'Candidatus Phytoplasma solani'(PHYPSO)
EPPO Datasheet: 'Candidatus Phytoplasma solani'
Authority: Quaglino, Zhao, Casati, Bulgari, Bianco, Wei & Davis
Taxonomic position: Bacteria: Tenericutes: Mollicutes: Acholeplasmatales: Acholeplasmataceae
Other scientific names: Grapevine bois noir phytoplasma, Maize redness phytoplasma, Phytoplasma solani Quaglino, Zhao, Casati, Bulgari, Bianco, Wei & Davis, Potato stolbur phytoplasma, Stolbur phytoplasma
Common names in English: STOL, black wood of grapevine, maize redness, metabolbur, parastolbur, stolbur of potato, stolbur of tobacco, stolbur of tomato
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Notes on taxonomy and nomenclature
Phytoplasmas are wall-less plant pathogenic bacteria (class Mollicutes) that survive and multiply in the plant phloem and insect haemolymph (IRPCM, 2004). The name ‘Candidatus (Ca.)’ represents the ‘unculturable’ status of the phytoplasma (Murray & Stackebrandt, 1995). The taxonomy of phytoplasmas is complex and based on 16S ribosomal gene sequence as well as on biological, phytopathological, and genetic properties (IRPCM, 2004). Based on highly conserved 16S ribosomal gene sequence, phytoplasmas are categorized into 33 groups (Bertaccini & Lee, 2018).
‘Ca. Phytoplasma solani’ was first described as a distinct species in the genus ‘Ca. Phytoplasma’ by Quaglino et al. (2013). To be classified as ‘Ca. Phytoplasma solani’, a strain should (i) share >99% sequence similarity over a minimum length of 1.2kb within the 16S rRNA gene of the reference strain STOL11 (GenBank accession number AF248959), (ii) contain the identical STOL11-unique 16S rDNA signature sequence and (iii) contain two distinguishing sequence blocks noted for the reference strain STOL11 with a tolerance of a single nucleotide difference in no more than one of the sequences. Strains that do not fulfill either criterion (ii) or (iii) are considered ‘Ca. Phytoplasma solani’-related strains, even if they fulfil criterion (i).
Based on 16S rDNA sequence analyses, ‘Ca. Phytoplasma solani’ strains are classified into taxonomic subgroups 16SrXII-A, -F, -G, -J, and –K (Quaglino et al., 2017). Molecular typing, based on sequence analyses of several other genes (e.g., tuf, secY, stamp, vmp1), highlighted the presence of numerous genetically distinct strains of ‘Ca. Phytoplasma solani’ (e.g. Aryan et al., 2014; Murolo & Romanazzi, 2015; Quaglino et al., 2016; Balakishiyeva et al., 2018).
EU Categorization: RNQP (Annex IV)
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EPPO Code: PHYPSO
‘Ca. Phytoplasma solani’ has a wide plant host range, including many wild/weed species, ornamentals and crops. Cultivated hosts affected include, grapevine (Vitis vinifera), tomato (Solanum lycopersicum), potato (Solanum tuberosum), maize (Zea mays), pepper (Capsicum annuum), lavender (Lavandula angustifolia), aubergine (Solanum melongena), celery (Apium graveolens), carrot (Daucus carota), strawberry (Fragaria ananassa), tobacco (Nicotiana tabacum), sugar beet (Beta vulgaris). Fruit tree species, such as plum (Prunus domestica), peach (Prunus persica), cherry (Prunus avium), almond (Prunus dulcis) and apple (Malus domestica), have also been described as ‘Ca. Phytoplasma solani’ hosts. The main natural reservoirs for ‘Ca. Phytoplasma solani’ are wild plants such as bindweed (Convolvulus arvensis) and stinging nettle (Urtica dioica) (Quaglino et al., 2013; EFSA, 2014; CABI, 2020).Host list: Achillea millefolium, Actinidia deliciosa, Allium ampeloprasum, Amaranthus retroflexus, Ammi majus, Anethum graveolens, Apium graveolens, Artemisia scoparia, Artemisia vulgaris, Bellis perennis, Beta vulgaris, Brassica oleracea var. gemmifera, Bromus inermis, Bupleurum tenuissimum, Calendula officinalis, Calystegia sepium, Capsella bursa-pastoris, Capsicum annuum, Carica papaya, Carum carvi, Centaurium erythraea, Cephalaria