Virus and virus-like diseases

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Virus and virus-like diseases are known to have been present in citrus trees in Turkey for more than 30 years (Chapot, 1956; Reichert, 1959; Norman, 1963; Moreira, 1965; Chapot and Bahcecioglu, 1969; Ozbeck et al., 1976). A number of attempts have been made to prevent further spread of infectious diseases into new orchards. However, they have been discontinued and disease pathogens continue to occur in the plantings. They should be considered a major factor limiting high yield and reducing growers' profits.

Virus and virus-like disorders reported in citrus trees in Turkey include psorosis in various forms, stubborn, cachexia-xyloporosis, impietratura, rumple, exocortis and possibly tristeza. Most of these diseases, except tristeza, are widespread in most areas of the Mediterranean countries, as pointed out by Bové (1966) and Salibe (1986). Since most citrus propagative material used in Turkey was probably imported from other Mediterranean countries and from North America, it must be supposed that the intracellular disease agents existing there were inadvertently introduced at the same time.

Comments are made below on some major virus and virus-like diseases and their incidence in Turkish citrus.

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

Psorosis A is widespread in the citrus orchards of Turkey, causing early death of many trees and materially reducing vigour and yields. Norman (1963), during a field survey, found leaf symptoms of psorosis in the spring growth flush in trees of various sweet orange varieties including Jaffa, Balady,

Dortyol, Pineapple, Valencia, Akcay, Sanguinella Muscata and Washington navel. Psorosis was also found in varying degrees in Yerli common, Dancy, Marsh and Rize mandarin varieties. In the Iskenderun area, about 68 percent of all trees examined were found to be infected. Moreira (1965) reported psorosis affecting navel and other sweet orange varieties, with typical bark-scaling symptoms. Both authors emphasized that psorosis seemed to be present generally throughout Turkish citrus plantings, and pointed out that this highly destructive disease was found more frequently expressing leaf symptoms than eruptive bark scaling. Moreira (1965) observed that bark symptoms were frequently found in orchards near Mersin and Izmir, but were less common in the Antalya area. Salibe observed old sweet orange and grapefruit trees exhibiting symptoms of psorosis A bark scaling and concave gum in orchards of the various regions visited. Symptoms of other forms of psorosis were not found. Trees of Shamouti orange were seen with cracks and scaling in the bark of branches and trunk in varying amounts in orchards of Adana. Concave gum was observed in the trunk of Shamouti orange trees, budded on sour orange rootstock of about 50 years old in the Antalya area. Lemon trees were apparently free from psorosis.

Indexing with proper indicator test plants may reveal the true extent of psorosis contamination in the citrus orchards of Turkey. It is possible that many commercial varieties will be found entirely infected by psorosis. It will require proper methods, such as shoot-tip grafting, to free budwood from this intracellular pathogen. Since psorosis has been shown to be seed-transmitted, indexing of mother trees of rootstock-seed sources should also be included in the indexing programme.


Cachexia-xyloporosis is a disease widespread in the Mediterranean basin, expressing symptoms in most mandarin orchards. The presence of cachexia-xyloporosis in Turkey was reported by Reichert (1959), Norman (1963) and Moreira (1965). The disease is of economic importance in mandarin and mandarin hybrids, and was found by Norman to be affecting trees of common, Clementine, Daidai and Youssef mandarins and Thornton and San Jacinto tangelos at Iskenderun. Moreira reported that very few trees of common mandarin and Clementine tangerine were found without symptoms of cachexia-xyloporosis. In trees of Shamouti orange budded on sweet lime imported from Israel and about 28 years old, the authors also found normal cachexia-xyloporosis in the rootstock portion of the trunk and inverse xyloporosis above the budding point. Bové observed severe cachexia-xyloporosis at Finike on the mandarin sandwich of an old sweet orange tree on sour orange roots (Fig. 55).

Inspections made by Salibe during his visits to Turkey confirmed previous reports that cachexia-xyloporosis is seriously affecting mandarin trees. Typical gum pockets, plus conoid pits and wood pinholing typical of the disease, were found in the trunk of mandarin trees above the bud-union in many orchards. Knowledge of the real distribution of the viroid in sweet orange, grapefruit and lemon trees (which do not exhibit typical symptoms) will depend upon an indexing programme. Varieties found with symptoms of cachexia-xyloporosis included Clementine, satsuma (imported from Egypt), Speciale (Willowleaf) mandarins and San Jacinto tangelo. The problem appeared to be more severe in the Antalya area. Symptoms ranged from mild to very severe in some blocks of trees, but not all trees were affected, suggesting that more than one source of budwood was used in the formation of the orchard.

