Candidatus Phytoplasma solani (Stolbur phytoplasma)
- Summary of Invasiveness
- Taxonomic Tree
- Notes on Taxonomy and Nomenclature
- Distribution Table
- History of Introduction and Spread
- Risk of Introduction
- Hosts/Species Affected
- Growth Stages
- List of Symptoms/Signs
- Biology and Ecology
- Means of Movement and Dispersal
- Plant Trade
- Vectors and Intermediate Hosts
- Impact Summary
- Economic Impact
- Environmental Impact
- Social Impact
- Risk and Impact Factors
- Detection and Inspection
- Similarities to Other Species/Conditions
- Prevention and Control
- Gaps in Knowledge/Research Needs
- Links to Websites
- Distribution Maps
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PicturesTop of page
IdentityTop of page
Preferred Scientific Name
- Candidatus Phytoplasma solani Quaglino et al., 2013
Preferred Common Name
- Stolbur phytoplasma
Other Scientific Names
- Phytoplasma solani
International Common Names
- English: black wood of grapevine; grapevine 'bois noir'; maize redness; metastolbur; parastolbur; potato stolbur disease; stolbur
- French: bois noir de la vigne
- German: Vergilbungskrankheit der Rebe
Local Common Names
- France: dépérissement de la lavande
- Italy: legno nero
Summary of InvasivenessTop of page
Phytoplasmas are cell-wall-less plant pathogenic bacteria of the class Mollicutes, which inhabit the phloem sieve tubes of plants and have been associated with several hundred diseases affecting economically important crops. Over the past few decades ‘Candidatus Phytoplasma solani’, belonging to the 16SrXII-A ribosomal subgroup, has been found to cause a range of plant diseases in different agro-ecosystems in many countries in Europe and the eastern Mediterranean area and a number of others all over the world. It is thought likely that it has always been present, at least in its European range, but has only been noticed in recent years. Diseases caused include bois noir in grapevines, stolbur in tomatoes, potatoes and other wild and cultivated plants, maize redness, lavender decline, and yellowing, reddening, decline, dwarfism, leaf malformation and degeneration diseases of other plants. 'Ca. P. solani’ is usually transmitted from plant to plant by the polyphagous insect vector Hyalesthes obsoletus (Cixiidae) which, although it can complete its life cycle on only a small number of plant species, feeds on a much wider range. Recent studies have demonstrated the presence of additional insect vectors of this phytoplasma in Europe, such as Reptalus panzeri in Serbia, possibly R. quinquecostatus in Serbia and France, and Anaceratagallia ribauti in Austria. This scenario highlights the extreme complexity of the ecology of both ‘Ca. Phytoplasma solani’ and its insect vectors, underlying the difficulty in studying the epidemiology of diseases associated with this pathogen and in developing efficient control strategies. ‘Ca. Phytoplasma solani’ is also transmitted by parasitic plants and by grafting and vegetative propagation of infected host plants; it can be spread when host plants are transported by people. In the European Union it is listed as a harmful organism necessitating restrictions on the import of plants in the family Solanaceae.
Taxonomic TreeTop of page
- Domain: Bacteria
- Phylum: Firmicutes
- Class: Mollicutes
- Order: Acholeplasmatales
- Family: Acholeplasmataceae
- Genus: Candidatus Phytoplasma
- Species: Candidatus Phytoplasma solani
Notes on Taxonomy and NomenclatureTop of page
Phytoplasmas are cell-wall-less plant pathogenic bacteria of the class Mollicutes with a small genome size, which ranges from 530 to 1350 kilobases (Marcone, 2014). Based on unique molecular and biological features, they have been classified into 40 species within the provisional genus ‘Candidatus Phytoplasma’ (International Research Programme for Comparative Mycoplasmology Phytoplasma\Spiroplasma Working Team - Phytoplasma Taxonomy Group, 2004; Marcone, 2014); moreover, taxonomic groupings have been delimited according to the similarity coefficients derived from the comparison of collective restriction profiles of the 16S rRNA gene sequence digested with a selected pool of endonucleases (Lee et al., 1998; Wei et al., 2008; Zhao et al., 2009).
Phytoplasmas classified in the 16S rRNA gene RFLP group 16SrXII infect a wide range of wild and cultivated plants worldwide and are transmitted by polyphagous planthoppers of the family Cixiidae. Three species of the ‘Ca. Phytoplasma’ genus have thus far been formally described within group 16SrXII: (i) ‘Candidatus Phytoplasma australiense’, infecting the grapevine and other plant hosts in Australia and New Zealand; (ii) ‘Candidatus Phytoplasma japonicum’, infecting the Japanese hydrangea (Hydrangea macrophylla) in Japan; and (iii) ‘Candidatus Phytoplasma fragariae’, infecting the strawberry in Europe (Quaglino et al., 2013; Sawayanagi et al., 1999).
