Virus and virus-like diseases

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Virus and mycoplasma diseases are known to have been affecting citrus trees in Tunisia for more than 20 years. The incidence of stubborn, psorosis, cachexia-xyloporosis and exocortis diseases in various citrus trees was reported by Chapot (1959) and Jamoussi (1961, 1966). These problems are widespread in most Mediterranean countries, as reported by Bové (1966). They are recognized as a major factor preventing high crop yield and an intensive effort is being made towards production, maintenance and distribution to growers of healthy citrus-planting material in many areas of the basin. However, it will take many years to replace gradually disease-affected trees in the orchards. During his visit to Tunisia, Salibe observed symptoms of virus diseases in several orchards of the Cap Bon region and also learnt about the programme under way to eradicate these diseases from the country.

It should be pointed out that field observations for determining the incidence of virus diseases are necessarily limited to the presence of conspicuous symptoms in susceptible hosts. Those with experience can easily detect symptoms indicative of virus diseases. These include tree stunting; malformation of branches, leaves and fruits; vein clearing, ringspots and chlorosis of various types in leaves; bark scaling; stem and trunk pitting; and gumming. Some viruses induce specific and reliable diagnostic symptoms in mature trees and can be easily detected during field inspections. This is, however, not always true and many scion-rootstock combinations can harbour viruses without exhibiting specific symptoms, thus acting as symptomless carriers. Detection of viruses in these trees requires appropriate indexing, which may include greenhouse and laboratory tests. Moreover, extensive losses may result to growers when budwood taken from apparently healthy trees is propagated on rootstocks other than those of the original mother trees, thus allowing the manifestation of latent viruses or bud-union incompatibilities.

It has become evident that appropriate indexing, using modern techniques, should be carried out to determine the exact extent and status of virus and virus-like diseases in the citrus trees of the country.

Scaly bark psorosis (psorosis A) and concave gum-blind pocket

Psorosis A has a worldwide distribution and is found in most Mediterranean orchards. It has a long incubation period and usually requires a period of about 12 years or more to produce bark lesions, which are followed by slow tree deterioration. Bark scaling rarely occurs before a tree is six years old and symptoms may take many years to appear, sometimes up to 30 or 40 years.

Psorosis A bark scaling is said to be widespread in the orange orchards of Tunisia. Salibe observed typical bark scaling caused by psorosis in Maltaise orange trees of about 50 years old. Since this disease has no known insect vectors and is not normally spread by mechanical means, it must have come from the budwood used for the propagation of the trees.

Trunk malformations, indicative of the presence of concave gum-blind pocket, were also encountered in trees of Maltaise orange and Youssef Effendi mandarin. Careful inspection of the leaves of young shoots of many trees of various citrus varieties revealed no psorosis young leaf symptoms.

Elimination of psorosis virus from new plantings depends simply on using only budwood from healthy mother trees when propagating new trees. Nucellar clones of Maltaise Demi-Sanguine and healthy old-line clones of other varieties have been selected, and use of these should exclude the problem in new orchards. Attention should be paid to seed transmission of psorosis virus, found to occur in certain rootstock types (trifoliate and citranges).


Cachexia-xyloporosis is widespread in the mandarin orchards of the Mediterranean basin, and the plantations of Cap Bon are no exception. Salibe observed typical symptoms of the disease in the trunk of trees of Clementine and Youssef Effendi mandarins, above the bud-union. Apparently, in the same orchard, trees with and without cachexia coexist, implying that more than one clone of these varieties was used in the formation of the orchards. The incidence of this disease in the orange and lemon orchards will require proper indexing, since they are symptomless carriers.

The use of cachexia-free budwood is the recommended method for excluding this disease from future plantations.


Stubborn was said to be prevalent in the citrus orchards of Tunisia by both Chapot (1959) and Jamoussi (1966), and this was corroborated by information provided by local technicians. However, Salibe, during his visit to the citrus-growing areas of Cap Bon, did not find a single tree with typical symptoms of stubborn. Some trees thought to be affected by stubborn were considered by him to be abnormal owing to mutation, and not diseased. Inverse colouring, considered a symptom of stubborn, is a normal situation occurring in practically all fruits of all varieties in Tunisia. Some trees of Washington navel orange in Cap Bon and one in Ain Ben Mourra displayed some abnormalities which could be a mild form of stubborn. Indexing of these trees for stubborn was recommended.

