Tomato Chlorotic Dwarf Viroid

California Pest Rating for

Pest Rating: A

PEST RATING PROFILE

Initiating Event:

On October 23, 2014 CDFA was notified by USDA APHIS of the detection of Tomato chlorotic dwarf viroid (TCDVd) in four experimental Petunia samples that were shipped under federal permit from California to Illinois (Kress, 2014). The detection was made by the plant pathologist of an ornamental plant breeding company, and communicated to USDA APHIS as per federal permit requirement that “APHIS is notified within 10 days on receipt of permitted materials if the permitee detects a pathogen that is not widely prevalent in the State from which the infected material was obtained.” The Petunia plant samples came from plants raised in a greenhouse environment by a different plant breeding company in Arroyo Grande, California. Following that detection the Company took action by discarding all infected Petunia plants and administering phytosanitary measures. Furthermore, the Company reported to San Luis Obispo County that they had the (remaining) Petunia plants in the greenhouse tested for TCDVd and the results were negative. Nevertheless, following the disposal and sanitary action taken by the Company, official samples of the remainder Petunia plants in the greenhouse were collected for diagnostic analysis conducted by the CDFA Plant Pathology Laboratory (Taylor, 2014). The current status and pest rating of TCDVd is re-evaluated and a permanent rating is proposed.

History & Status:

Background: Tomato chlorotic dwarf viroid (TCDVd) belongs to the genus Pospiviroid. PSTVd has a circular single stranded RNA molecule with 360 nucleotides and lacks a coat protein. It is closely related to the Potato spindle tuber viroid but significantly differs from it in sequence homology. Little is known about the pathogen’s host range, host-pathogen interactions, transmission and epidemiology however, the pathogenicity properties of TCDVd are expected to be similar to those of the Potato spindle tuber viroid. As with other members of its genus, TCDVd use the infected plant cell nucleolus to multiply in numbers and accumulate. TCDVd then move from cell to cell through natural openings in the cell wall (plasmodesmata) and throughout the plant via the phloem. In general, viroids survive in nature outside a host or in dead plant material for only brief periods of a few minutes to a few months. They overwinter and oversummer within infected perennial hosts. TCDVd is active at high temperatures and therefore, warm climates are expected to increase its rate of transmission.

Hosts: Tomato (Solanum lycopersicum) is the major host. Incidental hosts include Brugsmania hybrids (Angel’s trumpet), Petunia, Verbena and Vinca minor (periwinkle) (EPPO, 2014; CABI, 2014). Several artificially inoculated, experimental, susceptible hosts belonging to the family Solanaceae have been reported (Singh, et al., 1999).

Symptoms: Symptoms are difficult to distinguish as specific to TCDVd – as several viroids and viruses can produce similar symptoms. Symptoms expressed by tomato plants are influenced by the TCDVd strain, tomato variety, age and vigor of the plant, and climatic conditions. Initial symptoms, produced in tomato plants 3-6 weeks after initial infection, are exhibited as reduction in growth and chlorosis (yellowing) of young terminal leaves. Over time infected plants become stunted, distinctly chlorotic leaves that may turn bronze and/or purplish, sometimes with lesions, and turn brittle and distorted. However, commonly observed symptoms include stunting, bunchiness, reduced leaves and fruit, leaf chlorosis, necrosis and leaf and petiole, downward bending of leaves, distorted fruit and may lead to death of the plant.

The pathogen has been detected in petunia and verbena although no symptoms were exhibited by these hosts (Sabaratnam, 2012). Symptomless ornamental plants may serve as a source of inoculum.

Damage Potential: Estimates of crop/yield loss caused by the pathogen are not available however TCDVd can be a serious threat to tomato production in field and greenhouse environments. Extensive damage has especially been noted in greenhouse-grown tomato plants.

Transmission: Similar to other members of the genus pospiviroid, Tomato chlorotic dwarf viroid is mechanically transmitted in infected plant sap spread through handling of contaminated plants, pruning tools, cultivation equipment, clothing, and plant to plant contact. The pathogen is also spread through vegetative propagation and contaminated seed (Singh & Dilworth, 2009). Natural transmission of TCDVd by insects and pollen is not known, however, Ling (2010) stated the transmission of TCDVd by bumblebee pollinators of tomato plants grown in greenhouse environments. The pathogen is transmitted less efficiently from older mature plants during the picking of fruit and old leaves (Sabaratnam, 2012).

