Phytoplasma prunorum (apricot chlorotic leafroll)
- Taxonomic Tree
- Notes on Taxonomy and Nomenclature
- Distribution Table
- Risk of Introduction
- Hosts/Species Affected
- Growth Stages
- List of Symptoms/Signs
- Biology and Ecology
- Means of Movement and Dispersal
- Plant Trade
- Vectors and Intermediate Hosts
- Detection and Inspection
- Prevention and Control
- Distribution Maps
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IdentityTop of page
Preferred Scientific Name
- Phytoplasma prunorum Seemüller & Schneider, 2004
Preferred Common Name
- apricot chlorotic leafroll
Other Scientific Names
- Apricot chlorotic leafroll phytoplasma
- Candidatus Phytoplasma prunorum
- European stone fruit yellows phytoplasma
- Phytoplasma prunorum [Candidatus] Seemüller & Schneider, 2004
International Common Names
- English: apricot dieback; cherry Molières disease; decline of Japanese plum; nectarine chlorotic leafroll; peach decline; peach rosette (Italian); peach vein clearing; peach vein enlargement; peach yellows (European); plum leptonecrosis
- Spanish: desarreglos vegetativos del albaricoquero; enrollamiento clorótico del albaricoquero
- French: dépérissement de Molières; enroulement chlorotique de l'abricotier
Local Common Names
- Germany: Chlorotisches Blattrollen (Steinobst)
- Italy: accartocciamento clorotico dell'albicocco
- PHYPPR (Phytoplasma prunorum)
Taxonomic TreeTop of page
- Domain: Bacteria
- Phylum: Firmicutes
- Class: Mollicutes
- Order: Acholeplasmatales
- Family: Acholeplasmataceae
- Genus: Phytoplasma
- Species: Phytoplasma prunorum
Notes on Taxonomy and NomenclatureTop of page Recently, Lorenz et al. (1994), Seemüller and Foster (1995) and Marcone et al. (1996) have concluded that several diseases of Prunus in Europe, described under different names (apricot chlorotic leafroll, cherry Moliéres disease, Japanese plum decline, nectarine chlorotic leaf roll, peach decline, peach rosette (as found in Italy, Marcone and Ragozzino, 1994), peach vein clearing, peach vein enlargement, peach yellows (European), plum leptonecrosis and other diseases affecting almond and flowering cherry (P. serrulata) are caused by one and the same phytoplasma (or genetically very similar phytoplasmas), for which the name European stone fruit yellows phytoplasma is proposed. Several strains differing in virulence, host specificity and the ability to induce off-season growth have been observed. European stone fruit yellows phytoplasma (ESFYP) is closely related to apple proliferation (EPPO/CABI, 1996a), pear decline (EPPO/CABI, 1996b) and a few other phytoplasmas of the apple proliferation group, but different from several European stone fruit-derived phytoplasmas maintained on periwinkle, and also different from peach X-disease phytoplasma which is a major pathogen in North America and absent from Europe (Ahrens et al., 1993, Lorenz et al., 1994, Seemüller et al., 1994). Certain authors maintain that different phytoplasma strains can be distinguished within ESFYP, for example, Gentit et al. (1998) found distinct symptoms on a common indicator (peach GF305) for apricot chlorotic leaf roll on the one hand and peach vein clearing and Japanese plum decline on the other (and also for the American phytoplasmas peach yellows and peach yellow leaf roll). Lee et al. (1995) found that phytoplasma strains associated with nectarine chlorotic leaf roll were members of the aster yellows group.
In 2004 it was proposed to accommodate phytoplasmas within the novel genus 'Candidatus (Ca.) Phytoplasma', and European stone fruit yellows as the species Candidatus Phytoplasma prunorum (Seemüller and Schneider, 2004).
DescriptionTop of page Németh (1986) described the morphological features of apricot chlorotic leafroll phytoplasmas as pleomorphic bodies. However, bacilliform particles were also found. Rod-shaped or spherical intravacuolar bodies can be found in young and lightly infested phloem cells. Bodies in old and heavily infested cells are compressed and degenerated (Németh, 1986).
