Grapevine flavescence doree phytoplasma (flavescence dorée of grapevine)
- 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
- Notes on Natural Enemies
- Vectors and Intermediate Hosts
- 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 flavescence doree phytoplasma
Preferred Common Name
- flavescence dorée of grapevine
Other Scientific Names
- Flavescence dorée MLO
- Flavescence dorée mycoplasmalike organism
- Grapevine yellows
International Common Names
- English: grapevine bois noir
- Spanish: flavescencia dorada de la vid; flavescencia dorada de la viña
- French: flavescence dorée de la vigne; rougeau
Local Common Names
- Italy: flavescenza dorata della vite
- PHYP64 (Grapevine flavescence dorée phytoplasma)
Taxonomic TreeTop of page
- Domain: Bacteria
- Phylum: Firmicutes
- Class: Mollicutes
- Order: Acholeplasmatales
- Family: Acholeplasmataceae
- Genus: Phytoplasma
- Species: Grapevine flavescence doree phytoplasma
Notes on Taxonomy and NomenclatureTop of page Phytoplasmas were called mycoplasma-like organisms or MLO from their discovery in 1967 until 1994, when the International Committee of Systematic Bacteriology (ICSB) Subcommittee on the Taxonomy of Mollicutes (1993, 1997) adopted the term phytoplasma to describe these organisms as they were found to comprise a new phylogenetic clade in the Class Mollicutes. The phytoplasma clade is currently subdivided into twenty major groups or subclades (groups). Flavescence dorée phytoplasma belongs to the elm yellows group. At least five other different phytoplasmas induce symptoms similar to flavescence dorée on grapevine. A generic name for these collective diseases is grapevine yellows (Bovey and Martelli, 1992).
Due to an earlier lack of methods for characterisation of phytoplasmas, other grapevine yellows diseases have been called flavescence dorée or flavescence dorée-like diseases in the past, and are now known to be symptomatically similar diseases caused by taxonomically different phytoplasmas. For example, Bois noir of grapevine (Caudwell, 1961) and Vergilbungskrankheit (Gärtel, 1965), present in most European viticultural countries and associated with phytoplasmas in the stolbur group (Daire et al., 1993a, 1993b, 1997b; Maixner et al., 1994; Lavila et al., 1995), whereas American grapevine yellows is associated with X disease or aster yellows group phytoplasmas (Chen et al., 1993; Daire et al., 1993b; Prince et al., 1993; Davies et al., 1998). Aster yellows group phytoplasmas are also associated with grapevine yellows in Australia (Padovan et al., 1995), Italy and Croatia (Prince et al., 1993; Saric et al., 1997).
DescriptionTop of page Phytoplasmas (McCoy et al., 1989) are small wall-less organisms in the class Mollicutes. They are heterogeneous in shape and size (50 to 1000 nm). They are associated with diseases of several hundred plant species. Phytoplasmas have the smallest genome (600 to 1000 kilobase) known for self-replicating organisms. They are intracellular parasites that are recalcitrant to in vitro cultivation, and very difficult to purify from their hosts because of their fragility and low titres. They move and multiply in the phloem sieve tubes of plants and in the body of their insect vector. They survive only a short period of time in extracts. They are transmitted to plants by insect vectors, by grafting or by dodder bridges established between the infected donor and the recipient plant only.
Numerous phytoplasma strains infecting dicotyledonous plant hosts have been experimentally transmitted to periwinkle (Catharanthus roseus) and are maintained in this species for reference purposes. They have been classified, mainly on the basis of the sequence of their 16S rDNA, into as many as 20 major phylogenetic groups (see review by Seemüller et al., 1998). Grapevine flavescence dorée phytoplasma belongs to the elm yellows (EY) group (Daire et al., 1993a, 1997b). It is specifically transmitted by the leafhopper species Scaphoideus titanus Ball (Schvester et al., 1963) and may be differentiated readily from other phytoplasmas in the EY group by PCR-RFLP analysis of non-ribosomal DNA (Daire et al., 1997a).
DistributionTop of page As grapevine yellows develop symptoms that are similar whatever the associated phytoplasma, there may still be some confusion regarding the distribution of different grapevine yellows. Descriptions of grapevine yellows as 'flavescence dorée' or 'flavescence dorée-like disease' in the 1970s and 1980s should be revisited and the associated phytoplasmas characterized, particularly in regions inhabited by the leafhopper vector species of flavescence dorée.
