia plants were first described as “severe leaf necrosis” or “complex disease” which is progressive and may cause death of plants before flowering (Van Dorst, 1973; Meekes & Verbeek, 2011). The natural occurrence of FreMV has also been found in Peruvian lily in Italy, and besides its spread in Europe, the pathogen has been reported from Freesia spp. in India, Australia, Korea, and New Zealand (Bellardi, 1992; Brunt et al., 1996 onwards; Kumar, et al., 2008; Jeong et al., 2014).
In the USA, Freesia mosaic virus was reported from infected Freesia spp. in Virginia in 2009 (Vaira et al., 2009). The pathogen was first detected in California, in symptomatic freesia plant samples collected during April 2014, from a nursery in San Luis Obispo County, and identified by Tongyan Tian, CDFA plant pathologist. Subsequently, all infected plant material was destroyed.
Hosts: Freesia spp. F. refracta, (common freesia; Iradaceae) and Alstroemeria sp. (Peruvian lily; Alstroemeriaceae). Freesia and Peruvian lily are monocots and although presently naturalized in several countries including the USA, both plant species are native to South Africa and South America respectively (Bellardi, 1992; Brunt et al., 1996 onwards). Freesia mosaic virus was also detected in Lily (Lilium sp.) by the CDFA (see ‘Initiating Event’) and is included as an associated host.
Symptoms: Symptoms of Freesia mosaic virus-infected freesia plants include mild chlorosis. The pathogen may also be present in symptomless plants (Brunt et al., 1996 onwards). Experimentally, Alstroemeria sp. plants that were mechanical inoculated FMV infested plant sap, failed to show symptoms three months after inoculation, although the virus was detected serologically (Bellardi, 1992).
Complex infections of Freesia mosaic virus and Freesia sneak virus may result in severe leaf necrosis showing symptoms of chlorotic spots and stripes that appear on the first leaf of freesia plants grown from corms, and later turn grey-brown and necrotic as the disease progresses rapidly often resulting in rot of corms, and death of plants before flower formation (Van Dorst, 1973).
Damage Potential: In California, nursery and private productions of freesia and lily plants may be impacted if infected with FreMV.
Transmission: In nature, Freesia mosaic virus is transmitted by the potato aphid, Macrosiphum euphorbiae and green peach aphid, Myzus persicae. It is also transmitted by mechanical inoculation and spread via infected nursery plants and propagative parts. The virus pathogen is not transmitted by seed, pollen or contact between plants (Brunt et al., 1996 onwards).
Worldwide Distribution: Asia: India, Korea; Europe: United Kingdom, Ireland, Italy, the Netherlands; North America: USA (Virginia); Australia; New Zealand (found, but with no evidence of spread) (Bellardi, 1992; Brunt, et al., 1996 onwards; Kumar et al., 2008; Jeong et al., 2014; Vaira et al., 2009).
Official Control: Freesia mosaic virus is on the ‘Harmful Organism List’ for Colombia, Georgia, Israel, Japan, Peru, and Taiwan (USDA-PCIT, 2016). Currently, FreMV has a temporary Q-rating in California.
California Distribution: San Luis Obispo (nursery).
California Interceptions: There have not been any interceptions of Freesia mosaic virus-infected plants entering California.
The risk Freesia mosaic virus would pose to California is evaluated below.
1) Climate/Host Interaction: Evaluate if the pest would have suitable hosts and climate to establish in California. Score:
– 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.
Risk is Medium (2) – Freesia mosaic virus is likely to establish wherever freesia and Peruvian lily and lily plants are grown in limited areas of California. These host plant species have limited production in state, mostly in the north coast and mountain regions, and few southern coast regions, as well as cultivated in nursery and private production sites – including home gardens.
2) Known Pest Host Range: Evaluate the host range of the pest. Score:
– Low (1) has a very limited host range.
– Medium (2) has a moderate host range.
– High (3) has a wide host range.
Risk is Low (1) – Freesia mosaic virus is limited to Freesia spp. (Iradaceae), Alstroemeria sp. (Alstroemeriaceae), and Lilum spp. (Liliaceae).
3) Pest Dispersal Potential: Evaluate the natural and artificial dispersal potential of the pest. Score:
– 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.