Salibe, during his recent visits to citrus areas of 'Mediterranean countries, observed trees with typical symptoms of severe stubborn in Cyprus, Egypt, Jordan and the Syrian Arab Republic, but not in the Libyan Arab Jamahiriya, Morocco or Tunisia. It is possible that a more exhaustive survey would reveal the presence of stubborn in these countries as well. Indeed, as shown by Chapot, Cassin,

Nhami, Bové and others, stubborn is widespread in Morocco. In the Tadla area of Morocco, whole orchards have been removed because of stubborn. Furthermore, Spiroplasma citri has been isolated from many trees, and natural transmission of the spiroplasma occurs (see also Chapters 7 and 15).


Symptoms of exocortis include stunting of trees, bark splitting and scaling of the rootstock portion. The time taken for bark scaling to appear has usually been from four to eight years on trees budded on trifoliate or Rangpur lime rootstocks. Symptoms of exocortis also appear when intolerant varieties used as scion varieties are infected. The symptoms include yellowing of the bark of young branches, splitting and limited shelling. Infected Etrog citron plants of certain very sensitive selections also develop leaf epinasty and are used as indicators of exocortis.

Since no exocortis-intolerant rootstock is used in Tunisia, no conspicuous symptoms could be expected in commercial orchards. However, on the basis of evidence obtained in most citrus-growing areas of the world, exocortis is the most widely distributed pathogen of citrus and probably infects many trees in Tunisia. It is certainly causing tree debilitation in the so-called "symptomless" carriers, but the real destructive capacity of the disease will appear only should intolerant rootstocks (such as Troyer citrange and Rangpur lime) come into use.

Indexing is urgently needed for exocortis, since it may invade the germplasm collection, recently established in the country, through the use of infected tools.

Tristeza and stem pitting

As reiterated in the chapters above, tristeza is a very destructive viral disease affecting trees of sweet orange, mandarin and grapefruit on sour orange and certain other intolerant rootstocks. It occurs in most citrus areas of the world and, to date, tristeza has destroyed about 25 million trees in South America and about 3 million trees in California. It therefore represents a tremendous threat to the citrus industry of the Mediterranean basin, one of the last areas free from the virus, where mainly intolerant scion-rootstock combinations are used. Spain is the first Mediterranean country where the pathogen has become established, and extensive spread of tristeza has occurred, more exactly in the region of Alcira-Carcagente-Carlera in the district of Valencia, starting in 1957. More recently, tristeza was suddenly discovered in Israel and an identification and suppression programme was immediately launched (Raccah et al., 1976; Bar-Joseph et al., 1980), but has apparently failed.

Clearly the early cases of tristeza disease found in the citrus areas of the Mediterranean basin can be traced back to the introduction of infected budwood from abroad. All countries that have introduced Meyer lemon trees have also introduced tristeza, and these include Algeria, Israel, Italy, Morocco and Tunisia (Bové, 1966). Other varieties imported from Australia, Japan, South Africa and the United States of America have also been reported to have introduced tristeza into Mediterranean countries.

Rebour in 1950, as mentioned by Bové (1966), reported the occurrence of tristeza in Meyer lemon in Tunisia. Possibly the eradication of this variety from the country eliminated all possible sources of the tristeza virus.

Salibe found no abnormal trees with symptoms resembling those of tristeza during his visit to citrus areas of Tunisia. However, the extensive use of sour orange as rootstock in the orchards makes them susceptible to massive destruction should tristeza and its vector be introduced into the country. A list of insects captured by entomologists of INRAT included Myzus persicae, Aphis citricola, Aphis gossypii and Aphis fabae among other aphids which occur in Tunisia.

Other virus and virus-like diseases

Gummy bark of sweet orange, cristacortis, impietratura and rumple are diseases that are present in many citrus-growing areas of the Mediterranean basin. Symptoms of these diseases were not seen by Salibe during his visit to Tunisia. A more careful inspection may reveal the presence of one or more of these problems in citrus trees of the Cap Bon area.