DistributionTop of page Apart from an isolated unconfirmed report in South Africa (Németh, 1986), apricot chlorotic leaf roll is apparently present only in Europe (Morvan, 1977), in the following countries: France (throughout the areas of apricot cultivation), Germany, Greece (Rumbos and Bosabalidis, 1985), Italy, especially in Emilia-Romagna (Giunchedi et al., 1978; Ragozzino et al., 1983), Hungary (Seemüller and Foster, 1995), Romania (Ploaie, 1980), Spain (especially in Valencia province), Switzerland and Yugoslavia. Plum leptonecrosis seems to be present in all European countries where Japanese plum is grown. Diseases of peach caused by ESFYP have been observed in Campania, southern Italy (Marcone et al., 1996) and are probably present in other peach-growing areas in Europe. A disease called 'peach rosette' was described in the province of Salerno in Campania (Marcone and Ragozzino, 1994) and appears to be caused by ESFYP (and not by the North American pathogen called peach rosette phytoplasma which is absent from Europe and listed as an EPPO A1 quarantine pest). Cherry Moliéres disease was first observed in 1952 in south-western France (département Tarn-et-Garonne) affecting sweet cherry (P. avium) and plum (P. domestica). The disease remained limited to this area and seems to be rare at present.
It can be concluded that ESFYP occurs in all Mediterranean countries of Europe and as far north as Germany (Seemüller and Foster, 1995). EPPO used to consider apricot chlorotic leafroll phytoplasma as an A2 quarantine pest, on the basis of its limited distribution in Europe. However, the pest has been deleted from the EPPO A2 list since it was recognized that the pathogen causing the disease in apricot was the same (European stone fruit yellows phytoplasma) as that occurring much more widely on other Prunus in Europe.
Distribution TableTop of page
The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.
|Continent/Country/Region||Distribution||Last Reported||Origin||First Reported||Invasive||Reference||Notes|
|Azerbaijan||Present, few occurrences||CABI/EPPO, 2010; EPPO, 2014|
|Turkey||Restricted distribution||Serçe et al., 2006; CABI/EPPO, 2010; EPPO, 2014|
|South Africa||Absent, invalid record||EPPO, 2014|
|Tunisia||Restricted distribution||Ben et al., 2011; Khalifa and Fakhfakh, 2011; EPPO, 2014|
|Albania||Restricted distribution||CABI/EPPO, 2010; EPPO, 2014|
|Austria||Restricted distribution||CABI/EPPO, 2010; EPPO, 2014|
|Belarus||Present||Valasevich and Schneider, 2016|
|Belgium||Present, few occurrences||CABI/EPPO, 2010; EPPO, 2014|
|Bosnia-Hercegovina||Restricted distribution||CABI/EPPO, 2010; EPPO, 2014|
|Bulgaria||Restricted distribution||CABI/EPPO, 2010; EPPO, 2014|
|Croatia||Restricted distribution||EPPO, 2014|
|Cyprus||Absent, formerly present||CABI/EPPO, 2010; EPPO, 2014|
|Czech Republic||Restricted distribution||Navratil et al., 1998; CABI/EPPO, 2010; EPPO, 2014|
|France||Restricted distribution||Morvan, 1977; Audergon et al., 1991; CABI/EPPO, 2010; EPPO, 2014|
|-France (mainland)||Restricted distribution||CABI/EPPO, 2010|
|Germany||Restricted distribution||Seemüller & Foster, 1995; CABI/EPPO, 2010; EPPO, 2014|
|Greece||Restricted distribution||Rumbos and Bosabalidis, 1985; Syrgianidis, 1989; CABI/EPPO, 2010; EPPO, 2014|
|-Greece (mainland)||Restricted distribution||CABI/EPPO, 2010|
|Hungary||Restricted distribution||Seemüller & Foster, 1995; CABI/EPPO, 2010; EPPO, 2014|
|Italy||Restricted distribution||Poggi-Pollini et al., 1993; Giunchedi et al., 1978; Ragozzino et al., 1983; Marcone et al., 1996; CABI/EPPO, 2010; EPPO, 2014|
|-Italy (mainland)||Present||CABI/EPPO, 2010|