transsylvanica, Chenopodium album, Chrysanthemum indicum, Cichorium intybus, Cirsium arvense, Cistus ladanifer, Convolvulus arvensis, Convolvulus tricolor, Coronilla varia, Crepis foetida, Crepis sp., Cucumis sativus, Cuscuta sp., Cynodon dactylon, Datura stramonium, Daucus carota, Dianthus barbatus, Digitalis purpurea, Echinacea angustifolia, Echinacea purpurea, Echium vulgare, Epilobium sp., Erigeron annuus, Erigeron bonariensis, Erigeron canadensis, Eucalyptus camaldulensis, Euonymus japonicus, Euphorbia falcata, Fallopia convolvulus, Ficus carica, Fragaria x ananassa, Galium sp., Geranium dissectum, Gomphocarpus physocarpus, Helianthus annuus, Helminthotheca aculeata, Helminthotheca echioides, Hibiscus cannabinus, Hydrangea macrophylla, Hypericum barbatum, Hypericum perforatum, Hyssopus officinalis, Jasminum officinale, Laburnum anagyroides, Lactuca saligna, Lactuca sativa, Lactuca serriola, Lapsana communis, Lavandula angustifolia, Lavandula x intermedia, Levisticum officinale, Lilium longiflorum, Linaria vulgaris, Liquidambar styraciflua, Lupinus polyphyllus, Macroptilium lathyroides, Malus domestica, Malva sylvestris, Matricaria chamomilla, Medicago lupulina, Medicago sativa, Melilotus albus, Melissa officinalis, Mentha arvensis, Mercurialis annua, Monarda fistulosa, Myrtus communis, Narcissus tazetta, Nicotiana tabacum, Oenothera biennis, Olea europaea, Origanum vulgare, Oxalis sp., Paeonia suffruticosa, Paeonia tenuifolia, Parietaria judaica, Parietaria officinalis, Pastinaca sativa, Persicaria maculosa, Petroselinum, Phaseolus vulgaris, Picris hieracioides, Pistacia vera, Pisum sativum, Plantago lanceolata, Plantago major, Polygonum aviculare, Portulaca oleracea, Potentilla reptans, Prunella vulgaris, Prunus armeniaca, Prunus avium, Prunus domestica, Prunus dulcis, Prunus mahaleb, Prunus mume, Prunus persica, Punica granatum, Pyrus communis, Raphanus sativus, Rhododendron sp., Rubia peregrina, Rubus fruticosus, Rumex acetosa, Salix alba, Salix babylonica, Salvia miltiorrhiza, Salvia rosmarinus, Salvia sclarea, Sambucus nigra, Saponaria officinalis, Senecio vulgaris, Setaria viridis, Silene latifolia subsp. alba, Silene noctiflora, Silene vulgaris, Solanum glaucophyllum, Solanum lycopersicum, Solanum melongena, Solanum nigrum, Solanum tuberosum, Sonchus oleraceus, Sonchus sp., Sophora alopecuroides, Sorghum halepense, Spartium junceum, Spinacia oleracea, Styphnolobium japonicum, Tagetes erecta, Taraxacum officinale, Thymus vulgaris, Trifolium medium, Trifolium pratense, Trifolium repens, Trigonella foenum-graecum, Triticum aestivum, Tussilago farfara, Ulmus glabra, Urtica dioica, Urtica urens, Vaccinium corymbosum, Valeriana officinalis, Veronica persica, Viola odorata, Vitex agnus-castus, Vitis vinifera, Zea mays
GEOGRAPHICAL DISTRIBUTION 2021-06-11
A yellows-type disease, named ‘stolbur’, was found several decades ago affecting various plants in the Solanaceae family (mainly potato and tomato) in Southern and Eastern Europe (CABI, 2020). Unusual symptoms of reddening were first observed on maize in 1957 in Serbia, and disease was called maize redness (Duduk & Bertaccini, 2006). The first observation of lavender decline is from France in the late 1960s (Sémétey et al., 2018). A yellows-type disease of grapevine, named bois noir was first reported in 1961 in vineyards in North-Eastern France, and a few years later, similar symptoms were observed in vineyards in the Mosel and Rhine valleys in Germany. The disease was named ‘Vergilbungskrankheit’ and further studies showed that this was the same disease as bois noir (Belli et al., 2010). Soon after bois noir was observed in France and Germany, it was reported in many countries in the Euro-Mediterranean area (a few reports were also made in other continents), where it is responsible for serious crop losses (Gajardo et al., 2009; Belli et al., 2010). Quaglino et al. (2013) demonstrated that phytoplasmas associated with stolbur, maize redness, lavender decline, and yellows-type diseases of grapevine and other wild and cultivated plants, are members of the same species i.e. 