Virus and virus-like diseases: General conclusions

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In addition to tristeza and stubborn, eight other virus and virus-like diseases are present in Iran: cachexia, ring pattern (ringspot), woody gall, exocortis, impietratura, concave gum, scaly bark psorosis and cristacortis.

All of these diseases have been seen on citrus cultivars imported into Iran from abroad: tristeza on satsuma trees from Japan; stubborn, woody gall, impietratura and concave gum on many sweet orange varieties from California and probably Morocco; exocortis on sweet orange from Italy; and, on cultivars of Mediterranean origin, cristacortis on blood orange, cachexia on satsuma and ring pattern on Clementine.

Some of the diseases have also been seen on local citrus cultivars, including stubborn and ring pattern on local sweet orange, and cachexia and woody gall on local mandarin. However, in general, local cultivars - especially sweet oranges - seem to be little infected, probably for two reasons. First, prior to the introduction of "modern" citrus cultivars from abroad, citrus in Iran was propagated by seed, and hence was free of infectious diseases, since these diseases are not transmitted through seed. Second, most infectious diseases of citrus present in Iran are not naturally transmitted by insect vectors.

The diseases present in Iran for which natural transmission can occur are tristeza, stubborn and woody gall. Some natural transmission of tristeza virus has probably occurred recently in the Mahdasht orchard, where 55000 infected satsuma trees have been growing since 1968-70. The eradication of this orchard for phytosanitary reasons is most urgent.

There is clear-cut evidence that natural transmission of S. citri, the causal agent of stubborn disease, is occurring in Iran. The two major leafhopper vectors of S. citri, N. haematoceps and N. tenellus, have been reported in, or close to, the major citrus-growing areas, the former leafhopper being more widely distributed and more abundant than the latter. Some of the host plants of these leafhoppers, such as S. kali or A. camelorum, are extremely common in Iran.

There is little doubt that stubborn was brought into Iran from California and Morocco, though it was probably present in the country before this. The disease may have remained unnoticed because some of the local varieties may be less susceptible to stubborn than the imported varieties, such as navel oranges. There are, however, local sweet orange varieties in the Khafr region (Fars province) which express typical stubborn symptoms.

The pathogen of woody gall is transmitted by the same aphid species as those that propagate tristeza virus. In the Minab area at least, woody gall does not seem to be naturally transmitted.

The exocortis and cachexia viroids have no insect vectors, but humans can mechanically pass the agents from infected trees to healthy ones.

The presence of the pathogens of woody gall, impietratura and concave gum in certified citrus material introduced from California in 1963-64 and 1971 is surprising, as already discussed. Impietratura and concave gum affect Washington navel sweet orange trees from the 1963-64 introductions. Both diseases induce psorosis young leaf symptoms and could hardly have been missed when the Washington navel lines were indexed in California. Woody gall is present in at least three Valencia late sweet orange selections, Campbell, Frost and Olinda, and in two mandarins, Kinnow and Batangas. All five cultivars were introduced in 1971. While it cannot be excluded that indexing missed certain diseases in certain cultivars, as stated above, the possibility remains that some of the rootstock seedlings used for the propagation of the imported budwood were already infected by previous budding of infected buds that did not take, but were alive long enough to transmit their disease agent(s).

Iran decided to modernize its citrus industry in 1934. At that time the importance of virus and virus-like diseases was not known and the cultivars that were imported, essentially from Mediterranean countries, were probably infected by a number of infectious diseases. The first international meeting on virus diseases of citrus was held in 1957, in California, and stressed the importance of using citrus budwood material certified free of virus diseases. Iranian citrus scientists were well aware of these developments, and in 1963-64 they imported budwood from California because only California at that time was able to offer certified budwood. In 1971, more certified cultivars were introduced from California into Minab and Jiroft, and the Caspian Sea region. Today, the fact is that some of these cultivars turn out to be not only infected with naturally transmissible diseases such as stubborn, but also with diseases that are not naturally spread, such as impietratura and concave gum. This situation casts doubt on all the imported budwood.

