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Production of nucellar lines

According to information given by Dr Mohamed El Shourbagy, former director of the Citrus Division, the production and selection of nucellar lines was initiated in 1964. First plantings were made in 1975 and 1976 and the work of selection is still going on.

A mother block of nucellar trees of commercial varieties was visited at the Horticultural Research Institute in Giza. Nucellar varieties were Valencia, Washington navel and blood oranges and grapefruit. One of the Washington navel trees in the block, when inspected by Salibe, showed typical symptoms of stubborn disease. Since Washington navel orange is considered to be one of the varieties more susceptible to stubborn disease, insect transmission may have been responsible for the infection of this tree.

A visit was also made to a commercial orchard consisting of a block of about 1 000 trees of nucellar Washington navel orange and nucellar Balady mandarin. Trees were very vigorous and productive but very thorny. Stubborn symptoms were found in a number of the Washington navel orange trees.

Citrus nurseries in Egypt are private and produce a large number of budded plants for replacement and planting of new orchards.

According to available information, there is also a fairly high export of budded plants to neighbouring countries. A visit was made to a few small nurseries and, while young trees were of a fairly high standard, they were said to be produced with budwood taken from unselected mother trees. This means that Egypt is unwittingly exporting virus-infected plants.

Horticultural Research Institute

The Horticultural Research Institute is located in Orman, Giza, on the outskirts of Cairo. It is divided into several research divisions, which deal with citrus, grapes and deciduous fruit, among others. Research work is conducted both at the institute and at six experiment stations in the agricultural areas of the country. According to available information, about 30 researchers work on the various aspects of citrus production in the institute and its experiment stations. The researchers are of an outstandingly high standard, but the laboratories of the institute need new equipment and the library is badly in need of more up-to-date books and other publications.

A fairly large collection of citrus is maintained at the institute, composed of varieties of commercial and potential value, with all trees budded on sour orange rootstock. Mixed in the orchard are trees of nucellar lines and of old clones, a few of which show symptoms indicative of various pathogens.

According to available information, 130 superior trees of commercial varieties plus 11 introductions of nucellar varieties are being tested by the institute as candidates for certification.

Barrage Horticultural Experiment Station

At Barrage the River Nile splits into channels to form the delta. Citrus orchards are concentrated in this area and all over the fertile soil of the delta. The Barrage Horticultural Experiment Station is dedicated to research work with fruits, vegetables, flowers and medicinal plants. Ample and intensive work with citron is being carried out there.

The Station has a large germplasm collection which is about 20 years old, containing local and imported varieties of citrus. Symptoms of psorosis, cachexia-xyloporosis and tristeza were observed in a few trees of this plot. A new collection of citrus varieties, imported as nucellar lines from Florida and California, is being prepared for planting in the field. It will include, in a first phase, 11 varieties budded on rough lemon Citrus jambhiri Lush. and sour orange rootstocks. Indexing of this imported material for tristeza virus has given negative results.

Rootstock experiments and a block of mother trees used to produce seeds of rootstock varieties were also visited at the station. The general impression was that Egypt has an advanced programme of citrus research but that the benefit of acquired knowledge is not reaching growers.

Visit to the Faculty of Agriculture, Al Azhar University

Egypt has 12 universities, of which four are in Cairo, namely, Cairo University, Ein-Shams University, Al Azhar University and Helwan University. A visit was made to the Faculty of Agriculture of Al Azhar University, Nasr City, where a large citrus research programme is being conducted to study the performance of various rootstock varieties under the environmental conditions prevailing in the Nile River delta area. This project is partially supported by USAID funds. The faculty has a modern laboratory for micrografting and tissue culture that can be used for freeing citrus varieties from virus and virus-like pathogens.