Risk is Medium (2) – Freesia mosaic virus has high reproductive potential. In nature, its spread to non-infected plants is through aphid vectors, Macrosiphum euphorbiae and Myzus persicae. It is also transmitted by mechanical inoculation and spread via infected nursery plants and propagative parts. The virus pathogen is not transmitted by seed, pollen or contact between plants.
4) Economic Impact: Evaluate the economic impact of the pest to California using the criteria below. Score:
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.
– 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.
Risk is High (3) – Incidents of Freesia mosaic virus infections could lower plant value resulting in loss in market sales of nursery-grown freesia and lily plants. The pathogen is vectored by the potato aphid and green peach aphid, Macrosiphum euphorbiae and Myzus persicae respectively.
5) Environmental Impact: Evaluate the environmental impact of the pest on California using the criteria below.
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.
Score the pest for Environmental Impact. Score:
– 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.
Risk is Medium (2) – Plant infections caused by Freesia mosaic virus are likely to have a minimal impact on the overall environment but may significantly impact home gardening and ornamental plantings. The pathogen may impact California State and federal endangered western lily (Lilium occidentale) and Pitkin Marsh lily (L. pardalinum ssp. pitkinense (ref: State and Federally listed endangered, threatened, and rare plants of California, July, 2015, California Department of Fish and Wildlife, Biogeographic Data Branch, California Natural Diversity Database).
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 Freesia mosaic virus to California = 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 not established. Freesia mosaic virus-infected freesia plants have only been detected in a contained nursery environment in California. Those plants were subsequently destroyed and therefore, the pathogen is not considered established in the State.
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 = 10.
Currently, the possible distribution of Freesia mosaic virus in California is not known. Future confirmed detection of its in-state presence and distribution may affect its overall score and alter its current proposed rating.
Based on the evidence provided above the proposed rating for Freesia mosaic virus is B.
Bellardi, M. G. 1992. Natural occurrence of Freesia mosaic virus in Alstroemeria sp. Plant Disease 76:643. DOI: 10.1094/PD-76-0643B.
Bouwen, I. 1994. Freesia leaf necrosis: some of its mysteries revealed. Virus Diseases of Ornamental Plants VIII, Acta Horticulturae 377: 311-318.
Brunt, A.A., K. Crabtree, M. J. Dallwitz, A. J. Gibbs, L. Watson, and E. J. Zurcher. (eds.) (1996 onwards). `Plant Viruses Online: Descriptions and Lists from the VIDE Database. Version: 16th January 1997.’ URL http://biology.anu.edu.au/Groups/MES/vide/
Jeong, M. I., Y. J. Choi, J. H. Joa, K. S. Choi, and B. N. Chung. 2014. First report of Freesia sneak virus in commercial Freesia hybrida cultivars in Korea. Plant Disease 95:162. http://dx.doi.org/10.1094/PDIS-05-13-0484-PDN.
Kumar, Y., V. Hallan, and A. A. Zaidi. 2008. First finding of Freesia mosaic virus infecting freesia in India. New Disease Reports 18:3. http://www.ndrs.org.uk/article.php?id=018003.
Meekes, E. T. M., and M. Verbeek. 2011. New insights in Freesia leaf necrosis disease. Proceedings XIIth IS on Virus Diseases of Ornamental Plants; Editors A. F. L. M. Derks et al. Acta Horticulturae 901, ISHA 2011.
USDA- PCIT. 2016. USDA Phytosanitary Certificate Issuance & Tracking System. June 6, 2016. https://pcit.aphis.usda.gov/PExD/faces/ReportHarmOrgs.jsp .
Vaira, A. M., V. Lisa, A. Costantini, V. Masenga, S. Rapetti, and R. G. Milne. 2006. Ophioviruses infecting ornamentals and a probable new species associated with a severe disease in Freesia. Proceeding XIth IS on Virus Diseases in Ornamentals, Ed. C. A. Chang. Acta Horticulturae 722, ISHA 2006.
Van Dorst, H. J. M. 1973. Two new disorders in freesias. Netherland Journal of Plant Pathology 79:130-137.
Van Koot, Y., D. H. M. van Slogteren, M. C. Cremer, and J. Camfferman. 1954. Virusverschijnselen in freesia’s. Tijdschrlfot over Planienziekten 60:157-192
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.