Since the cachexia-xyloporosis viroid is perpetuated by the use of infected budwood and as no insect vector is known, it can be excluded from new plantings by the use of healthy propagative material.


Stubborn disease is probably the most serious infectious disease affecting citrus in Turkey. Chapot (1956) first reported the occurrence of the disease in the country, pointing out that the symptoms were highly characteristic of those of severe stubborn, also named "crazy top", "acorn disease", "pink nose", "little leaf" and "xeromorphosis". Norman (1963) and Moreira (1965) confirmed the widespread presence of stubborn in Turkey, and the fact that it is especially damaging in the areas of Adana and Iskenderun.

Spiroplasma citri, the stubborn pathogen, was cultured from the following symptomatic trees by the Bordeaux group in 1980-81 : Washington navel (Midik area, Adana); local sweet orange (Tarsus area); Frost navel, Carter, Skagg's Bonanza navel and Parent Washington navel sweet oranges (Mersin area); Skagg's Bonanza navel (Adana and Alata Erdenti areas); Frost navel and Carter sweet oranges (AIata Erdenti area); and two undetermined sweet oranges (Missis area). These results show that stubborn is widespread in the Adana region.

Salibe observed many citrus trees exhibiting the entire syndrome of stubborn symptoms. Symptoms were more easily recognized in Washington navel orange trees, and included stunting, leaf mottle (Fig. 154), shoot growth with erect or rosetted leaves and multiple buds, many acorn-shaped fruits with curved columella, and off-season blooming. Both local and imported varieties were found affected.

Severe cases of stubborn were observed in the Yesilkent-Dortyol (Hatay) area in several orchards. Other affected trees of Washington navel orange on sour orange rootstock, in addition to the known stubborn symptoms, showed bud-union creasing on the trunk and tristeza-like honeycombing in the rootstock. Washington navel was the variety most affected, with up to 20 percent of trees diseased. Valencia orange and satsuma mandarin also showed symptoms of stubborn, but grapefruit did not. No stubborn-diseased trees were found in the Antalya area.

During a visit to the Horticultural Research Centre in Erdemli, Mersin, a collection of citrus varieties, all of nucellar origin, and established using budwood imported from California in 1975, was inspected for stubborn symptoms. All trees of Bonanza navel were found to be severely affected by stubborn. They were all stunted trees, with typical leaf symptoms and overgrowth and honeycombing in the trunk. Some Valencia orange trees were also affected, but not the grapefruit trees, which were all vigorous and healthy-looking. New orchards propagated from this mother block showed a high percentage of stubborn-diseased trees.

The problem of stubborn is extremely serious in Turkey and, apparently, some field spread of the disease seems to be occurring, in addition to the spread by infected budwood. Indeed, Neoaliturus haematoceps, the major leafhopper vector of S. citri, the stubborn pathogen, has been identified in the Adana region (Fos et al., 1986) and has long been known in Turkey as a vector of sugar beet curly top virus (Bennett and Tanrisever, 1957). Periwinkle plants exposed to natural contamination became infected with S. citri at Abdioglu, Missis and Adana University (Barrage area), showing that natural spread of the stubborn agent occurs.

Extensive work on the transmission of S. citri by leafhoppers has been carried out recently in the Adana region of Turkey (Kersting and Sengonca, 1992 and personal communication). N. haematoceps was shown to be a major vector of S. citri, thus confirming the observations made by Fos et al. (1986) in Syria. In addition, the workers in Turkey showed that Sesamum indicum was a good host not only for N. haematoceps but also for S. citri. The N. haematoceps populations captured on sesamum were infected with S. citri and they were able to transmit the spiro-plasma to healthy periwinkle plants. A second leafhopper was encountered: Neoaliturus opacipennis. This leafhopper was only found on Salsola kali, but was unable to transmit S. citri.

Satisfactory control of citrus stubborn disease is not an easy task in areas where the leafhopper vectors occur in fairly high populations. An intensive study is urgently needed to determine the rate of field spread and identify the insect vectors of the disease in Turkey. Other necessary control measures include an annual survey of orchards, removal of all infected plants and replanting with disease free plants, and using only budwood from disease-free trees for all propagations, including top-working.