According to IRPCM guidelines (International Research Programme for Comparative Mycoplasmology Phytoplasma\Spiroplasma Working Team - Phytoplasma Taxonomy Group, 2004), phytoplasmas sharing >97.5% 16S rDNA nucleotide sequence similarity can be described as separate species if they are clearly distinguished by evident molecular diversity and ecological niche. 'Ca. Phytoplasma solani’ shares 97.6% 16S rDNA sequence similarity with ‘Ca. Phytoplasma australiense’. Based on Quaglino et al. (2013), ‘Ca. Phytoplasma solani’ strains share an intra-species sequence similarity remarkably and consistently greater than the inter-species similarity between ‘Ca. Phytoplasma solani’ and ‘Ca. Phytoplasma australiense’ strains, and constitute a distinct gene pool. Moreover, 'Ca. Phytoplasma’ species within group 16SrXII possess distinct biological properties. 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. Hyalesthes obsoletus, the most common vector, is not known to transmit any other phytoplasma, possibly indicating a long and intimate co-evolution of phytoplasma and vector, and a unique phytoplasma-vector association distinguishing ‘Ca. Phytoplasma solani’ from other species. In summary, the distinct molecular characteristics and unique vectorship support recognition of ‘Ca. Phytoplasma solani’ as a distinct species in the genus ‘Ca. Phytoplasma’.
On the basis of unique biological properties and exclusive molecular markers within multiple genes (tufB, rplV-rpsC, secY), phytoplasma strains associated with stolbur and stolbur-related diseases in wild and cultivated herbaceous and woody plants and with bois noir (BN) disease in cultivated grapevines have been attributed to the species ‘Candidatus Phytoplasma solani’ (‘Ca. P. solani’) (Quaglino et al., 2013). Briefly, to be classified as ‘Ca. P. solani’, a strain should (i) share >99% sequence similarity with a minimum of 1.2kb (fragment F2n/R2) within the 16S rRNA gene of the reference strain STOL; (ii) contain the identical STOL-unique 16S rDNA signature sequence (5’-ATTTTTAAAAGACCTAGCAATAGGTATGCTTAG-3’, nt 189..221); and (iii) contain both distinguishing sequence blocks (DSBs) sequences [DSB1 (5’-ATGGTGGAAAAACCATTATGACGGTACCT-3’, nt 452..480) and DSB2 (5’-GCAACGCTCAACGTTGTGATGCTATA-3’, nt 602..627)] noted for the reference strain STOL, 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. P. solani’-related strains (Quaglino et al., 2013).
Many different strains have been identified by molecular characterization, mainly based on tufB, secY, vmp1 and stamp sequencing (Fabre et al., 2011; Fialova et al., 2009; Murolo and Romanazzi, 2015; Quaglino et al., 2016). Distribution of these genotypes among the different host plants seems to be specific (Kosovac et al., 2016; Kosovac et al., 2019). Based on similarity coefficients generated by comparison of restriction fragment length polymorphism (RFLP) profiles, ‘Ca. P. solani’ strains are classified into taxonomic subgroups 16SrXII-A, -F, -G, -J, and -K, distinguished by unique patterns from digestions carried out by the enzymes AluI, BfaI, BstUI, and MseI. Moreover, alignments of 16S rDNA nucleotide sequences revealed the presence of several 16S rDNA single nucleotide polymorphism (SNP) lineages among ‘Ca. P. solani’ strains based on mutations at nucleotide positions 43, 469, 488, 747, 875, 971, and 1219 from the annealing site of the primer F2n (Quaglino et al., 2017).
DescriptionTop of page
Phytoplasmas are cell-wall-less plant pathogenic bacteria of the class Mollicutes, with a small genome size which ranges from 530 to 1350 kilobases (Marcone, 2014).
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|
|Azerbaijan||Present||2010||Balakishiyeva et al., 2010; Balakishiyeva et al., 2016; EPPO, 2018|
|China||Present, few occurrences||2010||Duduk et al., 2010; EPPO, 2018|
|-Shaanxi||Present||2015||Yang et al., 2016; EPPO, 2018|
|-Shandong||Present, few occurrences||2015||Gao et al., 2013; EPPO, 2018|
|Georgia (Republic of)||Present||2014||Quaglino et al., 2014; Quaglino et al., 2016; EPPO, 2018|
|India||Present, few occurrences||EPPO, 2018|
|-West Bengal||Present, few occurrences||2014||Chinmay Biswas et al., 2014; EPPO, 2018|
|Iran||Present||2010||Karimi et al., 2009; Rashidi et al., 2010; Zirak et al., 2010; Hosseini et al., 2011; Allahverdi et al., 2014; Mirchenari et al., 2015; Zamharir and Taheri, 2017; Zamharir et al., 2017; EPPO, 2018|