However, the work carried out in Iran since 1963 remains very useful. It has been possible at the Kotra, Khorram Abad and Ramsar stations to evaluate the behaviour of the 1963-64 and 1971-72 citrus introductions with regard to their adaptation to the Caspian Sea conditions. Similar observations have been made at the Minab and Jiroft collections in the southern citrus belt. Efforts should be concentrated on those species, varieties or cultivars that have been shown to perform best in the various citrus-growing regions of the country. These cultivars could form the basis for renewed progress in citrus development in Iran. For total security, they could be submitted to shoot-tip grafting followed by indexing, and then used for foundation groves and mother tree orchards. At the present time, the citrus collections at Minab and Jiroft are so large that they do not receive the required attention. The new citrus programme should be conducted on a smaller scale, but with high standards, following the recommendations that have been made in order to eradicate tristeza and to keep stubborn disease at a reasonable level.

Other important, non-viral diseases

Phytophthora gummosis

Several cases of gummosis were encountered during the survey. The usual causes of gummosis are poor horticultural practices, in particular: the tendency to plant trees too deep, with the bud-union line too close to the soil or even buried; low budding; or use of phytophthora-sensitive rootstocks such as acid lime or the Bakravi hybrid. With appropriate cultural methods, gummosis should not be a problem.

According to Banihashemi (1983), it appears that Phytophthora nicotianae var. parasitica (PNP) is predominant in hot areas and Phytophthora citrophthora (PC) in temperate regions. PC was isolated from soil collected in Darab, Jahrom, Kazerun, Shiraz, Khafr (Fars province), and also in Jiroft (Kerman province), the latter by Mansoori. PNP was isolated from samples collected in Hormozgan province and in Jiroft.

Salt injury

In the southern citrus belt, irrigation water carries high levels of salts, and the soil pH can be as high as 8.5. Severe leaf symptoms of boron excess (see Figs 255 to 257) and lithium excess were observed at the Isin Citrus Station (Hormozgan province) - where all citrus is on sour orange rootstock - and of chloride excess at the Minab Station (Hormozgan province), where many trees are on acid lime rootstock. Lime tolerates soils with high pH and has the reputation of being more drought-resistant than sour orange. However, Cleopatra mandarin is more salt-tolerant than acid lime.

Reuther (1976) has also pointed out that, at the Minab Experiment Station, all varieties showed salt toxicity symptoms. Water for this station comes from several deep wells which have a high salt content (electrical conductivity x 106 ranging from 1 320 to 3 250) with 43-57 percent sodium. The least-saline well is marginal and the others too saline for economic citrus production.

Autumn blast

Autumn blast refers to twigs that suddenly die and dry up in situ (Figs 252 to 254), with gum material conspicuous on parts of the stem (Fig. 253). The dry leaves do not fall off. There is a clear-cut margin between the upper, brownish, dead bark of the stem of the dried-up twig and the lower bark that is green and alive. This twig dieback appears on the uppermost part of the canopy, though in severe cases lower branches show dead twigs too. The symptoms start around mid-October. Mandarin and Clementine trees are most susceptible, followed by sweet orange and grapefruit trees. Lemon trees are much less affected and sour orange trees never. Bové observed a similar affliction in the Libyan Arab Jamahiriya in 1974 and in Iraq in October 1985. In Florida, "firing" resembles autumn blast. Obviously, the disorder is less of a problem in more temperate climates.

The cause of autumn blast is not known. It is probably not due to parasitic microorganisms or pests, but seems rather to reflect the failure of the terminal twigs to secure sufficient moisture and water. Factors that could be responsible for insufficient water supply in the autumn in Iran are the wide temperature difference between day and night, or the relatively low soil temperatures that contrast with high air temperatures in the day. These temperature differences might induce twig dieback, especially if the root system is inadequate because of poor cultivation, root injury, attack by fungi such as Phytophthora spp., unbalanced water supply, etc.

The threat of witches' broom disease of Lime

Witches' broom disease is a new MLO disease which has already killed a large proportion of the lime trees in Oman, where 22 percent of all lime trees are affected. The disease is spreading and had reached the United Arab Emirates in 1989. It represents a very serious threat for the lime orchards in the southern parts of Iran. Quarantine measures must be strictly reinforced so as to keep the disease out of Iran (see also Chapter 16).