Integrated protection programme for citrus improvement

It is evident that virus and virus-like diseases are limiting yields in Egyptian citrus orchards, perhaps by as much as 10 or 20 percent overall, and much more severely in certain orchards. During past decades, the area under citrus has expanded considerably and the trend has been to plant fewer varieties, concentrated in larger areas of more or less continuous orchards. These conditions favour rapid spread of virus and other diseases, particularly when insanitary mass-propagation techniques are used to produce nursery trees. It is clear that the problem, if not contained, will grow steadily worse. There are no known methods for freeing trees in commercial orchards from virus and virus-like pathogens, as viruses are generic parasites for which no remedy has yet been found. The use of disease-free budwood for new plantings and the imposition of stringent regulations to limit movement, sale and use of infected budwood or nursery plants are the principal measures for controlling these pathogens. The use of virus-free propagative materials also helps to prevent or limit damage from diseases that have insect vectors, provided that natural spread is limited or absent, as in the case of tristeza and stubborn disease in Egypt. Appropriate quarantine, detection and suppression measures for the exclusion of unwanted pathogens and their vectors must be integrated into the protection programme.

Quarantine and eradication measures

Citrus trees are not native to any country of the Mediterranean basin. They were brought into the region from their origins in Southeast Asia and the Malayan archipelago. Many, but not all, major pests and diseases were imported through early plant introductions. For this reason, strict quarantine regulations are vital to prevent further undesirable parasites from entering the citrus-growing areas of Egypt. It is well known that in all important citrus-producing areas of the world there is a constant interest in new and better varieties and stocks of the genus Citrus, and that a more or less continuous flow of plant introductions is occurring everywhere. Government agencies should import new, desirable varieties, using modern laboratory techniques to preclude diseases and pests, before it is done by unskilled people. In the event that any unwanted pest or pathogen is introduced into Egypt, plant pathologists and entomologists should be prepared to identify the problem and start proper action for immediate eradication before dispersal within the citrus area occurs. Special attention should be given to the exclusion and suppression of the agents of three diseases that can completely wipe out the citrus industry of any country. These are greening, tristeza-seedling yellows and citrus canker. Citrus decline (blight of Florida, declinio of Brazil, marchitamiento repenting of Uruguay and fruta bolita of Argentina), a disease of unknown nature but suspected to be caused by a virus, should also be prevented from entering the country.

The threat of greening disease. Greening is one of the most destructive diseases affecting citrus. It was first reported long ago in mainland China, where it was called yellow-shoot disease (Lin, 1956). Apparently, from there it moved to neighbouring countries and received local names: likubin in Taiwan Province, vein-phloem degeneration in Indonesia, leaf mottling in the Philippines and citrus decline in India. The vector of the causal agent (an intracellular bacterium) was determined to be the psyllid Diaphorina citri in the Southeast Asian countries. The disease also appeared in South Africa where it was named greening disease and where it is spread by another psyllid, Trioza erytreae. Scientists have recently reached the conclusion that the greening bacterium and its two known vectors are moving towards the Mediterranean citrus countries. Pakistan, Saudi Arabia and Thailand have already been invaded by the Asiatic greening bacterium and by the vector D. citri. At the same time, the South African greening bacterium and its vector, T. erytreae, have spread to eastern Africa, Ethiopia, Madagascar, Mauritius, Reunion, northern Yemen and Zimbabwe, and may eventually reach the citrus orchards of northern Africa. The entire citrus industry of all the Mediterranean countries is now menaced by greening disease.

Citrus canker. Citrus canker was introduced into Australia, Florida and South Africa and was eradicated through great efforts and expense, after it had become well established. This disease should be excluded from Egypt by all available means.

Tristeza. Practically all Egyptian citrus is on sour orange rootstock and this situation makes it extremely vulnerable to destruction by tristeza virus. The situation is very similar 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, diffusion of tristeza in the orchards of the region would result from:

Stubborn disease. A great effort has already been made to eliminate this disease from Egypt. According to Nour-Eldin (1959), the major source of the mycoplasma, the sweet orange variety Safargali, was prohibited by law from being propagated in the country. Additional efforts to identify infected trees and eradicate them may completely suppress the disease in Egypt. However, the threat remains permanent, since favourable conditions may occur which would allow the buildup of high populations of the leafhopper vectors of the spiroplasma. Studies of the biology of N. tenellus and N. haematoceps, the two major leafhopper vectors of S. citri present in Egypt, should be initiated to obtain better knowledge of transmission and to develop strategies to control the problem. Non-rutaceous hosts of S. citri should be identified as they are most probably the sources of S. citri inoculum on which the leafhoppers become infected with the spiroplasma.