The leafhopper Scaphoideus titanus is ampelophagous. It was introduced to Europe a few decades ago and has been doing very well in the climate of the Northern border of the Mediterranean sea. It 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 (Lavila 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 flavescence dorée is hopefully not as extensive as that of the leafhopper vector. In France, the epidemic pressure is very high in the Southern part of the extension area of S. titanus, but the disease has not reached the Northern border. However, Bois noir is present in all French vine regions (Daire et al., 1997b) and may be confused with flavescence dorée.
In Italy, flavescence dorée is restricted to the Veneto and Liguria regions at present (Osler et al., 1992; Daire et al., 1993b; Refatti, 1993; Carraro et al., 1994; Bertaccini et al., 1995; Bianco et al., 1996; Marcone et al., 1996; Belli et al., 1997) whereas Bois noir is present in almost all the viticultural areas.
In Spain, flavescence dorée was identified for the first time in Northern Cataloña in 1996 (Batlle et al., 1997). The disease has not been identified in Croatia, Slovenia or Switzerland, but other grapevine yellows have been reported.
Not enough evidence has been given for the presence of flavescence dorée in North America, though S. titanus specimens were found carrying a flavescence dorée-related phytoplasma in New York (Maixner et al., 1993). It is known that other grapevine yellows affect grapevine in New York and Virginia (Chen et al., 1993, Daire et al., 1993b; Prince et al., 1993). S. titanus is also known in California (A Purcell, University of California, Berkeley, California, USA, unpublished data) where grapevine yellows has not been reported. It must be emphasized, however, that the presence of S. titanus in any viticultural region should be considered as a threat because any introduction of grapevine planting material latently contaminated by flavescence dorée phytoplasma might result in serious epidemics of the disease, due to the highly specialized and efficient transmission process by the vector.
Distribution TableTop of page
The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.
|Continent/Country/Region||Distribution||Last Reported||Origin||First Reported||Invasive||Reference||Notes|
|USA||Absent, unreliable record||EPPO, 2014|
|-New York||Absent, unreliable record||Maixner et al., 1993; EPPO, 2014|
|Uruguay||Absent, confirmed by survey||EPPO, 2014|
|Austria||Present, few occurrences||EPPO, 2014|
|Belgium||Absent, no pest record||EPPO, 2014|
|Croatia||Restricted distribution||Seljak, 1987; EPPO, 2014|
|France||Restricted distribution||Daire et al., 1997a; Daire et al., 1997b; Caudwell et al., 1986; Boudon-Padieu et al., 1987; Boudon-Padieu et al., 1989; Daire et al., 1989; CABI/EPPO, 1998; EPPO, 2014|
|-Corsica||Present||Caudwell et al., 1978; CABI/EPPO, 1998; EPPO, 2014|
|Germany||Absent, invalid record||CABI/EPPO and, 1998; EPPO, 2014|
|Hungary||Restricted distribution||EPPO, 2014|
|Italy||Restricted distribution||Daire et al., 1993b; Osler et al., 1993; Refatti, 1993; Carraro et al., 1994; Bertaccini et al., 1995; Bianco et al., 1996; Marcone et al., 1996; CABI/EPPO, 1998; EPPO, 2011; EPPO, 2014|
|Netherlands||Absent, confirmed by survey||NPPO of the Netherlands, 2013; EPPO, 2014|
|Portugal||Restricted distribution||Sousa et al., 2010; EPPO, 2014|
|Serbia||Restricted distribution||EPPO, 2014|
|Slovenia||Restricted distribution||Seljak, 1987; EPPO, 2014|
|Spain||Present, few occurrences||Daire et al., 1997a; Batlle et al., 1997; CABI/EPPO, 1998; EPPO, 2014|
|-Balearic Islands||Absent, confirmed by survey||EPPO, 2014|
|Switzerland||Present, few occurrences||Schaerer et al., 2007; Schaub, 2007; EPPO, 2014|
|UK||Absent, no pest record||EPPO, 2014|
Risk of IntroductionTop of page Flavescence dorée 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 serve as symptomless carriers of the disease agent that they will distribute by grafting to V. vinifera scions (Caudwell et al., 1994). Unpublished data indicate that incubation of the disease for as long as several years before any overt expression of symptoms may occur in scions grafted onto infected rootstocks. Certification must include indexing on susceptible varieties and observation in quarantine nurseries of scions and grafted plants.
