Grapevine yellows phytoplasmas
- Taxonomic Tree
- Notes on Taxonomy and Nomenclature
- Distribution Table
- Risk of Introduction
- Hosts/Species Affected
- Host Plants and Other Plants Affected
- Growth Stages
- List of Symptoms/Signs
- Biology and Ecology
- Means of Movement and Dispersal
- Plant Trade
- Detection and Inspection
- Similarities to Other Species/Conditions
- Prevention and Control
- Distribution Maps
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PicturesTop of page
IdentityTop of page
Preferred Scientific Name
- Grapevine yellows phytoplasmas Seemüller et al., 1998
International Common Names
- Spanish: flavescencia dorada
- French: bois noir; flavescence dorée
Local Common Names
- Australia: Australian grapevine yellows
- Germany: Vergilbungskrankheit
- Italy: flavescenza dorata; giallumi della vite; legno nero
Taxonomic TreeTop of page
- Domain: Bacteria
- Phylum: Firmicutes
- Class: Mollicutes
- Order: Acholeplasmatales
- Family: Acholeplasmataceae
- Genus: Phytoplasma
- Species: Grapevine yellows phytoplasmas
Notes on Taxonomy and NomenclatureTop of page
During the last decade, considerable progress has been made in detecting, identifying and classifying phytoplasmas. Using hybridization, restriction fragment length polymorphism (RFLP) and sequence analyses of polymerase chain reaction (PCR)-amplified ribosomal DNA (rDNA), GY phytoplasmas have been characterized and assigned to six different groups. These are the elm yellows (EY), stolbur (STOL), X-disease, aster yellows (AY), Australian grapevine yellows (AUSGY) and faba bean phyllody (FBP) phytoplasma groups, respectively (Bianco et al., 1993, 1996; Daire et al., 1992, 1993, 1997a, b; Davis et al., 1993, 1997a, b, 1998; Prince et al., 1993; Chen et al., 1994; Maixner et al., 1995a, b, 1997; Alma et al., 1996; Padovan et al., 1996; Lee et al., 1998; Seemüller et al., 1998; Gibb et al., 1999; Martini et al., 1999).
The flavescence dorée (FD) agent and related phytoplasmas that have been detected in grapevine in the Palatinate region of Germany (Daire et al., 1997b; Reinert and Maixner, 1997) as well as in northern Italy (Bianco et al., 1993, 1996; Daire et al., 1997b; Seemüller et al., 1998; Martini et al., 1999) are members of the EY group. Members of the stolbur group are the agents causing bois noir (BN) and Vergilbungskrankheit (VK) diseases, which have been described from northern France (Caudwell, 1961) and Germany (Gärtel, 1965), respectively.
Other GY diseases occur in several European countries and Israel (Daire et al., 1993, 1997a; Maixner et al., 1995a; Davis et al., 1997a; Refatti et al., 1998; Seemüller et al., 1998). The X-disease group includes strain FDU, which was experimentally transmitted by dodder from naturally infected grapevines to the experimental host Catharanthus roseus (periwinkle) in the Friuli-Venezia Giulia region of Italy (Davis et al., 1993), and phytoplasmas infecting grapevine in the USA (Prince et al., 1993; Davis et al., 1998).
In addition, a phytoplasma of the X-disease group has been associated with GY in northern Italy (Bertaccini et al., 1994). AY phytoplasmas of 16SrI-A and 16SrI-B subgroups were identified in diseased grapevines in the USA and northern Italy, respectively (Alma et al., 1996; Davis et al., 1998).
Candidatus Phytoplasma australiense, a member of the AUSGY group and a phytoplasma which proved to be indistinguishable on the basis of RFLP profiles from tomato big bud (TBB) agent, a member of the FBP group, was associated with GY diseases in Australia (Padovan et al., 1996; Davis et al., 1997b, Gibb et al., 1999).
DescriptionTop of page
The phytoplasma bodies were bound by a unit membrane 6-7 nm thick and contained DNA strands and ribosome granules in their cytoplasm. They were typically pleomorphic, although generally spherical or filamentous in appearance. Unusual structures, considered to be senescent and degenerative forms of phytoplasmas were also seen in ultra-thin sections of diseased grapevine (Credi, 1994b). These structures had a high cytoplasmatic electron density, granulation and irregular condensation of the cytoplasmic contents, ruptures of plasma membranes and cell fragmentation.