|Israel||Present, few occurrences||1970||Zimmerman-Gries, 1970; Tanne and Nitzany, 1973; Kuszala et al., 1993; Boudon-Padieu, 1996; EPPO, 2018|
|Jordan||Present||2012||Salem et al., 2013; EPPO, 2014; EPPO, 2018|
|Korea, Republic of||Present||2013||Chung et al., 2013|
|Lebanon||Localised||2002||Choueiri et al., 2002; Karimi et al., 2009; EPPO, 2018|
|Saudi Arabia||Present||1971||Yaman, 1971; EPPO, 2018|
|Syria||Present||2011||Contaldo et al., 2011|
|Turkey||Localised||2001||Ozdemir et al., 2009; Eroglu et al., 2010; Canik et al., 2011; Alp et al., 2016; EPPO, 2018|
|Niger||Present||1988||Reckhaus et al., 1988; EPPO, 2018|
|Tunisia||Absent, formerly present||EPPO, 2018|
|Chile||Present||2009||Gajardo et al., 2009; EPPO, 2018|
|Albania||Present||2003||Myrta et al., 2003; EPPO, 2018|
|Austria||Present, few occurrences||2003||Riedle-Bauer et al., 2008; EPPO, 2018|
|Bosnia-Hercegovina||Present||2006||Delić et al., 2006; Kovačević et al., 2014; Delić et al., 2016; EPPO, 2018|
|Bulgaria||Localised||2007||Sakalieva et al., 2007; Bobev et al., 2013; Genov et al., 2014; EPPO, 2018|
|Croatia||Localised||2000||Seruga et al., 2000; Voncina and Cvjetkovic, 2007; Plavec et al., 2015; EPPO, 2018|
|Cyprus||Absent, formerly present||EPPO, 2018|
|Czech Republic||Present, few occurrences||2004||Mertelik et al., 2004; Fialova et al., 2009; Franova et al., 2009; Navratil et al., 2011; Stary et al., 2013; EPPO, 2018|
|France||Localised||1961||Cousin et al., 1971; Daire et al., 1993; Kuszala et al., 1993; Cimerman et al., 2009; EPPO, 2018|
|Germany||Localised||1971||Seemuller et al., 1994; Maixner et al., 1995; EPPO, 2018|
|Greece||Localised||2013||Lotos et al., 2013; Holeva et al., 2014; Moraki et al., 2014; EPPO, 2018|
|Hungary||Localised||2006||Palermo et al., 2006; Acs et al., 2011; EPPO, 2018|
|Italy||Localised||1982||Marcone et al., 1997; Minucci and Boccardo, 1997; Terlizzi et al., 2006; Iriti et al., 2008; Berger et al., 2009; Belli et al., 2010; Calari et al., 2010; EPPO, 2018|
|Macedonia||Widespread||2014||Kostadinovska et al., 2014; Atanasova et al., 2015; EPPO, 2018|
|Moldova||Absent, unreliable record||EPPO, 2018|
|Montenegro||Widespread||2009||Radonjić et al., 2009; Radonjic et al., 2016; EPPO, 2018|
|Netherlands||Absent, confirmed by survey||EPPO, 2018|
|Poland||Present, few occurrences||1999||Żandarski, 1999; Zwolinska et al., 2012; EPPO, 2018|
|Portugal||Absent, confirmed by survey||EPPO, 2014|
|Romania||Absent, formerly present||2011||Ember et al., 2011; Lindner et al., 2011; EPPO, 2018|
|Russian Federation||Localised||EPPO, 2018|
|-Central Russia||Present||2008||Girsova et al., 2008; EPPO, 2018|
|-Southern Russia||Present||2011||Ember et al., 2011; EPPO, 2018|
|Serbia||Localised||2006||Adamovic et al., 2014a; Adamovic et al., 2014b; Pavlovic et al., 2014a; Pavlovic et al., 2014b; Duduk and Bertaccini, 2006; Jović et al., 2007; Jović et al., 2009; Ivanović et al., 2011; Trkulja et al., 2011; Josic et al., 2012; Pavlovic et al., 2012; Josic et al., 2013; Josic et al., 2015; Mitrović et al., 2016; Trkulja et al., 2016; EPPO, 2018|
|Slovenia||Localised||2011||Mehle et al., 2011; EPPO, 2018|
|Spain||Localised||1995||Avinent and Llàcer, 1995; Batlle et al., 1995; Alfaro-Fernandez et al., 2011; Sabaté et al., 2014; EPPO, 2018|
|Switzerland||Localised||2002||Gugerli et al., 2002; EPPO, 2018|
|UK||Transient: actionable, under eradication||2015||Hodgetts et al., 2015; EPPO, 2018|
|New Zealand||Absent, unreliable record||EPPO, 2018|
History of Introduction and SpreadTop of page
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 (transmitted by the cixiid planthopper Hyalesthes obsoletus): on pepper in southern Russia (Sukhov and Vovk, 1946) and Yugoslavia (Panjan, 1950), and on tomatoes in Italy (Ciccarone, 1951) and France (Cousin et al., 1968). In France, lavender (Lavandula angustifolia) and lavandin (L. latifolia x L. angustifolia) were found in 1970 to be affected by a yellows-type decline, named “dépérissement jaune” (Cousin et al., 1970). The disease was associated with the presence of stolbur phytoplasma, transmitted by H. obsoletus. Stolbur phytoplasma was also spread by vegetative propagation through lavender and lavandin nurseries.