The incidence of impietratura in sweet orange fruits in Turkey was first reported by Chapot (1961), who found the problem in almost all areas of the country, with a greater predominance along the south coast, especially around Dortyol, Adana and Finike. This author reported that in one orchard, with 70 percent local orange varieties and 30 percent Washington navels, a large number of severe cases of impietratura were found, but only on local varieties. He also claimed that trees producing abnormal fruits were less vigorous and the leaves were slightly wilted. On the variety named Finike Yerli, which normally has round fruits, the fruits from the impietratura-infected trees were definitely pear-shaped.

According to growers, this disease has existed for several years in Turkey and was first noticed because of the premature drop of many fruits and gum pockets in the albedo. Norman (1963) also found impietratura symptoms in the albedo of both oranges and grapefruits in the Iskenderun, Adana and Finike areas.

Salibe's visit was made early in the season and no typical impietratura symptoms were found. On the basis of surveys made by local scientists and virus experts visiting the country, impietratura seems to be a serious problem, reducing growers' profits. Since no insect vector of impietratura is known to exist, the use of healthy budwood should exclude the problem from new orchards. The problem of impietratura may become more serious should grapefruit, which is very susceptible to the disease, be grown on larger areas in the country.


The disease was first reported to be affecting lemons in Turkey by Chapot and Bahcecioglu (1969). They stated that rumple was widespread during the 1960/61 crop in the areas of Antalya, Mersin, Adana and Arsus, and that extreme damage was occurring in some orchards, with as much as 75 percent of fruits being affected. Ozbek et al. (1976) described a number of experiments conducted to determine the nature of rumple in Turkey. They found that manganese deficiency in particular was responsible for the development of rumple and that 3 kg MnSO4 per 1 000 litres of water was the most effective treatment. However, results were considered preliminary and further investigations were thought to be necessary to clarify the true nature of the disorder.

Salibe visited a number of lemon orchards, but it was not the best season for seeing rumple symptoms. A few abnormal fruits were observed in a local variety named Kut Diken in the Mersin areas, where rumple is known as Cokuntu, Copur and Benek disease. Rumple appears to be a serious problem and, until its true nature is determined, careful selection from only healthy trees of budwood for propagation is recommended.

Gummy bark of sweet orange

Gummy bark disease was first reported to occur in orange trees in Turkey by Moreira (1965). Salibe found xyloporosis-like symptoms on some common sweet orange trees budded on sour orange rootstock in an orchard near Koycogiz, between Dalaman and Mugla. Bové observed symptoms of gummy bark on Valencia late sweet orange trees in the Antalya area (Figs 64 and 65).

Salibe was taken by local scientists to visit an orchard in Yesilkent-Dortyol, where typical symptoms of gummy bark were found in trees of Washington navel and other local varieties of sweet orange budded on sour orange rootstock. Trees were stunted and showed abundant gum impregnation in the bark above the bud-union, plus wood pitting in the trunk, sometimes extending to large limbs. To determine the actual incidence of gummy bark of sweet orange in the orchards of Turkey, a large-scale indexing programme is necessary. Budwood for propagation should be taken only from healthy trees to avoid introducing the problem into future orchards.


Exocortis disease was found by both Norman (1963) and Moreira (1965) affecting citrus trees budded on trifoliate rootstock and hybrids. Moreira reported symptoms of exocortis in four-year-old Washington navel orange trees budded on Troyer citrange rootstock in one orchard near Mersin. Troyer citrange trees budded on sour orange rootstock showing exocortis-like symptoms in the branches were also found in the Antalya and Aksu experiment stations.

Salibe was not able to inspect any citrus orchards budded on exocortis-intolerant rootstock. Exocortis-like yellowing and splitting of the bark of branches were seen in stunted trees of Di Genova shaddock at the Antalya Experiment Station. The evidence is that the exocortis viroid is present in Turkish citrus, and indexing may show that, as in most other citrus areas of the world, the viroi is widespread in Turkish commercial citrus varieties. Should trifoliate or its hybrids be used on a wide scale, exocortis may become a serious problem for citrus growers.

Exocortis is perpetuated by budwood and is also spread by contaminated tools. Special care is therefore required to prevent it spreading into selected mother trees.


Cristacortis-like symptoms were found by Moreira (1965) in Shamouti orange trees of about 28 years old at the Antalya Experiment Station. Salibe found gumless pitting resembling cristacortis in orange trees in the Adana and Antalya areas. Local scientists also informed him that cristacortis is present in Turkey. A careful field survey and proper indexing are necessary to determine the real extent of the disease in Turkish citrus.

