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Candidatus Phytoplasma solani
(Stolbur phytoplasma)

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Datasheet

Candidatus Phytoplasma solani (Stolbur phytoplasma)

Summary

  • Last modified
  • 22 February 2019
  • Datasheet Type(s)
  • Invasive Species
  • Pest
  • Natural Enemy
  • Preferred Scientific Name
  • Candidatus Phytoplasma solani
  • Preferred Common Name
  • Stolbur phytoplasma
  • Taxonomic Tree
  • Domain: Bacteria
  •   Phylum: Firmicutes
  •     Class: Mollicutes
  •       Order: Acholeplasmatales
  •         Family: Acholeplasmataceae
  • Summary of Invasiveness
  • 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 c...

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Pictures

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PictureTitleCaptionCopyright
Candidatus Phytoplasma solani; grapevine yellows symptoms on Vitis vinifera.
TitleSymptoms
CaptionCandidatus Phytoplasma solani; grapevine yellows symptoms on Vitis vinifera.
Copyright©Dr Fabio Quaglino/Department of Agricultural & Environmental Sciences, University of Milan, Italy
Candidatus Phytoplasma solani; grapevine yellows symptoms on Vitis vinifera.
SymptomsCandidatus Phytoplasma solani; grapevine yellows symptoms on Vitis vinifera.©Dr Fabio Quaglino/Department of Agricultural & Environmental Sciences, University of Milan, Italy
Candidatus Phytoplasma solani; grapevine yellows symptoms on Vitis vinifera.
TitleSymptoms
CaptionCandidatus Phytoplasma solani; grapevine yellows symptoms on Vitis vinifera.
Copyright©Dr Fabio Quaglino/Department of Agricultural & Environmental Sciences, University of Milan, Italy
Candidatus Phytoplasma solani; grapevine yellows symptoms on Vitis vinifera.
SymptomsCandidatus Phytoplasma solani; grapevine yellows symptoms on Vitis vinifera.©Dr Fabio Quaglino/Department of Agricultural & Environmental Sciences, University of Milan, Italy
Candidatus Phytoplasma solani; grapevine yellows symptoms on Vitis vinifera.
TitleSymptoms
CaptionCandidatus Phytoplasma solani; grapevine yellows symptoms on Vitis vinifera.
Copyright©Dr Fabio Quaglino/Department of Agricultural & Environmental Sciences, University of Milan, Italy
Candidatus Phytoplasma solani; grapevine yellows symptoms on Vitis vinifera.
SymptomsCandidatus Phytoplasma solani; grapevine yellows symptoms on Vitis vinifera.©Dr Fabio Quaglino/Department of Agricultural & Environmental Sciences, University of Milan, Italy
Candidatus Phytoplasma solani; grapevine yellows symptoms on Vitis vinifera.
TitleSymptoms
CaptionCandidatus Phytoplasma solani; grapevine yellows symptoms on Vitis vinifera.
Copyright©Dr Fabio Quaglino/Department of Agricultural & Environmental Sciences, University of Milan, Italy
Candidatus Phytoplasma solani; grapevine yellows symptoms on Vitis vinifera.
SymptomsCandidatus Phytoplasma solani; grapevine yellows symptoms on Vitis vinifera.©Dr Fabio Quaglino/Department of Agricultural & Environmental Sciences, University of Milan, Italy

Identity

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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 Invasiveness

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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 Tree

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  • Domain: Bacteria
  •     Phylum: Firmicutes
  •         Class: Mollicutes
  •             Order: Acholeplasmatales
  •                 Family: Acholeplasmataceae
  •                     Genus: Candidatus Phytoplasma
  •                         Species: Candidatus Phytoplasma solani

Notes on Taxonomy and Nomenclature

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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).

Description

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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 Table

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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/RegionDistributionLast ReportedOriginFirst ReportedInvasiveReferenceNotes

Asia

ArmeniaPresentEPPO, 2018
AzerbaijanPresent2010Balakishiyeva et al., 2010; Balakishiyeva et al., 2016; EPPO, 2018
ChinaPresent, few occurrences2010Duduk et al., 2010; EPPO, 2018
-ShaanxiPresent2015Yang et al., 2016; EPPO, 2018
-ShandongPresent, few occurrences2015Gao et al., 2013; EPPO, 2018
Georgia (Republic of)Present2014Quaglino et al., 2014; Quaglino et al., 2016; EPPO, 2018
IndiaPresent, few occurrencesEPPO, 2018
-West BengalPresent, few occurrences2014Chinmay Biswas et al., 2014; EPPO, 2018
IranPresent2010Karimi 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
IsraelPresent, few occurrences1970Zimmerman-Gries, 1970; Tanne and Nitzany, 1973; Kuszala et al., 1993; Boudon-Padieu, 1996; EPPO, 2018
JordanPresent2012Salem et al., 2013; EPPO, 2014; EPPO, 2018
Korea, Republic ofPresent2013Chung et al., 2013
KyrgyzstanPresentEPPO, 2018
LebanonLocalised2002Choueiri et al., 2002; Karimi et al., 2009; EPPO, 2018
Saudi ArabiaPresent1971Yaman, 1971; EPPO, 2018
SyriaPresent2011Contaldo et al., 2011
TajikistanLocalisedEPPO, 2018
TurkeyLocalised2001Ozdemir et al., 2009; Eroglu et al., 2010; Canik et al., 2011; Alp et al., 2016; EPPO, 2018
UzbekistanPresentEPPO, 2018

Africa

NigerPresent1988Reckhaus et al., 1988; EPPO, 2018
TunisiaAbsent, formerly presentEPPO, 2018

North America

CanadaEradicatedEPPO, 2018

South America

ChilePresent2009Gajardo et al., 2009; EPPO, 2018

Europe

AlbaniaPresent2003Myrta et al., 2003; EPPO, 2018
AustriaPresent, few occurrences2003Riedle-Bauer et al., 2008; EPPO, 2018
BelgiumEradicatedEPPO, 2018
Bosnia-HercegovinaPresent2006Delić et al., 2006; Kovačević et al., 2014; Delić et al., 2016; EPPO, 2018
BulgariaLocalised2007Sakalieva et al., 2007; Bobev et al., 2013; Genov et al., 2014; EPPO, 2018
CroatiaLocalised2000Seruga et al., 2000; Voncina and Cvjetkovic, 2007; Plavec et al., 2015; EPPO, 2018
CyprusAbsent, formerly presentEPPO, 2018
Czech RepublicPresent, few occurrences2004Mertelik et al., 2004; Fialova et al., 2009; Franova et al., 2009; Navratil et al., 2011; Stary et al., 2013; EPPO, 2018
FranceLocalised1961Cousin et al., 1971; Daire et al., 1993; Kuszala et al., 1993; Cimerman et al., 2009; EPPO, 2018
GermanyLocalised1971Seemuller et al., 1994; Maixner et al., 1995; EPPO, 2018
GreeceLocalised2013Lotos et al., 2013; Holeva et al., 2014; Moraki et al., 2014; EPPO, 2018
HungaryLocalised2006Palermo et al., 2006; Acs et al., 2011; EPPO, 2018
ItalyLocalised1982Marcone 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
-SicilyPresentEPPO, 2018
MacedoniaWidespread2014Kostadinovska et al., 2014; Atanasova et al., 2015; EPPO, 2018
MoldovaAbsent, unreliable recordEPPO, 2018
MontenegroWidespread2009Radonjić et al., 2009; Radonjic et al., 2016; EPPO, 2018
NetherlandsAbsent, confirmed by surveyEPPO, 2018
PolandPresent, few occurrences1999Żandarski, 1999; Zwolinska et al., 2012; EPPO, 2018
PortugalAbsent, confirmed by surveyEPPO, 2014
RomaniaAbsent, formerly present2011Ember et al., 2011; Lindner et al., 2011; EPPO, 2018
Russian FederationLocalisedEPPO, 2018
-Central RussiaPresent2008Girsova et al., 2008; EPPO, 2018
-Southern RussiaPresent2011Ember et al., 2011; EPPO, 2018
SerbiaLocalised2006Adamovic 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
SlovakiaLocalisedEPPO, 2018
SloveniaLocalised2011Mehle et al., 2011; EPPO, 2018
SpainLocalised1995Avinent and Llàcer, 1995; Batlle et al., 1995; Alfaro-Fernandez et al., 2011; Sabaté et al., 2014; EPPO, 2018
SwitzerlandLocalised2002Gugerli et al., 2002; EPPO, 2018
UKTransient: actionable, under eradication2015Hodgetts et al., 2015; EPPO, 2018
UkraineLocalisedEPPO, 2018

