Plum Pox Virus: Stone Fruit's most feared plant pathogen

By Kimberley Thomas

Plum pox virus (PPV) is currently the most feared and devastating viral disease affecting stone fruit in the world. The disease was first observed in 1917 on plums growing in Bulgaria and is now widespread throughout Europe and is present in Turkey, Syria, Egypt, India, the United Kingdom, Africa, the former USSR, and parts of Asia, Canada and South America.

In 2019 the United States declared freedom from PPV following an extensive and costly 20-year battle against the disease and is the only country to have successfully eradicated the virus. PPV is not present in Australia (or New Zealand) and the disease’s entry and establishment here would pose considerable risk to Australia’s stone fruit industries.

The disease is caused by the PPV and has numerous strains which may infect various stone fruit species including almonds, apricots, nectarines, peaches, plums as well as sweet and sour cherries. Some strains of the virus may also infect ornamental and wild species of stone fruit. The movement of infected plant material such as budwood, rootstock and young plants is the main cause of long distance spread and introduction of PPV to new regions. Long distance dispersal (and the most likely means of entry into Australia) is through importation of infected propagating material. Once established in an area, the virus is spread locally within and to nearby orchards via aphid vectors including the green citrus aphid (Aphis spiraecola) and the green peach aphid (Myzus persicae), both of which are present and widespread in Australia.

A winged green peach aphid (Myzus persicae), an important vector of plum pox virus. Source: Scott Bauer, USDA Agricultural Research Service, Bugwood.org

PPV can cause significant economic losses with the impact associated with the disease’s management worldwide estimated to be over 10 billion euros (2006), (AU)$10.6 billion. The infection of host trees results in severely reduced fruit production and premature fruit drop. In addition, the fruit from infected trees is deformed or blemished and marked with rings or spots, rendering it unmarketable because of its unattractive appearance, low sugar content, poor flavour and decreased shelf life. The presence of plum pox can also enhance the effects of other endemic viruses infecting stone fruit, including Prune Dwarf Virus (PDV), Prunus Necrotic Ringspot Virus (PNRSV) and Apple Chlorotic Leafspot Virus (ACLSV), resulting in further losses. Additional losses occur with the management protocols for the disease, requiring the destruction of all infected trees, to prevent further spread of the virus.

Disease Description

Common name: Plum Pox Virus (PPV)
Scientific name: Plum pox virus (Potyvirus)
Synonyms: Sharka, Plum pox, Peach sharka, Pox disease of plum, Sharka disease of plum
Division: Virus
Family: Potyviridae
Genus: Potyvirus

PPV belongs to the family Potyviridae (potyvirus) and is a linear single stranded RNA virus with at least 8 different strains including: PPV-D, PPV-M, PPV-EA, PPV-C, PPV-Rec, PPV-W, PPV-T and PPV-CR. Within these strains, individual isolates can vary in the severity of symptoms they induce. The most common strain is D (Dideron) which was first isolated from apricots in France. It can also infect peaches, nectarines, and plums naturally and is well established in many European countries. The D strain is the only strain found in North America.

The EA (El Amar) strain was originally isolated from apricots in Egypt but can also infect plums, nectarines and peaches. It has only been found in North African countries. The C (Cherry) strain has only been isolated from sweet and sour cherries. The C strain is present in several European countries but has not been found in North America.

The M (Marcus) strain was first identified on peaches in Greece and is now found in many European countries but not in North America. It is usually found on peaches but has been isolated from naturally infected plums and apricots. PPV-M isolates are more aggressive in peach, are aphid vectored more efficiently, and spread more rapidly in an orchard. Once established in a region, the M strain spreads quickly and is extremely difficult to eliminate.

Host range

The main hosts of PPV are fruit producing species of the stone fruit (Prunus) genus:

Table 1. Major hosts of PPV
Almonds Prunus dulcis	Dwarf flowering almond Cherry almond Prunus glandulosa	Myrobalan plum Prunus cerasifera	Sweet cherry Prunus avium
Apricot Prunus armeniaca	Garden plum (prune) Prunus domestica	Nectarine Prunus persica var. nectarina	Sour cherry Prunus cerasus
Damson plum Prunus insititia	Japanese plum Prunus salicina	Peach - Prunus persica

*It is also thought that many other cultivated or weedy annual plant species can potentially carry PPV.