Satsuma dwarf

Satsuma dwarf was reported for the first time in the Izmir region of Turkey by Azeri in 1973. He showed typical symptoms of the disease to Bové in 1978 (Fig. 118).

Satsuma mandarin is an important commercial variety in Turkey. It is an early ripening fruit that is first picked at about the same time as early lemons, towards the end of September. However, owing to the destructive capacity of the disease, a careful survey of satsuma orchards is recommended to serve as the basis for a control programme for this disease.

Reichert (1959) asserted that tristeza virus was not present in local varieties of citrus in Cyprus, France, Greece, Israel, Italy, Portugal, Spain, Turkey and Yugoslavia. Norman (1963) was the first to report that some citrus trees of an orchard near Adana were displaying symptoms indicating the possible presence of tristeza. Anatomical studies of bark samples taken at the bud-union of these and some other declining trees gave inconclusive results. Indexing, using Mexican lime seedlings as indicator, conducted by Moreira (1965) and his counterpart at the Antalya Experiment Station, gave negative results. It is possible that indexed trees were declining owing to severe stubborn, which also causes honeycombing below bud-union, though this symptom is not generally known to be also typical of stubborn.

Salibe was told by local scientists that indexing of satsuma mandarin trees budded on trifoliate rootstock in the western region was positive for tristeza virus. Indeed, Azeri has used small-fruited acid lime to index many satsuma trees on P. trifoliata for tristeza virus in the Izmir region. He found that more than 15 percent of the trees were infected (Azeri, personal communication). Colette Bové used ELISA to detect tristeza virus in the 499 50-year-old satsuma trees on P. trifoliata in the Ahmet Coskun orchard at Inciralti-lzmir. Thirty-three trees (6 percent) were found to be infected, scattered throughout the orchard. She has also indexed severely stunted Owari satsuma trees on sour orange showing conspicuous pinholing in the sour orange bark below the bud-union line (Fig. 129). The ELISA reaction was strongly positive, showing that the trees were infected with tristeza virus. As one of the countries still extensively using sour orange as rootstock, tristeza virus represents a tremendous threat to the citrus industry of Turkey.

Bud-union crease

Bud-union crease was found by Salibe in some trees of Washington navel orange budded on sour orange rootstock. These trees also showed symptoms of severe stubborn disease.

This abnormality may become a serious problem in Turkey should incompatible scion-rootstock varieties be recommended in commercial orchards. New rootstocks should not be used for local varieties before experimental trials have shown freedom from bud-union crease symptoms.

Virus and virus-like diseases not found in Turkey

None of the following virus and virus-like diseases was observed during the FAO consultants' visits to the citrus orchards: vein enation-woody gall, citrus tatterleaf, infectious variegation, gum pocket, leaf curl, leprosis, yellow vein, citrus blight and citrus decline. Local plant pathologists should make themselves familiar with the symptoms of these and other unwanted diseases in order to be able to recognize them quickly and promptly eradicate any tree suspected of harbouring their pathogens. Good descriptions of such disease problems have been made by Childs et al. (1968); Bové and Vogel (1980); and Wallace (1978).

Other disease problems

Mal secco disease of lemon trees, caused by the fungus Deuterophoma tracheiphila, is a major problem in the lemon orchards of Turkey. Many local and imported lemon varieties are affected (Figs 233 and 235). It takes five years for a lemon tree to come into bearing and usually mal secco destroys the tree after five to ten crops. Selection of lemon clones with resistance to the disease is at present under way, with promising results. Interdonato lemon, the variety most widely grown for its superior fruit quality, is very sensitive to mal secco disease. Selections more resistant to the fungus must therefore be found.

Pseudomonas syringae, a bacterium affecting leaves, twigs and fruits, is present in Turkey and has caused some damage to citrus, but is being controlled with the use of copper sprays.

Shell bark is another problem affecting lemon trees. Citrus bergamia was also seen displaying bark cracks and scaling in the trunk of trees, characteristic of shell bark, a disease considered to be of a physiological nature.

Sieve-tube necrosis is another serious problem affecting lemon trees on sour orange rootstock.

Gummosis, caused by various soil-borne fungi of the genus Phytophthora, is also present in Turkey, affecting the trunk of trees. However, damage is limited owing to the high resistance of sour orange rootstock to the attack of this pathogen. Low budding and deep planting favour the attack of lemon trunk by gummosis.