Oceania

New ZealandAbsent, unreliable recordEPPO, 2018

History of Introduction and Spread

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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 Introduction

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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 Affected

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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 Stages

Top of page Flowering stage, Fruiting stage, Seedling stage, Vegetative growing stage

Symptoms

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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.

Bois noir

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).

Tomato stolbur

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.

Potato stolbur

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).

Maize redness

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).

Lavender decline

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/Signs

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SignLife StagesType
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 Ecology

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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).

Climate

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ClimateStatusDescriptionRemark
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 Dispersal

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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 Trade

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Plant parts liable to carry the pest in trade/transportPest stagesBorne internallyBorne externallyVisibility of pest or symptoms
Seedlings/Micropropagated plants Pest or symptoms usually invisible

Vectors and Intermediate Hosts

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Impact Summary

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CategoryImpact
Economic/livelihood Negative
Environment (generally) Negative
Human health Negative

Economic Impact

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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 Impact

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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 Impact

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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 Factors

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  • Host damage
  • Negatively impacts agriculture
  • Negatively impacts cultural/traditional practices
  • Negatively impacts forestry
  • Negatively impacts human health
  • Negatively impacts animal health
Impact mechanisms
  • Interaction with other invasive species
  • Pathogenic
Likelihood of entry/control
  • 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

Diagnosis

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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 Inspection

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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/Conditions

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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 Control

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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.

Prevention

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).

Control

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 Needs

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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.

References

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Acs, Z., Jovic, J., Ember, I., Cvrkovic, T., Nagy, Z., Talaber, C., Gergely, L., Toševski, I., Kölber, M., 2011. First report of maize redness disease in Hungary. Bulletin of Insectology, 64(Supplement), S229-S230. http://www.bulletinofinsectology.org/

Adamovic D, Djalovic I, Mitrovic P, Kojic S, Pivic R, Josic D, 2014a. First report on natural infection of Paeonia tenuifolia by 'Candidatus phytoplasma solani' in Serbia. Plant Disease, 98(4):565. http://apsjournals.apsnet.org/loi/pdis

Adamovic D, Djalovic I, Mitrovic P, Kojic S, Starovic M, Purar B, Josic D, 2014b. First report of 16SrXII-A subgroup phytoplasma (stolbur) associated with reddening of Oenothera biennis in Serbia. Plant Disease, 98(6):841. http://apsjournals.apsnet.org/loi/pdis

Alfaro-Fernández, A., Cebrián, M. del C., Villaescusa, F. J., Font-San-Ambrosio, M. I., 2011. Detection and identification of aster yellows and stolbur phytoplasmas in various crops in Spain. Bulletin of Insectology, 64(Supplement), S63-S64. http://www.bulletinofinsectology.org/

Allahverdi, T., Rahimian, H., Babaeizad, V., 2014. Prevalence and distribution of peach yellow leaf roll in north of Iran. Journal of Plant Pathology, 96(3), 603. http://sipav.org/main/jpp/index.php/jpp/article/view/3179/1851

Alp, S., Usta, M., Sipahioglu, H. M., Güller, A., 2016. First report of "Candidatus Phytoplasma solani" on a new host marigold (Tagetes erecta L.). Turkish Journal of Agriculture and Forestry, 40(3), 311-318. http://journals.tubitak.gov.tr/agriculture/issues/tar-16-40-3/tar-40-3-2-1506-58.pdf

Angelini, E., Bianchi, G. L., Filippin, L., Morassutti, C., Borgo, M., 2007. A new TaqMan method for the identification of phytoplasmas associated with grapevine yellows by real-time PCR assay. Journal of Microbiological Methods, 68(3), 613-622. http://www.sciencedirect.com/science?_ob=ArticleURL&_udi=B6T30-4MSY89D-1&_user=10&_coverDate=03%2F31%2F2007&_rdoc=22&_fmt=summary&_orig=browse&_srch=doc-info(%23toc%234932%232007%23999319996%23644511%23FLA%23display%23Volume)&_cdi=4932&_sort=d&_docanchor=&view=c&_ct=29&_acct=C000050221&_version=1&_urlVersion=0&_userid=10&md5=c015ba083e6a1a8149db7e014ff7411d doi: 10.1016/j.mimet.2006.11.015

Atanasova, B., Jakovljevic, M., Spasov, D., Jovic, J., Mitrovic, M., Toševski, I., Cvrkovic, T., 2015. The molecular epidemiology of bois noir grapevine yellows caused by 'Candidatus Phytoplasma solani' in the Republic of Macedonia. European Journal of Plant Pathology, 142(4), 759-770. http://rd.springer.com/journal/10658 doi: 10.1007/s10658-015-0649-0

Avinent, L., Llácer, G., 1995. Stolbur detection in Spain by polymerase chain reaction (PCR). Boletín de Sanidad Vegetal, Plagas, 21(3), 417-423.

Balakishiyeva G, Danet JL, Qurbanov M, Mamedov A, Kheyr-Pour A, Foissac X, 2010. First report of phytoplasma infections in several temperate fruit trees and vegetable crops in Azerbaijan. Journal of Plant Pathology, 92(S4), S4.115. http://www.sipav.org/main/jpp/index.php/jpp/article/download/348/214

Balakishiyeva G, Mammadov A, Foissac X, Huseynova I, Aliyev J, 2016. First report of grapevine 'bois noir' in Azerbaijan. Plant Disease, 100(12):2522. http://apsjournals.apsnet.org/loi/pdis

Batlle A, Larrue J, Clair D, Daire X, Boudon-Padieu E, Lavina A, 1995. Identificacion del fitoplasma asociado al Bois Noir de la vina en Espana (Identification of the phytoplasma associated with bois noir of grapevine in Spain). Phytoma-Espana, 68: 40-44

Belli, G., Bianco, P. A., Conti, M., 2010. Grapevine yellows in Italy: past, present and future. Journal of Plant Pathology, 92(2), 303-326. http://www.sipav.org/main/jpp/

Berger, J., Dalla Via, J., Baric, S., 2009. Development of a TaqMan allelic discrimination assay for the distinction of two major subtypes of the grapevine yellows phytoplasma Bois noir. European Journal of Plant Pathology, 124(3), 521-526. http://springerlink.metapress.com/link.asp?id=100265 doi: 10.1007/s10658-008-9424-9

Bertaccini, A., Duduk, B., Paltrinieri, S., Contaldo, N., 2014. Phytoplasmas and phytoplasma diseases: a severe threat to agriculture. American Journal of Plant Sciences, 5(12), 1763-1788. http://www.scirp.org/journal/PaperInformation.aspx?PaperID=46299 doi: 10.4236/ajps.2014.512191

Bianco, P. A., Casati, P., Marziliano, N., 2004. Detection of phytoplasmas associated with grapevine flavescence dorée disease using real-time PCR. Journal of Plant Pathology, 86(3), 257-261.