♦ 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
None. The risk of introduction of Squash vein yellowing virus to California is assessed and a permanent rating for SqVYV is herein proposed.
Background: In 2003 in Hillsborough County, Florida, an unknown virus was detected in squash plants (Cucurbita pepo) exhibiting vein yellowing symptoms and soon after in 2005, this virus was found to cause watermelon vine decline in watermelon plants in Florida (Webb et al., 2003; Adkins et al., 2007). In 2006, the virus was identified and characterized as a new species, Squash vein yellowing virus. SqVYV is a whitefly-transmitted member of the genus Ipomovirus in the family Potyviridae which induces necrosis of watermelon stems and petioles resulting in rapid wilt and death of plants at or near harvest. In the field, SqVYV is often detected in watermelon in mixed infections with other viruses (Adkins et al., 2013).
Squash vein yellowing virus was reported from California in 2015 following the fall of 2014 detection of diseased pumpkin plants grown from seed at the University of California Desert Research Extension Center in Holtville, California. Molecular analysis of pathogens associated with the diseased plants revealed mixed infections with the crinivirus Cucurbit yellow stunting disorder virus, the begomovirus Squash leaf curl virus and SqVYV. Symptoms of infection and association of a divergent strain of SqVYV were confirmed through pathogenicity trials and molecular diagnostic tests of infected pumpkin and squash plants. SqVYV-infected melon plants were also detected in commercial fields in the Imperial Valley (Batuman et al., 2015). Subsequently, during December 2014, official melon and pumpkin samples from the infected sites were collected by Imperial County Agricultural Commissioner’s staff and sent to CDFA Plant Pathology Laboratory for diagnosis. Tongyan Tian, CDFA plant pathologist, detected SqVYV from the samples using a RT-PCR protocol and sequence analysis. The detection of SqVYV in Imperial County marked the first report of an Ipomovirus in California (Batuman et al., 2015).
Hosts: The host range is limited to species in Cucurbitaceae with more dramatic symptoms produced in squash (inc. pumpkin) and watermelon. Plant hosts include two varieties of cucurbit weeds, namely, Momordica charantia (Balsam-apple) and Melothria pendula (creeping cucumber) (Adkins et al., 2008). The weeds may serve as reservoir hosts for SqVYV.
Symptoms: Initial symptoms consist of a slight yellowing of leaves. This is followed by browning and collapse of entire vines within weeks of the first symptoms. These symptoms appear as the fruit develops to a harvestable size. Infected fruit internally often exhibit discolored and necrotic blotches in the rind, discolored flesh (too red) and an off-taste (Baker et al., 2008). SqVYV-infected cucurbit weed hosts are asymptomatic (Adkins et al., 2008). In Puerto Rico, symptoms of watermelon vine decline on field-grown watermelon included leaf curling, mosaic, and internode necrosis. During the early stage of plant growth reduced vigor and general stunting occurred, and at the flowering stage, symptoms progressed to necrosis and wilting of vines (Acevedo, et al., 2013). Adkins et al. (2013) reported that symptoms of vine decline in watermelon appeared 12-16 days after inoculation regardless of plant age at time of inoculation and greenhouse or field location. However, younger watermelon plants exhibited more severe symptoms than older ones.
Damage Potential: In Florida, watermelon plants suffering from vine decline and fruit rot disease caused by SqVYV has resulted in severe losses in spring and fall plantings. During this period the disease may rapidly increase in incidence from 10 to >80% within a week (Adkins et al., 2007). The disease can result in total crop loss with collapsed vines and unmarketable fruit with discolored and necrotic rinds.
Transmission: SqVYV is transmitted by the whitefly Bemisia tabaci. The pathogen is not transmitted by aphids unlike other common cucurbit-infecting species of the family Potyviridae (Adkins et al., 2003). Experimentally, Adkins and others determined that whiteflies required 1-2 days to feed and acquire the virus from infected plants followed by 2 hours or 2 days to inoculate or transmit the virus to non-infected squash and watermelon plants. Transmission occurs in a semi-persistent mode by the whitefly which remains infective for 4-6 hours after acquiring the virus. Adkins et al. (2008) experimentally demonstrated that the whitefly vector was able to acquire SqVYV from inoculated cucurbit weed host Momordica charantia and subsequently transmit it to squash and watermelon to produce typical symptoms. While the virus has been artificially inoculated to plants under greenhouse conditions, the main mode of natural field transmission is through its whitefly vector.
