Plum Pox Virus (PPV) on Ornamentals

Plum pox is a serious disease of Prunus species caused by a virus. This disease, also known as Sharka, was first reported occurring in plums in Bulgaria in 1915 and spread rather slowly northward through eastern Europe reaching the former Yugoslavia in 1935 and Hungary about 1941. After about 1950 the disease spread more rapidly reaching Germany in 1956, Poland and Russia in 1961, and France in 1970. The disease appeared in England in 1965, but was quickly eradicated successfully. However, from about 1970 onward the disease reappeared in English nurseries in imported rootstocks and now occurs throughout England. Spain was the most recent Western European country to be invaded by plum pox in 1984. Throughout Europe plum pox is considered the most devastating disease of stone fruits and it has been estimated that over 100 million European trees are infected. Unfortunately for the nursery industry, PPV can also infect many ornamental Prunus species. In 1992, plum pox symptoms were first detected in the western hemisphere in Chile. In October 1999, PPV (D-strain; see strain information below.) was positively identified for the first time in North America in peaches growing in Latimore and Huntington townships, Adams County, PA. Because of the serious threat PPV poses to fruit production, all susceptible species including ornamentals will be subject to quarantines, stop-sales, and shipping restrictions imposed by domestic and foreign government agencies.

The following summarizes information from the scientific literature on PPV with the intention of informing the general reader about what PPV is, the symptoms it causes, how it spreads, and about control strategies.

Host Range

Plant viruses are named according to the plant host in which they are first identified, hence the name plum pox virus or PPV. The name, however, does not indicate its complete plant host range. PPV infects not only plums but also peach, nectarines, apricot, almond, cherry, and wild Prunus species. Under laboratory conditions, scientists have also been able to infect a very large number of wild native and introduced weed species including lamb's quarter (Chenopodium sp.), shepherds purse (Capsella bursa-pastoris), ground cherry (Physalis sp.), buttercup (Ranunculus sp.), red and white clovers (Trifolium sp.), and sweet clovers (Melilotus sp.). Common garden hosts include tomato, peas, petunias, and zinnias. It is not known what role many of these plants play in PPV survival and spread because most of these studies used entirely artificial methods in order to obtain infection. However, the possibility of weeds acting as survival hosts for the virus exists and needs to be examined.

The following plants have been reported, by European scientists, as susceptible to the D-strain (see strain information below):

• Damson plum (Prunus insititia; syn. Prunus domestica)
• Blackthorn, Sloe (Prunus spinosa)
• Japanese plum (Prunus salicina)
• Flowering almond (Prunus glandulosa and Prunus triloba)
• Japanese flowering cherry (Prunus serrulata)
• Black cherry (Prunus serotina)
• Mahaleb, St. Lucie cherry (Prunus mahaleb)

Many other species of Prunus are grown or are found wild in Pennsylvania. The susceptibility of these species to PPV is currently being tested at the USDA high security quarantine greenhouses at Fort Detrick, Maryland.

Symptoms

Symptoms vary considerably with the host plant species, cultivar, age and nutrient status of the plant, and environmental conditions. In addition, different strains of PPV may cause different degrees of disease severity. Unfortunately, many trees fail to show symptoms for the first few years following the initial infection of the tree. The lack of symptoms cannot be relied upon as proof that a plant does not have the disease. When symptoms do occur, however, they are frequently very diagnostic and easily recognized.

Diagnostic leaf symptoms:

• mild light green discoloration bordering the leaf veins (vein yellowing)
• chlorotic light green or yellowed rings.

These symptoms may be barely visible to the eye or obvious depending on factors described above.

Diagnostic fruit symptoms on peach and apricot:

• lightly pigmented chlorotic rings or line patterns
• deformed fruit
• necrotic or dead areas on fruit
• the internal stone may have white to yellow colored rings on its surface

Diagnostic symptoms on plums:

• infected fruits drop prematurely
• fruits develop darker rings or spots on the skin
• fruits are severely deformed
• reddish discoloration of the flesh

Characteristics and Mechanisms for Spread

Plum pox virus is considered a virus species in the genus Potyvirus in the family Potyviridae. Some well-known relatives of PPV are potato virus Y, bean common mosaic virus, maize dwarf mosaic virus, and watermelon mosaic virus. These are transmitted by aphids. Plum pox virus is known to occur in different forms or strains (PPV-D, PPV-M, PPV-C, and PPV-EA). The most common European strains are PPV-D and PPV-M. The strain found in Pennsylvania, PPV-D, is not readily seed transmitted and seems to be more slowly spread by aphids in Europe compared to PPV-M

Short-distance spread within orchards and nurseries:

In natural settings such as orchards, PPV is spread only by aphids. About 12-15 species of aphids reported to transmit PPV occur in the fruit growing region of southeastern Pennsylvania. One of the most efficient vectors, the green peach aphid (Myzus persicae) colonizes peaches and other stone fruits in Pennsylvania. Therefore, the potential exists for aphid spread of PPV in Pennsylvania.

