Tomato apical stunt viroid
- Summary of Invasiveness
- Taxonomic Tree
- Notes on Taxonomy and Nomenclature
- Distribution Table
- History of Introduction and Spread
- Risk of Introduction
- Habitat List
- Hosts/Species Affected
- Growth Stages
- List of Symptoms/Signs
- Means of Movement and Dispersal
- Seedborne Aspects
- Pathway Causes
- Pathway Vectors
- Plant Trade
- Impact Summary
- Impact: Economic
- Risk and Impact Factors
- Uses List
- Similarities to Other Species/Conditions
- Prevention and Control
- Principal Source
- Distribution Maps
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PicturesTop of page
IdentityTop of page
Preferred Scientific Name
- Tomato apical stunt viroid
Other Scientific Names
- Tomato apical stunt pospiviroid
- TASVD0 (Tomato apical stunt viroid)
Summary of InvasivenessTop of page
Tomato apical stunt viroid (TASVd) is a serious pathogen of tomato. Pathways for introduction include tomato seedlings, tomato seeds and ornamentals. If spread to tomato, considerable losses could result. TASVd is spread easily through plant sap, e.g. during pruning and propagation, and there is some evidence of insect transmission in the greenhouse. No symptoms appear on infected ornamental solanaceous plants, but these plants can act as a reservoir for the spread of viroids in tomato production, especially in greenhouse conditions. TASVd outbreaks in tomato are rare although it has occurred in several countries in Asia, Africa and Europe. The economic impact of TASVd in tomato production is not known, but heavy yield losses may result from infection with certain strains. This viroid has not been reported as an invasive species.
Taxonomic TreeTop of page
- Domain: Virus
- Unknown: Viroids
- Family: Pospiviroidae
- Genus: Pospiviroid
- Species: Tomato apical stunt viroid
Notes on Taxonomy and NomenclatureTop of page
Viroids are small, covalently closed, circular single-stranded RNA molecules that are highly base-paired and range in size from 239 to 401 nucleotides. They do not encode peptides or proteins but use host proteins for replication, movement and processing of replication intermediates, which distinguishes them from plant viruses (Diener, 1971, 1987). All viroids contain the -Vd ending in their name to distinguish them from viruses. There are over 30 known viroid species (43 complete genomes, and more than 4700 sequence variants described and assigned to eight genera) taxonomically divided into two families, the Pospiviroidae (the type species of which is Potato spindle tuber viroid, PSTVd) and the Avsunviroidae (the type species of which is Avocado sunblotch viroid, ASBVd). There are also several proposed, unclassified viroids (Di Serio et al., 2014). Most known viroids are members of the Pospiviroidae. The first viroid classification scheme was proposed in the early 1990s (Elena et al., 1991) and was revised in 2014 (Di Serio et al., 2014). Tomato apical stunt viroid is a member of the family Pospiviroidae, genus Pospiviroid.
DescriptionTop of page
TASVd contains a central conserved region located in the upper and lower strands of the viroid rod-like secondary structure. Isolates range from 362 to 364 nucleotides in length and, phylogenetically, it is most closely related to Citrus exocortis viroid, CEVd (Di Serio et al., 2014). The nucleotide sequences of several TASVd isolates are located in GenBank (NCBI).
DistributionTop of page
TASVd has been reported in tomato and in asymptomatic ornamentals in parts of Asia (Indonesia and Israel), Africa (Cote d’Ivoire, Senegal, Ghana and Tunisia) and in many European countries, including Belgium, Finland, Germany and Italy (Candresse et al., 1987; Spieker et al., 1996; Antignus et al., 2002; Verhoeven et al., 2004, 2006, 2008a, 2008b, 2012; Candresse et al., 2007; EVIRA, 2008; Batuman et al., 2013; Parella and Numitone, 2014). TASVd was reported as the most prevalent pospiviroid in ornamentals in the Netherlands (Verhoeven et al., 2012).
