Tomato Yellow Leaf Curl Virus (TYLCV)

California Pest Rating for
Tomato Yellow Leaf Curl Virus (TYLCV)
Pest Rating: B

 


PEST RATING PROFILE
Initiating Event: 

The risk of infestation of Tomato yellow leaf curl virus (TYLCV) in California is evaluated and a permanent rating is proposed.

History & Status:

Background:    During the early 1960s in Israel, Tomato yellow leaf curl virus was the name first given to diseased tomatoes that in 1959 were found to be infected by an agent identified as a whitefly-transmitted viral agent in the Jordan Valley, Israel.  Since then and in less than 25 years, TYLCV spread worldwide.    TYLCV belongs to the genus Begomovirus in the Family Geminiviridae – which includes whitefly transmitted viruses.  The pathogen is accurately identified by the analysis of DNA sequences. The Israel strain was isolated in 1988 and was the first one to be sequenced in 1991. Sequence comparisons of different geographical isolates revealed that TYLCV is actually a complex of begomovirus species that affect tomato.  Subsequently, begomoviruses affecting tomato were separated into several groups and named accordingly.  Tomato yellow leaf curl virus is the name of the virus isolated in Israel (CABI, 2014; Nakhla & Maxwell, 1998; Fauquet et al., 2000). Seven different species belonging to the Tomato yellow leaf curl virus complex have been identified.

Tomato yellow leaf curl virus was identified in 2007 for the first time from infected tomato plants grown in a greenhouse in Brawley, Imperial County, California (Rojas et al., 2007).  Since then the pathogen has been detected in commercial fields, nurseries and private residences within Imperial and Riverside counties.

Hosts: Solanum lycopersicum (tomato) is the major host.  Other hosts include diagnostic experimental plant species belonging to several families: Datura stramonium, Lycopersicon esculentum, Nicotiana glutinosa, N. benthamiana, Phaseolus vulgaris, Petunia hybrida, and Eustoma grandiflorum (lisianthus).   Other cultivated minor hosts include abelmoschus esculentus (okra), C. annum (bell pepper), C. frutescens (cayenne/chili pepper), Nicotiana tabacum (tobacco), Physalis philadelphica (tomatillo), and Vigna unguiculata (cowpea).  Weeds and other wild hosts include Acalypha australis, Artemisia annua, Ageratum conyzoides (billy goat weed), Convolvulus (morning glory), Chenopodium murale (nettleleaf goosefoot), Cuscuta europaea (European dodder), Datura stramonium (jimsonweed), Malva parviflora (pink cheeseweed), Moringa oleifera (horse-radish tree), Sida acuta (sida), Solanum elaegniflolium (silverleaf nightshade) and S. nigrum (black nightshade) (CABI, 2014; VIDE, 1996; EPPO 2014).

In a survey in Cyprus, Papayiannis et al., (2011) found that 49 plant species were TYLCV hosts belonging to 15 families, namely, Amaranthaceae, Chenopodiaceae, Compositae, Convolvulaceae, Cruciferae, Euphorbiaceae, Geraniaceae, Leguminosae, Malvaceae, Orobanchaceae, Plantaginaceae, Primulaceae, Solanaceae, Umbelliferae and Urticaceae.

Symptoms:  The disease is easily identified when tomato are infected at seedling stage.

Young leaves and shoots are severely stunted resulting in bushy and upright seedling growth.  Leaves exhibit the most diagnostic symptoms of small leaves, upward and inward rolling of the margins, interveinal and marginal yellowing, distinct stunting and often a bushy appearance.  Flowers either do not develop or fall off.  When plants are infected early, they lose vigor and fruit production is reduced or stopped. When infected at a later stage of development, fruit already formed continue to develop more or less normally however, additional fruit are not produced.

Leaf curl symptom is not limited to tomato but also produced in TYLCV-infected varieties of common bean and lisianthus (Eustoma grandiflorum).

Most wild tomato species include members that are either immune or symptomless carriers of the virus. Certain weeds are also asymptomatic (Malva parviflora). It is not known how well whiteflies acquire virus from symptomless hosts (Gilbertson, 2008). Plants used to rear whiteflies are immune to the virus (CABI, 2014).

Damage Potential:  TYLCV is one of the most damaging pathogens of tomato and losses up to 100% in commercial fruit production in fields are not uncommon (UCIPM, 2008).  Yield loss results in fewer numbers of fruit produced.  Fruit present at time of infection remain on the plant but few will set more or less normally.  It has been shown experimentally that the younger the plants are at the time of infection, the more severe is the reduction in fruit yield.  Experimentally, compared to non-inoculated plants, 3-10 week old TYLCV inoculated tomato plants showed 63% reduction in number of fruit, while 15 week old plants did not show significant yield reduction (CABI, 2014).  In the USA, mostly minor losses of less than 10% were noted in 1997-2000 due to aggressive actions taken by tomato growers.