|Poland||Restricted distribution||CABI/EPPO, 2010; EPPO, 2014|
|Romania||Restricted distribution||Ploaie, 1980; CABI/EPPO, 2010; EPPO, 2014|
|Serbia||Present||EPPO/CABI, 1996c; CABI/EPPO, 2010; EPPO, 2014|
|Slovakia||Present, few occurrences||EPPO, 2014|
|Slovenia||Restricted distribution||CABI/EPPO, 2010; EPPO, 2014|
|Spain||Restricted distribution||Llacer and Medina, 1988; CABI/EPPO, 2010; EPPO, 2014|
|-Spain (mainland)||Present, few occurrences||CABI/EPPO, 2010|
|Switzerland||Restricted distribution||EPPO/CABI, 1996c; CABI/EPPO, 2010; EPPO, 2014|
|UK||Restricted distribution||EPPO, 2014|
|-England and Wales||Restricted distribution||EPPO, 2014|
|Ukraine||Absent, unreliable record||EPPO, 2014|
|Yugoslavia (Serbia and Montenegro)||Present|
Risk of IntroductionTop of page Though ESFYP is no longer considered to be a disease warranting quarantine regulations in Europe, it presents a substantial risk for other continents in which phytoplasmas of the apple proliferation group that attack stone fruit do not occur. Its importance would, however, depend on the presence of suitable vectors.
Hosts/Species AffectedTop of page The main hosts are apricots, peaches and Prunus salicina. Plums can be symptomless carriers of the disease (Németh, 1986). Most related Prunus species can be experimentally infected and some show severe symptoms. Weeds such as Convolvulus arvensis and Cynodon dactylon can be naturally infected (Németh, 1986).
Growth StagesTop of page Vegetative growing stage
SymptomsTop of page Symptoms
Symptoms caused by ESFYP are influenced by species, cultivar and undefined environmental factors. In general, they include premature bud-break, leaf vein enlargement, leaf coloration, phloem necrosis and off-season vegetative growth.
Disease symptoms can be detected throughout the year, since one effect is stimulation of new growth during winter dormancy. This, however, is blocked by frost. The best times for observing symptoms are before flowering and at the end of the summer. In spring, infected trees bear leaves before the flower buds open. If winter temperatures fall below -5°C, infected trees show browning of the middle layer of the bark, darker and thicker according to the severity of the winter. The cambium may be affected, but in spring the outer bark appears normal, remaining green if the suber layer is sufficiently thin. One to two months later, the exterior bark dries out. Leafroll symptoms develop through the summer, becoming most clearly visible at the end of September (except in cases of heavy rust attack). The lamina rolls up along lines running from the petiole to the tip, possibly touching the leaf margin at one or two points on the way, giving either a cone or a polygonal outline. Irregular interveinal chlorosis is also seen. Finally, there is a proliferation of rudimentary buds at the end of short shoots and a tendency for buds to open on old wood.
On Japanese plum
The symptoms on Prunus salicina are similar but less typical. Leaves are smaller and reddish, and show cylindrical rather than conical rolling. Defoliation is earlier than normal and often new growth is initiated between October and December. Diseased trees are in leaf during bloom and are easily distinguished from healthy trees that show only white flowers. Fewer flowers and fruits develop on diseased trees, fruits are smaller and ripen later than on healthy trees. Phloem necrosis can be seen after a winter frost. Tree decline is somewhat slower than in apricot. Diseased branches die within a few years and eventually the entire tree dies (Seemüller and Foster, 1995).
