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Surveys for virus and virus-like diseases of citrus were conducted between 1 9X I and 1990 in the following countries of the Near East region: Algeria, Cyprus, Egypt, the Islamic Republic of Iran, Iraq, Jordan, the Libyan Arab Jamahiriya, Morocco, Oman, Pakistan, Saudi Arabia, Somalia, the Sudan, the Syrian Arab Republic, Tunisia, Turkey, the United Arab Emirates and Yemen. Data from additional surveys in 1991, 1992 and 1993 and from recent laboratory work in Bordeaux have been used to update the previous surveys.
The geographical distribution of citrus diseases in the countries of this region, as well as other countries of the world, is summarized in the Annex Table. The following diseases are present in most, if not all, countries of the Near East: cachexia-xyloporosis, concave gum-blind pocket, exocortis and scaly bark psorosis. Gummy bark and impietratura were seen in many countries of the region and especially those of the Mediterranean basin. These diseases are not transmitted by insect vectors and can be eliminated, by shoot-tip grafting, for instance. There is no reason for them to be seen in new orchards in the future.
Symptoms of stubborn and/or the presence of Spiroplasma citri, the stubborn agent, were detected in all countries of the region, except Pakistan. The leafhopper Neoaliturus (syn. Circulifer) haematoceps has been identified as a major vector of S. citri in the Near East. In certain countries such as Iran and Morocco, the closely related species, Neoaliturus tenellus, a vector of the stubborn agent in California, was also encountered. Salsola kali (tumbleweed, Russian thistle), a plant of the Chenopodiaceae family, is the preferred host of the two leafhopper species. The distribution of these leafhoppers follows that of S. kali, which itself is widely distributed throughout most of the region, from Morocco to Iran. In the Syrian Arab Republic, the high percentage of stubborn-affected trees in young mother trees of a newly established nursery could be correlated with the presence of S. kali and N. haematoceps within and around the nursery.
The occurrence of S. kali must be taken into account when new citrus nurseries or orchards are to be established. Its presence favours the development of high populations of the two S. citri vectors and, hence, abnormally high transmission rates of the stubborn spiroplasma can be obtained.
Sesamum indicum is another important plant. In the Adana region of Turkey, sesamum is infected with S. citri. N. haematoceps leafhoppers collected on sesamum fields were infected with S. citri and these naturally infected leafhoppers were shown to transmit the spiroplasma to healthy plants.
Another major result of the surveys was the discovery of greening disease in the southwestern part of the Arabian Peninsula, involving both Saudi Arabia and Yemen. The Asian form of greening and the Asian citrus psyllid vector, Diaphorina citri, are present in Saudi Arabia from Jeddah, in the north of the affected region, to Abha in the south. The African form of greening and the African citrus psyllid vector, Trioza erytreae, are present both in Saudi Arabia and Yemen, and extend from Ta'izz in the south of Yemen to Abha in Saudi Arabia. In the Abha area the two psyllid vectors of the greening agent have been observed in the same orchards. D. citri has probably been introduced from Asia into the Mecca area and has moved southwards until, in 1983, it reached the Abha area. T. erytreae has probably entered Yemen from Ethiopia and has progressed from south to north, entering Saudi Arabia and overlapping with D. citri in the Abha area. After Reunion, Mauritius and Saint Helena islands, the Abha area is only the fourth region in the world where the two vectors of greening occur together. In Saudi Arabia, Asian greening, the more severe form of the disease, is responsible for the decline and disappearance of practically all sweet orange and mandarin trees, and, in the affected areas, only small-fruited acid lime trees survive as they are less susceptible to greening. In addition, lime is the citrus host on which the two psyllid vectors prefer to feed. The numerous greening-affected lime trees are thus as many host plants on which the feeding psyllids become infected with the disease agent. This situation explains why there is such a high rate of transmission of the greening agent in Saudi Arabia. In Yemen, the form of greening present is the African form. African greening and the African psyllid, ;T. erytreae, are sensitive to heat and occur only in relatively cool regions. This is why African greening and T. erytreae in Yemen and Saudi Arabia are present only at altitudes above 1 000 m and do not occur on the coastal plains.
The surveys have also revealed that African greening is present in the northwestern part of Somalia, near Hargeisa. This is not surprising as the disease and T. erytreae are present in neighbouring areas of Ethiopia. However, the greening-affected trees in the Hargeisa area were found to be infected with citrus tristeza virus as well. This lends weight to the idea that the trees might have been imported from Kenya, where both tristeza and greening are endemic.
Greening and the Asian citrus psyllid vector are present in Pakistan. The disease is probably the cause of the decline that has been affecting sweet orange and mandarin trees for many years. Except for Ethiopia, the Hargeisa region of Somalia and the southwestern pan of the Arabian Peninsula, no countries west of Pakistan in the Near East region are as yet affected by greening. Iran, Iraq and the Mediterranean countries are still free of the disease and its two psyllid vectors. Greening remains, however, a major threat to these countries. The recent development of DNA probes for the detection of the greening BLO in plants and insects will undoubtedly help to prevent greening from entering these countries.
