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Plum Pox Potyvirus

On October 20, 1999, the U.S. Department of Agriculture and Pennsylvania Department of Agriculture announced the discovery of the D-strain of plum pox virus on peaches grown in an orchard in Adams County, Pennsylvania. This is the first North American report of PPV. This facts sheet has been prepared to provide preliminary background information on the virus, its hosts and its importance worldwide.

IDENTITY

Name: Plum Pox Potyvirus
Taxonomic position: Viruses: Potyvirus
Common names:PPV (acronym), Sharka, Plum pox, Variole du prunier

Various strains of PPV have been recognized. Originally described as necrotic, intermediate and yellow on the basis of symptoms obtained by inoculation into herbaceous plants, these variations can now be distinguished serologically. The D (Dideron) strain was originally characterized on apricot in France (Kerlan & Dunez, 1979) and the M (Markus) type on peach in Greece (Dunez, 1979). These two have now been determined to be the two major types known, on the basis of various modern techniques (Bousalem et al., 1994), but other types have also been characterized. These include the SP strain which is aggressive on peach and described from France (Adamolle et al., 1994) and the El Amar strain from Egypt (Wetzel et al., 1991). A new strain, PVP-C, which differs from other strains in both serological and biological properties, has been described on cherry (Nemchinov et al., 1996).

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PHOTOS

Plum pox symptoms on peaches (photo courtesy of J. McDonald, CPQP, Nepean, ON)

Plum pox symptoms on plum leaves (photo courtesy of J. McDonald, CPQP, Nepean, ON)

Foliar symptoms of PPV-infected Siberian C peach seedlings; healthy leaf on left (photo provided by D. Thompson, Centre for Plant Health, Sidney, BC)

More photos

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HOST RANGE

Plum pox virus infects virtually all cultivated fruit tree species of the genus Prunus. Severe symptoms are observed on apricot, plum, and peach trees. Almond trees may be infected occasionally but show few symptoms. Sweet and sour cherries have only recently been confirmed to be natural hosts also.

The virus also infects some wild Prunus species, especially P. spinosa which is an important natural source of infection in many countries.

Host ranges for different plum pox strains can be variable. For example, Jordovic (1985) demonstrated that a peach isolate of the virus infected all plum and peach cultivars except 'Sunhigh' peach, while plum isolates infected plum cultivars and indicators, but not peach. Natural plum pox virus infection on peach could not be found in Bulgaria or, until recently, in Yugoslavia. The plum pox virus-infected peach trees at the northern border of Yugoslavia originated in Hungary, and the strains isolated from them differ from the local Yugoslavian plum strains (Nemeth, 1986).

Natural hosts include: Prunus armeniaca, P. cerasifera, P. domestica, P. glandulosa, P. instititia, P. persica, P. salicina and P. spinosa (Nemeth, 1986). Hosts by artificial inoculation include: Prunus amygdalo-persica, P. amygdalus, P. besseyi, P. blireana, P. brigantia, P. cerasifera var. divaricata, P. cerasifera var. myrobalana, P. cistena, P. coccomilia, P. curdica, P. dasycarpa, P. davidiana, P. dulcis, P. holosericea, P. hortulana, P. japonica, P. juxa, P. kurdina, P. laurocerasus, P. mahaleb, P. mandschurica, P. mariana, P. maritima, P. microcarpa, P. ume, P. munsoniana, P. nigra, P. pissardii, P. pseudoarmeniaca, P. pumila, P. siberica, P. simonii, P. tomentosa and P. triloba.

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GEOGRAPHIC DISTRIBUTION

Africa: Egypt

Asia: Azerbaijan (unconfirmed), Cyprus, Georgia (unconfirmed), India, Syria, Turkey

Europe: Albania, Austria, Belgium, Bosnia & Herzegovina, Bulgaria, Croatia, Czech Republic, Denmark, Estonia, France, Germany, Greece, Hungary, Italy, Lithuania, Luxembourg, Moldova, Netherlands, Norway, Poland, Portugal, Romania, Russia, Slovakia, Slovenia, Spain, Sweden (not established), Switzerland, Ukraine, United Kingdom, former USSR, and Yugoslavia.

Although reported in practically all European countries, the level to which plum pox occurs there is highly variable (Smith et al., 1997). In the central and eastern European countries, PPV spread relatively early and levels of infection are generally high. In the Mediterranean countries, PPV is a more recent event and further spread is possible. In the northern and western countries, levels of PPV are very uneven and outbreaks are sporadic and usually localized, although it is fairly widespread in some areas. Further details are available in the Plum Pox PRA (MacLatchy, 1992) or in Smith et al. (1997).