Ribosomes and DNA strands found in normal phytoplasma bodies were either absent or obscured by the cytoplasm opacity. Numerous anomalous phytoplasma bodies were observed in collapsing sieve elements. One type was spherical, mostly 90-280 nm diameter, with homogeneous cytoplasm containing highly electron-dense granules and a poorly-defined unit membrane, with external amorphous material. The bodies were sometimes distorted with disrupted membranes and were intermixed with surrounding shapeless and membranous debris of disorganised host protoplasts and phytoplasma cells.
A second type of anomalous phytoplasma was densely packed in degenerate cells and appeared as strongly electron-dense pleomorphic structures with irregular condensation of cytoplasmic substances and surrounded by electron transparent borders.
DistributionTop of page
FD phytoplasma is present in southern France, northern Italy and Catalonia, while EY-related phytoplasmas are known to occur in grapevine in Germany and northern Italy (Batlle et al., 1997; Daire et al., 1997b; Reinert and Maixner, 1997; Seemüller et al., 1998; Martini et al., 1999).
STOL phytoplasmas infect grapevine in several European countries and Israel while AY and X-disease phytoplasmas have been detected in diseased grapevine in northern Italy and eastern North America (Maixner et al., 1995a, 1997; Alma et al., 1996; Daire et al., 1997a; Davis et al., 1997a, 1998; Seemüller et al., 1998).
GY phytoplasmas of the AUSGY and FBP groups are only known to occur in Australia (Padovan et al., 1996; Davis et al., 1997b; Gibb et al., 1999).
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.Last updated: 10 Jan 2020
|Continent/Country/Region||Distribution||Last Reported||Origin||First Reported||Invasive||Reference||Notes|
|United States||Present||Present based on regional distribution.|
Risk of IntroductionTop of page
FD phytoplasma is a quarantine organism in the EU (Directive EEC 77/93). Multiplication and plantation vine material must be free of the organism. Certification cannot be obtained by mere diagnosis on the material, due to the uneven distribution of phytoplasma in the canes and in the mother stock which makes sampling uncertain. Rootstock varieties are an additional hazard because they may be tolerant to the phytoplasma and act as symptomless carriers of the disease agent that they will distribute by grafting to Vitis vinifera scions (Caudwell et al., 1994). Certification must include indexing on susceptible varieties and observation in quarantine nurseries of scions and grafted plants.
Hosts/Species AffectedTop of page
The FD phytoplasma was transmitted from naturally diseased grapevine plants to the experimental hosts Vicia faba (broad bean) and Chrysanthemum carinatum (tricolor chrysanthemum) using the insect vector Scaphoideus titanus while several strains of the STOL phytoplasma including the VK agent as well as strain FDU were transmitted by means of dodder (Cuscuta species) bridges from infected grapevines to periwinkle (Caudwell et al., 1970; Credi and Santucci, 1992). Broad bean and Datura stramonium (thorn apple) are also reported as experimental hosts of VK and BN agents (Maixner et al., 1995a; Sforza et al., 1998).
Host Plants and Other Plants AffectedTop of page
|Apium graveolens (celery)||Apiaceae||Other|
|Capsicum annuum (bell pepper)||Solanaceae||Other|
|Carica papaya (pawpaw)||Caricaceae||Other|
|Convolvulus arvensis (bindweed)||Convolvulaceae||Wild host|
|Datura stramonium (jimsonweed)||Solanaceae||Wild host|
|Fragaria ananassa (strawberry)||Rosaceae||Other|
|Nicotiana tabacum (tobacco)||Solanaceae||Other|
|Phormium tenax (New Zealand flax)||Agavaceae||Other|
|Solanum lycopersicum (tomato)||Solanaceae||Other|
|Solanum melongena (aubergine)||Solanaceae||Other|
|Taraxacum (dandelion)||Asteraceae||Wild host|
|Vitis vinifera (grapevine)||Vitaceae||Main|
Growth StagesTop of page
SymptomsTop of page
The leaves of affected plants are thicker than normal, brittle, rolled downward and show veinal yellowing followed by necrosis. Shoots of affected branches exhibit rows of black pustules that develop along the internodes. Due to incomplete lignification, these shoots are more flexible than normal and confer a drooping aspect to the plants. Flowers and bunches are whiter and desiccated.