Blanchard D, 2012. Tomato Diseases: Identification, Biology and Control - A Colour Handbook, 2nd Ed. London, UK: Manson Publishing Ltd

Bobev, S. G., Jonghe, K. de, Maes, M., 2013. First report of Candidatus phytoplasma solani on blackberry (Rubus fruticosus) in Bulgaria. Plant Disease, 97(2), 282. http://apsjournals.apsnet.org/loi/pdis doi: 10.1094/PDIS-08-12-0793-PDN

Boudon-Padieu, E., 1996. Grapevine yellows induced by phytoplasmas. Diagnosis, epidemiology and research. Comptes Rendus de l'Académie d'Agriculture de France, 82(1), 5-20.

Boudon-Padieu, E., Cousin, M. T., 1999. Yellow decline of Lavandula hybrida Rev and L. vera DC. International Journal of Tropical Plant Diseases, 17(1/2), 1-34.

Calari A, Contaldo N, Ardizzi S, Bertaccini A, 2010. Phytoplasma detection in corn with reddening in Italy. In: Working Groups of COST Action FA0807: Integrated management of phytoplasma epidemics in different crop systems, Sitges, Spain, 1-2 February 2010. p 5. [Abstract]

Canik D, Topkaya X, Bayram S, Soylemezoglu G, Ertunc F, 2011. Occurrence and distribution of bois noir phytoplasma in Turkey. Petria, 21(2/3): 118-119

Chinmay Biswas, Piyali Dey, Subrata Satpathy, 2014. First report on molecular detection of a stolbur phytoplasma (Group16SrXII-A) associated with kenaf (Hibiscus cannabinus L.) in India. Archives of Phytopathology and Plant Protection, 47(14):1746-1751. http://www.tandfonline.com/loi/gapp20

Choueiri, E., Jreijiri, F., El-Zammar, S., Verdin, E., Salar, P., Danet, J. L., Bové, J., Garnier, M., 2002. First report of grapevine "bois noir" disease and a new phytoplasma infecting solanaceous plants in Lebanon. Plant Disease, 86(6), 697. doi: 10.1094/PDIS.2002.86.6.697A

Chuche, J., Danet, J. L., Salar, P., Foissac, X., Thiéry, D., 2016. Transmission of 'Candidatus Phytoplasma solani' by Reptalus quinquecostatus (Hemiptera: Cixiidae). Annals of Applied Biology, 169(2), 214-223. http://onlinelibrary.wiley.com/journal/10.1111/(ISSN)1744-7348 doi: 10.1111/aab.12291

Chung N, Jeong Ml, Choi SK, Joa JH, Choi KS, Choi IM, 2013. Occurrence of Stolbur Phytoplasma Disease in Spreading Type Petunia hybrida Cultivars in Korea. Plant Pathology Journal, 29(4): 465-470

Ciccarone, A., 1949. Preliminary note on the big bud disease of tomato in the neighbourhood of Rome. (Sintomi di " virescenza ipertrofica " (big bud) del pomodoro nei pressi di Roma. Nota preliminare). Bollettino della Stazione di Patologia Vegetale, 7, 193-8.

Cimerman, A., Pacifico, D., Salar, P., Marzachì, C., Foissac, X., 2009. Striking diversity of vmp1, a variable gene encoding a putative membrane protein of the stolbur phytoplasma. Applied and Environmental Microbiology, 75(9), 2951-2957. http://aem.asm.org doi: 10.1128/AEM.02613-08

Clair, D., Larrue, J., Aubert, G., Gillet, J., Cloquemin, G., Boudon-Padieu, E., 2003. A multiplex nested-PCR assay for sensitive and simultaneous detection and direct identification of phytoplasma in the Elm yellows group and Stolbur group and its use in survey of grapevine yellows in France. Vitis, 42(3), 151-157.

Contaldo, N., Soufi, Z., Bertaccini, A., 2011. Preliminary identification of phytoplasmas associated with grapevine yellows in Syria. Bulletin of Insectology, 64(Supplement), S217-S218. http://www.bulletinofinsectology.org/

Cousin MT, Maillet PL, Gourret JP, Grison C, Staron T, 1968. Présence de particules de type “jaunisse européenne”. Le stolbur de la tomate, l’aster yellow du glaïeul, la phyllodie du trèfle. Etudes cytologiques et ultrastructurales. Premiers essais de lutte chimique. Comptes Rendus de l’Académie des Sciences Série D, 54, 887-895.

Cousin MT, Moreau JP, Kartha KK, Staron T, Faivre-Amiot A, 1971. Polymorphisme des microorganismes de type mycoplasme rencontrés dans les tubes criblés de lavandins “Abrial” atteints de “Dépérissement jaune”. Compte Rendu de l’Académie des Sciences de Paris, 272: 2082-2085

Cousin MT, Moreau JP, Staron T, Faivre-Amiot A, 1970. Yellow wilt of lavandin; new mycoplasma disease. (Le "dépérissement jaune" du lavandin: nouvelle maladie a mycoplasmes). Annales de Phytopathologie, 2, 227-237.

Cvrkovic, T., Jovic, J., Mitrovic, M., Krstic, O., Toševski, I., 2014. Experimental and molecular evidence of Reptalus panzeri as a natural vector of bois noir. Plant Pathology, 63(1), 42-53. http://onlinelibrary.wiley.com/doi/10.1111/ppa.12080/full doi: 10.1111/ppa.12080

Daire, X., Clair, D., Larrue, J., Boudon-Padieu, E., Caudwell, A., 1993. Diversity among mycoplasma-like organisms inducing grapevine yellows in France. Vitis, 32(3), 159-163.

Delic, D., Contaldo, N., Lolic, B., Moravcevic, Ð., Bertaccini, A., 2016. First report of 'Candidatus Phytoplasma solani' in pepper and celery in Bosnia and Herzegovina. Journal of Plant Pathology, 98(1), 184. http://www.sipav.org/main/jpp/index.php/jpp/article/view/3496

Delic, D., Martini, M., Ermacora, P., Carraro, L., Myrta, A., 2006. First report of grapevine Bois noir in Bosnia and Herzegovina. Journal of Plant Pathology, 88(2), 226. http://www.agr.unipi.it/sipav/jpp/index.html

Duduk, B., Bertaccini, A., 2006. Corn with symptoms of reddening: new host of stolbur phytoplasma. Plant Disease, 90(10), 1313-1319. HTTP://www.apsnet.org doi: 10.1094/PD-90-1313

Duduk, B., Tian JanBao, Contaldo, N., Fan XinPing, Paltrinieri, S., Chen QiuFang, Zhao QiFeng, Bertaccini, A., 2010. Occurrence of phytoplasmas related to stolbur and to 'Candidatus Phytoplasma japonicum' in woody host plants in China. Journal of Phytopathology, 158(2), 100-104. http://www.blackwell-synergy.com/loi/jph doi: 10.1111/j.1439-0434.2009.01586.x