North America: Canada (Ontario, Niagara Region - under eradication) United States (Present, first found in Pennsylvania (1999) and on a few trees in New York State and Michigan (2006), under eradication.)

South America: Chile (first reported1992)

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BIOLOGY

The main source of inoculum is infected trees. From these, PPV is transmitted either by grafting or by aphids in a non-persistent, stylet- borne manner to uninfected hosts (Smith et al., 1997). Efficiency of transmission is dependent on the virus strain and host cultivar. Aphis spiraecola and Myzus persicae are considered to be the most efficient vectors, but other occasional vectors include the following species, all aphids: Aphis craccivora, Brachycaudus cardui, Brachycaudus helichrysi, Hyalopterus pruni, Myzus varians, Phorodon humuli (EPPO, 1981; Leclant, 1973; Minoiu, 1973).

The virus can survive in the roots of rogued infected trees and can also spread by natural root grafting. The suckers produced from the remaining roots of rogued infected trees often carry the virus and as a consequence must be removed if control is to be achieved.

The proximity of orchards in relation to sources of infection is an important factor in within orchard spread. Jordovic (1980) indicates that between 1956 and 1975 only 2.62% of the plum trees in a particular orchard became infected with plum pox virus, compared to 76.25% of trees in another orchard in the same locality. The difference was the orchard with the lower spread was insulated from a virus source (an older infected orchard) by a forest. In addition, aphids appear to spread the virus, not to immediately adjacent trees, but to trees several spaces away (Gottwald et al., 1995). The number of trees becoming infected in any particular year is directly related to the number of aphids present that season (Smith et al., 1997).

Systemic spread of the virus within a tree may take several years, and in the meantime the virus may be distributed very irregularly within the tree (Smith et al., 1997).

Seed transmission has been demonstrated experimentally (Nemeth & Kolber, 1983), but is not known to occur in practice (Smith et al., 1997). Nemeth and Kolber (1983) provide evidence of seed transmission of PPV in apricot, peach and plum. According to Coman & Cociu (1976) the seed transmission rates for plum pox virus were 13.9% and pollen transmission ranged from 20-80%. In tests on several plum varieties, however, the virus could not be transmitted by seed (Jordovic, 1982). Nemeth (1986) summarizes various research on seed and pollen transmission studies and confirms seed and pollen transmission does occur but will vary depending on the host.

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DETECTION AND IDENTIFICATION

Symptoms:
Symptoms may appear on leaves or fruits of infected trees, and are particularly evident on leaves in spring when chlorotic spots, bands or rings, vein clearing and even leaf deformation is evident (Smith et al., 1997). Infected fruits show chlorotic spots or rings, and diseased plums and apricots are deformed with internal browning of the flesh and pale rings or spots on the stones. Symptoms, however, are highly variable. See photos.

Morphology:
Plum pox potyvirus is a filamentous virus with particles 750 nm long and 15 nm in diameter. It has single-stranded RNA with a molecular weight of 3.5 x 106 Da. Pinwheel protein inclusions are present in the cytoplasm of infected leaves and fruit.

Detection and inspection methods:
Visual inspection of trees, especially during the period of active growth, allows detection of PPV on the basis of symptoms. Testing on susceptible indicators by use of chip-buds, or mechanical inoculation of herbaceous indicators provides distinctive symptoms within 6 - 8 weeks but is limited by the potential for uneven distribution of the virus within the host tree.

Great progress, however, has been made in the development of detection techniques for PPV. The ELISA test is widely used to confirm or quantify the presence of the virus even at very low levels in roots, bark, flowers, leaves, fruits or seeds (Adams, 1978; Himmler et al., 1987). Methods based on electron microscopy (Kerlan et al., 1981) and colloidal gold staining (Himmler et al., 1988) have been developed. Monoclonal antibodies can now be used very effectively and are able to distinguish different strains (M and D types) (Cambra et al., 1994). Molecular hybridization tests, dot-blot molecular tests using radioactive DNA or RNA probes, enzymatic amplification of the DNA sequence by PCR, immunocapture-PCR techniques and others have been developed assuring a rapid and accurate determination of plum pox virus when present.

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MEANS OF MOVEMENT AND DISPERSAL

Long distance spread of sharka virus is through the movement and use of infected propagative materials (grafting and budding of infected material or seed) (Oosten, 1973; Nemeth, 1986). Even imported cut flowers of infected hosts can even act as a pathway for the virus, since domestic aphids could acquire the virus from the flowers and spread the virus to nearby fruit trees or weeds (Chang, 1987).

