EPPO Global Database

Potato spindle tuber viroid(PSTVD0)

EPPO Datasheet: Potato spindle tuber viroid

Last updated: 2021-03-02

IDENTITY

Preferred name: Potato spindle tuber viroid
Taxonomic position: Viruses and viroids: Viroids: Pospiviroidae: Pospiviroid
Other scientific names: PSTVd, Potato gothic virus, Potato spindle tuber pospiviroid, Potato spindle tuber virus, Tomato bunchy top viroid
Common names in English: bunchy top of tomato, spindle tuber of potato
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Notes on taxonomy and nomenclature

Potato spindle tuber viroid (PSTVd) was the first species to be identified as a viroid, a new type of pathogen different from bacteria and viruses (Diener, 1971). Gross et al. (1978) was able to determine the nucleotide sequence and predicted its characteristic secondary structure, a covalently closed circular RNA molecule of 359 nucleotides forming a rod-like structure by internal base pairing. Analysis of the sequence showed that all open reading frames were too small to encode a protein. It was consequently understood that viroids occur as naked RNA molecules. PSTVd is the type species of both the genus Pospiviroid and family Pospiviroidae (Di Serio et al., 2017; 2020).

EPPO Categorization: A2 list
EU Categorization: Emergency measures (formerly), RNQP (Annex IV)
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EPPO Code: PSTVD0

HOSTS 2021-03-01

The main host is potatoes (Solanum tuberosum and other tuber-bearing Solanum spp.). Many other Solanaceous species have been reported as hosts, including important vegetable crops such as tomato (Solanum lycopersicum), pepper (Capsicum spp.), and a wide range of other fruit and ornamental crops and weeds (see Host list). Infections in ornamental crops and weeds often remain symptomless. A wide range of other members of the Solanaceae have been experimentally infected, as well as a few species in other families (Singh, 1973). In the EPPO region, potatoes and tomatoes are the main hosts of concern.

Host list: Atriplex semilunaris, Brugmansia hybrids, Brugmansia sanguinea, Brugmansia suaveolens, Calibrachoa sp., Capsicum annuum, Cestrum aurantiacum, Cestrum elegans, Cestrum endlicheri, Cestrum nocturnum, Chenopodium eremaeum, Dahlia sp., Datura leichhardtii, Datura sp., Erigeron bonariensis, Hevea brasiliensis, Ipomoea batatas, Lycianthes rantonnetii, Nicandra physalodes, Persea americana, Petunia sp., Physalis angulata, Physalis peruviana, Solanum anguivi, Solanum coagulans, Solanum dasyphyllum, Solanum laxum, Solanum lycopersicum, Solanum muricatum, Solanum nigrum, Solanum pseudocapsicum, Solanum sisymbriifolium, Solanum tuberosum, Streptoglossa sp., Streptosolen jamesonii

GEOGRAPHICAL DISTRIBUTION 2021-03-01

Potato spindle tuber disease caused by PSTVd was first described in the United States of America (EFSA, 2011 citing Martin, 1922). Since then, the viroid has been reported from the Americas, Asia, Africa, Europe and Oceania. PSTVd has been reported to be successfully eradicated from various countries throughout the world (Singh & Crowley, 1985; Verhoeven et al., 2018). However, since PSTVd infections may remain symptomless in many hosts, there is some uncertainty on the current distribution (EFSA, 2011).

EPPO Region: Austria, Azerbaijan, Belarus, Belgium, Croatia, Czech Republic, Georgia, Germany, Greece (mainland, Kriti), Hungary, Israel, Italy (mainland), Kazakhstan, Malta, Montenegro, Netherlands, Poland, Russia (Central Russia, Eastern Siberia, Far East, Northern Russia, Southern Russia), Slovenia, Spain (mainland), Switzerland, Turkey, Ukraine, United Kingdom (England)
Africa: Egypt, Ghana, Kenya, Nigeria, Uganda
Asia: Afghanistan, Bangladesh, China (Hebei, Heilongjiang, Jiangsu, Neimenggu, Qinghai), India (Himachal Pradesh, Maharashtra), Iran, Israel, Japan (Honshu), Kazakhstan, Pakistan
North America: Mexico
Central America and Caribbean: Costa Rica, Dominican Republic
South America: Peru, Venezuela
Oceania: Australia (Queensland, Western Australia)