In parallel, a yellows-type disease of grapevine, named "bois noir" (BN) was first reported in 1961 in vineyards of north-eastern France. Its symptoms were indistinguishable from those of Flavescence dorée (FD) but, because it was spreading more slowly, it was considered a non-epidemic form of FD. Later it was established that BN was a disease distinct from FD, primarily on the basis of its non-transmissibility by the leafhopper Scaphoideus titanus. A few years later, similar symptoms were observed in vineyards of the Mosel and Rhine valleys in Germany, where S. titanus did not occur. Experimental evidence showed that this disease, originally named “Vergilbungskrankheit” (VK), was transmitted by H. obsoletus. Further studies showed that BN and VK were the same disease (Belli et al., 2010). Following these first reports, BN spread to many countries in the Euro-Mediterranean area and some in other continents, where it is responsible for serious crop losses (Gajardo et al., 2009; Belli et al., 2010).
Molecular tools have now demonstrated that phytoplasmas associated with stolbur, stolbur-related and yellows-type diseases of solanaceous plants, grapevine, lavandin and other wild and cultivated plants are members of the same species, determined as 'Candidatus Phytoplasma solani' (Quaglino et al., 2013).
Hyalesthes obsoletus, the main insect vector of Ca. Phytoplasma solani’, has a European origin and is ubiquitous in the European countries. Although phytoplasmas were discovered at the end of the 1960s, phytoplasma-like symptoms on plants had been reported previously (erroneously associated with viruses for their plant-to-plant transmissibility). For these reasons, it is reasonable to hypothesize that the pathogen has always been widespread in much of its current range but has only been noticed in recent decades.
Risk of IntroductionTop of page
Due to its complex ecology and epidemiological cycle, and its high capability to adapt to different agro-ecosystems, the risk of introduction of ‘Ca. Phytoplasma solani’ is related to the dispersal of its vectors and to the trade in cultivated host plants (e.g. symptomless seedlings). Pathways of transmission and propagation are determined by the interaction between the host plants and the insect vectors. Several native plants as reservoirs and many hemipteran species as vectors contribute to rapid and wide expansion in the field. ‘Ca. Phytoplasma solani’ has a wide range of diverse host plants, although many of them represent dead-end hosts because the vectors do not develop on them.
In the European Union it is listed as a harmful organism necessitating restrictions on the import of plants in the family Solanaceae (EFSA Panel on Plant Health, 2014).
Hosts/Species AffectedTop of page
Phytoplasmas as a group have been associated with several hundred diseases affecting economically important crops, such as ornamentals, vegetables, fruit trees and grapevines (Bertaccini et al., 2014). As for ‘Ca. Phytoplasma solani’ in particular, more than 100 plant species, belonging to 40 different families and 22 orders, have been described as being infected by it; they include many wild plants, ornamental plants and major and minor crops. Crops affected include tomato, potato, tobacco, pepper (Capsicum annuum), celery, carrot, parsley, garden bean, grape and maize (EFSA Panel on Plant Health, 2014). Many different strains of ‘Ca. Phytoplasma solani’ have been identified by molecular characterization, mainly based on tufB, secY, vmp1 and stamp sequencing (Fabre et al., 2011; Fialova et al., 2009; Murolo and Romanazzi, 2015; Quaglino et al., 2016); distribution of these genotypes among the different host plants seems to be specific (Kosovac et al., 2016; Kosovac et al., 2019). Generally, the crop host (e.g., grapevine, potato, tomato) represents a dead-end host for ‘Ca. Phytoplasma solani’, which is only incidentally transmitted by the vector Hyalesthes obsoletus from other host plants to the crop during its feeding probing (Weintraub and Beanland, 2006). For example, the nettle (Urtica dioica) allows the development of both ‘Ca. Phytoplasma solani’ and H. obsoletus, while the grapevine (Vitis vinifera) can be affected by the pathogen but not constitute a host plant of the vector (Johannesen et al., 2008). Adult H. obsoletus can feed on grapevines occasionally and so transmit the pathogen, but do not do so often enough to be likely to pick it up from the plant; grapevines and other crops are not a suitable food source for nymphs, which acquire the pathogen when they feed over the winter on the roots of a limited number of wild host species (including nettles, bindweed and Vitex agnus-castus). Lavender is an exception among crop plants in that H. obsoletus can complete its life cycle on it and acquire the pathogen from it; microsatellite analysis indicates that there are lavender-specific strains (Séméty et al., 2018).
Three main natural ecologies have been described: (1) the host system bindweed - H. obsoletus - crop, related to type tuf-b strains; (2) the host system nettle - H. obsoletus - crop, related to type tuf-a; and (3) the host system Calystegia sepium - H. obsoletus - crop, related to type tuf-c (Langer and Maixner, 2004). In detail, Convolvulus arvensis (bindweed) and Urtica dioica (nettle) have been reported as being the main host plants of H. obsoletus in Europe (Mori et al., 2013). Several weeds, such as Chenopodium album and Malva sylvestris, host 'Ca. Phytoplasma solani’ and can play a role in its diffusion (Marchi et al., 2015; Mori et al., 2015).