EFSA Panel on Plant Health, 2014. Scientific opinion on the pest categorisation of Candidatus phytoplasma solani. EFSA Journal, 12(12), 3924. http://www.efsa.europa.eu/en/efsajournal/doc/3924.pdf

Ember, I., Acs, Z., Munyaneza, J. E., Crosslin, J. M., Kolber, M., 2011. Survey and molecular detection of phytoplasmas associated with potato in Romania and southern Russia. European Journal of Plant Pathology, 130(3), 367-377. http://springerlink.metapress.com/link.asp?id=100265 doi: 10.1007/s10658-011-9759-5

EPPO, 2014. EPPO Reporting Service, No. 2014/015. Paris, France: European and Mediterranean Plant Protection Organization

EPPO, 2018. PQR database. Paris, France: European and Mediterranean Plant Protection Organization. http://www.eppo.int/DATABASES/pqr/pqr.htm

EPPO/CABI, 1997. Potato purple-top wilt phytoplasma. In: Smith IM, McNamara DG, Scott PR, Holderness M, eds. Quarantine pests for Europe (2nd ed.). Wallingford, UK: CAB International, 1053-1057

Eroglu, S., Ozbek, H., Sahin, F., 2010. First report of group 16SrXII phytoplasma causing stolbur disease in potato plants in the eastern and southern Anatolia Regions of Turkey. Plant Disease, 94(11), 1374. http://apsjournals.apsnet.org/loi/pdis doi: 10.1094/PDIS-06-10-0439

Fabre, A., Danet, J. L., Foissac, X., 2011. The stolbur phytoplasma antigenic membrane protein gene stamp is submitted to diversifying positive selection. Gene, 472(1/2), 37-41. http://www.sciencedirect.com/science?_ob=ArticleURL&_udi=B6T39-51C4RSN-1&_user=10&_coverDate=02%2F01%2F2011&_rdoc=6&_fmt=high&_orig=browse&_origin=browse&_zone=rslt_list_item&_srch=doc-info(%23toc%234941%232011%23995279998%232846776%23FLA%23display%23Volume)&_cdi=4941&_sort=d&_docanchor=&_ct=8&_acct=C000050221&_version=1&_urlVersion=0&_userid=10&md5=fa183257cc8705a299631eb2d24c0b8c&searchtype=a doi: 10.1016/j.gene.2010.10.012

Fialová, R., Válová, P., Balakishiyeva, G., Danet, J. L., Šafárová, D., Foissac, X., Navrátil, M., 2009. Genetic variability of stolbur phytoplasma in annual crop and wild plant species in south Moravia. Journal of Plant Pathology, 91(2), 411-416. http://www.sipav.org/main/jpp/

Firrao, G., Moretti, M., Rosquete, M. R., Gobbi, E., Locci, R., 2005. Nanobiotransducer for detecting flavescence dorée phytoplasma. Journal of Plant Pathology, 87(2), 101-107.

Foissac X, Carle P, Fabre A, Salar P, Danet JL, 2013. “Candidatus Phytoplasma solani” genome project and genetic diversity in the Euro-Mediterranean basin. In: Third European Bois Noir Workshop, Barcelona, Spain, 20-21 March 2013 [Third European Bois Noir Workshop, Barcelona, Spain, 20-21 March 2013], [ed. by Torres E, Laviña A, Batlle A]. 11-14.

Fránová, J., Navrátil, M., Jakešová, H., 2009. Molecular identification of stolbur phytoplasma associated with red clover dwarf disease symptoms. Journal of Phytopathology, 157(7/8), 502-506. http://www.blackwell-synergy.com/loi/jph doi: 10.1111/j.1439-0434.2008.01508.x

Gajardo, A., Fiore, N., Prodan, S., Paltrinieri, S., Botti, S., Pino, A. M., Zamorano, A., Montealegre, J., Bertaccini, A., 2009. Phytoplasmas associated with grapevine yellows disease in Chile. Plant Disease, 93(8), 789-796. http://apsjournals.apsnet.org/loi/pdis doi: 10.1094/PDIS-93-8-0789

Galetto, L., Bosco, D., Marzachì, C., 2005. Universal and group-specific real-time PCR diagnosis of flavescence dorée (16Sr-V), bois noir (16Sr-XII) and apple proliferation (16Sr-X) phytoplasmas from field-collected plant hosts and insect vectors. Annals of Applied Biology, 147(2), 191-201. http://www.blackwell-synergy.com/servlet/useragent?func=showIssues&code=aab doi: 10.1111/j.1744-7348.2005.00030.x

Gao Ying, Qiu PingPing, Liu WenHao, Su WenMin, Gai ShuPeng, Liang YuanCun, Zhu XiaoPing, 2013. Identification of 'Candidatus Phytoplasma solani' associated with tree peony yellows disease in China. Journal of Phytopathology, 161(3), 197-200. http://onlinelibrary.wiley.com/journal/10.1111/(ISSN)1439-0434 doi: 10.1111/jph.12025

Genov, N., Mitrovic, J., Genov, M., Duduk, B., 2014. First report of corn reddening caused by 'Candidatus Phytoplasma solani' in Bulgaria. Plant Disease, 98(7), 991. http://apsjournals.apsnet.org/loi/pdis doi: 10.1094/PDIS-12-13-1220-PDN

Girsova, N., Bottner, K. D., Mozhaeva, K. A., Kastalyeva, T. B., Owens, R. A., Lee, I. M., 2008. Molecular detection and identification of group 16SrI and 16SrXII phytoplasmas associated with diseased potatoes in Russia. Plant Disease, 92(4), 654. HTTP://www.apsnet.org doi: 10.1094/PDIS-92-4-0654A

Gugerli, P., Cazelles, O., Genini, M., Emery, S., Colombi, L., 2002. Maladie du bois noir de la vigne en Suisse romande et au Tessin (Black wood disease of grapes in French-speaking Switzerland and Ticino). Revue Suisse de Viticulture, Arboriculture et Horticulture, 34(1), 15-17.

Hodgetts J, Flint LJ, Daly M, Harju VA, Skelton AL, Fox A, 2015. Identification of 'Candidatus Phytoplasma solani' (16Sr XII-A) infecting strawberry plants in the United Kingdom. New Disease Reports, 31:5. http://www.ndrs.org.uk/article.php?id=031005

Holeva MC, Glynos PE, Karafla CD, Koutsioumari EM, Simoglou KB, Eleftheriadis E, 2014. First report of Candidatus phytoplasma solani associated with potato plants in Greece. Plant Disease, 98(12):1739. http://apsjournals.apsnet.org/loi/pdis

Hosseini, P., Bahar, M., Madani, G., Zirak, L., 2011. Molecular characterization of phytoplasmas associated with potato purple top disease in Iran. Journal of Phytopathology, 159(4), 241-246. http://onlinelibrary.wiley.com/journal/10.1111/(ISSN)1439-0434 doi: 10.1111/j.1439-0434.2010.01757.x

International Research Programme for Comparative Mycoplasmology Phytoplasma\Spiroplasma Working Team - Phytoplasma Taxonomy Group, 2004. 'Candidatus Phytoplasma', a taxon for the wall-less, non-helical prokaryotes that colonize plant phloem and insects. International Journal of Systematic and Evolutionary Microbiology, 54(4), 1243-1255. doi: 10.1099/ijs.0.02854-0