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Ghorbani, S. 1983. Detection of citrus tristeza virus in its aphid vectors in northern Iran by immunosorbent electron microscopy. In Proc. 7th Plant Prot. Cong of Iran, p. 8. Karaj, Iran, College of Agric., Univ. Teheran.

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Minassian, V. 1983a. A survey of citrus tristeza virus (CTV) in Mazandaran using ELISA method. In Proc. 7th Plant Prot. Cong of Iran, p. 78. Karaj, Iran, College of Agric., Univ. Teheran.

Minassian, V. 1983b. Use of enzyme-linked immunosorbent assay (ELISA) for detection of citrus tristeza virus (CTV) in aphids from the north of Iran. In Proc. 7th Plant Prot. Cong. of Iran, p. 82. Karaj, Iran, College of Agric., Univ. Teheran.

Minassian, V. & Ghorbani, S. 1983. Further studies on citrus tristeza virus (CTV) in the Caspian region in Iran. In Proc. 7th Plant Prot. Cong. of Iran, p. 77. Karaj, Iran, College of Agric., Univ. Teheran.

Nielson, M.W. 1975. The leafhopper vectors of phytopathogenic viruses (Homoptera, Cicadellidae): taxonomy, biology and virus transmission. USDA/ ARS Tech. Bull. No. 1382 AC.

Norman, P.A. & Grant, T.J. 1956. Transmission of tristeza virus by aphids in Florida. Proc. Fla. Hort. Soc., 38-42.

Planes, S. & Marti, F. 1972. Leaf variegation with ringspots. In Proc. 5th Conf. IOCV, p. 194-196. Gainesville, Univ. Fla. Press.

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Rahimian, H. 1983. Distribution and symptoms of citrus stubborn disease in the southeast of Iran. In Proc. 7th Plant Prot. Cong of Iran, p. 74. Karaj, Iran, College of Agric., Univ. Teheran.

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Roistacher, C.N., Nauer, E.M., Kishaba, A. & Calavan, E.C. 1980. Transmission of citrus tristeza virus by Aphis gossypii reflecting changes in virus transmissibility in California. In Proc. 8th Conf: IOCV p. 76-82. Riverside, Univ. Calif.

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Saillard, C. & Bové, J.M. 1983. Application of ELISA to spiroplasma detection and classification. In S. Razin & J.G. Tully, eds. Methods in mycoplasmology, p. 471-476. New York, Academic Press.

Timmer, L.W. & Garnsey, S.M. 1980. Natural spread of citrus ringspot virus in Texas and its association with psorosis-like diseases in Florida and Texas. In Proc. 8th Conf: IOCV, p. 167-173. Riverside, Univ. Calif.

Vogel, R. & Bové, J.M. 1980. Citrus ringspot in Corsica. In Proc. 8th Conf: IOCV, p. 180-182. Riverside, Univ. Calif.

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Chapter 12: Iraq

Virus and virus-like diseases in Iraq
Obsolete horticultural practices and phytophthora gummosis
Diseases of unknown cause
Genetic problems

Citrus in Iraq is grown almost entirely under date-palms (Fig. 156), whose shade is intended to protect against high temperatures and solar radiation in the summer. Protection against frost in the winter is provided by the retention of warm air. Indeed, the climate in central Iraq where citrus is grown is continental and arid, characterized by extreme heat in summer, the threat of frost in winter (normal monthly temperatures: 35°C in July and 10°C in January, with mean monthly maxima of 43°C and 4°C in July and January respectively) and low rainfall (150 mm per year).

Citrus is grown in alluvial soil and located mainly in central Iraq, north and south of Baghdad, along the banks of the River Tigris and its tributary, the River Diyala, as well as along the River Euphrates, north and south of Kerbala.

There are about 2.5 million trees in production, of which 90 percent are sweet orange. Practically all sweet oranges are the local Mahali (common) variety, a seedy, midseason fruit. In the 1960s, the Zafarania Experiment Station imported cultivars of the better-known citrus varieties, such as Washington navel and Valencia late sweet oranges, Eureka and Lisbon lemons, mandarins, Clementines, etc. Yields of the Mahali sweet orange trees are generally extremely low because of obsolete cultural practices, phytophthora gummosis and competition from date-palms and other interspersed fruit trees.