Abnormal leaf drop was observed in lemon trees in the area of Mersin, resembling the autumn leaf drop disorder. Local scientists attributed the problem to the presence of high populations of the nematode Tylenchulus semipenetrans. Autumn leaf drop is a serious problem affecting citrus in some Mediterranean countries and may also be occurring in certain areas of Turkey. The problem is characterized by abnormal leaf drop during the late autumn and winter months. It probably results from a physiological disorder, caused by cold temperatures in the mornings (7-8°C) that act as a form of localized frost. Damaged trees produce lower yields.

Bové observed strong symptoms of ringspot on sweet orange leaves in the Adana area (Figs 125 and 126).

Visits to agricultural agencies

Antalya Experiment Station

The Experiment Station at Antalya is located in the centre of an important citrus-producing area. It is the main orange-producing centre of Turkey, and about 80 percent of the orchards are planted with sweet orange trees budded on sour orange rootstock. According to local information, about 60 percent of trees are Washington navels, 30 percent are local orange types (such as Alanya and Finike Yerli) and 10 percent are Valencia and Shamouti orange.

The station is provided with modern laboratories and greenhouses, guesthouses and a large experimental field area, split into three plots, that covers about 1 000 ha. Here, several research projects were initiated during the 1960s, involving production and selection of nucellar lines, selection of superior old-line mother trees, indexing for viruses and other projects aimed at providing healthy budwood to citrus growers. Most of these research studies were paralysed around 1978.

There is a large citrus collection with many varieties represented by 45- to 50-year-old trees. Trees of Marsh seedless grapefruit were large and healthy-looking. Some orange trees such as Navalencia were seen with concave gum symptoms on the trunk. Shell bark was found in the lemon interstock of a Shamouti orange tree. Iron deficiency is a problem in most trees of the collection. Careful inspection of the mandarin and mandarin hybrids plot revealed cachexia-xyloporosis symptoms, ranging from mild to very severe, in the trunk of satsuma (from Egypt), Clementine (from Italy), Speciale tangerine, Dancy mandarin and San Jacinto tangelo trees. Thornton tangelo trees were found with concave gum symptoms. One tree of Washington navel orange displayed leaf abnormalities indicative of stubborn disease, but this problem is more rare in Antalya, although widespread in the Adana area.

The collection contains several lemon varieties of great value for work in hybridization and selection for mal secco control. Lemons are more widely grown in the Alanya and Mersin areas than in Antalya.

A large greenhouse in the station still maintains a great number of old seedlings of indicator varieties for virus indexing.

A mother block of young potted trees of commercial varieties is maintained in a screenhouse at the station. Budwood for these trees was taken from selected, apparently healthy trees located in a countrywide survey. The block comprises three to four trees of each variety, including satsuma mandarin, Interdonato lemon, Clementine mandarin, and Washington navel, Shamouti (Jaffa) and Valencia oranges.

A large collection of 88 varieties was established with budwood imported from California. First introductions were made in 1967, followed by further introductions in 1970. They are mostly nucellar clones, each one represented by five trees budded on sour orange rootstock. In this plot, most lemon varieties were destroyed by mal secco disease, with only a few trees remaining alive, including those of Femminello Santa Teresa lemon.

Trees of Rangpur lime, citrons and a few other varieties were eliminated by phytophthora gummosis and cold damage. Most orange trees are vigorous, but with low yields. Trees of one variety, namely Skragg Bonanza navel orange, were stunted and possibly infected with the stubborn mycoplasma. Shoot-tip grafting of all varieties was recommended.

A second block of nucellar trees was visited. These were nucellar clones of local orange varieties, produced over 15 years ago, following the visits of two FAO citrus specialists (Norman and Moreira). No attempt was made to accelerate ageing of these clones to reduce juvenility, nor were comparison trials made with similar old-line clones.

A large citrus nursery was visited at the station, where budwood was taken from trees selected at the station and from commercial orchards on the basis of their healthy appearance. It was said that another government nursery was located in Alanya and that several other private nurseries existed in the area. Private nurseries were all small, except one in Gozipasa, Antalya, that produces 50 000 to 60 000 plants annually. Small nurseries seen by Salibe produce citrus plants in pots or large cans, with a very low standard of quality. He was informed that nursery plants are being used for local orchards and also for export, e.g. to Saudi Arabia.