Iriti, M., Quaglino, F., Maffi, D., Casati, P., Bianco, P. A., Faoro, F., 2008. Solanum malacoxylon, a new natural host of Stolbur phytoplasma. Journal of Phytopathology, 156(1), 8-14. http://www.blackwell-synergy.com/doi/abs/10.1111/j.1439-0434.2007.01311.x

Ivanovic, Ž., Trkulja, N., Živkovic, S., Dolovac, E. P., Dolovac, N., Jovic, J., Mitrovic, M., 2011. First report of stolbur phytoplasma infecting celery in Serbia. Bulletin of Insectology, 64(Supplement), S239-S240. http://www.bulletinofinsectology.org/

Johannesen, J., Lux, B., Michel, K., Seitz, A., Maixner, M., 2008. Invasion biology and host specificity of the grapevine yellows disease vector Hyalesthes obsoletus in Europe. Entomologia Experimentalis et Applicata, 126(3), 217-227. http://www.blackwell-synergy.com/loi/eea doi: 10.1111/j.1570-7458.2007.00655.x

Josic D, Starovic M, Kojic S, Pivic R, Stanojkovic-Sebic A, Zdravkovic M, Pavlovic S, 2015. Dianthus barbatus - a new host of Stolbur phytoplasma in Serbia. Plant Disease, 99(2):283. http://apsjournals.apsnet.org/loi/pdis

Josic D, Starovic M, Stojanovic S, Popovic T, Dolovac N, Zdravkovic J, Pavlovic S, 2013. First report of group 16SrXII-A phytoplasma causing stolbur disease in Saponaria officinalis plants in Serbia. Plant Disease, 97(3):420. http://apsjournals.apsnet.org/loi/pdis

Josic, D., Pavlovic, S., Pivic, R., Kuzmanovic, S., Stojanovic, S., Popovic, T., Starovic, M., 2012. Cultivated and wild plantain (Plantago major) as a host of Stolbur phytoplasma in Serbia. Journal of Medicinal Plants Research, 6(2), 284-288. http://www.academicjournals.org/JMPR/abstracts/abstracts/abstracts2012/16Jan/Josic%20et%20al.htm

Jovic, J., Cvrkovic, T., Mitrovic, M., Krnjajic, S., Petrovic, A., Redinbaugh, M. G., Pratt, R. C., Hogenhout, S. A., Toševski, I., 2009. Stolbur phytoplasma transmission to maize by Reptalus panzeri and the disease cycle of maize redness in Serbia. Phytopathology, 99(9), 1053-1061. doi: 10.1094/PHYTO-99-9-1053

Jovic, J., Cvrkovic, T., Mitrovic, M., Krnjajic, S., Redinbaugh, M. G., Pratt, R. C., Gingery, R. E., Hogenhout, S. A., Toševski, I., 2007. Roles of stolbur phytoplasma and Reptalus panzeri (Cixiinae, Auchenorrhyncha) in the epidemiology of Maize redness in Serbia. European Journal of Plant Pathology, 118(1), 85-89. http://springerlink.metapress.com/link.asp?id=100265 doi: 10.1007/s10658-007-9105-0

Karimi M, Contaldo N, Mahmoudi B, Duduk B, Bertaccini A, 2009. Identification of stolbur-related phytoplasmas in grapevine showing decline symptoms in Iran. Le Progres agricole et viticole, Hors Serie (Extended abstract of the 16th Meeting ICVG, Dijion, France, 31 August-4 September 2009), 208-209

Kosovac A, Jakovljevic M, Krstic O, Cvrkovic T, Mitrovic M, Tosevski I, Jovic J, 2014. Crepis foetida L. - new host plant of Cixiid planthopper Hyalesthes obsoletus Signoret 1865 (Hemiptera: Cixiidae), vector of stolbur phytoplasma. (Crepis foetida L. - nova biljka domacin cikade Hyalesthes obsoletus Signoret 1865 (Hemiptera: Cixiidae), vektora stolbur fitoplazme.) Zastita Bilja, 65(1):7-14. http://www.izbis.com/casopis/2014/Zastita-bilja-Vol.65-(1)-2014.pdf

Kosovac, A., Jakovljevic, M., Krstic, O., Cvrkovic, T., Mitrovic, M., Toševski, I., Jovic, J., 2019. Role of plant-specialized Hyalesthes obsoletus associated with Convolvulus arvensis and Crepis foetida in the transmission of 'Candidatus Phytoplasma solani'-inflicted Bois noir disease of grapevine in Serbia. European Journal of Plant Pathology, 153(1), 183-195. https://link.springer.com/article/10.1007%2Fs10658-018-1553-1

Kosovac, A., Radonjic, S., Hrncic, S., Krstic, O., Toševski, I., Jovic, J., 2016. Molecular tracing of the transmission routes of bois noir in Mediterranean vineyards of Montenegro and experimental evidence for the epidemiological role of Vitex agnus-castus (Lamiaceae) and associated Hyalesthes obsoletus (Cixiidae). Plant Pathology, 65(2), 285-298. http://onlinelibrary.wiley.com/doi/10.1111/ppa.12409/full doi: 10.1111/ppa.12409

Kostadinovska, E., Quaglino, F., Mitrev, S., Casati, P., Bulgari, D., Bianco, P. A., 2014. Multiple gene analyses identify distinct "bois noir" phytoplasma genotypes in the Republic of Macedonia. Phytopathologia Mediterranea, 53(3), 491-501. http://www.fupress.com/pm/

Kovacevic, M., Ðuric, Z., Jovic, J., Perkovic, G., Lolic, B., Hrncic, S., Toševski, I., Delic, D., 2014. First report of stolbur phytoplasma associated with maize redness disease of maize in Bosnia and Herzegovina. Plant Disease, 98(3), 418. http://apsjournals.apsnet.org/doi/abs/10.1094/PDIS-04-13-0371-PDN doi: 10.1094/PDIS-04-13-0371-PDN

Kuszala, C., Cazelles, O., Boulud, J., Credi, R., Granata, G., Kriel, G., Magarey, P., Magnien, C., Pearson, R. C., Refatti, E., Tanne, E., Caudwell, A., 1993. Contribution to the study of grapevine yellows in the world: investigation by ELISA using flavescence dorée-specific antibodies. Agronomie, 13(10), 929-933. doi: 10.1051/agro:19931007

Langer, M., Maixner, M., 2004. Molecular characterisation of grapevine yellows associated phytoplasmas of the stolbur-group based on RFLP-analysis of non-ribosomal DNA. Vitis, 43(4), 191-199.

Lee IngMing, Gundersen-Rindal, D. E., Davis, R. E., Bartoszyk, I. M., 1998. Revised classification scheme of phytoplasmas based on RFLP analyses of 16S rRNA and ribosomal protein gene sequences. International Journal of Systematic Bacteriology, 48(4), 1153-1169.

Lindner, K., Haase, N. U., Roman, M., Seemüller, E., 2011. Impact of stolbur phytoplasmas on potato tuber texture and sugar content of selected potato cultivars. Potato Research, 54(3), 267-282. http://www.springerlink.com/content/el7247666170n7tp/ doi: 10.1007/s11540-011-9192-3

Lotos, L., Tsialtas, J. T., Maliogka, V. I., Kaloumenos, N., Eleftherohorinos, I. G., Katis, N. I., 2013. First report of a "Candidatus Phytoplasma solani" related strain associated with a disease of Datura stramonium in Greece. Journal of Plant Pathology, 95(2), 447. http://sipav.org/main/jpp/index.php/jpp/article/view/2836

Maixner M, 2011. Recent advances in Bois noir research. Petria, 21: 17-32

Maixner, M., Rüdel, M., Daire, X., Boudon-Padieu, E., 1995. Diversity of grapevine yellows in Germany. Vitis, 34(4), 235-236.