Citrus budwood certification programme

A well-planned citrus budwood certification programme was launched in Egypt in 1981. Nearly 200 candidate trees were selected and placed under test for registration as mother trees. No additional information has been made available regarding the progress of the programme. According to Nour-Eldin (1959), a citrus budwood certification programme was started in Egypt as early as 1955, when budwood was obtained from old seedling trees (Balady sweet orange, Sukkary orange and Balady mandarin) and propagated on sour orange rootstock.

Propagations were also made from a navel nucellar seedling tree. Progenies of these nucellar lines were examined and found to be free from psorosis. From there, "it will be a matter of organizing the distribution of virus-free budwood" (Nour-Eldin, 1959). At the time, no mention was made of trials to compare old-line and nucellar line trees. Nucellars are not necessarily identical to parent trees and may differ among themselves. Certain varieties have a periclinal chimerical nature (such as Thompson and Burgundy grapefruit) and they do not produce nucellars of the new varieties but that of the original variety (Cameron, Soost and Olson, 1964; Olson, Carpenter and Soost, 1966). Virus-free bud-wood of these varieties must be obtained through micrografting.


An integrated protection programme is outlined here as a contribution to the maintenance of the wealth that the citrus industry generates for Egypt. The country has the scientific knowledge and the human resources to develop an intensive programme to protect existing citrus orchards from new diseases and to pursue measures to increase crop yields. It is a matter of coordinating the efforts of Egyptian scientists towards a major aim that will benefit the citrus growers and consequently help to improve the economy of the country.

The recommendations for measures to be taken to integrate the protection programme are as follows:


Bar-Joseph, M. & Loebenstein, B. 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. 8.th 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 Phytopharmacy, Marseilles (France), 1965, updated for the 4th Conf. IOCV. 44 pp. (mimeo)

Bové, J.M. & Vogel, R. 1975. Description and illustration of virus and virus-like diseases of citrus: an IOCV project. Institut Français de Recherches Fruitières Outre-Mer. Paris, Editions SETCO.

Calavan, E.C. & Carpenter, J.B. 1965. Stubborn disease of citrus trees retards growth, impairs quality and decreases yields. Calif: Citrog, 50(3): 86-87, 96, 98-99.

Cameron, J.W., Soost, R.K. & Olson, E.O. 1964. Chimeral basis for colour in pink and red grapefruit. J. Hered., 55(1): 23-28.

Childs, J.F.L., Nour-Eldin, F., Jacob, K. & El-Hosseiny, N. 1955. A report to the Egyptian Ministry of Agriculture on the survey of citrus diseases in Egypt. Ministry of Agriculture.

Childs, J.F.L., Nour-Eldin, F., Jacob, K. & El-Hosseiny, N. 1956. Observations on Egyptian citrus diseases. Citrus Ind., 47(10): 11-16.

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. Washington, DC, USDA/ARS Agriculture Handbook 333.

Fawcett, H.S. 1931. Observations on citrus conditions in Mediterranean countries. IV. Egypt. Calif. Citrog., 16: 339-340.

Frazier, N.W. 1953. A survey of the Mediterranean region for the beet leafhopper. J. Econ. Entomol., 46: 551-554.

Knorr, L.C. 1961. Virus diseases of citrus. Report to the Government of the United Arab Republic. Report No. 1432. 45 pp.

Lin, K.H. 1956. Observations on yellow shoot of citrus: aetiological studies of yellow shoot of citrus. Acta Phytopathologica Sinica, 2: 1-42.