Salibe was further informed that there is an official project to establish an indexing programme to free citrus from virus diseases, in the two centres (Antalya and Adana). The programme at Antalya is operational at the time of writing (1990). The need to introduce new citrus varieties, especially a mid-season ripening mandarin variety, was also clear.

A rootstock experiment, established on the third plot, was visited. Rootstock experiments were established in four different ecological zones of Turkey: Adana, Antalya, Icel and Mugla. They were planted in 1982 and included 11 rootstocks and the best scion varieties.

Faculty of Agricultural Sciences, Adana

The facilities for the control of virus and virus-like diseases of citrus at the Plant Protection Division of the Faculty of Agricultural Sciences at the University of Adana are limited and there is an urgent need for new laboratories, equipment and greenhouses for virus studies and indexing. However, research work is of a high level. The FAO consultant was extremely impressed with all the work carried out there, which included research on shoot-tip grafting, thermotherapy, tristeza indexing and stubborn.

Indexing for tristeza of satsuma trees budded on trifoliate rootstock has shown that 10 to 15 percent of all trees of this combination are infected with the virus.

A visit was made to the greenhouse dedicated to citrus virus-indexing work. There, seedlings of Mexican lime, Eureka lemon, sour orange, rough lemon as well as Etrog citron are available for a large indexing project. Etrog citron plants inoculated with Washington navel orange were seen to exhibit the typical symptoms induced by severe exocortis. However, most of the indexing work was discontinued a few years ago.

The work of shoot-tip grafting has produced young plants of Washington navel orange, satsuma mandarin, Encore mandarin, Freemont mandarin, Valencia orange and Yerli orange. All this extremely valuable material is now awaiting indexing to guarantee freedom from intracellular pathogens.

Studies with stubborn have confirmed the presence of the spiroplasmal agent in the citrus trees. The insect vector of stubborn, the beet leafhopper N. haematoceps, was found in the orchards, together with other leafhoppers. However, no insect transmission of stubborn resulted in the trials, as periwinkle (Catharanthus roseus) plants remained healthy in orchards contaminated with the disease. Similar results were also obtained by Bové and co-workers in the Syrian Arab Republic. It is now known from the work in Syria that very little or no natural transmission of S. citri occurs within adult orchards. For natural spread to be demonstrated the indicator periwinkle plants must be placed in young, newly planted orchards or in locations where N. haematoceps is known to occur, for instance near Salsola kali plants, known to be a favoured host plant of the leafhoppers.

No psyllid vectors of the greening organism are present in the citrus trees of the Adana region, an area with an estimated 14 million citrus trees.

The faculty is equipped with a modern laboratory prepared to perform ELISA testing that can be used for a tristeza-indexing project. Also, a growth chamber is available for biological indexing of tristeza virus. The consultant was informed that the government plans to establish a modern centre for virus indexing at the faculty in the near future.

Horticultural Research Centre, Mersin

A modern horticultural research centre (Alata Bahce Külturleri Arastirma ve Egitim Merkesi) is established at Erdemli, in Mersin. This centre has 200 ha of experimental fields plus another 200 ha dedicated to forestry. Out of 27 scientists working on various crops, four researchers are working on citrus.

Various citrus plots were visited at the centre. The first orchard was established with Freemont mandarin, a variety showing great promise. The centre recently sold about 5 000 trees of Freemont for commercial plantings.

Another orchard, established in sandy soil 500 m from the sea, included a collection of seedling trees of rootstock varieties. A third orchard was established with the best germ-plasm in the country. It included 14 lemon selections, two mandarins and one orange variety. This material was selected from the Mediterranean coastal area and was planted two years ago at the centre. The orange variety was a superior clone of Washington navel and the mandarins were satsuma and Clementine. Each variety is represented by seven trees budded on sour orange rootstock. Release of budwood from this future mother block will be made only when indexing for intracellular pathogens is completed. The mother block is a replication of that established at the Antalya Experiment Station.

Another plot at the centre is a collection of lemon types, selected for their resistance to mal secco disease. The trees are not yet six years old. Among the more resistant varieties is a local type named Molla Mehmet (Antalya Round).

The last citrus orchard visited at the centre was a collection of nucellar-line trees of various commercial varieties imported from California in 1975. Varieties included oranges, grapefruits and mandarins. Among the orange varieties were Carter, Bonanza and Gillette navel oranges as well as nucellar Frost Valencia orange. Severe symptoms of stub born were observed in many trees of the navel group. The Valencia orange trees were all healthy-looking with no stubborn symptoms. However, it was said that daughter trees in commercial orchards exhibit symptoms of the disease.