Worldwide Distribution: North America: USA (California, Florida, Georgia, Indiana, South Carolina, Puerto Rico (Acevedo et al., 2013; Egel & Adkins, 2007; Adkins et al., 2013).
Official Control: Squash vein yellowing virus currently holds a temporary Q rating by the CDFA. No other official control for SqVYV has been reported.
California Distribution: Currently, Squash vein yellowing virus has only been detected in Imperial County.
California Interceptions: There are no official records of interceptions of Squash vein yellowing virus in California.
The risk Squash vein yellowing virus would pose to California is evaluated below.
1) Climate/Host Interaction: Evaluate if the pest would have suitable hosts and climate to establish in California. Score:
– 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.
Risk is Medium (2) – SqVYV has already been able to establish in Imperial County, southern California Its further spread to non-infected sites cultivated to cucurbits is limited by the distribution of its vector, Bemisia tabaci, which to date, has not been found in natural cooler climates of northern California counties.
2) Known Pest Host Range: Evaluate the host range of the pest. Score:
– Low (1) has a very limited host range.
– Medium (2) has a moderate host range.
– High (3) has a wide host range.
Risk is low (1) – The natural host range is limited to plant species in the family Cucurbitaceae (which are grown extensively in the lower Sacramento Valley and in limited production in San Joaquin and Imperial Valleys).
3) Pest Dispersal Potential: Evaluate the natural and artificial dispersal potential of the pest. Score:
– 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.
Risk is High (3) – The virus is able to thrive in climates that are favorable for its vector. Its potential for spread is always artificial being completely dependent on the distribution of its vector and infected plant materials. Therefore, factors that increase movement and activity of the vector and infected plants will also influence that of the virus.
4) Economic Impact: Evaluate the economic impact of the pest to California using the criteria below. Score:
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.
– 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.
Risk is High (3) – SqVYV infections could lower crop yield and value, increase production costs, trigger loss of market, and the virus is vectored by the whitefly, Bemisia tabaci which would require implementation of management strategies to minimize the risk of the introduction and establishment of the virus in non-infected regions within California.
5) Environmental Impact: Evaluate the environmental impact of the pest on California using the criteria below.
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.
Score the pest for Environmental Impact. Score:
– 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.
Risk is Medium (2) – Infestations of SqVYV could significantly impact home/urban gardening of cucurbit host plants resulting in the imposition of additional official or private treatment programs in order to prevent spread of the virus and virus-carrying whitefly vector.
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 SqVYV to California = (11).
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).
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 = 10
While SqVYV is established in the Imperial Valley and there have been no further reports of its spread to other intrastate regions, targeted surveys for the pathogen have not been conducted in other cucurbit production sites. The distribution and establishment of the virus is largely dependent on the distribution and established infestations of virus-carrying Bemisia tabaci. Subsequently, detections outside the Imperial Valley may alter the proposed rating for this virus pathogen.
Based on the evidence provided above the proposed rating for Squash vein yellowing virus is B.
Acevedo, V., J. C. V. Rodrigues, C. E. de Jensen, C. G. Webster, S. Adkins and L. Wessel-Beaver. 2013. First report of Squash vein yellowing virus affecting watermelon and bitter gourd in Puerto Rico. Plant Disease 97:1516.
Adkins S., T. G. McCollum, J. P. Albano, C. S. Kousik, C. A. Baker, C. G. Webster, P. D. Roberts, S. E. Webb and W. W. Turechek. 2013. Physiological effects of Squash vein yellowing virus infection on watermelon. Plant Disease 97:1137-1148.
Adkins, S., S.E. Webb, D. Achor, P. Roberts, and C.A. Baker. 2007. Identification and characterization of a novel whitefly-transmitted member of the family Potyviridae isolated from cucurbits in Florida. Phytopathology 97: 145-154.
Adkins, S.T., S. Webb, C. Baker, and C.S. Kousik. 2008. Squash vein yellowing virus detection using nested polymerase reaction demonstrates the cucurbit weed Momordica charantia is a reservoir host. Plant Disease 92: 1119-1123.