Marchi, G., Cinelli, T., Rizzo, D., Goti, L. S., Bartola, M. della, Luvisi, A., Panattoni, A., Materazzi, A., 2015. Occurrence of different phytoplasma infections in wild herbaceous dicots growing in vineyards affected by bois noir in Tuscany (Italy). Phytopathologia Mediterranea, 54(3), 504-515. http://www.fupress.net/index.php/pm/article/view/16239/16652

Marcone, C., 2014. Molecular biology and pathogenicity of phytoplasmas. Annals of Applied Biology, 165(2), 199-221. http://onlinelibrary.wiley.com/journal/10.1111/(ISSN)1744-7348 doi: 10.1111/aab.12151

Marcone, C., Ragozzino, A., Seemüller, E., 1997. Detection and identification of phytoplasmas infecting vegetable, ornamental and forage crops in Southern Italy. Journal of Plant Pathology, 79(3), 211-217.

Margaria, P., Turina, M., Palmano, S., 2009. Detection of Flavescence dorée and Bois noir phytoplasmas, Grapevine leafroll associated virus-1 and -3 and Grapevine virus A from the same crude extract by reverse transcription-RealTime Taqman assays. Plant Pathology, 58(5), 838-845. http://www3.interscience.wiley.com/journal/122515832/abstract doi: 10.1111/j.1365-3059.2009.02119.x

Mehle N, Ravnikar M, Seljak G, Knapic V, Dermastia M, 2011. The most widespread phytoplasmas, vectors and measures for disease control in Slovenia. Phytopathogenic Mollicutes, 1(2): 1-12

Mertelik, J., Kloudova, K., Vanc, P., Mokra, V., Sediva, J., Navratil, M., Valova, P., 2004. First detection of phytoplasmas in rhododendron in the Czech Republic. Plant Disease, 88(8), 906. http://www.apsnet.org doi: 10.1094/PDIS.2004.88.8.906A

Minucci, C., Boccardo, G., 1997. Genetic diversity in the stolbur phytoplasma group. Phytopathologia Mediterranea, 36(1), 45-49.

Mirchenari SM, Massah A, Zirak L, 2015. 'Bois noir': new phytoplasma disease of grapevine in Iran. Journal of Plant Protection Research, 55(1):88-93. http://www.degruyter.com/view/j/jppr.2015.55.issue-1/jppr-2015-0012/jppr-2015-0012.xml?format=INT

Mitrovic M, Cvrkovic T, Jovic J, Krstic O, Jakovljevic M, Kosovac A, Tosevski I, 2015. First report of 'Candidatus Phytoplasma solani' infecting garden bean Phaseolus vulgaris in Serbia. Plant Disease, 99(4):551. http://apsjournals.apsnet.org/loi/pdis

Mitrovic, M., Jakovljevic, M., Jovic, J., Krstic, O., Kosovac, A., Trivellone, V., Jermini, M., Toševski, I., Cvrkovic, T., 2016. 'Candidatus Phytoplasma solani' genotypes associated with potato stolbur in Serbia and the role of Hyalesthes obsoletus and Reptalus panzeri (Hemiptera, Cixiidae) as natural vectors. European Journal of Plant Pathology, 144(3), 619-630. http://rd.springer.com/journal/10658

Moraki KN, Maligka VI, Katis NI, 2014. First report of a 'Candidatus Phytoplasma solani' related strain associated with a potato reddening disease in Greece. Journal of Plant Pathology, 96: S4.119

Mori, N., Mitrovic, J., Smiljkovic, M., Duduk, N., Paltrinieri, S., Bertaccini, A., Duduk, B., 2013. Hyalesthes obsoletus in Serbia and its role in the epidemiology of corn reddening. Bulletin of Insectology, 66(2), 245-250. http://www.bulletinofinsectology.org/

Mori, N., Pavan, F., Maixner, M., 2014. Control of Hyalesthes obsoletus nymphs based on chemical weeding and insecticides applied on Urtica dioica. Vitis, 53(2), 103-109. http://www.vitis-vea.de

Mori, N., Quaglino, F., Tessari, F., Pozzebon, A., Bulgari, D., Casati, P., Bianco, P. A., 2015. Investigation on 'bois noir' epidemiology in north-eastern Italian vineyards through a multidisciplinary approach. Annals of Applied Biology, 166(1), 75-89. http://onlinelibrary.wiley.com/journal/10.1111/(ISSN)1744-7348 doi: 10.1111/aab.12165

Murolo S, Romanazzi G, 2015. In-vineyard population structure of ‘Candidatus Phytoplasma solani’ using multilocus sequence typing analysis. Infection, Genetics and Evolution, 31: 221-230

Myrta, A., Ermacora, P., Stamo, B., Osler, R., 2003. First report of phytoplasma infections in fruit trees and grapevine in Albania. Journal of Plant Pathology, 85(1), 64.

Navratil M, Valova P, Savarova D, Lauterer P, Stary M, Korbasova Z, 2011. Occurrence and molecular characterization of stolbur phytoplasma infecting grapevine in South Moravia (Czech Republic). Petria, 21(2/3): 110-111

Navrátil, M., Válová, P., Fialová, R., Lauterer, P., Šafárová, D., Starý, M., 2009. The incidence of stolbur disease and associated yield losses in vegetable crops in South Moravia (Czech Republic). Crop Protection, 28(10), 898-904. http://www.sciencedirect.com/science/journal/02612194 doi: 10.1016/j.cropro.2009.05.008

Olivier, C. Y., Lowery, D. T., Stobbs, L. W., 2009. Phytoplasma diseases and their relationships with insect and plant hosts in Canadian horticultural and field crops. Canadian Entomologist, 141(5), 425-462. http://article.pubs.nrc-cnrc.gc.ca/RPAS/rpv?hm=HInit&calyLang=eng&journal=ent&volume=141&afpf=n08-CPA02.pdf doi: 10.4039/n08-CPA02

Osler, R., Vindimian, M. E., Filippi, M., Carraro, L., Refatti, E., 1997. Possibilità di propagazione del giallume della vite (Legno nero) a mezzo del materiale vivaistico (Possibility of propagation of grapevine yellows (black wood) by grafting). Informatore Fitopatologico, 47(11), 61-63.

Ozdemir, N., Saygili, H., Sahin, F., Karsavuran, Y., Bayrak, O. F., Oral, B., 2009. Host range and genetic characterization of a phytoplasma causing tomato stolbur disease in Turkey. Acta Horticulturae, (No.808), 255-261. http://www.actahort.org

Palermo, S., Ember, I., Botti, S., Elekes, M., Alma, A., Bertaccini, A., Orosz, A., Kölber, M., 2006. Detection of Stolbur phytoplasma in species of Cixiidae found in Hungarian vineyards. Növényvédelem, 42(6), 297-304.

Paltrinieri, S., Bertaccini, A., 2007. Detection of phytoplasmas in plantlets grown from different batches of seed-potatoes. Bulletin of Insectology, 60(2), 379-380. http://www.bulletinofinsectology.org/

Panjan M, 1950. (Ispitivanje stolbura Solanacea i nacin suzbijanja). Zaslita bilja, 2, 49-58.