A curing method involving soaking of dormant material for 45 min in 50°C hot water (Caudwell et al., 1990, 1997) kills phytoplasmas in situ and ensures healthy material. This method should be applied to all planting material in flavescence dorée-free regions, especially those inhabited by the leafhopper vector.
HabitatTop of page Due to the feeding preferences of the leafhopper vector Scaphoideus titanus, an oligophagous or monophagous species in natural conditions, the habitat of grapevine flavescence dorée phytoplasma is restricted to species of Vitis. No detection of phytoplasma strains similar to grapevine flavescence dorée strains on any weed or other crop has been reported.
Hosts/Species AffectedTop of page Flavescence dorée phytoplasma is transmitted by the leafhopper vector Scaphoideus titanus, formerly Scaphoideus littoralis (Schvester et al., 1963) which is an ampelophagous species. Thus, flavescence dorée phytoplasma is restricted to species of Vitis under natural conditions.
In laboratory conditions, it was possible to feed-inoculate a few herbaceous plant species (Caudwell et al., 1970). Broad bean (Vicia faba) is the host currently used for experimental transmission, but it is not a natural host, neither of flavescence dorée phytoplasma nor of S. titanus.
Host Plants and Other Plants AffectedTop of page
Growth StagesTop of page Flowering stage, Fruiting stage, Post-harvest, Vegetative growing stage
SymptomsTop of page Yellows diseases attributed to phytoplasmas induce symptoms on vegetative and reproductive organs of plants indicating that host nutrient circulation and hormonal balance are affected (McCoy et al., 1989). Symptoms of flavescence dorée are typical of these disturbances (Caudwell, 1957; Boudon-Padieu, 1996; Boudon-Padieu and Maixner, 1998). Leaves show yellowing discoloration and rolling down of laminae. Flower-withering and berry-shrivelling results in a reduction of quality and quantity of crop. Woody canes are poorly ripened and remain rubbery, thus giving the stock an overall 'weeping' aspect. Not enough young wood is produced and left for pruning. Stocks rapidly decline.
Vine stocks are affected in spots that extend radially in the vineyard, due to transmission from one stock to the next by mobile, winged adults of S. titanus.
List of Symptoms/SignsTop of page
|Fruit / mummification|
|Fruit / reduced size|
|Growing point / dieback|
|Inflorescence / blight; necrosis|
|Inflorescence / fall or shedding|
|Leaves / abnormal colours|
|Leaves / abnormal forms|
|Leaves / abnormal leaf fall|
|Leaves / abnormal patterns|
|Roots / reduced root system|
|Stems / discoloration of bark|
|Whole plant / plant dead; dieback|
Biology and EcologyTop of page Only insect vectors and dodder grafts transmit phytoplasmas. Infected vectors remain inoculative for the rest of their life. They are able to infect a plant on each feeding or probing event. Infection of grapevine with flavescence dorée phytoplasma by Scaphoideus titanus may occur at any time from the beginning of June (young larvae) until late September (old adults). The severity of the disease does not depend on the date of inoculation. Incubation of the phytoplasma takes place from the moment of inoculation until symptom expression. Symptoms will normally develop in the following year. Infected plant material used for vegetative propagation is infected definitively, and is a source for long-distance transportation of the disease.
Notes on Natural EnemiesTop of page Several studies have been conducted on the autochthonous fauna in vineyards in southern France to search for the possibility of a biological regulation of S. titanus. Though specimens may eventually be found carrying a chrysopid parasite, no significant natural enemies, either parasitoids or predators have been demonstrated. As the species originates from North America and has most probably been imported as eggs on dormant vine material, it is considered that it was transported without its natural enemies, if any. Thus, the latter should be searched for in the USA. Research is underway on the possible use of entomophagous fungi for biological control.
Vectors and Intermediate HostsTop of page
ImpactTop of page Flavescence dorée causes symptoms that are detrimental to infected vines. Depending on the intensity of infection the yields may decrease dramatically. Their vitality is affected, yields are reduced, and the quality of wine is decreased by high acid and low sugar contents of infected clusters. When no control of the vector has been undertaken, the number of infected vines may increase steadily about 10 times every year and may reach 80-100% within a few years. The economic viability of maintaining a vineyard ceases when the productive plants are less than 25% of the total.