BIOLOGY 2021-03-01

In tomato plants, PSTVd has been shown to spread systematically via the phloem, from an inoculated leaf to actively growing tissues such as young leaves and fruits (Palukaitis, 1987). It is likely to be the same for other hosts as this is a common route used by plant viruses. In potato, the viroid could be detected throughout the whole plant, including tubers (Weideman, 1987; Roenhorst et al., 2005). In leaves from different parts of the plant, only marginal differences in concentrations were found. The same was found for different parts of tubers. For pepper no details are available, but PSTVd has been detected in both leaves and fruit (Verhoeven et al., 2020). In early infections the highest concentrations are generally found in the top leaves. The incubation period is difficult to indicate, because it depends on the viroid strain, the amount of inoculum, host species and variety, as well as environmental conditions, in particular temperature.

PSTVd can be spread by vegetative propagation and transmission via contact, insects, pollen, and seeds (Owens & Verhoeven, 2009).

Vegetative propagation

The most efficient way of spreading of PSTVd is through vegetative propagation. Once an infection is established in ‘mother plants’, the viroid will be present in all progeny derived from these infected plants, including bulbs, tubers, cuttings, and microplants. Vegetative propagation has been the major cause of the spread of PSTVd in potatoes and vegetatively-propagated ornamentals (Singh et al., 1993; Owens et al., 2009; Verhoeven et al., 2010a).

Contact (mechanical transmission)

PSTVd-infected plants (including dried sap) form a source of inoculum for local spread by contact between diseased and healthy plants during cultivation. Mechanical transmission may be enhanced by crop handling, contaminated tools and machinery. The efficiency of transmission was found to increase at temperatures above 20°C (Verhoeven et al., 2010b). This might explain that PSTVd infections did not spread in potatoes under temperate maritime climates (Verhoeven et al., 2018), whereas extensive outbreaks in potatoes have been reported under continental climates in Canada, China, Ukraine and the USA in the past (Singh et al., 1993, 2014; Qiu et al., 2016). In protected tomato crops, with relatively high temperatures, PSTVd infections have been found to spread rapidly within a row (Verhoeven et al., 2004). The ease of mechanical transmission has been found to be related to the plant species and presence of leaf hairs (Navarro et al., 2009; Verhoeven et al., 2010b).

Pollen and seeds

Transmission of PSTVd via pollen and true seeds of potato has been demonstrated by Singh et al. (1992). In addition to potato, PSTVd has been reported to be seed borne in tomato and pepper (Singh, 1970; Matsushita & Tsuda, 2016). Seed-transmission rates have been reported from 0 to 100% for different plant species and circumstances (Hunter et al., 1969; Faggioli et al., 2015). Reports on high seed-transmission rates were mainly obtained under experimental conditions (Simmons et al., 2015; Verhoeven et al. (in preparation)). However, given that PSTVd is highly contagious and easily transmitted via contact and aerosols, it cannot be excluded that some reports of seed transmission are based on false positive results due to cross contamination during growing of plants, sample collection, and/or testing. Therefore, the role of pollen and seed transmission in the epidemiology of PSTVd is still a matter of debate (see Pathways for movement).

Insects

The role of insects in spreading of PSTVd is not clear (EFSA, 2011). In potato, transmission by aphids has been reported in the past (De Bokx & Piron, 1981), but was not confirmed in other studies (Schumann et al., 1980; Van Bogaert et al., 2016). However, aphid transmission of PSTVd in potato has been reported from plants co-infected by potato leaf roll virus (Querci et al., 1997; Singh & Kurz, 1997). In tomato, aphid transmission of pospiviroids has been reported, but could not be confirmed for PSTVd (EFSA, 2011). Pollination by bumblebees has been associated with the spread of tomato apical stunt viroid in protected tomato crops (Antignus et al., 2007; Matsuura et al., 2010), but was not observed for PSTVd (Nielsen et al., 2012). Given the non-specific interaction between the bumblebee and the viroid, transmission by pollinating insects cannot be excluded.