Within the framework of an Agricultural Development Project (the Khalis project), the French Institute for Research on Citrus and Tropical Fruits (IRFA) was asked to take over citrus development in Iraq. This assignment lasted from 1979 to 1982. During that period, many citrus cultivars from Corsica (free from virus and virus-like diseases) were introduced and propagated in the nursery. For reasons other than technical ones, this project was forced to come to a standstill, and the new cultivars have not yet been made available to growers.

Virus and virus-like diseases in Iraq


Cachexia-xyloporosis, which is caused by a viroid, is by far the most noticeable of all virus and virus-like diseases of citrus in Iraq. It was seen on many more trees than any other virus-like disease and was found in every one of the areas surveyed. In the orchards the disease was seen on mandarin and Clementine trees. These are susceptible varieties and they show the typical symptoms of the disease: gum in the bark and stem pitting in the wood with corresponding pegs on the inner face of the bark.

Cachexia-xyloporosis has also been identified in the experimental plots at the Zafarania Experiment Station, on trees of local (Indian) mandarin, Clementine and tangelo.

Cachexia could be identified in so many of Iraq's orchards because the mandarin and Clementine trees that are grown everywhere are susceptible varieties on which the symptoms can be observed. Sweet lime and Rangpur lime, two rootstock species, are also susceptible.

In contrast, orange and lemon trees, which come first and second in importance in Iraq, are species that are tolerant of cachexia: they show no symptoms of the disease, even when they carry the pathogen. Visual observation of such species will not reveal the presence of the agent; only indexing on indicator plants (Parson's Special mandarin: see Figs 58 and 59) or using sPAGE (see Table 13, p. 47) will provide confirmation.

Mild and severe strains of the cachexia agent are known, and the severe strains can be destructive. A severe strain was detected in the Fahama area on a declining local mandarin tree, where the cachexia-induced stem pitting on the trunk could still be seen at a height of 50 cm above the bud-union.

Gummy bark

The symptoms of gummy bark are very similar to those of cachexia, but the two diseases are unrelated. In the case of cachexia, the susceptible varieties are mandarin, Clementine, tangelo, satsuma, sweet lime and Rangpur lime. Gummy bark affects none of these species, but does affect sweet orange and rough lemon, which are cachexia-tolerant (see Table 7, p. 25). Gummy bark symptoms were observed on sweet orange in the Dorah and Mansourya areas.

The indicator plant for indexing gummy bark is sweet orange on sour orange or rough lemon rootstock.


Cristacortis affects sweet orange, tangelo, mandarin, Clementine, grapefruit and sour orange. It is one of the very few diseases which show up on sour orange trunks, branches or shoots. Typical symptoms were observed at Zafarania on a Clementine tree grafted on sour orange rootstock. The tree was also affected by cachexia.

Concave gum-blind pocket

Mild symptoms of this disease were seen on local mandarin trees observed at Zafarania and in the Fahama area. Old Clementine trees in the Mansourya area also showed mild deformations possibly due to the disease. Indexing should be carried out to confirm the presence of the agent. One must also look for psorosis young leaf symptoms on young leaves produced during cool seasons - early spring or late autumn.

Scaly bark psorosis (psorosis A)

Severe bark scaling was observed at Zafarania on grapefruit trees. Psorosis A bark scaling affects the outer part of the bark - under the scales, bark remains alive (whereas with phytophthora gummosis, bark is killed) and appears green when scratched with a knife. As in the case of concave gum and cristacortis, psorosis young leaf symptoms should be looked for in early spring or late autumn.


Clear-cut symptoms of exocortis, a viroid disease, were observed at Zafarania on various species.

Local (Abaichy) citron (Figs 88 and 89). Other nearby citrons did not show symptoms of the disease. Therefore, the possibility exists that the affected citron was mechanically contaminated from nearby old-line Eureka lemon trees showing pronounced symptoms of shell bark (a non-transmissible genetic problem see the section on genetic problems below). Indeed, it is known that almost all old-line Eureka lemon trees carry the exocortis viroid but show no symptoms because they are tolerant. However, shell bark seems to be enhanced by the exocortis viroid.