'Ca. Phytoplasma solani'.EPPO Region: Albania, Armenia, Austria, Azerbaijan, Bosnia and Herzegovina, Bulgaria, Croatia, Czech Republic, France (mainland), Georgia, Germany, Greece (mainland), Hungary, Israel, Italy (mainland, Sicilia), Jordan, Kyrgyzstan, Moldova, Montenegro, North Macedonia, Poland, Russia (Central Russia, Southern Russia), Serbia, Slovakia, Slovenia, Spain (mainland), Switzerland, Turkey, Ukraine, Uzbekistan
Asia: China (Shaanxi, Shandong), India (West Bengal), Iran, Israel, Japan (Shikoku), Jordan, Kyrgyzstan, Lebanon, Saudi Arabia, Taiwan, Tajikistan, Uzbekistan
South America: Chile
'Ca. Phytoplasma solani’ is not seed transmissible but can be transmitted by grafting and vegetative propagation of infected hosts, such as potato, tomato, grapevine, strawberry and lavender (EFSA, 2014). In diseased plants, phytoplasmas are restricted to the phloem sieve tubes, and are naturally transmitted between plants mainly by phloem-sap-feeding leafhoppers, planthoppers or psyllids (see below) as well as by parasitic plant species (see Pathways for movement) (Weintraub & Beanland, 2006).
In the Euro-Mediterranean region, 'Ca. Phytoplasma solani’ is usually transmitted from plant to plant by the polyphagous insect vector Hyalesthes obsoletus (Cixiidae) which is native to Europe and is ubiquitous in European countries. The acquisition stage is achieved by overwintering nymphs feeding on infected roots. All infected crops except lavender are generally epidemiological dead-end hosts for 'Ca. Phytoplasma solani’, as its main vector H. obsoletus does not develop on these crops (Weintraub & Beanland, 2006; Johannesen et al., 2008; Sémétey et al., 2018), but only incidentally transmits the phytoplasma from other host plants to these crops during its feeding probing at the adult stage. The same situation applies to many wild/weed hosts, but some weeds, such as bindweed and stinging nettle, act as plant reservoirs, hosting both 'Ca. Phytoplasma solani’ and its vector (Langer & Maixner, 2004; Bressan et al., 2007). There is no transovarial transfer of 'Ca. Phytoplasma solani’ from infected female planthopper vectors to their progeny. Therefore, the average six-week activity period of adult H. obsoletus feeding on annual plants could explain their infection. In addition, such plants are probably hosts (or incidental hosts) of one or more alternative vectors which could also transmit the phytoplasma between these plants, and these vectors are probably present in the agro-system as adults for a longer period during the same vegetative season (Weintraub & Beanland, 2006; EFSA, 2014; Mori et al., 2014b; CABI, 2020).
Within the other known vectors, the planthopper Reptalus panzeri has been reported as a natural vector of ‘Ca. Phytoplasma solani’ isolates causing maize redness and bois noir in Serbia (Jović et al., 2009; Cvrković et al., 2014). Adult R. panzeri lay eggs on infected maize roots. If these roots are infected, nymphs feeding on them will acquire the phytoplasma. The nymphs overwinter on the roots of wheat planted in maize fields in autumn or on Johnson grass (Sorghum halepense), allowing the emergence of infectious vectors the following summer (Jović et al., 2009; Cvrković et al., 2014). The planthopper Pentastiridius leporinus has been reported to transmit ‘Ca. Phytoplasma solani’ to sugar beet (Gatineau et al., 2001; EFSA, 2014). Anaceratagallia ribauti has been reported as a vector in Austria (Riedle-Bauer et al., 2008). Reptalus quinquecostatus has been reported as a putative vector in Serbia and France, but its capability to transmit the phytoplasma to plants has not been established (Chuche et al., 2016; Mitrović et al., 2016).