Distribution TableTop of page
The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.
|Continent/Country/Region||Distribution||Last Reported||Origin||First Reported||Invasive||Reference||Notes|
|Indonesia||Present||1987||Not invasive||Candresse et al., 1987; EPPO, 2017||Reported in 1987, but no further information is available on incidence or where the samples were collected|
|Israel||Present||Introduced||Not invasive||Antignus et al., 2002; EPPO, 2017|
|Côte d'Ivoire||Present||1980||Not invasive||Walter et al., 1980; Walter, 1981; EPPO, 2017||No reliable information on current status|
|Ghana||Present||Batuman et al., 2013|
|Senegal||Present||Not invasive||Candresse et al., 2007; EPPO, 2017|
|Tunisia||Present||Not invasive||Verhoeven et al., 2006; EPPO, 2017|
|Austria||Localised||Introduced||Not invasive||Grausgruber-Gröger and Gottsberger, 2011; EPPO, 2017|
|Belgium||Present, few occurrences||Introduced||Not invasive||Verhoeven et al., 2008b; Olivier et al., 2011; EPPO, 2017|
|Croatia||Localised||Introduced||Not invasive||Milanović et al., 2014||A survey of nurseries in 2009-2012 identified one imported S. laxum plant infected with TASVd in Split|
|Czech Republic||Present||Not invasive||Orságová et al., 2015||On symptomless S. laxum|
|Finland||Eradicated||Introduced||Not invasive||EVIRA, 2008||Greenhouse; on symptomless S. laxum|
|France||Eradicated||Not invasive||EPPO, 2017||Greenhouse; on symptomless Brugmansia, S. laxum, S. lycopersicum|
|Germany||Present||Introduced||Not invasive||Verhoeven et al., 2008b; Spieker, 1996; EPPO, 2017|
|Italy||Present||Parella and Numitone, 2014|
|Netherlands||Present||Introduced||Not invasive||Verhoeven et al., 2008a; Verhoeven et al., 2012|
|Poland||Present||Introduced||Not invasive||Hennig et al., 2013||On L. rantonnettii|
|Slovenia||Present||Introduced||Not invasive||Marn and Pleško, 2012; EPPO, 2017|
History of Introduction and SpreadTop of page
The tomato apical stunt disease was first described from tomato in Cote d’Ivoire, Africa in 1980 (Walter et al., 1980) and the causal agent was characterized as a viroid in 1981 (Walter, 1981). Since then, incidence of the disease has been sporadic and, in many cases, the viroid has been eradicated by destruction of infected material. It was recently detected in the Netherlands 24-year-old seed lots of Capsicum annuum (Verhoeven et al., 2017b). TASVd is likely to have spread through infected seed and by importation of asymptomatic ornamentals.
Risk of IntroductionTop of page
Although TASVd was added to the EPPO Alert List in 2003, it was deleted in 2017 and is now considered within the framework of the regulated, non-quarantine pest project (EPPO, 2017). Pathways for introduction include tomato seedlings, tomato seeds and ornamentals.
HabitatTop of page
TASVd has primarily been found in greenhouse-grown tomatoes and solanaceous ornamentals (Verhoeven et al., 2012). TASVd has been found infrequently in nurseries and garden plots (Grausgruber-Gröger and Gottsberger, 2011).
Habitat ListTop of page
|Terrestrial – Managed||Protected agriculture (e.g. glasshouse production)||Present, no further details||Harmful (pest or invasive)|
Hosts/Species AffectedTop of page
The primary host of TASVd is tomato (Solanum lycopersicum). TASVd can be mechanically transmitted to several species, most of which are in the family Solanaceae (Walter, 1987), with varying symptoms on susceptible hosts. Ornamentals are also infected by TASVd, but are asymptomatic (Verhoeven et al., 2010; Verhoeven et al., 2012). There are no reports of TASVd in weedy plant species. Mechanical inoculation of weed species did not result in the detection of additional hosts (Antignus et al., 2007).