List of Symptoms/SignsTop of page
|Fruit / abnormal shape|
|Fruit / mummification|
|Fruit / reduced size|
|Growing point / dieback|
|Growing point / discoloration|
|Growing point / distortion|
|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|
|Roots / reduced root system|
|Stems / dieback|
|Stems / distortion|
|Stems / stunting or rosetting|
|Stems / witches broom|
|Whole plant / distortion; rosetting|
|Whole plant / early senescence|
|Whole plant / plant dead; dieback|
Biology and EcologyTop of page
Transmission of the disease is persistent, with the pathogen multiplying first in the cells of the diseased plant and then in the body of the infected host insect. S. titanus is present, most of the time in very high numbers, in vineyards throughout Southern France including Bordeaux, the Loire valley and Burgundy, as well as in Corsica (Caudwell et al., 1978), Northern Spain (Laviña et al., 1995), Northern Italy (Osler et al., 1975; Belli et al., 1985), Switzerland (Clerc et al., 1997), Slovenia and Croatia (Gabrijel, 1987) and other viticultural countries of eastern Europe. The area of incidence of FD disease is not as extensive as that of the S. titanus.
Another insect vector, Euscelidius variegatus, which produces several broods each year and is easily bred in captivity, can transmit FD agent among Vicia faba plants. By this means, FD phytoplasma has been maintained for many years in this experimental host (Caudwell et al., 1987).
The planthopper Hyalesthes obsoletus is known to transmit the VK phytoplasma in Germany (Maixner, 1994) and BN phytoplasma in France (Sforza et al., 1998) whereas Macrosteles species and Neoaliturus fenestratus are reported to transmit the STOL phytoplasma to weeds and Solanaceous crop plants (Maixner et al., 1995a). Recently, Maixner et al. (2000) reported on the transmission of alder yellows (ALY) phytoplasma from diseased alder trees to grapevine by the leafhopper Oncopsis alni. ALY-infected grapevine plants showed typical symptoms of GY diseases.
GY phytoplasmas are also transmissible by dodder (Cuscuta species) (see Host Range).
Means of Movement and DispersalTop of page
Abiotic factors are not involved in the natural spread of the pathogen.
FD phytoplasma is naturally transmitted by the leafhopper Scaphoideus titanus while VK and BN agents are transmitted by the planthopper Hyalesthes obsoletus. The EY-related phytoplasma that has been detected in grapevine in the Palatinate region of Germany (Daire et al., 1997b; Reinert and Maixner, 1997) was transmitted by the leafhopper Oncopsis alni (Maixner et al., 2000).
Like other phytoplasmas, GY phytoplasmas are not seed-transmissible.
The use of infected plant material is responsible for long-distance movement of the pathogens.
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|
|Flowers/Inflorescences/Cones/Calyx||Yes||Pest or symptoms usually visible to the naked eye|
|Leaves||Yes||Pest or symptoms not visible to the naked eye but usually visible under light microscope|
|Roots||Yes||Pest or symptoms not visible to the naked eye but usually visible under light microscope|
|Seedlings/Micropropagated plants||Yes||Pest or symptoms usually visible to the naked eye|
|Stems (above ground)/Shoots/Trunks/Branches||Yes||Pest or symptoms not visible to the naked eye but usually visible under light microscope|
|Plant parts not known to carry the pest in trade/transport|
|Fruits (inc. pods)|
|Growing medium accompanying plants|
|True seeds (inc. grain)|
ImpactTop of page
According to studies by Maixner and Reinert (1997), the proportion of VK-infected vines in some vineyards in Germany, increased from 18% in 1990 to 26% in 1995. The disease incidence within individual vineyards varied from 5% to 65%. It was increasing in seven of the 12 vineyards investigated and decreasing in three. The increase in the number of symptomatic vines was highest in young plantings, which often provide favourable conditions for the insect vector Hyalesthes obsoletus and the alternative host of the VK phytoplasma, field bindweed. These vineyards are severely damaged, since young grapes systemically develop symptoms and die.