Nour-Eldin, F. 1956. Phloem discoloration of sweet orange. Phytopathol., 46: 238239.

Nour-Eldin, F. 1959. Citrus virus disease research in Egypt. In J.M. Wallace, ed. Citrus virus diseases, p. 219-227. Berkeley, Div. Agric. Sci., Univ. Calif.

Nour-Eldin, F. 1967. A tumor-inducing agent associated with citrus trees infected with safargali (stubborn) disease in the United Arab Republic. Phytopathol., 57: 108-113.

Nour-Eldin, F. & Bishay, F. 1958. Presence of the tristeza virus disease in Egypt. FAO Plant Prot. Bull., 6(10): 153- 154.

Nour-Eldin, F. & Childs, J.F.L. 1957. Sweet orange bark pitting, an unreliable symptom of tristeza infection. Plant. Dis. Rep., 41(12): 1011-1013.

Olson, E.O., Carpenter, J.W. & Soost, R.K. 1966. The Burgundy sport: further evidence of the chimera! nature of pigmented grapefruits. Hort. Sci., 1(2): 65-67.

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.

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

Wolff, J. 1977. Medium-term prospects for world citrus production. Proc. Int. Soc. Citricult., 2: 328-332.


Chapter 11: The Islamic Republic of Iran

Introduction of new citrus species and varieties
Incidence of virus and virus-like diseases
Other virus and virus-like diseases
Virus and virus-like diseases: General conclusions
Other important, non-viral diseases
The threat of witches' broom disease of Lime

Citrus has a long history in the Islamic Republic of Iran. Citron was the first citrus fruit to be cultivated in the country, some 2 500 years ago, in the times of the Median empire. Sour orange, lemon and small-fruited lime were spread throughout the Near East and Persia by the Arabs around AD 1000. Sweet orange, called "Portugal" in many Arab countries as well as in Iran, reached the Persian Gulf ports with Portuguese trade vessels during the crusades. Later, around 1500, when Vasco da Gama opened up the direct sea route from India to Portugal around the Cape of Good Hope, many citrus species were undoubtedly introduced from India. In more recent times, the former Union of Soviet Socialist Republics, especially the Black Sea ports (Suchumi, Batumi), were also sources for citrus introductions.

Fortunately, for many centuries, these varieties have been propagated by seed. Since most virus and virus-like diseases are not transmitted by seed from parent to progeny, this method of propagation has kept some of the major virus and virus-like diseases out of Iran for many years. This probably explains why, for instance, tristeza virus and its most efficient vector, Toxoptera citricida Kirk, have not become established in Iran through the propagation of budwood on trees from India while they have in South Africa.

There are three major citrus regions in Iran (see Map 2 on p. 70 and Map 6). The Caspian Sea belt (Mazandaran and Gilan provinces 26 000 ha) extends over 400 km from east to west, and lies between the shore of the Caspian Sea (29 m below sea level) and the first slopes of the Elburz mountain range (150 m see Map 6). Average annual rainfall is I 000 mm, with a dry period in June and July. Winter temperatures every year reach -1°C, and, every four to five years, -7°C with heavy snowfall (I m). Summer temperatures are much lower than in other citrus regions, but high enough for symptom expression of stubborn.

The percentage of the various citrus varieties grown is as follows: seedy local sweet orange seedling trees, 55 percent; seedy local sweet orange trees grafted on sour orange rootstock, 20 percent; Washington navel, Thompson navel and blood oranges, all on sour orange, 5 percent; satsuma, Clementine and local tangerine, all on sour orange, 15 percent; and others, 5 percent.

It should be pointed out that sour orange is the only commercial rootstock used. In particular, satsumas are grafted on sour orange, not on Poncirus trifoliata.