DETECTION AND IDENTIFICATION 2021-06-11
In Europe and in the Mediterranean basin, ‘Ca. Phytoplasma solani’ strains are associated with bois noir disease of grapevine, with stolbur disease in wild and cultivated herbaceous and woody plants, and with yellowing, reddening, decline, dwarfism, leaf malformation and degeneration diseases of other plants (Quaglino et al., 2013). The symptoms of ‘Ca. Phytoplasma solani’ infection are variable, depending on environmental factors. Annual crops develop symptoms a few weeks after inoculation by the insect, whereas symptoms on perennial hosts can appear one or more years after inoculation (EFSA, 2014).
On grapevine (bois noir disease)
‘Ca. Phytoplasma solani’ infection of grapevine, also known as bois noir disease, produces leaf yellows (in white-berried cultivars) or leaf reddening (in red-berried cultivars), downwards leaf rolling, irregular ripening of wood, growth reduction, and shriveling and drying up of berries and bunches. Young plants can die following infection, while older plants tend to recover (Belli et al., 2010). The severity of the symptoms depends on cultivar sensitivity (EFSA, 2014). The symptoms caused by ‘Ca. Phytoplasma solani’ cannot be distinguished from those caused by grapevine flavescence dorée. Symptoms are illustrated in EPPO (2018b).
On potato (potato stolbur)
Symptoms of ‘Ca. Phytoplasma solani’ on potato plants include upward rolling and purplish or red discoloration of the top leaves, shortened internodes, aerial tubers, early senescence and, finally, plant wilting and death (Holeva et al., 2014; Mitrović et al., 2016).
On tomato (tomato stolbur)
Typical symptoms on tomato plants infected with ‘Ca. Phytoplasma solani’ are short internodes near to the plant apex and smaller curled leaves with thicker tissues. The leaves are discoloured and show yellowing or purpling. Adventitious roots sometimes appear on the stem. Plants infected early are bushy because of the development of numerous axillary buds. The flowers of infected plants are abnormally straight, they are sterile and have altered morphological development: (i) sepals, with purple veins, remain completely sealed and the calyx is enlarged (big bud); (ii) petals are green with stamens of the same colour (virescence); (iii) sepals may be leaf-like (phyllody); (iv) dysfunction may occur in flower differentiation. Fewer fruits are produced, and they are smaller, lacking colour, and dense (CABI, 2020).
On maize (maize redness)
Symptoms on Zea mays caused by ‘Ca. Phytoplasma solani’ infection appear in late July and continue to intensify until the beginning of September. Typical symptoms are reddening of the leaf midrib, followed by reddening of leaves and stalks and then whole-plant desiccation. Ear development is abnormal and seed set is greatly reduced (Duduk & Bertaccini, 2006; Jović et al., 2007).
On lavender (lavender decline)
Early symptoms of lavender decline are low vigour and leaf yellowing, then the canopy of infected lavender dries in sectors and plants eventually die (Sémétey et al., 2018).
Symptom description in strawberry is available in EPPO (2017b).
Under transmission electron microscopy, phytoplasmas are pleomorphic, as they can appear in many shapes and sizes (Waters & Hunt, 1980). They can almost completely fill the phloem sieve tubes (Dermastia et al., 2017).
Detection and inspection methods
Plants, especially the leaves, should be inspected for symptoms. Attention should be paid to the presence of the leafhopper vectors. Where appropriate, samples for laboratory testing should be taken for the final identification of the pest. Crop inspection procedures for strawberry plants for planting (EPPO, 2017b), potatoes (EPPO, 2007), vegetable plants for planting (EPPO, 2016), and grapevine plants for planting (EPPO, 2018b) have been developed.