Baker, C., S. Webb and S. Adkins. 2008. Squash vein yellowing virus, causal agent of watermelon vine decline in Florida. Plant Pathology Circular No. 407, Florida Department of Agriculture and Consumer Services, Division of Plant Industry.
Egel, D. S. and S. Adkins. 2007. Squash vein yellowing virus identified in watermelon (Citrullus lanatus) in Indiana. Plant Disease, 91:1056.2.
Batuman, O., E. T. Natwick, W. M. Wintermantel, T. Tian, J. D. McCreight, L. L. Hladky, and R. L. Gilbertson. 2015. First report of an Ipomovirus infecting cucurbits in the Imperial Valley of California. Plant Disease 99:1042. http://dx.doi.org/10.1094/PDIS-12-14-1248-PDN.
Webb, S. E., E. Hiebert and T. A. Kucharek. 2003. Identity and distribution of viruses infecting cucurbits in Florida. Phytopathology 93:S89.
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
None.
Background: Freesia sneak virus (FreSV) is associated with freesia leaf necrosis disease. The disease has been reported in Europe since the 1970s. Although FreSV has been most closely correlated with freesia leaf necrosis symptoms in freesia plants, other species within the same genus may also be correlated (e.g., Freesia mosaic virus FreMV) and, therefore, the causal agent(s) is/are still being determined (Bouwen, 1994; Meekes & Verbeek, 2011).
Freesia sneak virus is a plant virus belonging to the genus Ophiovirus in the family Ophioviridae. Freesia sneak virus is soil-borne and vectored by the soil-borne fungus, Olpidium brassicae. Initially, the virus was provisionally called Freesia Ophiovirus, but is now known as Freesia sneak virus (Vaira et al., 2006).
In the USA, Freesia sneak virus was first reported from infected Freesia spp. in Virginia in 2009 (Vaira et al., 2009). The pathogen was detected in California, in symptomatic freesia plant samples collected during April 2014, from a nursery in San Luis Obispo County. The pathogen was identified by Tongyan Tian, CDFA plant pathologist. Subsequently, all infected plant material was destroyed.
Hosts: Freesia spp. (Iradaceae) and Lachenalia spp. (Hyacinthaceae) (Jeong, et al., 2014; Meekes & Verbeek, 2011; Vaira et al., 2007, 2009). Both hosts are monocots native to South Africa.
Symptoms: Symptoms may be affected by environmental conditions (Vaira et al., 2006).
Freesia leaf necrosis disease mainly affects the leaves exhibiting chlorotic spots and stripes that start at the leaf tip and usually spread over the entire leaf. Later these chlorotic spots turn grey-brown and become necrotic. Mildly infected plants show light chlorotic symptoms only on the lower leaves. Flowers and corms do not seem to be affected by the disease (Van Dorst, 1973; Bouwen, 1994; Meekes & Verbeek, 2011).
Damage Potential: In detection surveys conducted in Korea, Freesia sneak virus was detected from 71.7% of 138 plants tested (Jeong et al., 2014). Infection rates of 10-25% percent of plants shipped to the USA have been reported (Hansen, 2008; Vaira et al., 2009). In California, nursery and private productions of freesia and lachenalia plants, in particular, may be impacted if infected with Freesia sneak virus.
Transmission: in nature, Freesia sneak virus is vectored by the soil-borne fungus, Olpidium brassicae, and not by mechanical transmission. Resting spores of O. brassicae are very persistent and can survive for more than twenty years in soil without losing the capacity to transmit the disease (Meekes & Verbeek, 2011). Therefore, spread of FreSV is also through movement of contaminated soils and plants.
Worldwide Distribution: Asia: Korea; Africa: South Africa; Europe: Northern Europe including the Netherlands, Italy; North America: USA (Virginia) (Jeong et al., 2014; Meekes & Verbeek, 2011; Vaira, et al., 2007, 2009).
Official Control: None reported.
California Distribution: San Luis Obispo (nursery).
California Interceptions: There have not been any interceptions of Freesia sneak virus-infected plants entering California.
The risk Freesia sneak virus would pose to California is evaluated below.
1) Climate/Host Interaction: Evaluate if the pest would have suitable hosts and climate to establish in California. Score:
– 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.