Symptoms vary according to the cultivar. In some white-fleshed cultivars, red foliage in summer or early autumn and a slight rolling or curling of leaves is observed. In some yellow-fleshed cultivars, symptoms resemble those of peach X-disease and peach yellow leaf roll phytoplasmas. In recent studies (Kison et al., 1997), it appears that different phytoplasmas might be involved in peach yellow leaf roll disease. In California, one form of the disease is caused by a strain of the X-disease phytoplasma. But it has also been found that other strains isolates from symptomatic peach trees in California are closely related to apple proliferation, pear decline and European stone fruit yellows phytoplasmas. The peach yellow leaf roll phytoplasma could be clearly distinguished from the apple proliferation phytoplasma and ESFYP (by RFLP of ribosomal DNA and Southern blot analysis), but not from the pear decline phytoplasma (by RFLP of ribosomal DNA). Leaves appear normal until mid-summer, then become slightly chlorotic or pale green and develop necrotic lesions in the leaf lamina. Later, these lesions abscise to give a 'shot-hole' appearance, and foliar yellowing becomes more pronounced. Simultaneously, leaf margins roll upward longitudinally, leaf tips curl downward, and leaves turn hard and brittle and fall prematurely. More specific symptoms include swollen midribs resulting from corky deposition and a yellow or red coloration of the enlarged lateral veins. Premature foliar bud-break and phloem discoloration have been observed. Vigour and productivity of infected tree are reduced, scaffold branches exhibit die-back and trees decline within a few years (Seemüller and Foster, 1995).
On other Prunus hosts
Symptoms on other Prunus hosts have been less extensively described. First symptoms of Moliéres disease on European plum and cherry are mildly chlorotic leaves in summer, which are not usually observed until trees reach 3-7 years of age. The following year, trees bloom abundantly, but flowers are often malformed and fruit set is poor. Fruits that develop have short peduncles, remain small and drop prematurely. Small deformed leaves, rosetting, poor lignification of young shoots, phloem and bark necrosis are evident at this stage of the disease. Affected trees decline and die. Symptoms on almond have hardly been described.
List of Symptoms/SignsTop of page
|Leaves / abnormal colours|
|Leaves / abnormal forms|
|Leaves / leaves rolled or folded|
|Stems / discoloration of bark|
|Stems / witches broom|
Biology and EcologyTop of page The disease, being graft-transmissible, was originally attributed to a virus. However, the yellows-type symptoms, the detection of mycoplasma-like bodies in sieve tubes, and the partial remission of symptoms by tetracycline treatments showed in the 1970s that the probable aetiological agent was a phytoplasma (Morvan et al., 1973). The pathogen has not yet been cultured in cell-free media. Transmission by an insect vector certainly occurs and is the major means of disease spread. The leafhopper, Fieberiella florii, was considered a putative vector of apricot chlorotic leafroll. In Spain, cicadellids were found to be more abundant in apricot orchards where chlorotic leaf roll was common (Llacer et al., 1986). Some preliminary studies have showed that in infected orchards of apricot and plum in Italy, ESFYP was detected in the cicadellids Anaceratagallia and Euscelis, but further transmission studies are needed (Poggi Pollini et al., 1997). In France, specific PCR detection has failed to identify any infected insects (Jarausch et al., 1999), despite extensive surveys (Labonne et al., 1998). However, Duval et al. (1999) report that the pear psylla Cacopsylla pruni carries ESFYP in Japanese plum orchards. C. pruni was used by Carraro et al. (1998) to experimentally transmit European stone fruit yellows to 89% of all inoculated Japanese plum cv. 'Ozark Premier'.
Means of Movement and DispersalTop of page
In infested areas, the main mode of transmission is probably by cicadellid vectors. The importance of herbaceous hosts as a reservoir for ESFYP remains to be assessed.
Movement in trade
Infected planting material (young plants, budwood, and especially vegetatively propagated rootstocks) is the main potential means of introduction over long distances into uninfested areas.
Plant TradeTop of page
|Plant parts liable to carry the pest in trade/transport||Pest stages||Borne internally||Borne externally||Visibility of pest or symptoms|
|Seedlings/Micropropagated plants||Yes||Pest or symptoms usually invisible|
|Stems (above ground)/Shoots/Trunks/Branches||Yes||Pest or symptoms usually invisible|
|Plant parts not known to carry the pest in trade/transport|
|Fruits (inc. pods)|
|Growing medium accompanying plants|
|True seeds (inc. grain)|
Vectors and Intermediate HostsTop of page
ImpactTop of page The diseases caused by ESFYP on apricot and Japanese plum are among the most important infectious disorders of these hosts and the predominant causes of decline and death of productive trees. Apricot trees are killed 12-24 months after first appearance of symptoms. This period may be reduced in duration to weeks if the rootstock source is peach. Spontaneous recovery is rare for apricot, but does occur more often with Prunus salicina. In France, ESFYP is probably responsible for 60-70% of cases of apricot decline. Serious problems begin to arise when trees first start bearing fruit after 5 years; 5% of trees may then be killed every successive year. In other countries where the ESFYP occurs, P. salicina seems to be more important as a host. In France, Moliéres disease at one time killed thousands of plum and cherry trees but seems to be rare at present.