Lisbon lemon on Rangpur lime rootstock (Fig. 85). Bark scaling affects only the Rangpur lime rootstock - there are no symptoms on the tolerant lemon scion. It was, however, the lemon bud that carried the viroid and contaminated the rootstock on which it was grafted. The viroid is now present in the whole tree, but symptoms appear only on the susceptible part, in this case the rootstock. This tree also had phytophthora gummosis.

Troyer citrange on Cleopatra mandarin rootstock, top-worked with Duncan grapefruit (Fig. 86). The Troyer citrange trunk is present as a "sandwich" between the Cleopatra mandarin roots and the grapefruit top. Exocortis was very probably introduced with the grapefruit bud and has induced symptoms on the Troyer citrange, the only susceptible species of the three component parts of the tree.

Some years ago, Troyer citrange was officially recommended as a rootstock in government nurseries. Results have been very poor, which is not surprising. Troyer citrange is an exocortis-susceptible rootstock and therefore can only be used with exocortis-free budwood. Such budwood was not available in Iraq at the time. Also, unfortunately, nurseries give no consideration to the use of virus-free budwood. While the use of infected budwood is probably one of the main reasons for the poor results given by Troyer citrange, other reasons, such as alkalinity and salinity, could also be involved.

From the above examples, it should be clear that exocortis symptoms can only be seen on susceptible species or varieties which are mainly used as rootstocks. In their absence, exocortis cannot be detected by visual observation.

Since commercial citrus orchards in Iraq are mainly grafted on the exocortis-tolerant sour orange rootstock or not grafted at all, symptoms of exocortis cannot be seen in Iraq plantings, except in those rare cases where a susceptible stock is used. One such case was seen in the Fahama area - a grapefruit tree probably grafted on citron, as the consultant was informed. Citron is a mono-embryonic species. All citron seedlings are hybrids since they result from the development of a sexual embryo. The various citron hybrids have different degrees of susceptibility to exocortis, but many express symptoms. This was the case here, where typical exocortis symptoms (bark scaling and cracks) affected the rootstock (probably citron) of the grapefruit tree.

Obsolete horticultural practices and phytophthora gummosis

Trees planted too deep

On removing the soil around the trunk of declining trees it was found that many of them were planted much too deep. On certain farms, the crown was I m below soil level. Often, with budded trees, the bud-union line was well below soil level. In one orchard all the declining or dead trees were planted too deep, with the bud-union below soil level.

Trees planted too deep decline for two main reasons. First, being too far from the soil surface, the roots do not receive enough oxygen, and this lack is aggravated by excess humidity. Lack of oxygen and high humidity adversely affect the functioning of the roots, and the effect is physiological rather than pathological. Second, lack of oxygen and high humidity favour invasion by Phytophthora spp., which may cause feeder root decay and rot. This is a pathological effect.

Inadequate irrigation systems

The traditional one-furrow irrigation system, as it is practiced on Iraqi citrus farms, is certainly one of the main reasons for the abnormally poor yields obtained (20 kg per tree). Trees are planted on both sides of the furrow, or on one side only. The furrow meanders through the orchard, turning it into a labyrinth. Mechanical maintenance is impossible. Water is unevenly supplied as there is too much water on the furrow side of the tree, inducing root asphyxiation, and too little water on the other side. Water stress increases the "June" drop of young fruits. Trees often end up halfway down the side of the furrow; then, to "protect" the trees from water, soil is put around the trunk. All these factors favour phytophthora gummosis. The farmland between adjacent furrows is useless and wasted as it is not watered and no fertilizer can be applied.

Phytophthora gummosis

During the surveys, phytophthora gummosis was seen everywhere and every day. It is the most severe and destructive disease on traditional Iraqi citrus farms, and is primarily due to poor horticultural practices.