Nemeth and Kolber (1983) provide evidence of seed transmission of PPV in apricot, peach and plum. According to Coman & Cociu (1976) the seed transmission rates for plum pox virus were 13.9% and pollen transmission ranged from 20-80%. In tests on several plum varieties, however, the virus could not be transmitted by seed (Jordovic, 1982). Nemeth (1986) summarizes various research on seed and pollen transmission studies and confirms seed and pollen transmission does occur but will vary depending on the host.

Local spread occurs by means of insect-transmission between trees or local orchards, or root-grafting between neighbouring trees (see discussion on Biology).

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PEST SIGNIFICANCE

Economic impact:
Plum pox is generally considered one of the most serious diseases of plums, apricots and peaches and is of great economic importance in many European countries (eg. Austria, Germany, Hungary, Poland, Romania, Turkey, USSR, Yugoslavia) and causes some economic loss in others (eg. Greece, Switzerland, United Kingdom). Fruit quality, size and quantity are adversely affected, necessitating removal of infected trees (EPPO, 1981). Yield losses and overall economic losses have been catastrophic to plum and peach growers in large geographic areas of the affected countries. In these areas all affected trees have been removed by the growers and replaced with resistant varieties or with other crops (Agrios, 1990).

Much of the affected fruit drops prematurely, 20-30 days before the normal maturity date, and that fruit that does remain on the tree lacks flavour and is low in sugar content (Agrios, 1990). The virus so severely affects the fruit of diseased plum trees that the fruit becomes unsuitable for direct consumption or industrial processing (dried fruit, jam, brandy) (Nemeth, 1986).

In Bulgaria, in susceptible varieties (eg. cultivar 'Pocegaca'), 80 to 100% of the fruit falls prematurely and is unmarketable as a result of infection. Losses in 1968 were estimated to be 30,000 tonnes (EPPO, 1981). In some years losses were as high as 60,000 tonnes counted in fresh weight (Nemeth, 1986). In Poland, plum pox virus reduces the yield of the Common Prune variety of plum by greater than 50% as a result of premature fruit drop and reduced fruit size. In Czechoslovakia the average fruit yield dropped as much as 83.4% (Blattny & Heger, 1965). The disease also lowers fruit quality due to decreased acidity and unattractive appearance (Zawadzka & Millikan, 1971). In many countries, infected fruit is unsaleable as table fruit or can no longer be exported (Dunez, 1987).

Control:
Plum pox has proven to be a very difficult disease to control in Europe. Once introduced the virus can potentially spread and become quickly entrenched in the native vegetation. Control of the virus is primarily through surveys and removal of infected trees. There is no anti-virus treatment that can be applied to infected trees or orchards.

The use of disease-free propagative material at all times is fundamental to preventing introduction to new areas.

Measures to reduce the importance of plum pox in areas where it is present include the use of disease-free planting stock when planting new orchards or replenishing existing ones, removal of infected trees (including their roots), use of tolerant or less susceptible species or cultivars where possible, proper spacing of trees to reduce the rate of spread, chemical control of aphids to slow spread and weed control (including wild Prunus species) to eliminate reservoirs of infection. Breeding for resistance shows promise as a future strategy.

Phytosanitary risk:
Plum pox virus is a quarantine pest for many countries. In the EPPO region it presents a serious threat to many areas where it is not widely present and it is regulated specifically by many member countries. It is also a quarantine pest for the InterAfrican Phytosanitary Council and the North American Plant Protection Organization. In addition to the EU member countries where PPV is a quarantine pest, the virus is also a regulated pest for Australia and the United States.

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REFERENCES

Adamolle, C., M. Boeglin, G. Labonne, T. Candresse and J.B. Quiot, 1994. Une souche necrogene du plum pox potyvirus provoque un dépérissement sur certains cultivars de pêcher. Bulletin OEPP/EPPO Bulletin 24: 721 - 730.

Adams, A.N. (1978). The detection of plum pox virus in Prunus species by enzyme-linked immunosorbent assay (ELISA). Annals of Applied Biology 90:215-221.

Agrios, G.N. (1990). Economic Considerations. I.N. Mandahar (1990): pp. 1-22.

Blattny, C. and M. Heger (1965). Some remarks to the economic importance of sharka disease in Czechoslovakia. Zast. Bilja 16(85-88):417-418. I.N. Nemeth, 1986.

Bousalem, M., T. Candresse, L. Quiot-Douine and J.B. Quiot (1994). Correlation entre trois techniques permettant de différencier les isolats du plum pox potyvirus. Bulletin OEPP/EPPO Bulletin 24: 651 - 656.