Growth StagesTop of page Flowering stage, Fruiting stage, Pre-emergence, Seedling stage, Vegetative growing stage
SymptomsTop of page
Symptoms of TASVd on tomato include curling of leaves, apical stunting, necrotic lesions, vein yellowing, deformation and small fruit (Walter, 1987). Symptoms in tomato are similar to those of other pospiviroid species, therefore, molecular methods are required to determine that the infection is caused by TASVd.
Ornamentals infected by TASVd are asymptomatic (Verhoeven et al., 2017a).
List of Symptoms/SignsTop of page
|Fruit / premature drop|
|Fruit / reduced size|
|Growing point / dwarfing; stunting|
|Inflorescence / dwarfing; stunting|
|Leaves / abnormal forms|
|Leaves / yellowed or dead|
|Roots / reduced root system|
|Stems / stunting or rosetting|
|Whole plant / dwarfing|
Means of Movement and DispersalTop of page
Similarly to other pospiviroids, mechanical transmission of TASVd to tomato occurs very easily (Walter, 1987). It is also transmitted via tomato seed (Antignus et al., 2006, 2007; Matsushita and Tsuda, 2016).
TASVd was transmitted at a rate of 30% via commercial bumblebees (Bombus terrestris) in greenhouse tomato (Antignus et al., 2007). However, in the same study, no transmission was observed by aphids or whiteflies (Bemisia tabaci).
A study by Bogaert et al. (2015) sought to determine the mechanism of viroid transmission by aphids i.e. whether it is due to mechanical contact through contaminated mouth and body parts or by feeding through the stylet. The study examined the distribution of potato spindle tuber viroid (PSTVd) and TASVd in green peach aphids fed on viroid-infected plants, using quantitative real-time PCR and fluorescence in situ hybridisation with viroid-specific primers and probes. Viroid RNAs were detected in 29% of aphids after a 24-hour feeding period and were present in the stylets and the stomach, but not in the embryo. The partial and low concentration of viroid uptake shows that aphids can ingest viroids, potentially increasing the transmission risk. In another study, Bogaert et al. (2016) assessed the transmission of four viroids, including TASVd, by three insects and found that there was a low level of transmission of Tomato chlorotic dwarf viroid by Bombus terrestris. However, transmission of TASVd by insects was not reported.
Seedborne AspectsTop of page
Effect on Seed Quality
TASVd-infected tomato seed causes direct or indirect injury to the seed and failure of the infected seed to germinate (R. Hammond, USDA-ARS, Beltsville, personal observation, 2018).
TASVd was transmitted at a rate of 80% through tomato seed from plants mechanically inoculated at the four-leaf stage with crude sap of viroid-infected plants (Antignus et al., 2007). Disinfestation of the seed did not prevent viroid transmission to germinated seedlings. However, in separate studies, Fiaggioli et al. (2015) and Matsushita and Tsuda (2016) found no transmission of TASVd from tomato seeds to seedlings. Furthermore, Verhoeven et al. (2017b) found no transmission of TASVd from pepper seeds to seedlings. Contradictory results have also been reported on seed transmission for other pospiviroids (Faggioli et al., 2015; Simmons et al., 2015; Yanagisawa and Matsushita, 2017).
Decontamination of tomato seed with 1% sodium hypochlorite did not reduce seed transmission of the related PSTVd (Simmons et al., 2015).
Pathway CausesTop of page
Pathway VectorsTop of page
Plant TradeTop of page
|Plant parts liable to carry the pest in trade/transport||Pest stages||Borne internally||Borne externally||Visibility of pest or symptoms|
Impact SummaryTop of page
Impact: EconomicTop of page
Seed transmission of TASVd in tomato may cause direct or indirect injury to the seed as evidenced by smaller seeds and reduced rates of germination (R. Hammond, USDA-ARS, Beltsville, unpublished results), infected plants, survival of the inoculum from one crop season to the next and dissemination of the disease worldwide through exchange of seeds. The global production and international exchange of tomato seed is central to agricultural production. The economic impact of TASVd in tomato production is not known, but heavy yield losses may result from infection with certain strains.