Pap, S. M., Varga, J. G., Cervenski, J., Stepanovic, J., Rekanovic, E., Stepanovic, M., Duduk, B., 2018. First report of 'Candidatus Phytoplasma solani' infecting parsnip in Serbia. Plant Disease, 102(5), 1026. http://apsjournals.apsnet.org/loi/pdis doi: 10.1094/pdis-02-17-0197-pdn

Pavlovic S, Josic D, Starovic M, Stojanovic S, Aleksic G, Stojsin V, Radanovic D, 2012. The first Stolbur Phytoplasma occurrence on two St. John's Worth species (Hypericum perforatum L. and Hypericum barbatum L.) in Serbia. Journal of Medicinal Plants Research, 6(5):906-911. http://www.academicjournals.org/JMPR/PDF/pdf2012/9Feb/Pavlovic%20et%20al.pdf

Pavlovic, S., Starovic, M., Stojanovic, S., Aleksic, G., Kojic, S., Zdravkovic, M., Josic, D., 2014a. The first report of Stolbur phytoplasma associated with phyllody of Calendula officinalis in Serbia. Plant Disease, 98(8), 1152. http://apsjournals.apsnet.org/loi/pdis doi: 10.1094/PDIS-01-14-0085-PDN

Pavlovic, S., Starovic, M., Stojanovic, S.D., Kojic, S., Marinkovic, J., Josic, D., 2014b. First report of stolbur phytoplasma affecting Cichorium intybus in Serbia. Plant Disease, 98(6):839-840. http://apsjournals.apsnet.org/loi/pdis

Pelletier, C., Salar, P., Gillet, J., Cloquemin, G., Very, P., Foissac, X., Malembic-Maher, S., 2009. Triplex real-time PCR assay for sensitive and simultaneous detection of grapevine phytoplasmas of the 16SrV and 16SrXII-A groups with an endogenous analytical control. Vitis, 48(2), 87-95. http://vitis-vea.zadi.de

Plavec, J., Križanac, I., Budinšcak, Ž., Škoric, D., Music, M. Š., 2015. A case study of FD and BN phytoplasma variability in Croatia: multigene sequence analysis approach. European Journal of Plant Pathology, 142(3), 591-601. http://rd.springer.com/journal/10658 doi: 10.1007/s10658-015-0637-4

Quaglino, F., Maghradze, D., Casati, P., Chkhaidze, N., Lobjanidze, M., Ravasio, A., Passera, A., Venturini, G., Failla, O., Bianco, P. A., 2016. Identification and characterization of new 'Candidatus Phytoplasma solani' strains associated with bois noir disease in Vitis vinifera L. cultivars showing a range of symptom severity in Georgia, the Caucasus region. Plant Disease, 100(5), 904-915. http://apsjournals.apsnet.org/loi/pdis doi: 10.1094/PDIS-09-15-0978-RE

Quaglino, F., Maghradze, D., Chkhaidze, N., Casati, P., Failla, O., Bianco, P. A., 2014. First report of 'Candidatus Phytoplasma solani' and 'Ca. P. convolvuli' associated with grapevine bois noir and bindweed yellows, respectively, in Georgia. Plant Disease, 98(8), 1151. http://apsjournals.apsnet.org/loi/pdis doi: 10.1094/PDIS-01-14-0026-PDN

Quaglino, F., Murolo, S., Zhao, Y., Casati, P., Durante, G., Wei, W., Bianco, P. A., Romanazzi, G., Davis, R. E., 2017. Identification of new -J and -K 16SrXII subgroups and distinct single nucleotide polymorphism genetic lineages among 'Candidatus Phytoplasma solani' strains associated with bois noir in Central Italy. Australasian Plant Pathology, 46(1), 31-34. http://link.springer.com/article/10.1007/s13313-016-0461-0 doi: 10.1007/s13313-016-0461-0

Quaglino, F., Zhao Yan, Casati, P., Bulgari, D., Bianco, P. A., Wei Wei, Davis, R. E., 2013. 'Candidatus Phytoplasma solani', a novel taxon associated with stolbur- and bois noir-related diseases of plants. International Journal of Systematic and Evolutionary Microbiology, 63(8), 2879-2894. http://ijs.sgmjournals.org doi: 10.1099/ijs.0.044750-0

Radonjic S, Hrncic S, Kosovac A, Krstic O, Mitrovic M, Jovic J, Tosevski I, 2016. First report of 'Candidatus Phytoplasma solani' associated with potato stolbur disease in Montenegro. Plant Disease, 100(8):1775. http://apsjournals.apsnet.org/loi/pdis

Radonjic, S., Hrncic, S., Jovic, J., Cvrkovic, T., Krstic, O., Krnjajic, S., Toševski, I., 2009. Occurrence and distribution of grapevine yellows caused by stolbur phytoplasma in Montenegro. Journal of Phytopathology, 157(11/12), 682-685. http://www.blackwell-synergy.com/loi/jph doi: 10.1111/j.1439-0434.2009.01560.x

Rashidi, M., Habili, N., Ghasemi, A., 2010. First report of a stolbur phytoplasma associated with witches' broom of Japanese spindle (Euonymus japonicus). Plant Pathology, 59(4), 796. http://www.blackwell-synergy.com/loi/ppa doi: 10.1111/j.1365-3059.2009.02245.x

Reckhaus, P., Reckhaus, S., Adamou, I., 1988. Stolbur disease of tomato plants in Niger. Plant Disease, 72(3), 268. doi: 10.1094/PD-72-0268E

Rich, A. E., 1983. Potato diseases, New York/London, USA/UK: Academic Press, Inc.xiv + 238 pp.

Riedle-Bauer, M., Sára, A., Regner, F., 2008. Transmission of a stolbur phytoplasma by the agalliinae leafhopper Anaceratagallia ribauti (Hemiptera, Auchenorrhyncha, Cicadellidae). Journal of Phytopathology, 156(11/12), 687-690. http://www3.interscience.wiley.com/cgi-bin/fulltext/119879241/HTMLSTART doi: 10.1111/j.1439-0434.2008.01416.x

Riolo, P., Minuz, R. L., Anfora, G., Stacconi, M. V. R., Carlin, S., Isidoro, N., Romani, R., 2012. Perception of host plant volatiles in Hyalesthes obsoletus: behavior, morphology, and electrophysiology. Journal of Chemical Ecology, 38(8), 1017-1030. http://www.springerlink.com/link.asp?id=104273 doi: 10.1007/s10886-012-0154-2

Sabaté, J., Laviña, A., Batlle, A., 2014. Incidence of Bois Noir phytoplasma in different viticulture regions of Spain and Stolbur isolates distribution in plants and vectors. European Journal of Plant Pathology, 139(1), 185-193. http://rd.springer.com/journal/10658 doi: 10.1007/s10658-014-0378-9

Sakalieva, D., Paltrinieri, S., Calari, A., Bertaccini, A., 2007. Molecular identification of "bois noir" phytoplasmas in grapevine in Bulgaria. Bulletin of Insectology, 60(2), 153-154. http://www.bulletinofinsectology.org/

Salem, N. M., Quaglino, F., Abdeen, A., Casati, P., Bulgari, D., Alma, A., Bianco, P. A., 2013. First report of 'Candidatus phytoplasma solani' strains associated with grapevine bois noir in Jordan. Plant Disease, 97(11), 1505. http://apsjournals.apsnet.org/loi/pdis doi: 10.1094/PDIS-04-13-0428-PDN

Sawayanagi, T., Horikoshi, N., Kanehira, T., Shinohara, M., Bertaccini, A., Cousin, M. T., Hiruki, C., Namba, S., 1999. 'Candidatus Phytoplasma japonicum', a new phytoplasma taxon associated with Japanese Hydrangea phyllody. International Journal of Systematic Bacteriology, 49(3), 1275-1285.