Perennial plants are the main reservoirs of the phytoplasma and hosts of the vectors (Weintraub and Beanland, 2006), but annual plants (both wild and cultivated) could play a role in the diffusion of the phytoplasma. Firstly, these plants (generally weeds) could favour the phytoplasma diffusion over the years by means of seeds, as reported for other annual plants (Olivier et al., 2009) – however, ‘Ca. Phytoplasma solani’ is not thought to be transmitted in the true seed of any of its hosts. Secondly, some infections in the weeds might result from alternative epidemiological cycles with alternative vectors, with or without relation to the main crops. As H. obsoletus becomes infected during its larval stage, and its larval development is not possible on annual species, it cannot acquire ‘Ca. Phytoplasma solani’ from these plants. Considering the average six weeks activity period of adult H. obsoletus, feeding of infective adult vectors on annual plants could explain their infection. On the other hand, such plants could constitute the inoculation target and the acquisition source of one or more alternative vectors, probably present in the agro-system as adults for a longer period, during the same vegetative season (Mori et al., 2015).
Growth StagesTop of page Flowering stage, Fruiting stage, Seedling stage, Vegetative growing stage
SymptomsTop of page
Symptoms of the ‘Ca. Phytoplasma solani’-associated diseases affecting major crops are described in the following paragraphs. Diseases caused in other plants include yellowing, reddening, decline, dwarfism, leaf malformation and degeneration diseases.
In almost all varieties of Vitis vinifera L., ‘Ca. Phytoplasma solani’ produces typical grapevine yellows (GY) symptoms, including desiccation of inflorescences, berry shrivel, leaf discoloration, reduction of growth and irregular ripening of wood (Belli et al., 2010).
Symptoms of phytoplasma-infected tomato plants generally appear during summer. Internodes near to the plant apex are shorter and present smaller curled leaves with ticker tissues. The leaves are discoloured and/or show yellowing/purpling. Adventitious roots sometimes appear on the stem. Plants infected early are bushy because of the development of numerous axillary buds. The flowers are abnormally straight, they are sterile and they show different morphological changes: (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, uncoloured, and dense, leading to a significant yield loss.
Plants grown from infected tubers give rise to normal or spindly sprouts (hair-sprouting). Where normal sprouts arise, symptoms are first apparent about 60-80 days after sowing, as a yellowing and rolling of the leaves. This is followed by production of aerial stolons and tubers in different parts of the stems close to the axils (Mitrovic et al., 2016).
Symptoms of the disease begin to appear in late July and continue to intensify until the beginning of September. Midrib reddening is the first symptom to appear, followed by reddening of leaves and stalks and then whole-plant desiccation. Maize redness is also associated with abnormal ear development and reduced seed numbers, leading to yield reduction. Environmental factors play a role in both the intensity and incidence of the disease, with more severe disease being associated with early-planted fields and hot, dry summers (Jovic et al., 2009).
Symptoms of lavender decline are yellowing and either standing up or rolling down of the leaves, and reduction and abortion of inflorescences (Boudon-Padieu and Cousin 1999). As in other phytoplasma diseases, symptoms may be located only on some branches or affect the whole plant. After yellowing, the affected branches dry, resulting in plants with mixed dead and still green branches. After several growth cycles, the plants become completely brown and dry (Boudon-Padieu and Cousin, 1999).
List of Symptoms/SignsTop of page
|Fruit / abnormal patterns|
|Fruit / mummification|
|Inflorescence / abnormal leaves (phyllody)|
|Inflorescence / dieback|
|Inflorescence / discoloration (non-graminaceous plants)|
|Inflorescence / distortion (non-graminaceous plants)|
|Leaves / abnormal colours|
|Leaves / abnormal forms|
|Leaves / leaves rolled or folded|
|Leaves / yellowed or dead|
|Stems / discoloration|
|Stems / discoloration of bark|
|Stems / stunting or rosetting|
|Stems / witches broom|
|Vegetative organs / internal rotting or discoloration|
|Whole plant / dwarfing|
|Whole plant / early senescence|
|Whole plant / plant dead; dieback|
Biology and EcologyTop of page
Phytoplasmas are cell-wall-less plant pathogenic bacteria of the class Mollicutes, with a small genome size which ranges from 530 to 1350 kilobases (Marcone, 2014). In diseased plants, they are restricted to the phloem sieve tubes; they are transmitted between plants by phloem-sap-feeding leafhoppers, planthoppers or psyllids (Weintraub and Beanland, 2006).