Citrus orchards of the southern inland belt (36 000 ha) are scattered through the low valleys of the southern Zagros mountain range, essentially in the provinces of Khuzestan, Fars and Kerman (see Map 6: citrus areas around Dezful and Ahwaz, Kazerun, Jahrom, Darab, Minab, Jiroft, Bam, Shadad). The main characteristics of these areas are low annual rainfall (100-300 mm) and excessive heat in summer. In Khuzestan (Ahwaz, Dezful), citrus is grown under higher temperatures than in any other commercial citrus-growing area, the maximum daily temperatures ranging from 44° to 48°C between 15 June and 15 August. In the Jiroft area (Kerman province), the average monthly maximum temperature is close to 43°C in June, July and August. The high summer temperatures have been thought to simulate symptoms of stubborn (Cochran and Samadi, 1976).

MAP 6 The principal citrus-growing areas of the Islamic Republic of Iran

The main citrus species and varieties are seedy local sweet orange trees on sour orange, Bakravi or lemon rootstocks, 52.5 percent; small-fruited acid seedling trees, 28.7 percent; seedy local tangerine trees on Bakravi or lemon rootstock, l 1.6 percent; Palestine sweet lime cutting trees, 10.4 percent; and others, 2.X percent.

Bakravi is said to be a local natural hybrid between mandarin (Citrus reticulata Blanco) and small-fruited acid lime (Citrus aurantifolia Christm.).

About 6 000 ha of citrus are spread along the coasts of the Persian Gulf and the Gulf of Oman (southern coastal belt). The climate is tropical with no frost, and well suited to acid lime, sweet lime and lemon. Acid lime represents 90 percent of production. Salinity of water and high pH are the limiting factors.

In conclusion, in the two major citrus areas of Iran, the Caspian Sea belt and the southern inland belt, local sweet orange is predominant; acid lime dominates the coastal belt and is second in the inland belt; satsumas, Clementines and local tangerines are second in the Caspian Sea area.

Until 1918 there was no real "citrus industry" and all citrus varieties were propagated through seed. The heavy losses to footrot prompted growers to use the phytophthora-resistant sour orange rootstock, but seedling sweet orange trees still constitute 70 percent of all orange trees in the Caspian Sea area. Acid lime tolerates a high pH (8.5) and is more resistant to drought than sour orange, and so is often used as rootstock in the southern citrus areas.

Local cultivars still predominate, in spite of the many introductions that have been made since 1933.

Introduction of new citrus species and varieties

As part of the economic development of Iran, new citrus species and varieties were introduced for the first time into the Caspian Sea area (Ramsar) in 1933 from Turkey, Italy, Lebanon and the country then known as Palestine (Ebrahimi, 1975). The varieties imported were Willowleaf, Owari satsuma and Clementine mandarin; Marsh seedless and Duncan grapefruit; Thompson navel, Bouroukain, Jaffa, Shamouti, Italian and Dwarf Chinotto orange; Grosse Sanguine and Moro blood oranges; and variegated sour orange. At that time no attention was paid to the presence or absence of virus diseases.

In 1944, grapefruit budwood was sent from Ramsar to Ahwaz (Khuzestan province) and this was the beginning of a grapefruit industry in southern Iran.

In February 1962, a countrywide frost killed thousands of citrus trees. Minimum temperatures reached - 13°C in Ramsar (Mazandaran province), -6°C in Ahwaz (Khuzestan province), -7.5°C in Bam (Kerman province) and -8°C in Darab and Jahrom (Fars province). To rehabilitate the Iranian citrus industry, 700 000 certified buds were imported in 1963-64 from the Willits and Newcomb nursery in California and distributed among the various citrus experiment stations in the country, in particular the Kotra station in the Caspian Sea region. The imported varieties were Washington navel, Frost navel, Gillette navel and Parent navel orange; Frost Valencia, Olinda Valencia and Campbell Valencia orange; Algerian, Dancy and Frost Dancy tangerine; Fortune mandarin; Shambar, Redblush and Red grapefruit; Orlando and Minneola tangelo; Frost Eureka, Cook Eureka, Allen Eureka and Frost Lisbon lemon.