Various PCR based tests have been developed to detect ‘Ca. Phytoplasma solani’. A widely applied procedure is based on nested PCR amplification with phytoplasma-universal primer pairs, followed by sequencing or restriction fragment length polymorphism (RFLP) analyses (Lee et al., 1998; EPPO, 2018a). An online phytoplasma classification tool iPhyClassifier can be used for sequence similarity analysis and generation of virtual RFLP profiles (Wei et al., 2007; Zhao et al., 2009). Multiplex nested PCR developed by Clair et al. (2003) allows the detection of ‘Ca. Phytoplasma solani’ and allows it to be distinguished from grapevine flavescence dorée phytoplasma. Several real-time PCR tests have also been developed for ‘Ca. Phytoplasma solani’ detection (e.g. Angelini et al., 2007; Hren et al., 2007; Pelletier et al., 2009). Loop mediated isothermal amplification (LAMP) can be used for on-site detection as well as for screening in laboratories (Kogovšek et al., 2017).
PATHWAYS FOR MOVEMENT 2021-06-11
‘Ca. Phytoplasma solani’ is naturally dispersed over fairly long distances by its planthopper vectors (see Biology). It can be transmitted by the parasitic plant dodder (Cuscuta campestris, C. epilinum, C. trifolii). In addition, the plant Orobanche aegyptiaca, which parasitizes roots of diseased tomato plants, has been shown to contain phytoplasmas, so it could be involved in transmission in the field. ‘Ca. Phytoplasma solani’ is not thought to be transmitted in the true seed of any of its hosts, but it can be transmitted by vegetative propagation of infected host plants. The phytoplasma has a complex ecology and epidemiological cycle, and a high capability to adapt to different agro-ecosystems. The risk of introduction of ‘Ca. Phytoplasma solani’ to new regions is related to the dispersal of its vectors and to trade in cultivated host plants (e.g., symptomless seedlings) (EFSA, 2014; CABI, 2020).
PEST SIGNIFICANCE 2021-06-11
Severe ‘Ca. Phytoplasma solani’ outbreaks have been reported in potato fields in several countries, including the Czech Republic, Hungary, Romania and Russia, causing significant yield loss (30–80 %) and a reduction in seed potato quality (Paltrinieri & Bertaccini 2007; Girsova et al., 2008; Fialová et al., 2009, Lindner et al., 2011; EFSA, 2014). ‘Ca. Phytoplasma solani’ infection increases the sucrose content of tubers by three- to six-fold; severely affecting the suitability of tubers for fried potato processing (Lindner et al., 2011). In severe epidemics, yield losses as high as 60 % in tomato, 90 % in pepper, and 100 % in celery have been reported (Navrátil et al., 2009). Maize redness has been linked to yield reductions of 40–90 % in Serbia (Jović et al., 2007). As the main symptom caused by ‘Ca. Phytoplasma solani’ on grapevine is the loss of production due to berry shrivel, the economic impact of the disease, especially on susceptible varieties, is significant. As ‘Ca. Phytoplasma solani’ causes symptoms that cannot be distinguished from those caused by grapevine flavescence dorée, high local incidences of ‘Ca. Phytoplasma solani’ infection can severely complicate the surveys for grapevine flavescence dorée (EFSA, 2014). ‘Ca. Phytoplasma solani’ also has a high economic impact on lavender crops. Unlike the situation with most crop plants, H. obsoletus can complete its life cycle on lavender; thus, disease propagation is epidemic and lavender fields can be destroyed within 4–5 years in South-Eastern France (EFSA, 2014).
Economic impact of ‘Ca. Phytoplasma solani’ is variable, depending on yearly variations in insect vector abundance, and can also be significant in a range of other hosts. Economic impact may increase in the future from range extension and from increase in density of vector populations as a consequence of climate change (EFSA, 2014).