Other virus and virus-like diseases of citrus also not observed during the visit were greening, vein-enation woody gall, satsuma dwarf, yellow vein, multiple sprouting, citrus tatter-leaf, citrange stunt, leaf curl, bud-union crease and gum pocket.

Local specialists should be familiar with the symptoms of these diseases so that they can be immediately identified and eradicated should they appear in the country.

Other disease problems

Three diseases, not of a viral nature, were brought to the attention of Salibe during his visit to the citrus orchards of the Cap Bon area. They were the mal secco disease of lemon caused by the fungus P. tracheiphila

Petri; the trunk rot of many trees induced by Phytophthora spp.; and a decline with many symptoms resembling blight but apparently associated with a Fusarium fungus.

Mal secco is causing extensive destruction of lemon orchards in many countries neighbouring Tunisia. In Cyprus, on one farm Salibe observed that Eureka lemon trees were badly affected by the disease, while some local varieties of lemon, such as one called Lapithos lemon, appeared to have good resistance. Introduction and propagation, under strict phytosanitary supervision, of such resistant varieties was recommended as a priority if Tunisia wants to continue the production of lemons.

Other observations

The germplasm collection at Ain Ben Mourra

A block of mother plants of various fruit crops, including citrus, was established by GIAF in the region of Ain Ben Mourra. This is an isolated area as far as citrus is concerned, since there are no other orchards for many kilometres around.

There are about 500 citrus trees planted in the period 1975 to 1979. Budwood was obtained from INRAT, taken from trees confirmed to be virus-free by indexing carried out in Corsica. The orchard of citrus trees, to which Salibe made a one-day visit, is divided into five main blocks.

In addition to these five blocks, there are two lines of selected seedlings for seed production, including 140 trees of sour orange and another 140 trees of Troyer citrange.

Budwood from this germplasm collection is sufficient to meet all the requirements of the country for nursery purposes. However, these trees should be reindexed every three to five years, and this is not being done. Also, no special attention is being given to disinfection of pruning tools and so exocortis contamination may be occurring. Trees of Block 5 may be carrying exocortis and other pathogens, since not all the varieties have been indexed.

Trees of some blocks show bark scaling-type popcorn in the trunk but, according to a local specialist, these symptoms resulted from a severe hailstorm.

Trees of nucellar Maltaise Demi-Sanguine were found to be very vigorous and practically without thorns. However, the fruits were observed to be slightly flat while the old line produced round to oval fruits.

Three trees of Valencia orange were found in the Washington navel orange plot in Block 2 and it was recommended that they be eliminated to avoid future mixing of budwood. Also, one tree of Washington navel orange in this same block was suspected of carrying stubborn, and was condemned.

No symptoms of any virus disease were found after careful inspection of most trees of the orchards. However, mal secco is badly affecting the Eureka lemon trees and no budwood from these trees should be used for propagation. Autumn leaf drop was observed in some trees and the abnormality was attributed to the cold mornings (7-8°C) having the effect of a localized frost.

It was strongly recommended that all trees should be reindexed as soon as possible and that all plants found to be infected with any virus or virus-like pathogen should be eliminated.

Disinfection of all pruning instruments to avoid mechanical transmission of exocortis was also recommended.

The germplasm collection at Mornag

A block of healthy mother plants was established by INRAT in Mornag (about 20 km from Tunis) in 1974. This was set up as the National Bank of Healthy Germplasm of Citrus in Tunisia. From here, budwood was taken to produce the block of mother trees of GIAF in Ain Ben Mourra. At present the orchard is partially abandoned and there is a plan to eradicate it in the near future. Trees were severely pruned about two years ago and are not receiving fertilization.

Varieties included in this orchard were Eureka lemon, Citrus limon; Bearss lime, Citrus latifolia; sweet lime, Citrus limetta; Frost Willowleaf mandarin; Hamlin orange; Azizia mandarin; Pineapple orange; Salustiana orange; Barlerin orange; Boukhobza orange; Chami orange; Clementine mandarin; Valencia orange (nucellar); Maltaise Demi-Sanguine orange (nucellar); and Maltaise Petit Pierre orange.

No virus or virus-like diseases were observed on the trees of this mother block. In the same area, one orchard of trees of about 50 years old (apparently of Maltaise orange) was visited and some trees were found to be showing bark-scaling symptoms due to the psorosis A virus.