The mechanism by which aphids transmit PPV is called nonpersistent transmission. Once the aphid probes into an infected plant and acquires the virus, the virus can only be transmitted by the aphid for a short time (minutes). Aphids make two kinds of probes on leaf surfaces, test probes and feeding probes. To determine whether the plant is a good food source, the aphid will make a test probe for only a few seconds (Feeding probes may last for hours.). Immediately following a short test probe the aphid may withdraw the stylet, fly to another plant, and test probe that plant. Rapid transmission of nonpersistently transmitted potyviruses, including PPV, occurs during aphid test probes and not during the longer feeding probes. Aphids feeding on an infected cell can transmit that virus only to the next cell they feed on. The aphid cannot feed a single time on an infected plant and then transmit virus to several other healthy plants. Each aphid must feed directly on an infected plant, acquire sufficient virus, and then fly immediately to the next plant in order to effect a transmission. Because of this, aphids are thought to spread PPV from leaf to leaf or branch to branch while test probing a single tree resulting in multiple infection sites on one tree.

Long-distance spread:

Long distance spread of PPV is by movement of infected plants or plant parts by humans. Movement of infected nursery stock, seedlings, root stocks, or budding material are all implicated. Buds taken from infected trees will carry the virus and transfer the virus when grafted to healthy trees. Although long distance spread by flying aphids is possible, it is thought to be unlikely because aphids lose nonpersistently transmitted viruses when they probe on any non-Prunus species; and other potyviruses, like PPV, become noninfectious in the aphid usually within an hour after acquisition.

Control

Strategies for controlling PPV in Pennsylvania, listed in the order in which they should be implemented at this time, focus on (1) preventing the movement of PPV from its apparently limited location in Pennsylvania to new areas and (2) detecting and destroying infected plants in order to eliminate the virus from North America.

Exclusion

APHIS (Animal and Plant Health Inspection Service of the USDA) is responsible for testing all imported nursery stock for a range of pathogens and especially for those which are not known to occur in the United States. Only pathogen-free material is released for commercial use. The occurrence of PPV in Pennsylvania highlights the importance of testing imported nursery materials and not bringing plant material into the U.S. without having it first tested.

If the disease is localized to a small area, it may be contained by quarantines preventing movement of infected plants out of that area. Such a quarantine was implemented October 21, 1999, for Huntington and Latimore townships in Adams County, Pennsylvania, by the Pennsylvania Department of Agriculture. If the quarantine was implemented before movement of infected materials occurred, it will be effective in preventing spread of PPV. To determine exactly where the virus in located, an intense survey of trees is being done.

Virus testing of Prunus nursery stock is necessary to prevent the long range spread of PPV.

Eradication

Eliminating virus infected materials as quickly as possible, before it spreads, is the objective. Virus diseased trees cannot be cured and the virus cannot be eliminated from individual trees. Therefore, it is necessary to destroy PPV-infected trees once identified because an infected tree will serve as a virus source for all surrounding susceptible species. Because PPV does not induce easily recognized symptoms for the first few years of infection, serological tests, such as enzyme-linked immuosorbent assay (ELISA), or even more sensitive tests involving nucleic acid probes for specific viral RNA sequences must be employed. Tissue from trees to be tested can be collected by growers or scouts. PPV is generally not evenly distributed throughout the tree. Some branches, leaves, flowers, or fruits of infected trees may contain detectable levels of virus while other parts of the same tree appear uninfected. Therefore when sampling individual trees for serological tests, several samples must be taken from each tree.

Once infected trees are identified, they must be destroyed. PPV can survive in all living parts of infected trees, even infected roots. Sucker shoots developing from infected root stocks are good sources of PPV. Therefore, once infected trees are removed it is important to kill shoots that emerge from infected roots left in the ground. Once trees are removed, they should be destroyed promptly so that aphids on them do not have the opportunity to move to neighboring trees.

Protection

Although, insecticides can reducing total aphid populations on trees, insecticides do not completely protect trees from aphid inoculation with PPV because it may only take one or a few aphids to test probe and inoculate a tree.