DETECTION AND IDENTIFICATION 2021-03-01

Symptoms

The type and severity of symptoms of PSTVd depend on the viroid strain, host species and variety, as well as environmental conditions. PSTVd infections may be symptomless or produce symptoms ranging from mild to severe. PSTVd accumulates faster at higher temperatures, which might result in more severe symptoms (Harris & Browning, 1980). For the major crops, i.e. potato, tomato and pepper, symptoms have been described by Owens & Verhoeven (2009). A concise description of the most prominent symptoms in these crops is given below. Infections of PSTVd in other Solanaceous fruit crops, such as Solanum melongena (eggplant) and Solanum muricatum (pepino), and most ornamental species, generally remain symptomless.

On potatoes

Infected plants may be stunted, leaves may be smaller, more upright, darker green and slightly rugose in comparison to healthy plants. Infected tubers may be small, elongated (spindle-shaped), misshaped and cracked. Eyes may be more pronounced and knob-like protuberances may develop into small tubers. 

On tomatoes

At an early stage of infection, infected plants show reduced growth and chlorosis in the top part of the plant. In time growth reduction may become more severe, and chlorotic leaves may turn red and/or purple and become brittle. At this stage, flowering and fruit onset stops. Plants may eventually die or partially recover. 

On peppers

Infected plants generally show either no symptoms or mild symptoms, i.e. distortion of the margins of apical leaves (Lebas et al., 2005; Verhoeven et al., 2016). Under experimental conditions, flower onset was delayed and fruits irregularly coloured and malformed (Verhoeven et al., 2020).

Morphology

PSTVd consists of a covalently closed circular, single-stranded RNA molecule of approximately 359 nucleotides. The naked RNA molecule forms a rod-like structure by internal base pairing (Gross et al., 1978). 

Detection and inspection methods

PSTVd infections may be detected by visual inspection in the field or greenhouse, dependent on the circumstances, i.e. viroid variant, host species and cultivar, and environmental conditions. Crop inspection procedures for potato as well as for tomato and pepper are available respectively in EPPO Standards PM 3/71 (EPPO, 2007) and PM 3/77 (EPPO, 2015). Spindle-shaped potato tubers might be recognised during transit inspections. Laboratory tests are essential for detection in symptomless hosts and for identification of the viroid, particularly since other pospiviroids might induce similar symptoms (Verhoeven et al., 2004). The preferred testing methods for detection of PSTVd are molecular methods, i.e. RT-PCR and real-time RT-PCR. None of the tests currently available is able to discriminate PSTVd from other pospiviroids, in particular tomato chlorotic dwarf viroid and some isolates of tomato planta macho viroid. For identification, amplicons obtained by RT-PCR, preferably comprising the whole genome, should be sequenced and analysed. Further details and other tests for detection and identification of PSTVd are described in the EPPO and IPPC diagnostic standards (IPPC, 2016; EPPO, 2021).

PATHWAYS FOR MOVEMENT 2021-03-01

PSTVd can be spread by vegetative propagation and transmission via contact, insects, pollen, and seeds (Owens & Verhoeven, 2009). Infected propagation material, including bulbs, tubers, cuttings, microplants and seeds, may serve as vehicles for introduction of the viroid into newly established crops and regions worldwide. Transmission via contact (mechanical transmission), pollen and insects, can account for further spread within a crop and/or region.