A visit to the citrus nursery at El Gobba

A visit was made to the GIAF citrus nursery at El Gobba in Cap Bon. The nursery, previously in Sbikha, was established here in 1980, and produces around 20 000 to 50 000 budded plants annually, about half of the country's requirements. Nursery trees are budded mainly on sour orange rootstock, but also on Troyer citrange and Cleopatra mandarin. Budwood is taken from the block of mother trees in Ain Ben Mourra. Salibe was informed that the time required for producing a budded plant is about three years. Problems affecting the production of trees were discussed, mainly those related to nutrition, wind damage and virus and bud-union crease.

A plastic greenhouse is being established in this nursery and an agronomist who recently underwent training in Morocco is working to improve plant production.

The bacterium Pseudomonas syringae was observed to be affecting young seedlings in the nursery.

The INRAT laboratories

During Salibe's stay, two visits were paid to the laboratories of INRAT in Avenue de l'Indépendence in Ariana. Visits included the modern virology laboratory, where ELISA tests are made for several pathogens, the laboratory of shoot-tip grafting, the new laboratory for plant analyses and various others, including one for citrus fruit analysis.

No facilities for an indexing programme for citrus virus and mycoplasmas were shown to the consultant. The need for indexing facilities for citrus budwood certification was strongly emphasized. Training of a citrus virologist is another great need in Tunisia.

A visit to GIAF

GIAF is an organization of real importance to the development of the citrus industry in Tunisia. It provides permanent assistance to citrus growers, with an average of one agent per 1000 ha, in the various citrus locations: Menwel Bou Zelfa (2), Beni Kalled (2), Soliman (1), Grombalia (1), Bou Argoub (1), Hammamet (1), Nabeul (1), Soukra (1) and Mornag (1). Agronomists periodically visit the orchards to make recommendations regarding cultural practices, and to provide help in the acquisition of phytosanitary products and choice of equipment. GIAF produces nursery plants for citrus growers and sponsors courses for the training of qualified workers.

Every year GIAF promotes a control programme for the Mediterranean fruit-fly, Ceratitis capitata, free of charge to growers, which includes three to four spraying operations (aerial and ground applications) of the total area of citrus orchards in the country.

Other GIAF campaigns include control of aphids and scales; a foliar diagnostic service (Diagnostique Foliaire) throughout hundreds of orchards to evaluate the nutritional status of trees; the promotion of drip irrigation systems and many other campaigns.


Citrus trees are not native to any country of the Mediterranean basin. They were brought into the region from their centre of origin in Southeast Asia and the Malayan archipelago. Many, but not all, major pests and diseases were imported with early plant introductions. For this reason, emphasis should be placed on strict quarantine regulations to prevent further introductions of undesirable citrus parasites into the citrus orchards of Tunisia. Special attention should be given to excluding, or eradicating promptly - should they enter the country - the destructive agents of three diseases with the potential to wipe out the citrus industry of any country completely: greening, tristeza-seedling yellows and citrus canker. Citrus decline (blight in Florida, declinio in Brazil, marchitamiento in Uruguay and fruta bolita in Argentina), a disease of unknown nature - though it is thought to be caused by an infectious agent - also deserves attention to avoid its introduction into the country.

As practically the whole of the Tunisian citrus industry is based on sour orange rootstock, this makes it extremely vulnerable to destruction by tristeza virus. This situation is identical to that of most other citrus areas of the Mediterranean basin and the Near East. Only trees of true lemon, Citrus limon (L.) Burm., on sour orange rootstock would survive the invasion of orchards by tristeza virus. In the light of available knowledge, spread of tristeza in the orchards of the region would result from:

The establishment of a quarantine station should be considered of vital importance for the continued prosperity of the citrus industry. Finally, it is recommended that an identification and suppression programme for tristeza virus should be implemented in Tunisia.


Bar-Joseph, M. & Loebenstein, G. 1973. Effects of strain, source plant and temperature on the transmissibility of citrus tristeza virus by the melon aphid. Phytopathol., 63: 716-720.