Seemüller, E., Schneider, B., Mäurer, R., Ahrens, U., Daire, X., Kison, H., Lorenz, K. H., Firrao, G., Avinent, L., Sears, B. B., Stackebrandt, E., 1994. Phylogenetic classification of phytopathogenic mollicutes by sequence analysis of 16S ribosomal DNA. International Journal of Systematic Bacteriology, 44(3), 440-446.

Sémétey O, Gaudin J, Danet JL, Salar P, Theil S, Fontaine M, Krausz M, Chaisse E, Eveillard S, Verdin E, Foissac X, 2018. Lavender decline in France is associated with chronic infection by lavender-speci?c strains of “Candidatus Phytoplasma solani”. Applied and Environmental Microbiology, 84(24), e01507-18. https://doi.org/10.1128/AEM.01507-18

Seruga, M., Perica, M. C., Škoric, D., Kozina, B., Miroševic, N., Šaric, A., Bertaccini, A., Krajacic, M., 2000. Geographical distribution of Bois Noir phytoplasmas infecting grapevines in Croatia. Journal of Phytopathology, 148(4), 239-242. doi: 10.1046/j.1439-0434.2000.00484.x

Sharon, R., Harari, A. R., Zahavi, T., Raz, R., Dafny-Yelin, M., Tomer, M., Sofer-Arad, C., Weintraub, P. G., Naor, V., 2015. A yellows disease system with differing principal host plants for the obligatory pathogen and its vector. Plant Pathology, 64(4), 785-791. http://onlinelibrary.wiley.com/doi/10.1111/ppa.12316/full

Slack SA, 2001. Diseases caused by phytoplasmas. In: Compendium of potato diseases, [ed. by Stevenson WR, Loria R, Franc GD, Weingartner DP]. St. Paul, Minnesota, USA: APS Press. 56-57.

Starý, M., Válová, P., Šafárová, D., Lauterer, P., Ackermann, P., Navrátil, M., 2013. Survey and molecular detection of Bois noir in vineyards of the Czech Republic. Horticultural Science, 40(2), 83-87. http://agriculturejournals.cz/web/hortsci.htm

Sukhov KS, Vovk AM, 1946. (Cikadka Hyalesthes obsoletus Sign., perenoschik stolbur paslyonovykh). Doklady Academii Nauk SSSR, 53, 153-156.

Tanne, E., Nitzany, F. E., 1973. Virus diseases of grapevine in Israel. Vitis, 12(3), 222-225.

Terlizzi, F., Babini, A. R., Credi, R., 2006. First report of stolbur phytoplasma (16SrXII-A) on strawberry in Northern Italy. Plant Disease, 90(6), 831. doi: 10.1094/PD-90-0831A

Trkulja, N., Ivanovic, Ž., Dolovac, E. P., Dolovac, N., Živkovic, S., Jovic, J., Mitrovic, M., 2011. Stolbur phytoplasma infection of kale crops (Brassica oleracea var. gemmifera L.) in Serbia. Bulletin of Insectology, 64(Supplement), S81-S82. http://www.bulletinofinsectology.org/

Trkulja, V., Adamovic, D., Ðalovic, I., Mitrovic, P., Kovacic-Jošic, D., Lukac, Z., Komic, J., 2016. First report of stolbur phytoplasma associated with Anethum graveolens in Serbia. Plant Disease, 100(2), 516-517. http://apsjournals.apsnet.org/loi/pdis

Voncina, D., Cvjetkovic, B., 2007. Maize redness - demystifying the causal agent of one of the most destructive diseases of maize. Glasilo Biljne Zaštite, 7(5), 310-313.

Wei Wei, Lee IngMing, Davis, R. E., Suo XiaoBing, Zhao Yan, 2008. Automated RFLP pattern comparison and similarity coefficient calculation for rapid delineation of new and distinct phytoplasma 16Sr subgroup lineages. International Journal of Systematic and Evolutionary Microbiology, 58(10), 2368-2377. http://ijs.sgmjournals.org doi: 10.1099/ijs.0.65868-0

Weintraub, P. G., Beanland, L., 2006. Insect vectors of phytoplasmas. Annual Review of Entomology, 51, 91-111. http://www.annualreviews.org doi: 10.1146/annurev.ento.51.110104.151039

Yaman, I. K. A., 1971. Tomato stolbur virus: a new record. FAO Plant Protection Bulletin, 19(6), 140-141.

Yang RuiHuan, Wang GuiWei, Wang Sai, Zhang Di, Wei LiangZhu, Chen HaiMin, Li Ou, Hu XiuFang, 2016. Molecular identification and diversity of 'Candidatus Phytoplasma solani' associated with red-leaf disease of Salvia miltiorrhiza in China. Journal of Phytopathology, 164(11/12):882-889. http://onlinelibrary.wiley.com/journal/10.1111/(ISSN)1439-0434

Zamharir M, Paltrinieri S, Hajivand S, Taheri M, Bertaccini A, 2017. Molecular identification of diverse ‘Candidatus Phytoplasma’ species associated with grapevine decline in Iran. Journal of Phytopathology , 165(7-8), 407-413. doi: 10.1111/jph.12574

Zamharir MG, Taheri P, 2017. ‘Candidatus Phytoplasma solani’ related strain associated with Babylon willow witches’ broom in central provinces of Iran. Australasian Plant Disease Notes, 12: 47

Zandarski, J., 1999. Potato stolbur MLO - the threat for potato crops in Poland. Progress in Plant Protection, 39(2), 868-871.

Zhao, Y., Wei, W., Lee, I. M., Shao, J., Suo, X. B., Davis, R. E., 2009. Construction of an interactive online phytoplasma classification tool, iPhyClassifier, and its application in analysis of the peach X-disease phytoplasma group (16SrIII). International Journal of Systematic and Evolutionary Microbiology, 59(10), 2582-2593. http://ijs.sgmjournals.org doi: 10.1099/ijs.0.010249-0

Zimmerman-Gries, S., 1970. 'Stolbur'-a new Potato disease in Israel. Potato Research, 13(2), 146-150. doi: 10.1007/BF02355925

Zirak, L., Bahar, M., Ahoonmanesh, A., 2010. Molecular characterization of phytoplasmas associated with peach diseases in Iran. Journal of Phytopathology, 158(2), 105-110. http://www.blackwell-synergy.com/loi/jph doi: 10.1111/j.1439-0434.2009.01585.x

Zwolinska, A., Krawczyk, K., Pospieszny, H., 2012. Molecular characterization of stolbur phytoplasma associated with pea plants in Poland. Journal of Phytopathology, 160(7/8), 317-323. http://onlinelibrary.wiley.com/journal/10.1111/(ISSN)1439-0434 doi: 10.1111/j.1439-0434.2012.01903.x

Links to Websites

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WebsiteURLComment
COST action FA 0807: Integrated Management of Phytoplasma Epidemics in Different Crop Systemshttp://www.costphytoplasma.ipwgnet.org/
EPPO Global Databasehttps://gd.eppo.int
International Phytoplasmologist Working Group (IPWG)http://www.ipwgnet.org/

Contributors

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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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