Where trees that are very susceptible to phytophthora are not grafted, but propagated from cuttings, as is the case with sweet and acid lemons, planting the susceptible lemon cuttings directly in the soil will provide an excellent host for the soil-borne fungi - hence phytophthora root rot, decay of fibrous roots, and foot and crown root rot. High humidity and lack of oxygen favour the decay. Where cuttings of phytophthora-susceptible varieties, such as sweet or sour lemon, are used as root-stocks, the situation is the same as above.

Many trees are, however, grafted on phytophthora-resistant rootstocks, such as sour orange, but the protective effect of the resistant rootstock is lost because the trees are planted too deep, with the bud-union line below soil level (Fig. 228); or soil is put around the trunk, when the irrigation furrows are cleaned (Fig. 226) or to "protect" the trunk from flood irrigation; or the sour orange seedling is budded too low, thus producing a tree with a bud-union line too close to the soil.

With virus, viroid and mycoplasma diseases, protection lies in using clean budwood and controlling the insect vectors. With phytophthora, protection lies essentially in the choice of resistant rootstocks and in adequate horticultural practices, both in the nursery and the orchard, in order to preserve the benefit obtained from these rootstocks.

Competition from date-palms

The palm trees on traditional Iraqi citrus farms are intended to protect against heat in the summer and frost in the winter, to form windbreaks and to maintain some humidity in the air in summer. However, the palm trees interfere with mechanical maintenance, compete for food and deprive the citrus trees of light. There are a few successful "open" orchards without date-palms. During the 1985 survey, an open sweet orange orchard at the Citrus Experiment Station at Rachidiya was visited. The orchard had several rows of Shamouti sweet orange trees which were being compared with Mahali local sweet orange trees. The local trees had far fewer sunburn marks on leaves and fruits than the Shamouti trees, where sunburn lesions were severe. This indicates that there are differences between varieties regarding heat tolerance, and it should therefore be possible to breed for the characteristic.


Citrus stubborn disease is one of the major problems in modern citriculture, since most commercial varieties can be affected. A considerable amount of work has been devoted to the disease in Iraq by the Bordeaux group.

Proof of the disease in Iraq: early work

During his first survey of the country's citrus orchards for virus and virus-like diseases in June-July 1978, Bové suspected that stubborn disease was present in Iraq. However, as the survey was carried out in early summer, no suitable fruit was available to be used for the isolation and culture of Spiroplasma citri, the causal mycoplasma of the disease. Fruit material to assess the presence of stubborn in Iraq was necessary as some of the more typical symptoms, as known elsewhere, were rare For instance, the small cupped leaves, so characteristic of stubborn-infected trees, were rarely seen.

The first Mahali sweet orange fruit samples from Iraq to be analysed in Bordeaux were those collected by Al-Beldawi in early March 1979. S. citri was cultured from the samples. This result was the first unquestionable proof of the presence of stubborn disease in Iraq.

The consultant visited Iraq for the second time in February 1980, a period of the year when fruit was still available. In the Kerbala area, he again surveyed an orchard where stubborn disease had been suspected in the 1978 survey. Severe fruit symptoms could now be observed on sweet orange, namely small-sized fruits with many aborted seeds (Fig. 168). Abnormal shoots could also be seen on these trees. A few shoots had the typical small, cupped leaves. Many more shoots, from the previous autumn flush of growth, were characterized by peculiar leaves with some of the following symptoms: pinched-in tips, pale green to yellow tips and/or margins, ovoid leaves with short midribs, and lateral veins running parallel to midrib (palmate leaves).

Fruit was collected from these sweet orange trees and analysed for S. citri infection in Bordeaux. At the same time, fruit collected in the Abou Dali, Beled and Tarmia areas was also taken to Bordeaux for analysis. S. citri infection was assessed by culture of the causal mycoplasma and by ELISA carried out on the seeds and the fruit axes (columella). Out of a total of 20 fruit samples, 17 were positive for S. citri infection by culture and/or ELISA. S. citri cultures were obtained with fruit from the Beled, Kerbala and Tarmia areas, and the two samples from Abou Dali were positive by ELISA. Hence, the results from the February 1980 analyses amply confirmed the presence of stubborn disease in Iraq.