Additional varieties were introduced into Ramsar (Mazandaran province): in 1969 Emperor tangerine from Australia and Ishikawa and Sugiyama satsumas from Japan, and in 1971 - Salustiana, Hamlin and Marrs early sweet oranges from Willits and New-comb, California, and Wase satsuma and Cadoux Clementine from Morocco. At that time, Morocco could not certify that its citrus was virus-free.

In 1971, a large collection of citrus was established by Chapot at the Jiroft Development Organization (Kerman province) and at the Minab Experiment Station (Hormozgan province). The certified budwood came from Willits and Newcomb nursery in California and comprised 48 varieties, with 50 to 100 buds for each. The varieties were Frost navel, Parent navel, Atwood early, Skaggs bonanza, Marrs early, Salustiana, Hamlin, Pineapple, Parson Brown, Moro blood, Tarocco, Frost Valencia, Olinda Valencia and Campbell Valencia sweet oranges; Robinson, Osceola, Lee, Fortune, Fairchild, Fremont, Kinnow, Wilking, Kara (satsuma x king), Batangas, Honey, Ponkan, Dancy and Murcott mandarins; Temple tangor; Minneola, Orlando and Seminole tangelos; Wekiwa tangelo (tangelo x grapefruit); Frost Marsh, J.B.C. Marsh, Shambar, Redblush and Red grapefruits; Eustio limequats; Bouquet de fleurs sour orange; Nagamim kumquat; and Santarosa, Frost Lisbon, Caver's Lisbon, Limoneira Lisbon, Cascade Eureka, Frost Eureka and Allen Eureka lemons.

The collection at Jiroft was completed in 1972, when Chapot introduced another group of 28 varieties from the Souheila Experiment Station near Marrakech, Morocco. Budwood of the Moroccan varieties was not certified. The varieties were: Cadoux Clementine; Wase satsuma; Murcott, Ortanique, Carvaihal and Kinnow mandarin; Taroudan and South African sour lime; Lyddengurgh sweet lime; sweet lemon; Thornless common lime; Tunis sweet and Millsweet limetta; Limonette de Marrakech; Tavares limequat; Hairy, No. 103, No. 57 and Pink seedless Shaddock; Burneo lemon; Bergamot; Grasse Bouquetier, Double-flowered Bouquetier, soft-fruited Bouquetier, Granit and large-flowered Bouquetier sour orange; Dalaman navel orange and Cadenera orange.

The Caspian Sea citrus stations also hold the 1971 -72 introductions.

In 1967, a period of bad frost caused severe damage to citrus in the Caspian Sea region. In the Mahdasht area near Sari, an orchard owned by the royal family lost many trees, except the more cold-resistant satsuma trees. Since there were not enough local satsuma trees available, the royal family imported 40 000 trees from Japan in 1968 and 15 000 more in 1970. Tristeza virus being endemic in Japan, it could be predicted that each one of the 55 000 Japanese satsuma trees was infected with tristeza virus.

These trees were grafted on P. trifoliata, a rootstock tolerant of the virus and commonly used in Japan. Hence, the 55 000 Japanese trees have grown well since, but they are responsible for the introduction of tristeza virus into Iran.

In conclusion it can be said that well over 100 citrus species, varieties and cultivars were imported into Iran between 1933 and 1977. Citrus material imported from Egypt, India, Italy, Lebanon, Morocco, Palestine, Turkey and the former USSR was probably infected with one or more virus and virus-like pathogens, since these countries had no facilities for producing budwood certified free of pathogens. Only citrus imported in 1963-64 and 1971-72 from California was certified free of known diseases. It must however be recognized that, at that time, indexing techniques for stubborn disease were not satisfactory. In addition, it is now known that Spiroplasma citri, the agent of stubborn disease, is naturally transmitted by leafhoppers. For these reasons, budwood infected with S. citri could have been introduced from California. There is also a strong possibility that stubborn was already present in Iran prior to these introductions.

Finally, the 55 000 satsuma trees imported from Japan in 1968-70, all of which were probably infected with tristeza virus, are so many swords of Damocles suspended over Iran's citrus industry.

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