Whereas movement of infected vegetatively-propagated plants and plant material is the most efficient way of spreading PSTVd over long distances, the role of seed transmission is less clear. For potato, most publications on seed transmission date back to 1980-1990 and were related to germplasm collections. No recent reports on seed transmission are available, despite the fact that trading true potato seed for production is increasing. More insight in the role of true potato seed transmission as a pathway for movement of PSTVd is desirable. For tomato and pepper, PSTVd has been reported in many seed lots (Constable et al., 2019). Nevertheless, only limited numbers of outbreaks have been reported (Verhoeven et al. (in preparation)). Grow-outs of commercially produced seed lots of tomato and pepper, testing positive for PSTVd or other pospiviroids, did not result in any infection in over 100 000 seedlings (Verhoeven et al. (in preparation)). For PSTVd, Van Brunschot et al. (2014) reported one out of 370 seedlings from an infested tomato seed lot to be infected. Similarly, for tomato chlorotic dwarf viroid, Candresse et al. (2010) reported 2-20 out of 2,500 tomato seedlings to be infected. The fact that in 2016 tomato apical stunt viroid was detected in a pepper seed lot produced in 1992, at least 10 years before the testing of pospiviroids became mandatory (Verhoeven et al., 2017), indicates that pospiviroids were present in seed lots, whereas outbreaks were rarely recorded at that time. These results indicate that in practice seed transmission in tomato seems exceptional, whereas it has not been reported for pepper so far. The role of seed transmission in the spread of PSTVd, therefore, might have been overestimated in the past.

Regarding local spreading of PSTVd, mechanical transmission is the most important pathway, including human activities e.g. via equipment and machinery used during cultivation. For example, several outbreaks in tomato crops could be related to infections in vegetatively propagated ornamentals, based on a phylogenetic analysis of the viroid isolates in these crops (Navarro et al., 2009; Verhoeven et al., 2010a). Where nucleotide sequences of different PSTVd isolates from vegetatively propagated crops grouped per plant species, the isolates from tomato grouped with isolates from potato, Solanum laxum (synonyme Solanum jasminoides) and Physalis peruviana. The absence of a specific group of tomato isolates indicates that the infections in tomato are more likely to originate in these ornamentals than in tomato (seeds). In addition, an outbreak of PSTVd in vegetatively propagated peppers was thought to probably originate from infected plants of S. laxum that had been handled in the same facilities (Verhoeven et al., 2016). Pollen and insects may also contribute to local spread, but this pathway can be considered of minor importance.

PEST SIGNIFICANCE 2021-03-01

Economic impact

The economic impact of PSTVd consists of direct and indirect impacts. Direct impacts include yield and quality losses, whereas indirect impacts are related to changes in prices and effects on international trade. Soliman et al. (2012) made an assessment of the total economic impact based on modelling, taking into account prevalence, yield losses, climatic data (temperature), as well as price and changes in trade. This impact assessment showed large differences dependent on the estimated incidence of the viroid, and were difficult to quantify, in particular due to uncertainties about the possibility of introduction and further spread in a crop and region. Nevertheless, it was concluded that direct impacts combined with export losses for potatoes and tomatoes, justify the costs of current phytosanitary measures in the European Union.

Over the last century, significant yield losses due to PSTVd infections in potatoes have been reported (EFSA, 2011). It should be noted, however, that reported losses were recorded under different conditions than the current agricultural practices that include extensive phytosanitary measures. Similarly, PSTVd may occasionally cause serious infections in tomatoes (Verhoeven et al., 2004), but the overall significance in this crop seems limited seeing the low frequency and restricted extent of the outbreaks reported. For pepper crops no symptoms or only mild symptoms have been reported (Lebas et al., 2005; Verhoeven et al., 2016). Under experimental conditions fruit size was reduced (Verhoeven et al., 2020). Further data on outbreaks and impact in pepper are not available. For other crops that do not show symptoms, no direct impact is expected but export of these and other crops might be affected. 

Control

There are no chemical or biological methods available to control PSTVd within infected plants. Therefore, prevention is necessary to avoid infection with PSTVd. Eradication measures are necessary in the case of outbreaks (Owens & Verhoeven, 2009).