The biological complexity of ‘Ca. Phytoplasma solani’-associated diseases has stimulated research on molecular markers of genetic diversity. Multilocus sequence typing (MLST), based on molecular characterization of more variable genes, such as secY, vmp1 and stamp, showed a large variability among ‘Ca. Phytoplasma solani’ strains within the tuf-types (Murolo and Romanazzi, 2015). For example, based on RsaI-RFLP analyses of vmp1 gene amplicons, ‘Ca. Phytoplasma solani’ strain populations show almost 23 digestion profiles. Moreover, based on sequence identity of vmp1 (available for 161 ‘Ca. Phytoplasma solani’ strains) and stamp (available for 195 strains) gene sequences retrieved from NCBI GenBank, it was possible to determine the presence of 80 vmp1 (Vm1 to Vm80) and 46 stamp (St1 to St46) gene sequence variants within ‘Ca. Phytoplasma solani’ strain populations. The overall ratio of the non-synonymous to the synonymous mutations (dN/dS) was >1.0 for vmp1 (dN/dS = 4.567; P = 0.000) and stamp (dN/dS = 2.436; P = 0.008), indicating a high number of non-silent (dN) mutations. Based on phylogenetic analysis of concatenated nucleotide sequences of the genes vmp1 and stamp (available for 76 ‘Ca. Phytoplasma solani’ strains), 49 vmp1/stamp sequence variants were grouped in five vmp1/stamp clusters. The cluster vmp1/stamp-4 included strains (type tuf-A) was associated with the nettle-related biological cycle, while the other four clusters (vmp1/stamp-1, -2, -3, -5) included strains (type tuf-B) associated with the bindweed-related biological cycle (Quaglino et al., 2016).
Molecular epidemiology approaches, using novel vmp1- and stamp-based molecular markers, have increased knowledge of the population structure and dynamics, and transmission routes, of ‘Ca. Phytoplasma solani’ in the Mediterranean area (Murolo and Romanazzi, 2015). For example, recent studies reported (i) the direct epidemiological role of Vitex agnus-castus in the Hyalesthes obsoletus-mediated transmission of ‘Ca. Phytoplasma solani’ to grapevine (Kosovac et al., 2016), and (ii) the ability of Reptalus panzeri to transmit ‘Ca. Phytoplasma solani’ from maize, affected by corn reddening disease, to grapevine (Cvrković et al., 2014). Sequence analysis of tufB gene revealed that three tuf-types of 'Ca. Phytoplasma solani’ were present in diseased crops, as well as in specific plant hosts, suggesting that ecological differences could play a role in its molecular diversification. Up to now, three main natural ecologies have been described: (1) the host system bindweed - H. obsoletus - crop, related to type tuf-b strains; (2) the host system nettle - H. obsoletus - crop, related to type tuf-a; and (3) the host system Calystegia sepium - H. obsoletus - crop, related to type tuf-c (Langer and Maixner, 2004).
ClimateTop of page
|BS - Steppe climate||Tolerated||> 430mm and < 860mm annual precipitation|
|BW - Desert climate||Tolerated||< 430mm annual precipitation|
|Cs - Warm temperate climate with dry summer||Preferred||Warm average temp. > 10°C, Cold average temp. > 0°C, dry summers|
|Cf - Warm temperate climate, wet all year||Preferred||Warm average temp. > 10°C, Cold average temp. > 0°C, wet all year|
|Ds - Continental climate with dry summer||Tolerated||Continental climate with dry summer (Warm average temp. > 10°C, coldest month < 0°C, dry summers)|
|Dw - Continental climate with dry winter||Tolerated||Continental climate with dry winter (Warm average temp. > 10°C, coldest month < 0°C, dry winters)|
|Df - Continental climate, wet all year||Preferred||Continental climate, wet all year (Warm average temp. > 10°C, coldest month < 0°C, wet all year)|
Means of Movement and DispersalTop of page
In Euro-Mediterranean regions, ‘Ca. Phytoplasma solani’ is transmitted by the planthopper Hyalesthes obsoletus Signoret (Homoptera: Cixiide), a polyphagous vector living preferentially on nettle (Urtica dioica L.), bindweed (Convolvulus arvensis L.), mugwort (Artemisia vulgaris L.), and chaste tree (Vitex agnus-castus L.) in and/or around agrosystems (Langer and Maixner, 2004; Sharon et al., 2015). About 19 plant species belonging to 10 different families are known to harbour both nymphs and adults of H. obsoletus, but adults can be observed on more species (Riolo et al., 2012). Generally, the plant crop host (e.g., grapevine, potato, tomato) represents a dead-end host for ‘Ca. Phytoplasma solani’, which is only incidentally transmitted by H. obsoletus from other host plants to the crop during its feeding probing (Weintraub and Beanland 2006), although recent research indicates that H. obsoletus can compete its life cycle on lavender (Séméty et al., 2018). The planthopper Reptalus panzeri has also been reported as a natural vector of ‘Ca. Phytoplasma solani’ in Serbia; 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 (Cvrković et al., 2014; Chuche et al., 2016; Mitrovic et al., 2016). Anaceratagallia ribauti has been reported as a vector in Austria (Riedle-Bauer et al., 2008).
‘Ca. Phytoplasma solani’ can be transmitted by the parasitic plant dodder (Cuscuta campestris, C. epilinum, C. trifolii [C. epithymum]). Orobanche aegyptiaca, parasitizing 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 readily transmissible by grafting (EFSA Panel on Plant Health, 2014), irrespective of whether the stock or the scion is infective. For example, the transmissibility of bois noir (BN) has been tested by grafting healthy grapevines of cv. Chardonnay with buds from either healthy, infected or symptomless vines chosen at random in a vineyard with a low disease incidence. Five-year observations indicated that: (i) BN is graft-transmissible at a rate of less than 3%; (ii) grafting is much more successful when healthy rather than infected plants are used as donors; and (iii) the incubation period of BN in graft-inoculated grapevines may range from five months to as long as two years (Osler et al., 1997).