Detection and InspectionTop of page Positive identification requires a graft-transmission test onto a woody indicator. A rapid test that may be tried is the use of DAPI reagent (4,6-diamidino-2-phenylindole) to detect fluorescence of phytoplasmas in the sieve-tubes of the leaf veins. Molecular techniques using dot blot, Southern hybridization analysis, PCR (Avinent and Llacer, 1995; Carraro et al., 1998), nested PCR (Waterworth and Mock, 1999) and RFLP (Bertaccini et al., 1997) are now available to detect and identify ESFYP. The distribution of the pathogen is uneven in infected trees and is influenced by host and time of the year. Therefore, thorough sampling and replication of tests are important. An EPPO standard on the detection of fruit tree phytoplasmas has been published (OEPP/EPPO, 1994).
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.The use of pathogen-tested propagation material is essential when planting new orchards. The EPPO certification schemes for Prunus (OEPP/EPPO, 2001) cover ESFYP and should give assurance that planting material is free from phytoplasmas. As the spread of the disease by insect vectors needs to be further investigated, the impact of insect control on the epidemiology of the disease is unknown. In France, long-term studies have been carried out on the use of cross-protection against apricot chlorotic leaf roll with good results (Castelain et al., 1997). There are prospects of breeding apricots for resistance (Audergon, 1997).
ReferencesTop of page
Ben Khalifa M; Aldaghi M; Hacheche H; Kummert J; Marrakchi M; Fakhfakh H, 2011. First report of 'Candidatus Phytoplasma prunorum' infecting apricots in Tunisia. Journal of Plant Pathology, 93(2):517-519. http://sipav.org/main/jpp/index.php/jpp/article/view/1212
Bertaccini A; Pastore M; Vibio M; Izzo PP; Genovese MR; Santonastaso M, 1997. Use of molecular methods for identification of phytoplasmas associated with apricot chlorotic leafroll in Italy. Italus Hortus, 4(2):76-77; 9 ref.
Castelain C; ChastelliFre MT; Jullian JP; Morvan G; Lemaire JM, 1997. La prTmunition contre l'enroulement chlorotique de l'abricotier - bilan de dix annTes d'observations sur huit vergers. Phytoma - La DTfense des VTgTtaux, no. 493:39-44.
Duval H; Jullian JP; Lemaire JM, 1999. Enroulement chlorotique de l'abricotier: Tvaluation de la sensibilitT des principales variTtTs de prunier japonais et du nouveau sur un vecteur. Phytoma, no. 516:38-40.
EPPO, 2014. PQR database. Paris, France: European and Mediterranean Plant Protection Organization. http://www.eppo.int/DATABASES/pqr/pqr.htm
EPPO/CABI, 1996c. Apricot chlorotic leaf roll phytoplasma. In: Quarantine pests for Europe. 2nd edn. Wallingford, UK: 963-966.
Gentit P; Cornaggia D; Desvignes JC, 1998. Identification and comparison of different Prunus phytoplasma diseases by indexing on GF305 peach seedlings in the greenhouse. Acta Horticulturae, No. 472:723-729; 9 ref.
Jarausch W; Danet JL; Broquaire JM; Saillard C; Garnier M; Dosba F, 1999. Apricot chlorotic leaf roll in Roussillon: specific detection of the pathogen, search for alternative host plants, attempts to determine infection periods and attempts to identify the insect vector. Acta Horticulturae, No. 488:739-744; 11 ref.
Kison H; Kirkpatrick BC; Seemnller E, 1997. Genetic comparison of the peach yellow leaf roll agent with European fruit tree phytoplasmas of the apple proliferation group. Plant Pathology, 46(4):538-544; 30 ref.