Cambra, M., M. Asensio, M.T. Gorris, E. Perez, E. Camarassa, J.A. Garcia, J.J. Moya, A. Lopez-Abella, C. Vela and A. Sanz (1994). Detection of plum pox potyvirus using monoclonal antibodies to structural and and non-structural proteins. Bulletin OEPP/EPPO Bulletin 24: 569 - 577.

Chang, W.L. (1987). Pests not known to occur in the United States or of limited distribution No. 88: Plum Pox Virus. USDA-APHIS-PPQ Publication 81-50. 15 pp.

EPPO (1981). Plum Pox virus. Data Sheets on Quarantine Organisms. Sept., 1981. 7 pp. IN EPPO Bulletin (1983) Vol. 13 (No. 1):

Gottwald, T.R., L. Avinent, G. Llacer, A. Hermosos de Mendoza and M. Cambra (1995). Analysis of the spatial spread of sharka (plum pox virus) in apricot and peach orchards in eastern Spain. Plant Disease 79: 266 - 278.

Himmler, G., U. Brix, M. Laimer, D. Mattanovich and H.W.D. Katinger (1988). Goldlabelled-Immunosorbent-Electronmicroscopy with Plum Pox Virus Specific Monoclonal Antibodies. Acta Horticulturae 235:133-134.

Jordovic, M. (1980). An unusual spread of sharka virus. Acta Phytopathologica Acad. Scient. Hung. 15:227-229. IN Review of Plant Pathology 61 (No. 1809):152. (also in Acta Horticulturae (1981) Vol. 94:227-229.

Jordovic, M. (1982). Practical aspects of investigations of plum pox virus. Zastita-Bilja 33 (No. 4):445-458. IN Review of Plant Pathology 1984 Vol. 63 (No. 732).

Jordovic, M. (1985). Contribution to the study of sharka of plum and peach. Zastita-Bilja 36(No. 2):155-159. IN Review of Plant Pathology 1986 Vol. 65 (No.803).

Kerlan, C. and J. Dunez (1979). Differenciation biologique et sérologique des souches du virus de la sharka. Annales de Phytophathologies 11: 241 - 250.

Kerlan, C., B. Mille and J. Dunez (1981). Immunosorbent Electron Microscopy for Detecting Apple Chlorotic Leafspot and Plum Pox Viruses. Phytopathology 71:400-404.

Leclant, F. (1973). [Ecological aspects of the transmission of sharka disease (plum pox) in South-East France. Demonstrations of new aphid vectors.] Annales de Phytopathologie 5 (No. 4):431-439.

Mandahar, C.L. (1990). Plant Viruses Vol. II, Pathology. CRC Press, Boca Raton. 371 pp.

Minoiu, N. (1973). [The vectors transmitting plum pox virus (Prunus virus 7 Christ.) to plum]. Analele Institutului de Cercetari pentru Protectia Plantelor (1971, publ. 1973) Vol. 9:49-56. IN Review of Plant Pathology 53 (No. 3555):715.

Nemchinov, L., A. Hadidi, E. Maiss, M. Cambra, T. Candresse and V. Damsteegt (1996). Sour cherry strain of plum pox potyvirus (PPV): Molecular and serological evidence for a new subgroup of PPV strains. Phytopathology 86: 1215 - 1221.

Nemeth, M.V. (1986). Virus, mycoplasma and rickettsia diseases of fruit trees - Plum pox (Sharka). Boston: Martinus Nijhoff Publishers, pp. 463-479.

Nemeth, M.V. and M. Kolber (1983). Additional evidence on seed transmission of plum pox virus in apricot, peach and plum proved by ELISA. Acta Horticulturae 130:293-300.

Oosten, H.J. van (1973). Diagnosis of sharka (plum pox) and host range of its inciting virus. Agricultural Research Reports 796. Centre for Agricultural Publishing and Documentation. Wageningen, The Netherlands. 19 pp.

Smith, I.M., D.G. McNamara, P.R. Scott and M. Holderness, editors, 1997. Quarantine Pests for Europe. Second Edition. CAB International, Wallingford, UK. Plum Pox Potyvirus. Pp. 1287 - 1293.

Wetzel, T., T. Candresse, M. Ravelonandro, R.P. Delbos, H. Hazyad, A.E. Aboul-Ata and J. Dunez, 1991. Nucleotide sequence of the 3'-terminal region of the RNA of the El Amar strain of plum pox potyvirus. Journal of General Virology 72: 1741 - 1746.

Zawadzka, B. and D.F. Millikan (1971). Symptomology and some biological effects of the sharka disease on Common Prune in Poland. Phytoprotection 52 (No. 2):68-72. IN Review of Plant Pathology (1972) Vol. 51 (No. 1641):281.