Bar-Joseph, M., Garnsey, S.M., Gonsalves, D. & Purcifull, D.E. 1980. Detection of citrus tristeza virus. 1. Enzyme-linked immunosorbent assay (ELISA) and SDS-immunodiffusion methods. In Proc. 8th Conf: IOCV, p. 1-8. Riverside, Univ. Calif.

Bové, J.M. 1966. Citrus virus diseases in the Mediterranean area. Report presented at the meeting on Phytiatry and Phyto pharmacy, Marseilles (France), 1965, updated for the 4th Conf. IOCV. 44 pp. (mimeo)

Chapot, H. 1959. First studies on stubborn disease in citrus in some Mediterranean countries. In J.M. Wallace, ed. Citrus virus diseases, p. 109-117. Riverside, Univ. Calif.

GIAF [Groupement Interprofessionnel des Agrumes et des Fruits]. 1976. Résultats du Récensement des Agrumes de 1975. Tunis, Bull. 11 pp.

INRAT [Institut National de la Recherche Agronomique de Tunisie]. 1981. Les variétés fruitières recommandées en Tunisie. Documents Techniques No. 83. Ariana, Imprimerie Officielle, INRAT. 120 pp.

Jamoussi, B. 1961. Citrus virus diseases in Tunisia. In Proc. 2nd Conf: IOCV, p. 253255. Gainesville, Univ. Fla. Press.

Jamoussi, B. 1966. Les viroses des citrus en Tunisie et les moyens de lutte. Ann. Inst. Nat. Recherche Agric. Tunisie, 39(2): 1 -60.

Raccah, B., Loebenstein, G., Bar-Joseph, M. & Oren, Y. 1976. Transmission of tristeza by aphids prevalent on citrus, and operation of the tristeza suppression programme in Israel. In Proc. 7th Conf: IOCV, p. 47-49. Riverside, Univ. Calif.

Rebour, H. 1950. Les agrumes, 3rd edition. Alger. 120 pp. (no imprint)

Roistacher, C.N. 1981. A blueprint for disaster. II. Changes in transmissibility of seedling yellows. Citrog., 67(2): 28-32.


Chapter 23: Turkey

Citrus growing in Turkey
Virus and virus-like diseases
Other disease problems
Visits to agricultural agencies

Turkey has been growing citrus fruits for centuries, nearly all destined for the local market. In more recent years the citrus industry has started to modernize its production system, with a consequent sharp increase in fruit output and a growing presence in world trade. Citrus fruits from Turkey are renowned in the European markets for their high quality, and the lemons are particularly famous. Moreover, the exceedingly high quality fruits are presented in sophisticated and attractive packaging, coming from modern packing stations.

The 1984/85 crop totalled about 1.37 million tonnes, made up of 750 000 tonnes of oranges, 350 000 tonnes of lemons, 250 000 tonnes of mandarins and 25 000 tonnes of grapefruit. Exports in recent years have amounted to approximately 130000 tonnes of lemons, 45 000 tonnes of oranges and 50 000 tonnes of mandarins, mainly satsumas. As new plantings come into bearing, total Turkish citrus production is expected to continue to grow in the near future. Domestic consumption of citrus fruits in Turkey is high and will probably absorb most of the increase in fruit output, as a result of growth in population and the rapid improvement in the population's standard of living. Export volume is also expected to expand, particularly to European markets.

Productivity of citrus orchards in Turkey is considered to be fairly low. Considering that the average production of 1.0 to 1.3 million tonnes per year comes from around 70 000 ha, fruit production ranges from 15 to 20 tonnes per hectare. This level of production, while superior to that of most other neighbouring countries in the Mediterranean area, is fairly modest when compared with that of many advanced citrus areas of the world, where the average yield of adult orchards reaches 30,40 and 50 tonnes per hectare, and, exceptionally, as much as 80 tonnes per hectare.

New plantings using selected, virus-free propagative materials are necessary to increase productivity in citrus orchards, and attempts have been made in the last two decades to produce healthy budwood for distribution to citrus growers. However, all initiatives were subsequently discontinued, and most growers are still propagating materials infected with one or more intracellular pathogens. However, a well-planned programme of production, selection and indexing for freedom from virus and virus-like pathogens of local commercial citrus varieties is being launched, but the success of the new programme will depend on the maintenance of financial support from government agencies. International agencies could also be requested to contribute to the development of this programme.

