Tomato Brown Rugose Fruit Virus

California Pest Rating for
Tomato Brown Rugose Fruit Virus
Pest Rating:      A

PEST RATING PROFILE

Initiating Event:

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.

History & Status:

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.

Consequences of Introduction: 

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.

Consequences of Introduction to California for Tomato brown rugose fruit virus:

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.

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 = 13

Uncertainty:  

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.

Conclusion and Rating Justification:

Based on the evidence provided above the proposed rating for Tomato brown rugose fruit virus is A.


References:

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.


Responsible Party:

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


Comment Period:* CLOSED

11/07/18 – 12/22/18


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Pest Rating: A


Posted by ls