Finally, on a visit to Iraq in April 1981, Bové visited the Aboud El Neimi orchard in the Rachidiya area. Several Mahali sweet orange trees were abnormal (Fig. 157). Fruits on these trees were small in size, often lopsided, and contained many aborted seeds. Fruit samples from three trees were taken to Bordeaux for S. citri culture. A fourth sample of small lopsided sweet oranges was taken from boxes of picked fruit. All samples were positive for S. citri.

With these results, there was no doubt by 1981 that stubborn disease was present in Iraq and that certain orchards, in the Kerbala area for instance, contained a high percentage of infected trees.

January 1982 survey

Diagnosis of stubborn in the orchard. Fifteen orchards were surveyed for the presence of stubborn-infected trees in the Fahama, Rachidiya, Abou Dali and Houwesh areas, along the left bank of the Tigris, north of Baghdad.

The diagnosis of stubborn on the basis of symptoms is a difficult task, and this is particularly true in Iraq where the situation is complicated by the fact that the bunchy type of growth and the small, cupped leaves, so typical of stubborn trees in open orchards, were only rarely seen. However, three other types of symptoms helped to diagnose stubborn in Mahali sweet orange trees in the date-palm-shaded orchards of Iraq in the winter period. The constant isolation of S. citri from trees with these symptoms shows their value for stubborn diagnosis in Iraq in winter.

As mentioned above, the first symptom concerns the fruits. Stubbon-affected trees stand out from normal trees because of the small size of much of their fruit, which is often lopsided and contains many aborted seeds (Fig. 168). Acorn-shaped fruits can also be seen (see Fig. 165).

The second useful symptom is the presence of a few abnormal shoots on trees that have been identified on the basis of their small fruits. These shoots stick out from the top of the tree, or sometimes from the sides, in a somewhat sucker-like fashion. They bear various types of rather small, pale green leaves: ovoid with short midrib, palmate, with pinched-in tips and yellow tips and margins (Figs 160 to 163). The abnormal shoots sometimes, but not always, have short internodes (Fig. 163).

The third symptom is leaf mottle (Fig. 158). It affects relatively well-developed, mature leaves. Trees with such leaves are of a pale green colour (Fig. 157). Some trees have all three types of symptoms, but some have only fruit symptoms without the abnormal shoots and leaf mottle.

Detection of S. citri. Fruit samples were taken from 27 trees showing one or more of the above symptoms. For each fruit sample, two tissues were used, the seeds and the columellae. Two assay methods (culture and ELISA) were applied to both the seeds and the columellae. Hence, four assays were performed on each fruit sample. A total of 27 stubborn-infected trees and seven trees with dubious symptoms were analysed.

All 27 trees showing Iraqi stubborn symptoms gave positive assays. Nineteen (70 percent) had all four assays positive, while six (22 percent) had three positive assays. These results show that the majority of trees (90 percent) give either three or four positive assays. Seeds were somewhat superior to columellae for the culture assay since 28 S. citri cultures were obtained from the seeds and 22 from the columellae. The two fruit tissues were equally good for ELISA.

Among the seven dubious trees, four were negative by both the culture assay and ELISA. However, one was positive by culture and ELISA (tree 7) and two by culture only (trees 12 and 29). This brings the total number of S. citri-infected trees to 27+3=30.

Stubborn in the Fahama, Rachidiya, Abou Dali and Houwesh areas. On the basis of these results, it was found that every one of the 15 Mahali sweet orange orchards that were surveyed in January 1982 contained one or several trees that were infected by S. citri. Hence, stubborn disease is spread throughout the areas surveyed.

However, the majority of orchards (ten) had only a few stubborn-infected trees scattered among many normal trees. Five orchards had a higher percentage of stubborn-infected trees, four of these are located in the Rachidiya area and one in the Abou Dali area. One orchard in the Rachidiya area had up to 50 percent infected trees.

October 1985 survey

The 1985 survey made it possible to distinguish clearly between leaf symptoms due to excessive heat and those due to stubborn. As shown by Reuther, Nauer and Roistacher (1979), the effect of high temperatures (38°C by day and 28°C by night) on citrus in growth chambers resulted in reduced leaf size, blunting of the leaf tip, and even more striking modifications in shape such as leaves with lateral veins almost parallel to a much reduced midrib (cordate or palmate leaf). Reuther observed a high frequency of such leaves on certain shoots in almost all commercial orchards in the hottest citrus region of Iran.