‘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 (EFSA Panel on Plant Health, 2014). There is conflicting evidence for its transmission in potato tubers (Rich, 1983; Slack, 2001; Paltrinieri and Bertaccini, 2007).
‘Ca. P. solani’ is not transmitted from infected female planthoppers to their progeny (EFSA Panel on Plant Health, 2014).
Due to its complex ecology and epidemiological cycle, and to the 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 the trade in cultivated host plants (e.g., symptomless seedlings).
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|
|Seedlings/Micropropagated plants||Pest or symptoms usually invisible|
Vectors and Intermediate HostsTop of page
Impact SummaryTop of page
Economic ImpactTop of page
Potato stolbur is a serious disease in South Eastern Europe, Russia and the Mediterranean areas (Eroglu et al., 2010). Since 2006, it has also been observed in Germany. Depending on time of infection and environmental conditions, stolbur phytoplasmas cause considerable yield losses and reduce tuber quality (Ember et al., 2011); the main symptoms are top leaf rolling and purplish, shortened internodes, aerial tubers, early senescence and death. Severe outbreaks in European countries have caused significant yield loss (30%-80%) and a reduction in seed potato quality (Paltrinieri and Bertaccini, 2007; Lindner et al., 2011). Phytoplasmal infection severely impairs assimilate translocation, might be responsible for subtle changes in the bioenergetics of the phloem, and influences sugar metabolism. Recent studies have demonstrated that phytoplasmas affect carbohydrate production in infected grapevines. Similarly, carbohydrate metabolism in potatoes may also be affected, which is a likely cause of quality losses in processed potato products like crisps and French fries. In recent years, phytoplasma-induced discoloration of fried potatoes has been discussed more intensively. The dark brown discoloration that occurs during frying is a non-enzymatic reaction caused by an interaction between free aldehyde groups of reducing hexoses like glucose and fructose and free amino groups of amino acids and tuber proteins during high temperature processing. Therefore, the level of reducing sugars is a critical parameter for crisp production as crisps may become dark at high concentrations of reducing sugars during the frying process (Lindner et al., 2011).
From one year to another the effect of phytoplasmas on tomato crops can be very varied. In many situations, a few dispersed diseased plants occur in the crop; because of their low frequency they do not cause concern. On the other hand, considerable damage can occur in tomato crops: the proportion of affected plants may reach 30-40% or, in particularly serious situations, almost all plants. In addition, if infection occurs early, yields can become very low or zero, because of the sterility of many trusses, and the small size of the few fruits produced (Blanchard, 2012). Navratil et al. (2009) report that in severe epidemics, ‘Ca. P. solani’ can cause yield losses of 60 % in tomato, 90 % in pepper, and 100 % in celery.
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. In recent years, due to declining efficacy of the adopted control measures, bois noir disease has been increasing in Europe and in other countries of the Mediterranean basin (Belli et al., 2010).
The main symptoms in maize infected by ‘Ca. P. solani’ are leaf reddening, abnormal ear development, and reduction of seed size. The disease can cause strong yield reductions (40%-90%) and economic losses. (Jovic et al. 2009).
The main symptoms in lavender infected by ‘Ca. P. solani’ are low vigour, leaf yellowing, dried canopy, and in some cases death. 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 (Foissac et al., 2013).
Environmental ImpactTop of page
Most adverse effects associated with ‘Ca. Phytoplasma solani’ are reported in crop plants, and most non-crop hosts (the majority of which are weeds) do not show symptoms; the pathogen is not associated with direct adverse effects in natural habitats.
However, the control strategies used to manage the 'Ca. P. solani'-associated diseases can have negative effects. The use of herbicides against weeds acting as reservoirs (bindweed and stinging nettles) is under evaluation, and the use of insecticides against the vectors has also been studied. However, the use of herbicides and/or insecticides can have negative effects on non-target arthropods such as honeybees (EFSA Panel on Plant Health, 2014; Mori et al., 2014), as well as human health (in particular farmers) and biodiversity.
Social ImpactTop of page
The use of herbicides and/or insecticides to control reservoir hosts or vectors of ‘Ca. Phytoplasma solani’ could potentially have negative effects on human health, in particular that of farmers.
Risk and Impact FactorsTop of page Impact outcomes
- Host damage
- Negatively impacts agriculture
- Negatively impacts cultural/traditional practices
- Negatively impacts forestry
- Negatively impacts human health
- Negatively impacts animal health
- Interaction with other invasive species
- Highly likely to be transported internationally accidentally
- Difficult to identify/detect as a commodity contaminant
- Difficult to identify/detect in the field
- Difficult/costly to control
DiagnosisTop of page
A major improvement in the diagnosis and specific identification of phytoplasmas was achieved when polymerase chain reaction techniques became available. The availability in the NCBI database of the 16S rRNA gene sequences allowed the development of universal PCR assays for the detection of all known phytoplasmas and of phytoplasma-specific PCR protocols for the targeted identification of the pathogens associated with different diseases, including ‘Ca. Phytoplasma solani’. Various protocols were therefore devised for the reliable identification of ‘Ca. Phytoplasma solani’ based on nested PCR for the amplification of universal or group-specific phytoplasma 16S rRNA gene and on restriction fragment length polymorphism (RFLP) analysis of the amplicons using appropriate restriction enzymes for determining subgroup affiliation (Lee et al., 1998).