Symptoms

Plum pox disease symptoms are variable with a range of signs observed on leaves, flowers and fruit. The disease develops slowly over a period of several years, usually only affecting one or two branches before spreading throughout the entire tree as the virus replicates over time. Infected trees become less productive as the disease progresses. Tree death is rare but there is a measurable reduction in growth on severely infected trees and fruit may drop early.

Symptom expression can be erratic and may be confused with other disorders such as nutrient deficiencies or injury caused by pesticides. Expression of symptoms also varies depending on the host, the cultivar, the strain of plum pox, the age of the infected tree, the season and environmental conditions. Symptoms may appear in spring and early summer in some years but then fade or disappear during hot weather only to reappear when cooler weather commences. Plums and apricots tend to be more severely affected than peaches and nectarines.

Symptoms may be observed:

on leaves, flowers and fruit of all stonefruit and sometimes on the stones of apricots,
on only a few leaves or fruit, along one limb,
or throughout the entire tree.

Leaf symptoms

PPV induces multiple leaf symptoms on trees including pale chlorotic or yellow rings, spots and blotches, yellow line patterns along veins and vein clearing. The shape of the leaf may be distorted, and some cultivars have leaf spots that may appear as necrotic tissue. Alternatively, some host cultivars do not show obvious symptoms. For example, almond can be infected with PPV but expresses few, if any, symptoms.

Symptoms of plum pox on fruits and seed on apricot, showing brownish depressions and grooves on the surface.
Source: Ministry of Agriculture and Regional Development, Bugwood.org

Vein clearing symptoms on a peach leaf compared to healthy leaf. Source: Biologische Bundesanstalt für Land- und Forstwirtschaft, Bugwood.org

Fruit symptoms

Plum pox within an infected tree can be distributed unevenly resulting in some fruit on the same tree appearing asymptomatic (no symptoms) while other fruit appears severely diseased. Green fruit that is infected shows symptoms which may be observed as pale mottled yellow lines, patches and rings. Maturing fruit retains these markings which remain yellow and is surrounded by the normal blush colour of the fruit.

Infection impacts the quality of the fruit by affecting the fruit size, pigmentation and sugar content. Fruit flavour is modified resulting in tasteless, bitter fruit which is unsuitable for either the fresh market or processing and the shelf life of infected unmarked fruit is reduced.

Plum pox on plums

The plum leaves have pale green to yellow spots and blotches. Symptoms include green and yellow rings and blotches on young fruit. These symptoms fade as the fruit ripens but infected fruit drops from the tree prematurely. The plum fruit are often severely deformed with dark sunken rings. Sensitive plum varieties may also exhibit bark splitting.

Plum pox on peaches

Initial signs of the disease appear as yellowish zones along the veins of the newly expanding first leaves. This particular symptom is difficult to distinguish from other causes of yellowing along veins such as nutrient deficiency. Sometimes peach cultivars with showy flowers display colour breaking on the flower petals.

Plum pox symptoms with yellow rings on a yellow-fleshed peach cultivar. Source: European and Mediterranean Plant Protection Organization, Bugwood.org

Symptoms: yellow rings on a yellow-fleshed peach. Source: European & Mediterranean Plant Protection Organization, Bugwood.org

Plum pox symptoms on apricot fruit
Source: Biologische Bundesanstalt für Land- und Forstwirtschaft, Bugwood.org

Plum pox symptoms on plum leaves.
Source: Biologische Bundesanstalt für Land- und Forstwirtschaft, Bugwood.org

Infection on plum fruit showing dark sunken lesions. Source: Biologische Bundesanstalt für Land- und Forstwirtschaft, Bugwood.org

Colour breaking on the flower petals of a peach cultivar.
Courtesy: J.C. Desvignes, CTIFL (France).

Colour breaking on the flower petals of a peach cultivar. Source: J.C. Desvignes, CTIFL (France).

Diagnosis

Early detection and accurate diagnosis are required to successfully control PPV. Visual inspection of trees for symptoms is not a reliable method for detecting all infections. Infected trees may not show symptoms for up to 3 years after infection. Laboratory tests including Enzyme Linked Immuno-Sorbent Assay (ELISA) and Polymerase Chain Reaction (PCR) are needed to detect low concentrations of the virus in tissues from plants not expressing symptoms. Generally, these tests are conducted on leaf samples which should be taken from the previous year’s growth in different quadrants of the trees due to the uneven distribution of the virus in infected trees. Leaf samples for surveys should be taken at the start of the growing season when temperatures are moderate as the virus concentration can be reduced during prolonged periods of hot weather.