Severe losses in commercial bean production in Israel and southern Spain have been reported (Navot et al., 1992; Navas-Castillo et al., 1999).

Disease Cycle and Transmission: TYLCV is transmitted by the whitefly vector, Bemisia tabaci in a persistent manner.  The vector acquires the virus (acquisition access period) after feeding on an infected plant for 15-30 minutes, then there is a latent period of 18-24 hours within the insect after which the virus can be inoculated into a healthy plant during a feeding period of at least 15 minutes (inoculation access period) by the insect. A single white fly can inoculate more than one plant.  TYLCV is retained within the vector when the latter molts and is detected in every developmental stage of the vector.  It does not multiply within the vector and is not passed on from generation to generation through the eggs of the vector, although research results may be controversial:  Ghanim et al. (1998) detected TYLCV in whitefly eggs that suggested transovarial passage (CABI, 2014; VIDE, 1996).  Whiteflies remain viruliferous for approximately two weeks.  Large populations of B. tabaci moving between crops can cause rapid spread and high levels of disease.

The pathogen is spread over short distance by the white fly vector.  TYLCV is also transmitted by grafting and poorly by mechanical inoculation, but it is not transmitted by contact between plants.  Seed transmission has not been reported.  Over long distances, TYLCV is spread mainly through the movement of infected plants.  As symptoms can take up to 3 weeks to develop, symptomless infected plants can often go unnoticed.  Hitch-hiking, virus-carrying whiteflies can also accompany tomato and other host plants moved over long distances as well as strong winds and storms.

Worldwide Distribution:   TYLCV has been reported from several countries in Asia, Africa, North America (Mexico and USA), Central America and Caribbean, South America (Venezuela only), Europe, and Oceania (CABI, 2014, EPPO, 2014).

In the USA, TYLCV is present in Alabama, Arizona, California, Florida, Georgia, Hawaii, Kentucky, Louisiana, Mississippi, North Carolina, South Carolina, and Texas.

Official Control:  TYLCV is included on the Harmful Organism Lists of 49 countries in Asia, Europe, and South America, including Antigua and Barbuda Islands (PCIT, 2014). As a result of the estimated losses caused by TYLCV in 1999-2003, several countries in Australia and The European Union have established strict quarantine measures against the whitefly vector (CABI, 2014).

California Distribution: Imperial and Riverside Counties.

Major tomato-producing regions of California, including the Sacramento and San Joaquin valleys, do not promote the establishment of TYLCV.  According to Gilbertson (2008), the vector is not found in those regions for two main reasons.  First, the vector is intolerant of the region’s cool winter temperatures.  Second, the Central Valley has a natural tomato-free period from late November to early February during which period the amount of virus inoculum is significantly reduced until tomatoes are planted in late winter to early spring.  So, even if TYLCV is able to overwinter during the tomato-free period, it would take a long time for viral inoculum to build up to damaging levels in the field.  The virus is able to infect other host plants however, it builds up quickly on tomato.

There have not been any establishments of any Bemisia tabaci haplotype overwintering populations north of Fresno County due to the cooler winter temperatures and lack of the right amount of degree days for development (personal communication: Dr. Raymond Gill, CDFA Entomologist, 2013).  Nevertheless, it is not unusual for the whitefly vector species to be introduced into and possibly establish within contained controlled environments of nursery greenhouses in northern California regions (CDFA Pest Detection Records and personal communication: Dr. Gillian Watson, CDFA Entomologist).

California Interceptions:  There are no records of TYLCV detected in incoming plant shipments to California.

The risk Tomato yellow leaf curl virus would pose to California is evaluated below.

Consequences of Introduction: 

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) – The establishment of TYLCV within CA is closely related to the establishment of its whitefly vector, Bemisia tabaci. The virus (and the vector) is already established in commercial and urban environments in Imperial and Riverside Counties.  However, the vector is limited to the southern regions of the state as it is intolerant of the cooler winter temperatures present in the main tomato-growing regions in northern California.  Also, the vector is unable to build up to damaging levels because of the tomato-free production period present in the Central Valley.   

2)  Known Pest Host Range: Evaluate the host range of the pest:

– Low (1) has a very limited host range
– Medium (2) has a moderate host range
– High (3) has a wide host range.

Risk is Medium (2) While tomato is the main host for TYLCV, minor hosts include moderate numbers of cultivated plants, ornamentals, and weeds belonging to several plant species and families.