For a study of the risk management of solanaceous viroids in the EU territory, see ESFA Panel on Plant Health (2011).
Risk and Impact FactorsTop of page Impact outcomes
- Host damage
- Negatively impacts agriculture
- Highly likely to be transported internationally accidentally
Uses ListTop of page
- Research model
DiagnosisTop of page
Viroids can be identified by bioassay on indicator hosts (Nie and Singh, 2017), gel electrophoresis of known and unknown viroids based on the physical properties of circular viroid molecules (Singh and Boucher, 1987; Hanold and Vadamalai, 2017) and by nucleic acid hybridisation (Owens and Diener, 1981; Botermans et al., 2013; Pallas et al., 2017). More recently viroid detection methods have included RT-PCR, RT-PCR followed by nucleic acid sequencing of the amplicons (Bostan et al., 2004; Olivier et al, 2014; 2016; Orsagova et al., 2015; Faggioli et al., 2017), microarray (Tiberini and Barba, 2012; Zhang et al., 2013; Van Brunschot et al., 2014; Zhu et al., 2017) and Next Generation Sequencing (Barba and Hadidi, 2017).
Testing is an important tool to prevent the introduction of viroids in seed. Nucleic acid hybridisation tests were developed for large scale testing for PSTVd in potato seed, with a detection sensitivity of one contaminated seed in 80 or 150 non-contaminated seeds, respectively (Salazar et al., 1983; Borkhardt et al., 1994). Higher sensitivity using RT-PCR and real time RT-PCR has been obtained in potato and tomato seeds. Bakker et al. (2015) reported a high throughput, multiplex TaqMan real-time RT-PCR that could detect one infected seed in 1000 non-infected seeds in tomatoes infected with PSTVd and Tomato chlorotic dwarf viroid (TCDVd).
For more information on the detection of pospiviroids on tomato seed, see International Seed Federation (2015) and the reference protocols below.
In 2017, the Netherlands Inspection Service for Horticulture, Naktuinbouw, published an update of their reference protocol for testing tomato seed for pospiviroids, including TASVd. From a sample of 3000 or 20,000 seeds, either three subsamples of 1000 seeds or 50 subsamples of 400 seeds are used for RNA isolation. Seeds are soaked in extraction buffer for 30-60 minutes prior to extraction. Positive RNA controls are included in the analysis and several primer sets are used (Naktuinbouw, 2017). An earlier version of this protocol was used by Verhoeven et al. (2017b) to detect TASVd in pepper seed.
New revised emergency seed import (pre-export or on-arrival) requirements for tomato and pepper (sweet and chilli), were issued by the Department of Agriculture, Forestry and Fisheries, Australia in 2012 (FTA, 2012). Tomato seed lots are tested for six pospiviroids (including TASVd and PSTVd) based on the Australian testing requirements using RT-PCR. Testing requires a 20,000 seed sample. Seed lots of 300 g or less may be tested using a smaller seed sample and can be pooled.
Similarities to Other Species/ConditionsTop of page
Symptoms of TASVd infection on tomato are similar to those caused by other pospiviroids.
Prevention and ControlTop of page
Cultural Control and Sanitary Measures
Infected plant material (plants, seeds) should be discarded. The disease is often eradicated by the destruction of infected plant material. Sanitary measures include disinfection of tools and greenhouse benches with agents permitted for the control of viroids.
Crop and ornamental solanaceous species should be grown separately, and employees should take measures to prevent viroid introduction when they start working on host crops.
ReferencesTop of page
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20/04/18 Original text by:
Rosemarie W Hammond, Molecular Plant Pathology Laboratory, USDA-ARS, Beltsville, Maryland, USA
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