Many infectious diseases, such as psorosis, cachexia-xyloporosis, exocortis and stubborn, are known to occur in practically all citrus areas of the Mediterranean basin, including Turkey. They reduce vigour and productivity and shorten the lives of affected trees, with or without apparent symptoms. Tristeza virus is also suspected to be present in Turkey, in trees budded on trifoliate orange rootstock.

The new phytosanitary programme will certainly eliminate the pathogens that have no insect vector or are not yet present in the country. Fortunately, a number of important destructive diseases do not occur in Turkey, such as greening (induced by an intracellular bacterium and transmitted by psyllids), citrus canker (caused by the bacterium Xanthomonas campestris pv. citri), and the dreadful "blight disease", of unknown aetiology. Protection of new citrus plantations should include strict quarantine precautions to prevent the introduction of these and other diseases and their insect vectors into the country.

Citrus growing in Turkey

Citrus production is an ancient and important sector of agriculture in Turkey. An estimated 70 000 ha of fertile soil are at present under citrus orchards. The major citrus area is concentrated in the Adana-Mersin district, but many other smaller areas exist along the Mediterranean coast, of which Antalya and Izmir are among the most important. A smaller area, about 12.5 percent of all citrus, mainly dedicated to the production of satsuma mandarins, also exists along the Black Sea and Aegean Sea coastal region. Throughout the Mediterranean, winter is wet and mild and summers are hot and dry. The climate in Turkey is generally cool and damp, and frosts are common during winter months. Available data for total plantings in Turkey in 1960 and 1985 are shown in Table 56. A major percentage increase has occurred in lemon plantings, and further expansion of lemon culture is expected in the near future.

Commercial sweet orange varieties include Washington navel and other navel selections, Shamouti, Valencia and a number of local orange types, such as Trablus, Alanya and Finike. Lemon varieties include Interdonato (apparently a local selection of the Italian Interdonato lemon) and local Turkish varieties such as Lamas, Yedi Veren and Molla Mehmet. Some varieties are named Italian lemon and Cyprus lemon. Among mandarins or tangerines, the Clementine, satsuma and the local type of Willowleaf are grown. More recently some plantings of Freemont mandarin were made. Grapefruit trees are all of the Marsh seedless variety.

Major orange and lemon areas are in the Mediterranean provinces. Most oranges are produced in the areas of Mersin, Adana, Iskenderum and Antalya, and most lemons in the provinces of Antalya and Icel (Mersin area). Satsuma is the major variety grown in the Black Sea and Aegean Sea areas and is locally named Rize tangerine. It is important for the domestic markets of Istanbul and Ankara in November and December. Nearly all Turkish oranges and mandarins are consumed in the six-month period from November to May.

The lemon season starts as early as September every year for export. A technique used locally consists of storing fully wrapped packs of lemons in caves for domestic use through the summer months. As many as 500 000 boxes of these "sleeping lemons" are said to be stored every year.

TABLE 56 Total plantings in Turkey for 1960 and 1985

Species Number of trees
  1960 1985
Oranges 5 500 000 10 300 000
Tangerines 1 400 000 6 000 000
Lemons 850 000 4 000 000
Grapefruits   250 000

Source: Burke, 1965 (for 1960 data).

Groves are generally small and closely planted and are all irrigated. Many orchards have 40- to 50-year-old trees still producing fairly good crops.

Sour orange is the main rootstock variety used in the Mediterranean citrus areas, while trifoliate orange is used as rootstock for satsuma mandarin in the Black Sea and Aegean Sea regions.

Nurseries, both private and government, produce around 300 000 new plants every year for replanting and new orchards. No certified mother trees exist in the country for use by nursery workers, and registration is carried out only for government-produced trees.

Three juice-processing plants exist in Turkey, processing both citrus and other fruits.

Major pest problems include Mediterranean fruit-fly, red scale, aphids and a number of mites. Fruit losses are mainly due to fruit-fly, which limits the harvesting season of oranges and tangerines. They do not attack lemons. Major fungal diseases are phytophthora root rot on all citrus and mal secco on lemons. Virus and virus-like diseases reported include psorosis, cachexia-xyloporosis, stubborn and possibly tristeza disease.

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