3)  Pest Dispersal Potential: Evaluate the dispersal potential of the pest:

– 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 spread of TYLCV is through artificial means. Short distance spread is mainly through its white fly vector, Bemisia tabaci, whereas long distance spread is mainly through movement of TYLCV-infected plants and strong winds that may move the vector over longer distances than it own capability.

4)  Economic Impact: Evaluate the economic impact of the pest to California using these criteria:

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)TYLCV is one of the most economically damaging pathogens of tomato.  Incidence and spread of the virus could gravely affect the tomato industry in particular, by lowering crop yield, value, increasing production costs, affecting local and international  markets, negatively change normal cultivation practices to prevent incidence of further occurrence and spread of the virus and its whitefly vector.

5)  Environmental Impact: Evaluate the environmental impact of the pest on California using these criteria:

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:

– 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) – Several weeds and wild tomato varieties are considered hosts of TYLCV, however, wild tomato and several weed hosts are asymptomatic and it is not known how well the whitefly vector will acquire the virus from such infected hosts that may comprise natural environments.  The effect on these hosts is not known.  Nevertheless, TYLCV infections may impact home/urban gardening and cultivation of ornamentals.

Consequences of Introduction to California for Tomato yellow leaf curl virus

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 TYLCV 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)

Final Score:

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

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

Uncertainty:

Up-to-date field data is always needed on the probable establishment and spread of TYLCV beyond the known regions in Imperial and Riverside counties.  Such information would be obtained through periodic surveys of tomato fields.  Also not known is the distribution of the virus in natural environments and the potential that infected natural hosts may play in its possible spread to tomato fields.

Conclusion and Rating Justification:

Based on the evidence provided above the proposed rating for Tomato yellow leaf curl virus is B.

References:

CABI   2014.  Tomato yellow leaf curl virus full datasheet.  Crop Protection Compendium.  http://www.cabi.org/cpc/datasheet/1695

EPPO, 2014.  Tomato yellow leaf curl virus (TYLCV0).  New PQR database.  Paris, France:  European and Mediterranean Plant Protection Organization.  http://newpqr.eppo.int

Fauquet C. M, D. P.Maxwell, B. Gronenborn, and J. Stanley.  2000.  Revised proposal for naming geminiviruses. Archives of Virology, 145(8):1743-1761; 11 ref.

Ghanim, M., S. Morin, M. Zeidan and H. Czosnek, 1998. Evidence for transovarial transmission of tomato yellow leaf curl virus by its vector, the whitefly Bemisia tabaci. Virology (New York), 240(2):295-303.

Gilbertson, R. L.  2008.  Tomato Yellow Leaf Curl.  UC IPM Pest Management Guidelines: Tomato.  UC ANR Publication 3470.  http://www.ipm.ucdavis.edu/PMG/r783103311.html

Nakhla, M. K and D. P. Maxwell 1998. Epidemiology and management of tomato yellow leaf curl disease. In: Hadidi A, Khetarpal RK, Koganezawa H, eds. Plant Virus Disease Control. St Paul, USA: APS Press, 565-583.

Navas-Castillo, J. S., Sanchez-Campos and J. A. Diaz.  1999. Tomato yellow leaf curl virus causes a novel disease of common bean and severe epidemics in tomato in Spain. Plant Disease, 83:29-32.

Navot, N, M., Zeidan, E. Pichersky, D. Zamir and H. Czosnek.  1992. Use of the polymerase chain reaction to amplify tomato yellow leaf curl virus DNA from infected plants and viruliferous whiteflies. Phytopathology, 82(10):1199-1202.

Papayiannis, L. C., N. I. Katis, A. M. Idris and J. K. Brown.  2011. Identification of weed hosts of Tomato yellow leaf curl virus in Cyprus. Plant Disease, 95(2):120-125. http://apsjournals.apsnet.org/loi/pdis .

PCIT.  2014.  USDA Phytosanitary Certificate Issuance & Tracking System.  https://pcit.aphis.usda.gov/PExD/faces/ReportHarmOrgs.jsp .

Rojas, M. R., T. Kon, E. T. Natwick, J. E. Polston, F. Akad, and R. L. Gilbertson.  2007.  First report of Tomato yellow leaf curl virus associated with Tomato Yellow Leaf Curl Disease in California.  Plant Disease, 91:1056.

VIDE.  2014.  Tomato yellow leaf curl bigeminivirus.  Plant Viruses Online: Description and Lists from the VIDE Database.  http://pvo.bio-mirror.cn/descr840.htm

Responsible Party:

Dr. 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.


Comment Period:  CLOSED

The 45-day comment period opened on June 1, 2015 and closed on July 16, 2015.


PEST RATING: B


Posted by ls