To prevent infection, it is essential to produce healthy planting material (Morris & Smith, 1977). This implies that the absence of the viroid in mother plants or nuclear stock has to be confirmed by testing, as recommended in the certification scheme for seed potatoes (EPPO, 1999), Petunia (EPPO, 2002), and schemes for production of herbaceous ornamentals (EPPO, 2008a). During the whole production process hygiene procedures should be in place to prevent infection by cross contamination. Measures may concern spatial separation of (host) plants as well as the use of clean (disinfected) tools and protective clothing by staff during crop handling. Post-entry quarantine programs as implemented for potato (EPPO, 2019b), have been shown to be effective in preventing the introduction of PSTVd in potato breeding and subsequent production systems (Verhoeven et al., 2018). In addition, cold treatment can be used to eliminate PSTVd from infected germplasm or potato clones, before release from quarantine (Paduch-Cichal & Kryczynski, 1987).

For eradication in the case of outbreaks, all PSTVd-infected plants should be traced and destroyed. A regulated area should be demarcated, composed of places of production designated as ‘infested’ and places of production designated as ‘probably infested’ (EPPO, 2011). To prevent re-infection, strict hygiene procedures should apply and equipment and machinery, if applicable, should be cleaned thoroughly. Plants to be destroyed as well as disposables should be e.g. discarded in closed containers to an incinerator, or plants should be industrially processed, fermented and composted (EPPO, 2008b), steamed and fed to animals, or deposited at a waste disposal site and covered with soil. After completion of protected cultivations, all surfaces, substrates and equipment should be cleaned or destroyed. In the case of field-grown potatoes, crop rotation with non-PSTVd hosts is recommended, combined with elimination of volunteer plants (EPPO, 2020). Upon resuming the cultivation of PSTVd susceptible crops, monitoring for PSTVd symptoms and/or testing is advised. More detailed measures are recommended in Standard PM 9/13 National regulatory control system for PSTVd (EPPO, 2011).

Phytosanitary risk

The viroid is regulated as a quarantine pest or regulated non-quarantine pest (RNQP) by many countries worldwide. Given that PSTVd can be present in asymptomatic hosts, the current geographical distribution is unclear. This implies that PSTVd can be introduced without being noticed by plants not known to be infected and from countries where the viroid has not been reported. Once established PSTVd is expected to cause most direct damage under warm and dry climatic conditions. 

PHYTOSANITARY MEASURES 2021-03-01

To prevent the introduction and spread of PSTVd, import requirements for different host species apply worldwide. These requirements can vary with regards to crop, type of consignment, and prevalence at the place of origin. When deregulated as a quarantine pest, PSTVd was recommended for regulation as a RNQP for seed potatoes and propagation material (including seeds) of pepper and tomato during the EU Quality pest project (Picard et al., 2018). 

For potato, EPPO recommends that countries where PSTVd is not known to occur, or which have implemented eradication measures, should require measures for import of seed potatoes (except microplants and minitubers) and ware potatoes. According to EPPO Standard PM 8/1 (EPPO, 2017) seed and ware potatoes imported from a country where the pest occurs should be subject to transitional arrangements. Imported potatoes should come from a pest-free area and originate from a pest-free potato production and distribution system, according to EPPO Standard PM 3/61 (EPPO, 2019a), or the exporting country should have implemented an official regulatory control system according to EPPO Standard PM 9/13 (EPPO, 2011). If potatoes are imported from a country where PSTVd is not known to occur, the absence should be confirmed by survey following ISPM 6 Surveillance (IPPC, 2019). In addition, post-entry quarantine programs are established to allow safe movement of potato germplasm for research and breeding purposes (EPPO, 2019b).

For tomato and pepper seeds, quarantine testing requirements may apply to allow seed lots to be traded and/or imported (EPPO, 2016). 