The use of healthy planting material and control of surrounding weeds that are main hosts of H. obsoletus is considered crucial for ‘Ca. Phytoplasma solani’ control. Trials conducted to control nettle growth with glyphosate or other herbicides significantly reduced the density of emerging adult vectors (Mori et al., 2014a). Neonicotinoid insecticides, applied in early spring, gave protection levels comparable to those of herbicide treatments (Mori et al., 2014a). However, the use of herbicides and insecticides can have negative effects on beneficial insects (e.g. honeybees) as well as human health and biodiversity (EFSA, 2014). Preventive measures such as checking the phytosanitary status of propagation materials, and treating diseased mother plants through thermotherapy, are applied to limit long-distance dissemination and in-ﬁeld spread of the disease (CABI, 2020). Hot water treatment of dormant canes of grapevines may be used to eliminate phytoplasmas (EPPO, 2008; EPPO, 2012). In addition, other strategies to reduce ‘Ca. Phytoplasmas solani’ on grapevines are available, such as treatments with resistance inducers (Romanazzi et al., 2013).
‘Ca. Phytoplasma solani’ is included in the certification system for grapevine (EPPO, 2008), petunia (EPPO, 2002) and seed potato tubers (EPPO, 1999). This reduces the spread and impact associated with the plants for planting pathway.
‘Ca. Phytoplasma solani’ may cause serious losses in economically important cultivated species, such as grapevine, maize, potato, tomato. In addition, it can survive and complete its life cycle without cultivated host plants, because wild plants are main hosts of ‘Ca. Phytoplasma solani’. ‘Ca. Phytoplasma solani’ and its main vector have been found in different agro-ecosystems in many countries in Europe and the eastern Mediterranean area. In terms of disease epidemiology, the wide range of the vector’s host plants and ‘Ca. Phytoplasma solani’ plant hosts are factors which should be considered. Disease control is difficult in the field, and there is limited information about effective methods to control the insect vector or about the availability of resistant/tolerant crops. Finally, climate change might significantly influence the epidemiology of ‘Ca. Phytoplasma solani’ diseases.
PHYTOSANITARY MEASURES 2021-06-11
To prevent the introduction and spread of ‘Ca. Phytoplasma solani’, import requirements for different host species apply worldwide. These requirements can vary with regards to crop and prevalence at the place of origin. When deregulated as a quarantine pest, ‘Ca. Phytoplasma solani’ was recommended for regulation as a regulated non-quarantine pest (RNQP) for seed potatoes and propagation material of Lavandula and Vitis during the EU Quality pest project (Picard et al., 2018).
EPPO countries where ‘Ca. Phytoplasma solani’ does not occur, or where it is not widely distributed, may regulate it. If they do, EPPO recommends that they should require measures for import of seed potatoes (except microplants and minitubers). According to EPPO Standard PM 8/1 (EPPO, 2017a) seed potatoes imported from a country where the pest occurs should come from a pest-free area according to EPPO Standard PM 3/61 (EPPO, 2019b) or a pest-free place of production for ‘Ca. Phytoplasma solani’ since the last growing season. In addition, post-entry quarantine programs are established to allow safe movement of potato germplasm for research and breeding purposes. During post-entry quarantine for potato, it is recommended that Phytoplasmas should be tested for by using universal phytoplasma primers (EPPO, 2019a).
As well as preventing introduction, it is essential to start cultivation with non-infected plants. Therefore, the absence of the phytoplasma in germplasm, mother plants and nuclear stock should be assured before the start of breeding, propagation and/or production of plants. During the EU Quality pest project, recommended measures included a zero tolerance for all categories of seed potatoes, Lavandula and Vitis, based on absence of symptoms and/or testing.
There is no possibility of complete eradication of ‘Ca. Phytoplasma solani’ from the natural environment.
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CABI resources used when preparing this datasheet
CABI Datasheet on Pest ‘Candidatus Phytoplasma solani’ (Stolbur phytoplasma) (https://www.cabi.org/isc/datasheet/108243; date of the last modification: 10 December 2020; accessed on May 2021)
This datasheet was extensively revised in 2021 by Nataša Mehle (National Institute of Biology, Slovenia). Her valuable contribution is gratefully acknowledged.
How to cite this datasheet?
Datasheet history 2021-06-11
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) Data sheets on quarantine organisms No. 100, stolbur mycoplasm. EPPO Bulletin 8(2), 115-120. https://doi.org/10.1111/j.1365-2338.1978.tb02782.x