Control measures for stubborn

Control of stubborn disease is not an easy task. Bové (1966) pointed out that one can "live with" tristeza by replanting tolerant scion-rootstock combinations, but this is not the case with stubborn.

Sophisticated detection methods have been developed- for stubborn and are available for general use. Studies on the rate of field spread and identification of the pathogen vectors in each country will be very helpful to further understanding and control of the disease.

Stubborn is present in most Mediterranean countries, but fortunately the percentage of affected trees is generally low (about 5 percent) and growers are helping to reduce infection by eliminating diseased trees and avoiding propagation from infected orchards. The work under way at the Department of Plant Protection of the Faculty of Agricultural Sciences, in Adana, will certainly produce very valuable information for use in the control of the disease. Meanwhile, the following recommendations are made:

These recommendations are similar to those made to citrus growers in California, where stubborn is a serious problem.

Control of mal secco

Control measures used until now to combat mal secco disease of lemons are unsatisfactory. The fungus responsible for the disorder, Phoma tracheiphila - formerly known as Deuterophoma tracheiphila - is capable of infecting all citrus species and hybrids and closely related genera in the Rutaceae family. Eureka lemon, rough lemon, Rangpur lime, Bearss lime, sour orange and citron are very susceptible.

Fortunately, some citrus species have proved to have a high degree of resistance. These include sweet orange, Monachello and Santa Teresa lemons, Citrus volkameriana grapefruit and Palermo mandarin. Lapithos lemon, a lemon type grown in Cyprus, has been shown to be fairly resistant to the mal secco fungus.

The use of resistant lemon types in new plantings is the most convenient approach for the control of this disease. Deep cultivation, fertilization and other cultural practices that wound trees during the infection period should be avoided. Fallen leaves and trunk debris should be removed from the orchards and burnt to reduce inoculum. Diseased shoots and branches should be pruned during the summer to remove the organism and to prevent spread through the vascular system. Spraying with copper fungicides or benomyl during the infection period is another method of control. Mal secco is such a severely destructive disease in lemon orchards in the Mediterranean that it warrants a joint effort to develop control methods.

Other recommendations


Azeri, T. 1973. First report of satsuma dwarf virus disease on satsuma mandarins in Turkey. Plant Dis. Rep., 57: 149.

Bennett, C.W. & Taurisever, A. 1957. Sugar beet curly top disease in Turkey. Plant Dis. Rep., 41: 721-725.

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

Bové, J.M. 1985. Greening and Stubborn: Results and Perspectives. FAO Expert Consultation on Production, Maintenance and Distribution of Virus-Free Fruit Tree Planting Material. Rome, FAO. 37 pp.

Bové, J.M. 1986. Stubborn and its natural transmission in the Mediterranean area and the Near East. FAO Plant Prot. Bull., 34(1): 15-23.

Bové, J.M. & Vogel, R., eds. 1980. Description and illustration of virus and virus-like diseases of citrus. A collection of colour slides. Paris, IRFA SETCO-FRUITS.

Burke, J.H. 1965. Citrus industry of Turkey. USDA Foreign Agriculture Report, No. 127: 1-36.

Chapot, H. 1956. Une nouvelle maladie des agrumes dans le Moyen-Orient. C.R. Soc. Sci. Nat. Phys. Maroc., 22(6): 99-105.

Chapot, H. 1961. Impietratura in Mediterranean countries. In Proc. 2nd Conf IOCV, p. 177-181. Gainesville, Univ. Fla. Press.

Chapot, H. 1970. Les problèmes de la production des agrumes au Proche-Orient et en Afrique du Nord. UNDP/FAO Report AT 287. Rome, FAO. 93 pp.

Chapot, H. & Bahcecioglu, H. 1969. Some lemon culture troubles in Turkey. In H.D. Chapman, ed. Proc. Ist lnt. Citrus Symposium, p. 1279-1283. Riverside, Univ. Calif.

Childs, J.F.L., Bové, J.M., Calavan, E.C., Fraser, L.R., Knorr, L.C., Nour-Eldin, F., Salibe, A.A., Tanaka, S. & Weathers, L.G., eds. 1968. Indexing procedures for 15 virus diseases of citrus trees. USDA/ ARS Agric. Handhook 333. Washington, DC.