The more recent multilocus sequence analyses of ribosomal (rplV and rpsC) and extra-ribosomal genes (secY, map, uvrB, degV, and tuf) revealed a high level of genetic heterogeneity among flavescence dorée (FD) and bois noir (BN) phytoplasmas (Langer and Maixner, 2004). In some cases, significant differences among phytoplasmas causing different grapevine diseases were associated with single nucleotide mutations (insertion, deletion and substitution), a condition called SNPs (single nucleotide polymorphisms). The need then became evident for suitable diagnostic tests for a faster and specific detection of grapevine phytoplasmas. The innovative molecular approaches developed so far for this purpose are: (i) real time RT-PCR for FD and BN phytoplasma detection (Bianco et al., 2004; Galetto et al., 2005; Angelini et al., 2007; Margaria et al., 2009; Berger et al., 2009; Pelletier et al., 2009); (ii) nanobiotransducer for FD phytoplasma detection (Firrao et al., 2005); and (iii) multiplex nested PCR for the simultaneous identification of FD and BN agents (Clair et al., 2003).
Detection and InspectionTop of page
Diseases associated with ‘Ca. Phytoplasma solani’ can be recognized by ad hoc inspection methods, carried out in the field (agro-system) and based on the observation of typical symptoms.
Similarities to Other Species/ConditionsTop of page
In almost all varieties of Vitis vinifera L., 'Ca. Phytoplasma solani' produces typical grapevine yellows (GY) symptoms, including desiccation of inflorescences, berry shrivel, leaf discolorations, reduction of growth and irregular ripening of wood (Belli et al., 2010). Thus, based on visual symptom observation, grapevine infection by 'Ca. Phytoplasma solani' cannot be distinguished from infections by other phytoplasmas associated with GY (e.g., flavescence dorée). As the epidemiological cycle of GY complex diseases, associated with distinct phytoplasmas, is different and determines specific management strategies, it is crucial to identify the phytoplasmas infecting plants affected by GY. Molecular analyses, based on PCR amplification and further nucleotide sequence characterization carried out through RFLP profile comparison and/or sequence identity calculation, allow specific identification of 'Ca. Phytoplasma solani' and/or other phytoplasmas infecting grapevine (Lee at al., 1998; Berger et al., 2009).
Prevention and ControlTop of page
Due to the variable regulations around (de)registration of pesticides, your national list of registered pesticides or relevant authority should be consulted to determine which products are legally allowed for use in your country when considering chemical control. Pesticides should always be used in a lawful manner, consistent with the product's label.
In the European Union, ‘Ca. Phytoplasma solani’ is listed as a harmful organism necessitating restrictions on the import of plants in the family Solanaceae (EFSA Panel on Plant Health, 2014).
The complexity of the epidemiological cycle of ‘Ca. Phytoplasma solani’ renders it difﬁcult to design efﬁcient control strategies. Insecticides applied to the crop canopy inﬂuence neither the disease nor the presence of the main vector, Hyalesthes obsoletus. The management of H. obsoletus host plants in agro-systems and their surrounding areas is therefore considered crucial for ‘Ca. Phytoplasma solani’ control. In Europe, several studies showed that H. obsoletus host plants at the borders facilitate the spread of ‘Ca. Phytoplasma solani’. Thus, preventive measures such as checking the sanitary 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. In the case of bois noir, other strategies for reducing ‘Ca. Phytoplasma solani’ spread or incidence are based on: (a) the preventive removal of the grape suckers on which H. obsoletus could feed after grass mowing; (b) trunk cutting above the engagement point on symptomatic grapevines; and (c) treatments by resistance inducers (Belli et al., 2010).
Recent studies of the use of herbicides and insecticides against host weeds (bindweed and stinging nettles) and vectors have had some success. Trials conducted to control nettle growth with glyphosate or other herbicides significantly reduced the density of emerging adult vectors. Neonicotinoid insecticides, applied in early spring, gave protection levels comparable to those of herbicide treatments. However, the use of herbicides and/or insecticides can have negative effects on non-target arthropods (e.g. honeybees) (EFSA Panel on Plant Health, 2014; Mori et al., 2014), as well as human health (in particular farmers) and biodiversity.
Gaps in Knowledge/Research NeedsTop of page
Recent studies have added new, interesting information on ‘Ca. Phytoplasma solani’-associated diseases, showing that genetically distinct strains of this species, identified in different agro-ecosystems, can cause a range of diseases. Based on such evidence, it should be interesting to trace the movements of ‘Ca. Phytoplasma solani’ strains (and their insect vectors) through neighbouring fields where different crops are cultivated.
ReferencesTop of page
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30/09/17 Original text by:
Fabio Quaglino, Department of Agricultural and Environmental Sciences, University of Milan, Milan, Italy
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