Risk is Medium (2) – Freesia sneak virus is likely to establish wherever freesia and lachenalia plants are grown in limited areas of California. Freesia has limited production in state and is naturalized mostly in the north coast region, as well as cultivated in nursery and private production sites – including home gardens. Lachenalia is grown mainly in nurseries and in private productions as a hobbyist’s plant.
2) Known Pest Host Range: Evaluate the host range of the pest. Score:
– Low (1) has a very limited host range.
– Medium (2) has a moderate host range.
– High (3) has a wide host range.
Risk is Low (1) – Freesia sneak virus is limited to Freesia spp. (Iradaceae) and Lachnenalia spp. (Hyacinthaceae).
3) Pest Dispersal Potential: Evaluate the natural and artificial dispersal potential of the pest. Score:
– 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.
Risk is Medium (2) – Freesia sneak virus has high reproductive potential. In nature, its spread to non-infected plants is dependent on the presence of the soil-borne fungus vector, Olpidium brassicae. Resting spores of O. brassicae are very persistent and can survive for more than twenty years in soil without losing their viability. Therefore, FreSV is also spread through movement of contaminated soils and plants. The pathogen is not mechanically transmitted.
4) Economic Impact: Evaluate the economic impact of the pest to California using the criteria below. Score:
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.
– 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.
Risk is High (3) – Incidents of Freesia sneak virus infections could lower plant value resulting in loss in market sales of nursery-grown freesia and lachenalia plants. The pathogen is vectored by the soil fungus, Olpidium brassicae.
5) Environmental Impact: Evaluate the environmental impact of the pest on California using the criteria below.
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.
Score the pest for Environmental Impact. Score:
– 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.
Risk is Low (1) – Plant infections caused by Freesia sneak virus are likely to have a minimal impact on the overall environment but may significantly impact home gardening and ornamental plantings.
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 Freesia sneak virus to California = 9.
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 not established. Freesia sneak virus-infected freesia plants have only been detected in a contained nursery environment in California. Those plants were subsequently destroyed and therefore, the pathogen is not considered established in the State.
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
None.
Based on the evidence provided above the proposed rating for Freesia sneak virus is B.
Bouwen, I. 1994. Freesia leaf necrosis: some of its mysteries revealed. Virus Diseases of Ornamental Plants VIII, Acta Horticulturae 377: 311-318.
Hansen, M. A. 2008. Freesia sneak virus – a new find for the United States. Virginia Cooperative Extension, Virginia Tech Plant Disease Clinic: https://www.cals.ncsu.edu/plantpath/activities/societies/ornamental/2008_talks/freesia_sneak_virus_4.pdf.
Jeong, M. I., Y. J. Choi, J. H. Joa, K. S. Choi, and B. N. Chung. 2014. First report of Freesia sneak virus in commercial Freesia hybrida cultivars in Korea. Plant Disease 95:162. http://dx.doi.org/10.1094/PDIS-05-13-0484-PDN.
Meekes, E. T. M., and M. Verbeek. 2011. New insights in Freesia leaf necrosis disease. Proceedings XIIth IS on Virus Diseases of Ornamental Plants; Editors A. F. L. M. Derks et al. Acta Horticulturae 901, ISHA 2011.
Vaira, A. M., V. Lisa, A. Costantini, V. Masenga, S. Rapetti, and R. G. Milne. 2006. Ophioviruses infecting ornamentals and a probable new species associated with a severe disease in Freesia. Proceeding XIth IS on Virus Diseases in Ornamentals, Ed. C. A. Chang. Acta Horticulturae 722, ISHA 2006.
Vaira, A. M., R. Kleynhans, and J. Hammond. 2007. First report of Freesia sneak virus infecting Lachenalia cultivars in South Africa. Plant Disease 91:770. http://dx.doi.org/10.1094/PDIS-91-6-0770A.
Vaira, A. M. , M. A. Hansen, C. Murphy, M. D. Reinsel, and J. Hammond. 2009. First report of Freesia sneak virus in Freesia sp. in Virginia. Plant disease, 93:965. http://dx.doi.org/10.1094/PDIS-93-9-0965B.
Van Dorst, H. J. M. 1973. Two new disorders in freesias. Netherland Journal of Plant Pathology 79:130-137.
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.
♦ 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
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