In the Emilia-Romagna region (northern Italy), Credi and Callegari (1988) found that the percentage of GY-infected vines varied in the period 1983-1987 from 0.1 to 42.8% while crop losses of 47% were recorded in affected vineyards of cv. Sangiovese (Credi, 1989). Disease incidences of more than 70% with very heavy crop losses have been recorded in GY-affected vineyards of cv. Chardonnay in the Veneto region of northern Italy (Belli et al., 1994) while a disease incidence of 76% was recorded in the Latium region (central Italy) (Del Serrone et al., 1995).
In Slovenia, during a survey carried out during 1991-1995, the percentage of GY-infected grapevine plants varied from 2 to 38% and the crop losses in infected vineyard ranged from 20 to 40% (Koruza, 1996).
For details about economic impact of FD-phytoplasma and Candidatus Phytoplasma australiense see the corresponding data sheets.
DiagnosisTop of page
Polyclonal antisera and monoclonal antibodies have been raised against various phytoplasmas including some GY agents (Boudon-Padieu et al., 1989; Schwartz et al., 1989; Fos et al., 1992; Chen et al., 1993, 1994; Seddas et al., 1996).
An ELISA procedure based on an indirect double sandwich with rabbit polyclonal as trapping antibodies and a cocktail of mouse monoclonal antibodies specific for two or several epitopes of membrane proteins, has been used to assay FD phytoplasma in field-collected Scaphoideus titanus leafhoppers as well as in grapevines (Boudon-Padieu et al., 1989; Schwartz et al., 1989; Osler et al., 1992; Seddas et al., 1996). However, the procedure requires the presence of a high concentration of detergents in the extraction buffer in order to improve preservation and accessibility of phytoplasma antigens from grapevine tissues (Caudwell and Kuszala, 1992).
An ELISA procedure based on the use of monoclonal antibodies was used to assay BN and VK phytoplasmas (Kuszala, 1996; Maixner et al., 1997).
PCR technology has been widely adopted for the detection and identification of GY phytoplasmas (Bianco et al., 1993, 1996; Daire et al., 1993, 1997a, b; Maixner et al., 1994, 1995a, b; Marcone et al., 1996; Padovan et al., 1996; Batlle et al., 1997; Davis et al., 1997a, b, 1998; Gibb et al., 1999; Martini et al., 1999). PCR is well suited to PCR research because of its versatility, simplicity, specificity and high sensitivity. Primers derived from ribosomal and/or non-ribosomal DNA sequences have been designed, which enable phytoplasma detection in a universal or group-specific manner. PCR amplification may be performed as non-nested PCR using either universal or group-specific primer pairs, or as nested PCR employing universal phytoplasma primers for initial amplification and internal primers then used to reamplify products generated by universal primers (Bianco et al., 1996; Davies et al., 1997a, 1998; Martini et al., 1999).
Differentiation of GY phytoplasmas from other members of their respective phylogenetic group can usually be obtained by RFLP analysis of PCR-amplified 16S rRNA gene and 16S/23S rDNA spacer sequences employing suitable restriction endonucleases (Marcone et al., 1997; Davies et al., 1998; Gibb et al., 1999; Martini et al., 1999).
However, all GY agents of the STOL group proved to be indistinguishable from each other and from other member of the same group on the basis of RFLP analysis of PCR-amplified rDNA (Marcone et al., 1996; Seemüller et al., 1998; C. Marcone, unpublished data). The EY-related phytoplasma detected in grapevine in the Palatinate region of Germany (Daire et al., 1997b; Reinert and Maixner, 1997) was also indistinguishable according to RFLP profiles from the related ALY phytoplasma.
Detection and InspectionTop of page
Similarities to Other Species/ConditionsTop of page
Grapevine leafroll virus: leafroll may be confusing. Compared with GY diseases, veins remain green and lignification of canes occurs; bunches do not wither; and leaf symptoms always affect the whole stock.
Injuries on sieve circulation such as string restriction, circular incision of bark caused by mechanical injury or insects induce leaf discoloration. However, compared with GY diseases, foliar discoloration induced by these other causes affects the entire leaf laminae. Reddening of veins and petioles is also common and lignification of canes occurs.
Botrytis cinerea on canes and stems.
Esca disease: withering of bunches and leaf discoloration symptoms may be confusing. However, in the case of Esca disease, which is caused by a complex of several fungi including Phellinus igniarius and Stereum hirsutum, the stock will suddenly collapse in July or August.