Worldwide Distribution: Asia: India; America: Mexico, USA; Europe: Czech Republic, France, Slovenia. In the USA, TCDVd is present and limited in its occurrence in Arizona and Colorado (EPPO, 2014; CABI, 2014).

Official Control: The following countries include Tomato chlorotic dwarf viroid on their ‘Harmful Organism’ lists: Georgia, Japan, Republic of Korea, New Zealand, and Thailand (PCIT, 2014).

Tomato chlorotic dwarf viroid has been eradicated in Canada (Manitoba), Japan (Honshu), Finland and Norway, and is no longer present in Belgium. It is considered transient, under eradication in United Kingdom (Scotland) (EPPO, 2014; CABI, 2014).

California Distribution: There are no reports of TCDVd being established in field or natural environments within California – that would indicate an established distribution.

California Interceptions: There are no state reports of TCDVd detections in plant materials intercepted within or at points of entry in California.

The risk Tomato chlorotic dwarf viroid 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 High (3) – TCDVd is capable of establishing within greenhouse as well as field environments within California. Suitable climates for tomato and other host plants would also favor establishment of TCDVd.

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) – Of what is currently known, the host range of TCDVd is limited to tomato and few ornamental crops. However, tomato is grown in significant acreages throughout the State.

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) – TCDVd multiply autonomously in infected plant material and are easily transmitted through infected seed and mechanical means.

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) – TCDVd can potentially lower tomato crop value, yield, trigger loss of market through the imposition of quarantine regulations by other countries and states, and can influence normal cultural practices.

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 High (3) – At the very least, incidence of TCDVd could result in requirement of additional official and private treatments, impact cultural and horticultural practices.

Consequences of Introduction to California for Tomato chlorotic dwarf viroid

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 = (13).

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 (0). TCDVd is not established in California. TCDVd has only been detected in nursery plants contained in greenhouses. That detection led to destruction of infected plants and implementation of phytosanitary measures (see “Initiating event”) and does not indicate the establishment of the pathogen in California.

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 (High).

Uncertainty:

Information of the source of the pathogen is not known. The pathogen has not been reported from environments outside greenhouses.

Conclusion and Rating Justification:

Based on the evidence provided above the proposed rating for Tomato chlorotic dwarf viroid is A.

References:

CABI 2014. Tomato chlorotic dwarf viroid basic datasheet. Crop Protection Compendium. http://www.cabi.org/cpc/datasheet/1695.

EPPO, 2014. Tomato chlorotic dwarf viroid (TCDVD0). New PQR database. Paris, France: European and Mediterranean Plant Protection Organization. http://newpqr.eppo.int.

Kress, J. 2014. Email to John Chitambar (CDFA) and others (CDFA), subject: RE: Attention Shailaja Rabindran/Pathogen Detection, sent: Thursday 10/23/2014, 11:06 am.

Ling, K. S., J. Th. J. Verhoeven, R. P. Singh, and J. K. Brown. 2009. First report of tomato chlorotic dwarf viroid in greenhouse tomatoes in Arizona. Plant Disease, 93:1075.

Ling, K. S. 2010. Genetic diversity of tomato viroids in North America. USDA-ARS, U. S. Vegetable Laboratory Charleston, South Carolina, Power Point Presentation.

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

Sabaratnam, S. 2012. Tomato chlorotic dwarf viroid on greenhouse tomato. British Columbia Ministry of Agriculture, Abbotsford Agriculture Center. http://www.agf.gov.bc.ca/cropprot/tcdvd.htm.

Singh, R. P. and A. D. Dilworth. 2009. Tomato chlorotic dwarf viroid in the ornamental plant Vinca minor and its transmission through tomato seed. European Journal of Plant Pathology, 123:111-116.

Singh, R. P. X. Nie, and M. Singh. 1999. Tomato chlorotic dwarf viroid: an evolutionary link in the origin of pospiviroids. Journal of General Virology, 80:2823-2828.

Taylor, C. 2014. Email to Karen Lowerison (San Luis Obispo County Agricultural Commissioner’s office) and others (CDFA, SLO County), subject: Re: Tomato chlorotic dwarf viroid detection, sent: Friday 10/24/2014, 2:31 pm.

Responsible Party:

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.