In France and Corsica, where it is considered a major disease of grapevine, flavescence dorée has destroyed large viticultural areas and suppressed this crop from these regions since the 1950s. It is still progressing in spite of mandatory uprooting of the diseased stocks and mandatory insecticide control of S. titanus.
Several cultivars which are used for the production of high-quality products such as Chardonnay, Cabernet Sauvignon, Sauvignon blanc, Sémillon, Grenache, Barbera, Trebiano toscano (syn. Ugni blanc), Soave, Prosecco, Garganega, are highly susceptible to flavescence dorée. Furthermore, the culture of several varieties which are of regional importance only but are essential for the production of unique specialities, is endangered (Sancassani and Posenato, 1995; Posenato et al., 1996). Cultivars such as Sangiovese (syn. Nielluccio) and Garganega are extremely susceptible and killed immediately by flavescence dorée. Biodiversity of vine germplasm is endangered.
DiagnosisTop of page
A diagnostic protocol for Grapevine flavescence doree phytoplasma is given in OEPP/EPPO (2007).
The most important diagnostic methods for flavescence dorée (FD) disease are ELISA or DNA-based methods (see review by Maixner et al., 1997). They may be used to detect the causative phytoplasma in both vines and insect vectors.
Flavescence dorée-ELISA is based on an indirect double sandwich assay which uses anti-FD rabbit polyclonal antibodies (Boudon-Padieu et al., 1989) as trapping antibodies and a cocktail of mouse monoclonal antibodies (Schwartz et al., 1989; Seddas et al., 1996) specific for two or several epitopes of FD phytoplasma membrane proteins. The assay can be readily applied to wild leafhoppers from vineyards, and has also been adapted to plant extracts from grapevine leaves, veins, or petioles. However, detergents must be added to the extraction buffer when assessing grapevine tissues to ensure access to phytoplasma antigens (Caudwell and Kuszala, 1992). The latter conditions are a compromise between phytoplasma cell integrity and access to antigens as targets in the assays. Thus the sensitivity of the assay applied to grapevine is probably reduced by the presence of detergents that are nevertheless necessary.
The most widely used DNA-based method for diagnosis of FD disease is PCR. Two kinds of primers may be used, either for specific assays to identify flavescence dorée phytoplasma or for 'universal' detection assays that allow the detection of any phytoplasma (Seemüller et al., 1998). In the latter case, RFLP analysis of the amplification product will supply additional information on the taxonomic position of the detected phytoplasma.
Specific assays use nonribosomal primers constructed from a cloned anonymous DNA fragment of the flavescence doree phytoplasma (Daire et al., 1992). These primers specifically amplify the homologous sequence in this phytoplasma and other closely related strains in a group-specific manner (Daire et al., 1997a). PCR assays with these tools will detect only phytoplasmas similar or closely related to flavescence dorée phytoplasma. Primers with similar specificity have also been developed for rRNA gene sequences (Maixner et al., 1995). Such primer pairs are especially suited for use in PCR assays to enable sanitary certification for flavescence dorée as it is a quarantine disease with compulsory declaration and compulsory control in France.
'Universal' assays use primers constructed from conserved nucleotide sequences in phytoplasma ribosomal DNA (16S rDNA and intergenic spacer) (see review by Seemüller et al., 1998). The internal sequence of the amplified DNA fragment is further analysed by enzymatic restriction with an endonuclease and the observation of the restriction profile (RFLP). Comparison of RFLP profiles with those displayed by a reference phytoplasma allows the detected phytoplasma to be identified and assigned a special taxonomic group. These PCR assays are especially useful for the survey of grapevine yellows (Daire et al., 1997b), and also for the identification of still unknown grapevine yellows agents and the identification of insect vectors. They may also be used as second or verification assays whenever specific assays produce negative results from samples bearing flavescence dorée-like symptoms.