Because aphids tend to lose the virus if they test probe a non-host plant, decreased infection rates may occur when susceptible plants are surrounded by a barrier crop of a non-host species in which the virus does not multiply. In theory, Prunus species surrounded by several rows of a non-Prunus species might be protected from aphid spread from an adjacent wild or ornamental Prunus species

Testing for the Virus

Sampling and testing should be done so that infected trees can be found and destroyed before they serve as a source of PPV for other trees. If a nursery specializes in or relies on the sale of Prunus species as an important part of business, it is suggested that 4-5 cuttings be taken during the winter as soon as it is possible to force growth from them. It is thought that 90 days of chilling in the field is sufficient dormancy, following which, it is possible to force growth (Dr. C. Heuser, Dept. of Hort., pers. comm.). Force bud break and send the samples in for testing. If sampling is done during the growing season, four to five twigs and attached leaves should be removed from a tree and placed together in a plastic bag with a DRY paper towel. DO NOT ADD WATER TO THE SAMPLES. Use a separate bag for samples from each tree. Assign a label or code to each tree sampled. Keep a list of that information for later reference. Label the bags carefully so that when you receive the results, you will know exactly which result goes with each tree. While collecting samples, place them in a cooler, out of the sun. It is best to put some ice in the bottom of the cooler. Send the samples to the testing laboratory the fastest way possible.

Tree samples are being tested for PPV by Dr. Ruth Welliver, Pennsylvania Department of Agriculture, Bureau of Plant Industry, 2301 N. Cameron St., Harrisburg, PA 17110-9408 (717-787-4843). It is best to call the lab before sending samples so that they know samples are coming and also to obtain any additional guidelines for collecting and shipping samples.

Further information, including photos of PPV symptoms, can be found at the following Web sites:

http://www.cas.psu.edu/docs/issues/plumpox/

http://www.state.pa.us/PA_Exec/Agriculture/plum_pox/pda_press_release.html

References

Brunt, A. A., Crabtree, K., Dallwitz, M. J., Gibbs, A. J., Watson, L. and Zurcher, E. J. (eds.) 1999. "Plum pox potyvirus." In Plant viruses online: Descritpions and lists from the VIDE database. Version: 16 January, 1997. URLhttp://biology.anu.edu.au/Groups/MES/vide/

Dallot,S, Labenne, G., Bueglin, M. Quiot-Douine, L., Quiot, J. B., and Candresse, T. 1998. "Peculiar plum pox potyvirus D-populations are epidemic in peach trees." Acta Hortic. 472: 355-365.

Gaborjanyi, R., and Basky, S. 1995. "Correlation between migration of aphid vectors and natural spread of plum pox virus." Acta Hortic. 386: 201-206.

Hartman, W. 1998. "Hypersensitivity: A possibility for breeding Sharka-resistant plum hybrids." Acta Hortic. 472:429-432.

Herrera, G., Sepulvida, P., and Madariaga, M. 1998. "Survey of sharka disease (plum pox virus) on stone fruit trees in Chile." Acta Hortic. 472:393-399.

Labonne, G., Yvon, M., Quiot, J.B., Avinent, L., and Llacer, G. 1995." Aphids as potential vectors of plum pox virus: comparison of methods of testing and epidemiological consequences." Acta Hortic. 386: 207-218.

Llacer, G., and Cambra, M. 1998 . "Thirteen years of Sharka disease in Valencia, Spain." Acta Hortic. 472: 379-384.

Ravelonandro, M. dunez, J., Labonne, G., Scorza, R. 1998. "Challenging transgenic plums expressing potyvirus coat protein genes with viruliferous aphids." Acta Hortic. 472: 413-420

Scorza, R., Callahan, A.M., Levy, L., Damsteegt, V., and Ravelonandro, M. 1998. "Transferring potyvirus coat protein genes through hybridization of transgenic plants to produce plum pox resistance in plums (Prunus domestica L.)." Acta Hortic. 472:421-428.

Shukla, D. D., Ward, C. W., and Brunt, A. A. 1994. The Potyviridae. CAB International, Wallingford, Oxon, U.K.

Verhoever, J. Th. J., Hass, A. M. de, and Roenhorst, J. W. 1998. "Outbreak and eradication of plum pox potyvirus in the Netherlands." Acta Hortic. 472: 407-409.

Walkey, D. 1991. Applied plant virology. 2nd edition. Pages 216-217, Chapman and Hall, London.