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.
Use of healthy plant material, removal of infected plants and effective control of insect vectors are important measures for reducing the incidence of GY phytoplasmas. Healthy plants should be used for establishing new vineyards. Therefore, rootstocks and scionwood should be indexed by an appropriate method to ensure that they are free from infection. Also, GY phytoplasmas seem to be readily eliminated from plant material by hot-water treatment at 50°C for 45 minutes (Caudwell et al., 1997; Rivenez and Bonjotin, 1997; Bianco et al., 2000; Murari et al., 2000). Diseased grapevine plants as well as alternative plant hosts and insect vectors of the pathogens should be eliminated as they are identified.
Weber et al. (1998) reported a high disease incidence (30-34%) of VK disease in vineyards with a high number of field bindweed plants and an abundance of Hyalesthes obsoletus, which are dependent on field bindweed plants. Moreover, they found that some agricultural practices such as ploughing negatively affected populations of this planthopper vector.
In France, control of FD disease is subject to several legislative directives. One reason is the high adverse impact of this disease on the viticulture industry. Furthermore, the successful control of the disease is only feasible by well coordinated activity by producers within a particular area, due to the high mobility of the vector. All mother plots used as a source of propagation material must be treated with insecticides three times a year to protect against infestation by Scaphoideus titanus while all nurseries must be treated throughout the time when larval stages or adults of S. titanus occur.
Directives from the local authorities regulate the mandatory control of FD disease for particular areas where the disease is present. They also regulate the mandatory control of S. titanus by insecticides and the measures to be taken in order to reduce inoculum.
Prophylactic activities include the destruction of FD-infected vines as well as uprooting of both cultivated and wild Vitis plants in abandoned vineyards, both of which are potential sources of inoculum and provide a breeding reservoir for the vector. These measures, as well as the mandatory uprooting of complete vineyards when the disease incidence exceeds a certain level, are subject to prefectorial directives in France.
Control of the vector depends on insecticide treatments, which are applied either against the eggs during winter or against larvae and adult leafhoppers during the growing season. Pruned plant parts that carry the eggs of S. titanus should be burned. The number of viable eggs can be reduced by a treatment of vines in March before bud-burst. A wide range of insecticides, mainly organophosphates and pyrethroids, are available for summer treatments, which are usually applied three times. The first treatment is usually applied in June and should not be done later than 1 month after the beginning of hatching. The time of the second application depends on the stability of the compound used. The second treatment is usually applied in combination with insecticidal control of the second generation of grape berry moth. Adult leafhoppers immigrating into vineyards from surrounding areas are the target of a third treatment in August.
For further information see Caudwell (1965), Caudwell et al. (1971b, 1974) and Boudon-Padieu and Maixner (1998).
ReferencesTop of page
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Credi R; Santucci A, 1992. Dodder transmission of mycoplasma-like organisms (MLOs) from grapevines affected by a flavescence doree-type disease to periwinkle. Phytopathologia Mediterranea, 31(3):154-162
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Daire X; Clair D; Reinert W; Boudon-Padieu E, 1997. Detection and differentiation of grapevine yellows phytoplasmas belonging to the elm yellows group and to the stolbur subgroup by PCR amplification of non-ribosomal DNA. European Journal of Plant Pathology, 103(6):507-514; 28 ref.
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Davis RE; Dally EL; Gundersen DE; Lee IngMing; Habili N, 1997. "Candidatus phytoplasma australiense", a new phytoplasma taxon associated with Australian grapevine yellows. International Journal of Systematic Bacteriology, 47(2):262-269; 45 ref.
Davis RE; Dally EL; Tanne E; Rumbos IC, 1997. Phytoplasmas associated with grapevine yellows in Israel and Greece belong to the stolbur phytoplasma subgroup, 16SrXII-A. Journal of Plant Pathology, 79(3):181-187; 31 ref.
Davis RE; Jomantiene R; Dally EL; Wolf TK, 1998. Phytoplasmas associated with grapevine yellows in Virginia belong to group 16SrI, subgroup A (tomato big bud phytoplasma subgroup), and group 16SrIII, new subgroup I. Vitis, 37(3):131-137; 22 ref.
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