Detection and InspectionTop of page Symptoms of flavescence dorée first appear in early summer and increase in incidence and severity until harvest. Whole vines are often affected, indicating that the stock has been infected for several years. Symptoms during the first year of expression may be restricted to only a few shoots. Early season symptoms can be observed on inflorescence which partially or totally wither, or on aborted bunches. If berries are formed, summer symptoms will include drying of berry peduncles and consecutive shrivelling or drying of berries, leaf discoloration and backward curling of laminae. Late season symptoms are manifested by very poor ripening of affected canes that seem 'rubbery'. Plants lack structural integrity and will bend to the ground in a striking 'weeping' posture to the tree, manifested even when vines are not attached.
Similarities to Other Species/ConditionsTop of page Symptoms of flavescence dorée (Caudwell, 1957) do not distinguish this disease from other grapevine yellows diseases (Caudwell et al., 1971b; Bovey and Martelli, 1992; Boudon-Padieu and Maixner, 1998).
In addition, symptoms of flavescence dorée or grapevine yellows, may also be confused with other diseases or disorders. These include,
Grapevine leafroll virus. In contrast with flavescence dorée, veins remain green and lignification of canes occurs; bunches do not wither; leaf symptoms always affect the whole stock.
Disruption of phloem function (string restriction, circular incision of bark caused by mechanical accidents or insects) cause leaf discoloration. However, in contrast with flavescence dorée, the discoloration affects the whole laminae and reddening of veins and petioles is observed, lignification of canes also occurs.
Botrytis cinerea on canes and stems.
Esca de la vigne: withering of bunches and leaf discoloration, though with a different pattern, may be confusing. However in the case of Esca the stock will collapse suddenly in July or August. This is caused by a complex of several fungi including Phellinus igniarius and Stereum hirsutum.
Prevention and ControlTop of page
The improvement and maintenance of the phytosanitary quality of planting material by certification procedures and the protection of mother plots and nurseries from inoculation is an important prevention strategy for the establishment of healthy vineyards. This is even more important for planting material that is shipped into areas that are not yet affected.
Two principles of controlling the spread of flavescence dorée can be distinguished. One is decreasing the inoculum density and the second is controlling the vector. Inoculation pressure may be reduced by the destruction of sources of infection consisting of infected vines. Vector control is accomplished by the use of insecticides since no biological control of the vector is available.
In France, control of flavescence dorée is subject to several legislative directives. One reason is the high importance of this disease for viticulture. Furthermore, the successful control of flavescence dorée is only possible as a joint activity for a particular area, due to the high mobility of the vector. In France, all mother plots for propagation material have to be treated with insecticides against S. titanus three times a year. All nurseries have to be treated throughout the time when larval stages or adults of S. titanus are likely to occur. Directives from the local authorities regulate the mandatory control of flavescence dorée and its vector for particular areas where flavescence dorée is present. They also regulate the obligate control of S. titanus by insecticides and the measures to be taken in order to reduce inoculum.
Prophylactic measures include the destruction of infected vines to remove sources of flavescence dorée phytoplasma, destruction of abandoned vineyards and wild Vitis plants, which serve as sources of inoculum and breeding hosts for the vector. These measures, as well as the obligate uprooting of all plants in vineyards when the disease incidence is excessive, are subject to prefectorial directives in France.
Although removal of infected stocks is useful to reduce the inoculum of flavescence dorée, pruning of diseased wood of flavescence dorée-infected grapes is not advisable. In contrast, this kind of pruning as well as cutting of the trunk and rebuilding the stock can be dangerous for vineyards. Pruning can mask the infection while the vines are still sources of inoculum, since they are infected systemically by flavescence dorée phytoplasma. The frequency of obvious symptoms of flavescence dorée may be decreased but the epidemic spread, nevertheless, goes on.
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. Pruning wood that carries the eggs of S. titanus should be burned. The number of viable eggs can be reduced by a treatment of wood in March before bud-burst. A wide range of insecticides, mainly organophosphates and pyrethroids, are available for summer treatments, which are usually carried out three times. The first treatment is usually in June and should not be done later than one month after the beginning of hatching: the delay is the period of time necessary for the first insects to become infective if they could feed on infected vines soon after hatching. The time of the second treatment depends on the stability of the compound used, but it is usually applied in combination with the control of the second generation of grape berry moth. Adult leafhoppers immigrating into the vineyards from surrounding areas are the target of a third treatment in August.
For further information see Caudwell (1965), Caudwell et al. (1971, 1974), Boudon-Padieu and Maixner (1998) and Anon. (1999).
ReferencesTop of page
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