Prevention

Like all plant virus infections, prevention is best, as there is no cure for this disease. Stone fruit producing regions generally focus on preventing the introduction of PPV into a disease-free region. It is everyone’s responsibility to prevent the introduction of exotic pests including PPV into regions where the pest does not occur. As a grower, it is critical to source propagation and planting material from accredited suppliers. Propagating with virus-free budwood and graft-wood from mother trees that are regularly tested from certified production nurseries help prevent the introduction of PPV.

Also check your production nursery or orchard frequently for the presence of new pests and unusual disease symptoms. Ensure there is a crop monitoring procedure in place and that you are familiar with common pests and diseases so you can tell if you see something different. The BioSecure HACCP Guidelines has the appropriate crop monitoring procedure which can be accessed at APPS website and the Pest ID tool has been developed for industry to assist in identifying and managing pests, diseases and weeds. This resource is free and can be accessed at https://pestid.com.au

Quarantine

Many countries use quarantine as a method to exclude and prevent the introduction or spread of exotic diseases such as PPV into a disease-free region or nation. Quarantine zones may be used and placed around infected orchards or entire regions depending upon the distribution of the disease determined by detection surveys. Susceptible propagation material is prohibited from moving outside of the defined quarantine region, area or zone. Follow regulations regarding the importation and movement of propagative materials and commercial propagants.

In an effort to keep the disease from entering Australia, all imports of stone fruit planting material are screened, and virus tested in government quarantine facilities. Many stone fruit food products containing seeds require heat treatment to kill the seed and prevent the spread of the virus. Regulations and enforcement to prevent the introduction of exotic pests on plant material coming into Australia from other countries is the responsibility of the Department of Agriculture, Water and Environment. Details on the current import status of plant materials and can be obtained from the BICON website https://bicon.agriculture.gov.au/BiconWeb4.0

Eradication

If preventing the introduction of the disease into a disease-free region fails, the focus of the control strategy is the removal of the plant pathogen by eliminating all infected trees. However, once PPV becomes established in a region or in the wild native stone fruit population, it is very difficult and extremely costly to eliminate the virus. Eradication involves surveying orchards and nurseries regularly and immediately removing infected trees to prevent the virus from spreading.

Management

Disease management is implemented when prevention and eradication programs fail, or the disease becomes established in the native Prunus population of an infected region. Most management strategies involve regular surveys using visual symptoms to detect infected trees followed by their prompt removal in orchards. Regular testing also ensures an accurate disease diagnosis and virus-free propagating stock. The spread of PPV and other diseases by propagation can be reduced or eliminated by using virus-free budwood from a certified grower. Production of virus-free trees through the indexing of mother trees and the selection of virus-free budwood and rootstocks is critical in managing this disease.

Controlling aphids with insecticides does little to control the spread of the virus. A single aphid can transmit PPV to a new host in a short period of feeding and total control of aphid vectors with chemicals is impossible. Insecticide use can also disrupt established integrated pest management programs in stone fruit orchards, leading to increases in insecticide resistance and outbreaks of secondary pests. For example, most European countries do not include insecticide sprays in managing PPV in orchards.

Weed management in and around susceptible orchards may slow down the spread of PPV since some common weeds are natural hosts of PPV. However, the contribution of weeds to the spread of the disease is not clearly understood and more research is required to determine their importance in the spread, establishment and persistence of this disease in a region.

There are currently no commercially available varieties resistant to PPV. However, disease management with resistant cultivars appears promising with resistant genes identified and transferred to a plum cultivar in the USA. The transfer of resistance genes to other stone fruit crops is challenging and time consuming using conventional breeding techniques. Genetic engineering and the use of biotechnology can help develop PPV-resistant cultivars for most stone fruit crops. However, these scientific techniques alone are not the ‘magic bullet’ to completely resolve this devastating plant pathogen. A holistic approach encompassing all the management options outlined above is essential for successful disease prevention.

Further Information

To purchase or view the latest edition of the BioSecure HACCP Guidelines: https://nurseryproductionfms.com.au/biosecure-haccp-certification/
Hints for Diagnosing Diseases: https://pestid.com.au/disease
Details on the current import status of plant materials and can be obtained from the BICON website https://bicon.agriculture.gov.au/BiconWeb4.0
Integrated Pest Management Information: http://nurseryproductionfms.com.au/
Virus Identification and Management Video: https://youtu.be/2Mq0q0Inoig

PAST EDITIONS OF NURSERY PAPERS ARE AVAILABLE ONLINE on the Greenlife Industry Australia website: https://www.greenlifeindustry.com.au/communications-centre