On a visit to Iran in November 1985, Bové frequently noted such heat-affected leaves. Similar leaves were also present on sweet orange trees in Iraq, but more often in open than in shaded orchards. However, two types of shoots with palmate leaves could be distinguished in Iraq as well as in Iran: shoots with uniformly green leaves with or without short internodes (Figs 160 to 162) and shoots bearing leaves with yellow tips or margins (see Fig. 155), the tips often being pinched in (Figs 160 to 162). Internodes can be short (Fig. 163) or normal.

A search for S. citri in trees with these shoots showed that the trees with only uniformly green leaves were free of S. citri, but that trees with yellow-tipped leaves were infected with S. citri. These results clearly indicate that stubborn alone is not responsible for the leaf modification that results in cordate-shaped, palmate leaves, but that such leaves, when infected with S. citri, acquire yellow tips and margins, with the yellow portion sometimes extending over half of the leaf.

As stated above, the palmate leaves with yellow tips or margins are often carried by sucker-like shoots sticking out from the top or the side of the trees and such trees are often characterized by small fruits with aborted seeds. In the shaded Mahali sweet orange orchards in Iraq, small fruits with aborted seeds and shoots with yellow-tipped leaves, with or without short internodes, are diagnostic of stubborn.

The situation

The surveys of June-July 1978, January 1982 and October 1985, and the extended fruit analyses carried out in March 1979, February 1980, April 1981, January-February 1982 and October 1985, prove that citrus stubborn disease is present in Iraq in the following areas: Kerbala, El Dorah, Fahama, Rachidiya, Abou Dali, Houwesh, Beled and Tarmia. Other areas have not been investigated.

The majority of stubborn-affected sweet orange trees are of the local Mahali variety. In the general absence of other varieties, it is very probable that stubborn disease in Iraq was not introduced from abroad with the importation of foreign cultivars. Here we are undoubtedly faced with genuine "old world" stubborn.

This is in contrast with countries such as Iran, Morocco, the Syrian Arab Republic and Turkey, where at least some of the stubborn-affected trees result from the propagation of infected budwood introduced from places such as California.

Vectors of S. citri in Iraq

In October 1986, two members of the Bordeaux group, Fos and Vignault, carried out a survey for the presence of the leafhopper Neoaliturus haematoceps in the following citrus-growing areas of central Iraq: Baghdad, Baquba, Dorah, Kerbala and Tarmia. The leafhopper was found in the Baghdad, Kerbala and Dorah areas. In most cases, the insect was collected on Salsola kali, a wild Chenopodiacea, known to be a favoured host of N. haematoceps as well as of Neoaliturus tenellus. Wherever S. kali was sampled, N. haematoceps was found. Other host plants on which the insect was detected are Alhagi persarum and Atriplex spp. S. citri could be cultured from two N. haematoceps samples collected in the Baghdad area on S. kali plants growing along a paved road. N. tenellus was not encountered even though S. kali, a favoured host, was abundant in the areas examined. The leafhopper has however been reported in Iraq (Aziz and Al-Ali, 1977). As in most other countries surveyed, it seems that N. haematoceps is more common than N. tenellus.

These results demonstrate that N. haematoceps, the major vector of S. citri in the Mediterranean area and the Near East, (Fos et a/., 1986) as well as S kali, the major host plant of the leafhopper, occur in central Iraq. S. citri could be cultured from field-collected N. haematoceps samples, showing that the leafhopper can be naturally infected with the spiroplasma.

The effect of date-palms on natural transmission of S. citri in citrus orchards is not known. Even though stubborn-infected trees can be found in many shaded orchards, their proportion is generally low. This would indicate that the palm trees somehow provide protection against natural transmission of S. citri. It is to be feared that the incidence of transmission could be higher in open, unshaded orchards, especially when the trees are young. Although there is little doubt that modern citriculture in Iraq should turn to open orchards, natural transmission of S. citri by leafhoppers must not be overlooked, and measures to prevent it must be taken.

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