Lorenz KH; Dosba F; Poggi-Pollini C; Llacer G; Seemnller E, 1994. Phytoplasma diseases of Prunus species in Europe are caused by genetically similar organisms. Zeitschrift fur Pflanzenkrankheiten und Pflanzenschutz, 101(6):567-575
Marcone C; Ragozzino A; Seemnller E, 1996. European stone fruit yellows phytoplasma as the cause of peach vein enlargement and other yellows and decline diseases of stone fruits in southern Italy. Journal of Phytopathology, 144(11-12):559-564; 26 ref.
NTmeth M, 1986. Apricot chlorotic leaf roll. In: Virus, mycoplasma and rickettsia diseases of fruit trees. Budapest, Hungary: AkadTmiai Kiado, 626-633.
OEPP/EPPO, 1994. MLOs in fruit trees and grapevine. Quarantine procedures No. 57. Bulletin OEPP/EPPO Bulletin, 24:339-342.
OEPP/EPPO, 1999. EPPO Standards PM 1/2(8) EPPO A1 and A2 lists of quarantine pests. In: EPPO Standards PM 1, General Phytosanitary Measures. Paris, France: EPPO, 5-17.
OEPP/EPPO, 2001. EPPO Standards on production of healthy plants for planting PM 4/29 (cherry) and 4/30 (almond, apricot, peach and plum). Bulletin OEPP/EPPO Bulletin, 31 (in press).
Ploaie PG, 1980. Experimental evidence of the presence of mycoplasma (Mollicutes-mycoplasmatales) in apricot with decline symptoms and their role in apricot apoplexy. Analele Institutului de Cercetari pentru Protectia Plantelor, 16:29-34
Poggi Pollini C; Giunchedi L; Bussani R; Mordenti GL; Nicoli Aldini R; Cravedi P, 1997. Preliminary studies on the potential vectors of European stone fruit yellows phytoplasma. Bulletin OILB, 20(6):39-42.
Seemnller E; Foster JA, 1995. European stone fruit yellows. In: Ogawa JM, Zehr EI, Bird GW, Ritchie DF, Uriu K, Uyemoto JK, eds. Compendium of stone fruit diseases. St. Paul, MN, USA: American Phytopathological Society, 59-60.
Seemüller E; Schneider B, 2004. ’Candidatus Phytoplasma mali’, ’Candidatus Phytoplasma pyri’ and ’Candidatus Phytoplasma prunorum’, the causal agents of apple proliferation, pear decline and European stone fruit yellows, respectively. International Journal of Systematic and Evolutionary Microbiology, 54(4):1217-1266.
Seemüller E; Schneider B; Maürer R; Ahrens U; Daire X; Kison H; Lorenz KH; Firrao G; Avinent L; Sears BB; Stackebrandt E, 1994. Phylogenetic classification of phytopathogenic mollicutes by sequence analysis of 16S ribosomal DNA. International Journal of Systematic Bacteriology, 44(3):440-446
Serçe ÇU; Gazel M; Çaglayan K; Bas M; Son L, 2006. Phytoplasma diseases of fruit trees in germplasm and commercial orchards in Turkey. Journal of Plant Pathology, 88(2):179-185. http://www.agr.unipi.it/sipav/jpp/index.html
Smith IM; McNamara DG; Scott PR; Holderness M, 1997. Quarantine pests for Europe. Second Edition. Data sheets on quarantine pests for the European Union and for the European and Mediterranean Plant Protection Organization. Quarantine pests for Europe. Second Edition. Data sheets on quarantine pests for the European Union and for the European and Mediterranean Plant Protection Organization., Ed. 2:vii + 1425 pp.; many ref.
Valasevich N; Schneider B, 2016. Detection, identification and molecular diversity of 'Candidatus Phytoplasma prunorum' in Belarus. Journal of Plant Pathology, 98(3):625-629. http://www.sipav.org/main/jpp/index.php/jpp/article/view/3703/2358
Waterworth HE; Mock R, 1999. An assessment of nested PCR to detect phytoplasmas in imported dormant buds and internodal tissues of quarantined tree fruit germ plasm. Plant Disease, 83(11):1047-1050; 31 ref.
Distribution MapsTop of page
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