As well as preventing introduction, it is essential to start cultivation with non-infected plants or seeds. Therefore, the absence of the viroid in germplasm, mother plants and nuclear stock should be assured before the start of breeding, propagation and/or production of plants or seeds. During the EU Quality pest project, recommended measures included a zero tolerance for all categories of tomato and pepper plants, based on testing and absence of symptoms.

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Van Brunschot SL, Verhoeven JTJ, Persley DM, Geering ADW, Drenth A & Thomas JE (2014) An outbreak of Potato spindle tuber viroid in tomato is linked to imported seed. European Journal of Plant Pathology 139, 1–7.

Verhoeven JTJ, Jansen CCC, Willemen TM, Kox LFF, Owens RA & Roenhorst JW (2004) Natural infections of tomato by Citrus exocortis viroid, Columnea latent viroid, Potato spindle tuber viroid and Tomato chlorotic dwarf viroid. European Journal of Plant Pathology 110, 823-831.

Verhoeven JTJ, Jansen CCC, Botermans M & Roenhorst JW (2010a) Epidemiological evidence that vegetatively propagated, solanaceous plant species act as sources of Potato spindle tuber viroid inoculum for tomato. Plant Pathology 59, 3-12.

Verhoeven JTJ, Hüner L, Marn MV, Plesko IM & Roenhorst JW (2010b) Mechanical transmission of Potato spindle tuber viroid between plants of Brugmansia suaveolens, Solanum jasminoides and potatoes and tomatoes. European journal of plant pathology 128, 417-421.

Verhoeven JTJ, Voogd JGB, Strik N & Roenhorst JW (2016) First report of Potato spindle tuber viroid in vegetatively propagated plants of Capsicum annuum in The Netherlands. New Disease Reports 34, 12.

Verhoeven JTJ, Koenraadt HMS, Westenberg M & Roenhorst JW (2017) Characterization of tomato apical stunt viroid isolated from a 24-year old seed lot of Capsicum annuum. Archives of virology 162, 1741-1744.

Verhoeven JTJ, Vulling GWM, Voogd JGB, Janssen FJA, Roenhorst JW (2018) Potato germplasm poses the highest risk of introducing potato spindle tuber viroid in potatoes in the Netherlands: analysis and evaluation of an outbreak in potato breeding. European Journal of Plant Pathology 151, 201-211.

Verhoeven JTJ, Koenraadt HMS, Jodlowska A, Hüner L & Roenhorst JW (2020) Pospiviroid infections in Capsicum annuum: disease symptoms and lack of seed transmission. European Journal of Plant Pathology 156, 21-29.

Verhoeven JTJ, Botermans M, Koenraadt HMS, Schoen R & Roenhorst JW (in preparation) Role of seed transmission in the spread of pospiviroids in commercial pepper and tomato crops seems overestimated.

Weidemann HL (1987) The distribution of potato spindle tuber viroid in potato plants and tubers, EPPO Bulletin 17, 45-50.

ACKNOWLEDGEMENTS 2021-03-01

This datasheet was extensively revised in 2021 by Ruben Schoen and Annelien Roenhorst, Netherlands Food and Consumer Product Safety Authority (NVWA, the Netherlands). Their valuable contributions are gratefully acknowledged.

How to cite this datasheet?

EPPO (2021) Potato spindle tuber viroid. EPPO datasheets on pests recommended for regulation. Available online. https://gd.eppo.int

Datasheet history 2021-03-01

This datasheet was first published in the EPPO Bulletin in 1978 and revised in the two editions of 'Quarantine Pests for Europe' in 1992 and 1997, as well as in 2021. It is now maintained in an electronic format in the EPPO Global Database. The sections on 'Identity', ‘Hosts’, and 'Geographical distribution' are automatically updated from the database. For other sections, the date of last revision is indicated on the right.

CABI/EPPO (1992/1997) Quarantine Pests for Europe (1st and 2nd edition). CABI, Wallingford (GB).

EPPO (1978) EPPO Data Sheet on Quarantine Organisms no 97. Potato spindle tuber viroid. EPPO Bulletin 8(2), 105-109.