Fos, A., Bové, J.M., Lallemand, J., Saillard, C., Vignault, J.C., Ali, Y., Brun, P. & Vogel, R. 1986. La cicadelle Neoaliturus haematoceps (Mulsant & Rey) est vecteur de Spiroplasma citri en Mediterranée. Ann. Inst. Pasteur/Microbiol., 137A: 97-107.

Kersting, U. & Sengonca, C. 1992. Detection of insect vectors of the citrus stubborn disease pathogen Spiroplasma citri Saglio et al., in the citrus growing area of south Turkey. J. Appl. Entomol., 113: 356-364.

Moreira, S. 1965. Report to the Government of Turkey on Citrus Virus Diseases. FAO/UNDP Report No. 1982. 19 pp.

Norman, G.G. 1963. Report to the Government of Turkey on Citrus Virus Diseases. FAO/UNDP Report No. 1641. 19 pp.

Ozbek, N., Ozsman, M., Tuzcu, O. & Danisman, S. 1976. A preliminary study of rumple, a serious rind disorder of lemons in Turkey. In Proc. 7th Conf: IOCV, p. 157-166. Riverside, Univ. Calif.

Reichert, 1. 1959. A survey of citrus virus diseases in the Mediterranean area. In J.M. Wallace, ed. Citrus virus diseases, p. 23-28. Riverside, Div. Agric. Sci., Univ. Calif.

Salibe, A.A. 1986. Major virus and virus-like diseases of citrus in the Mediterranean. FAO Plant Prot. Bull. 34(1): 49-64.

Wallace, J.M. 1978. Virus and virus-like diseases. In The citrus industry, vol. IV, p. 67-184. Riverside, Div. Agric. Sci., Univ. Calif.


Chapter 24: The United Arab Emirates

Witches' broom disease of Lime
Virus and virus-like diseases
Citrus canker
Miscellaneous problems

After the discovery of greening disease and its psyllid vectors in Saudi Arabia and southern Yemen, a survey for greening was carried out in the United Arab Emirates (UAE) in 1983. Similarly, when witches' broom disease of lime (WBDL) became recognized as a major problem in small-fruited acid lime (Citrus aurantifolia) trees Oman, a search for WBDL was initiated in the UAE in 1987. Neither greening nor WBDL were encountered during the 1983 and 1987 surveys. However, symptoms resembling those of WBDL were seen in the UAE in 1989. Samples of witches' brooms were collected by Taher (FAO Regional Plant Protection Officer) in the UAE in 1990. They were analysed at Bordeaux and found to be infected with an MLO. This MLO was serologically identical to that associated with WBDL in Oman, demonstrating that WBDL is now also present in the UAE.

Another very serious disease of citrus was introduced into the UAE in the early 1980s citrus canker. This bacterial disease is also present in the Salalah area of Oman. A second focus of the disease was detected near Ibri but was eradicated in 1987.

Citrus has been introduced into various experiment stations or farms in the UAE, such as those at Hamraniyah, Dhaid, Fujairah and Kalba. Farmers grow primarily lemon and lime trees (650 ha), with other cultivars (sweet orange, mandarin) covering only 96 ha. Citrus represents 5 percent of total fruit production (65 000 tonnes). Dates amount to 80 percent and mangoes, with 10 percent, come second.

Witches' broom disease of Lime

The disease was first observed in 1989 in the Hatta and Bitna regions. By now (March 1993) the disease is present throughout the United Arab Emirates and has even reached the northern region. The affected areas include Dhaid, Kaber, Siji, Hatta, Daftah, Hamraniyah-Digdagga, Rul-Dhadna, Fujairah and Kalba.

Small-fruited acid lime is by far the major citrus species affected. While on his 1987 survey, Bové noticed not a single affected tree, in March 1993 he saw whole orchards fully destroyed by the disease. This indicates how fast the disease is spreading. The situation is now similar to that in Oman, and probably too advanced for an eradication programme to be effective. It is to be feared that all susceptible citrus trees will be wiped out within a few years.

While in Oman only acid lime trees are affected, in the UAE additional citrus species show the symptoms of the disease: citron, Palestine sweet lime and sweet limetta.

In the UAE, as in Oman, the leafhopper Hishimonus phycitis could be captured in great numbers on all acid lime trees tested, as well as on trees of the additional citrus species showing symptoms of the disease.

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