A new, lethal disease of lime has been discovered in the Sultanate of Oman: witches' broom disease of lime trees (WBDL). The causal agent of the disease is an MLO. WBDL is the first MLO disease of citrus. The disease is spreading fast and had reached the United Arab Emirates in 1989. An insect vector is probably involved in the transmission of the MLO. The leafhopper Hishimonus phycitis has been found on all lime trees tested in Oman and the United Arab Emirates. Its role as a vector of the WBDL MLO is being studied, especially in the light of the fact that the same leafhopper is known as the vector of an MLO disease in India - eggplant little leaf disease. Spread and development of WBDL may be connected to the recent introduction of H. phycitis from India to the Arabian Peninsula. In 1987 over 20 percent of all lime trees were already affected by WDBL in Oman. Death of the tree occurs within five years of the appearance of the first witches' broom. Whether citrus species other than lime can become infected in nature is not yet known. Troyer citrange was infected experimentally and found to be susceptible. MAs and DNA probes have been developed and will make it possible to identify the insect vector. WBDL represents a major threat to lime and perhaps other citrus species in the Arabian Peninsula, the Persian Gulf countries, including Iran, and other citrus areas.
Tristeza is widespread throughout Asia and Southeast Asia where the aphid Toxoptera citricida is an efficient vector. The tristeza virus and T. citricida are present in the Indian subcontinent. In Pakistan the virus was detected in the Peshawar area and several parts of the Punjab. In these areas, T. citricida is not present. However, Aphis gossypii, Myzus persicae and other aphid species known to be vectors of tristeza virus are present in Pakistan.
In Iran, tristeza virus was introduced at Mahdasht, near Sari. in the Caspian Sea area, with the importation of thousands of satsuma trees from Japan. As the trees are grafted on Poncirus trifoliata, they are tolerant of tristeza and show no signs of disease. This is probably why it has not yet been possible to obtain the eradication of these trees, even though they represent a threat of utmost importance to the whole citrus industry along the Caspian Sea, as sour orange is the only citrus rootstock used there. The 1985 survey showed that only very limited spread of tristeza had occurred. The low level of natural transmission is probably due to the fact that T. citricida is absent. Toxoptera aurantii and Aphis citricola are the predominant aphid species in the Caspian Sea area.
Tristeza is spreading and has caused considerable damage in Spain and Israel, even though the most efficient vector, T. citricida, is not present. Other aphid species, such as A. gossypii and A. citricola, are responsible for the spread. This shows that even in the absence of T. citricida, tristeza virus can be transmitted by less efficient species. This is the reason why tristeza-affected trees should be eradicated even in areas where apparently no spread of the virus has yet been observed. Such areas are those of Turkey in the Izmir region and the Black Sea coast, where quite numerous tristeza-infected satsuma trees occur. These trees are grafted on P. trifoliata and are thus tolerant of tristeza. Only ELISA offers a quick technique to detect the infected trees, and these trees must be eradicated. A similar situation exists in the former Yugoslavia and probably in Albania along the Adriatic coast. Italy also has tristeza-infected trees with no apparent spread of the virus. To repeat, these situations are dangerous, as tristeza decline may eventually sweep through these orchards as it has done in Spain and Israel.
The agent of vein enation-woody gall is transmitted by the same leafhoppers that spread tristeza virus - T. citricida, A. gossypii, A. citricola, etc. Except fore few cases in Iran, symptoms of this disease were not seen, as the usual scion-rootstock combinations are tolerant of this virus. It is however very possible that many trees harbour the pathogen. In Spain, indexing has shown this to be the case. It even seems that the vein enation-woody gall virus is more effectively spread by A. gossypii or A. citricola than is tristeza virus, since the former virus is transmitted in a persistent manner and the latter in a semi-persistent way (see Table 11). This means that, once infected with the vein enation virus, the aphid will remain viruliferous for a long period, while in the case of tristeza the retention period could be shorter, possibly only two to three weeks.
A virus disease not encountered in the surveys is that of tatterleaf-citrange stunt, again because most scion-rootstock combinations seen are tolerant of this virus. It is present to a significant extent in China. Indexing, on Rusk citrange, for instance, is required to determine the incidence of the virus in the Near East region.
Many cases of bud-union crease were observed during the surveys. Not all cases of this disorder are due to viruses. In one case at least, a graft-transmissible pathogen seems to be involved in the Near East region: the case of sweet orange trees on rough lemon rootstock when they are infected by the gummy bark agent. It has been revealed that gummy bark is much more widespread and a much more serious disease than was previously thought. It could be of a viroid nature and should be easily eliminated by shoot-tip grafting. While the agents of cachexia and gummy bark induce bark gumming and stem pitting respectively in mandarin and sweet orange, Kassala disease, discovered during the survey in the Sudan, produces similar symptoms in grapefruit. The disease was encountered also in southern Yemen. It, too, could be of a viroid nature.
Horticultural practices are generally poor in most of the countries surveyed. Trees are planted too deep in the soil, in depressions rather than on heaps, and rootstocks are budded too low. All this results in trees having their bud-union line close to, or buried in, the soil. This is the major cause of phytophthora gummosis, the most frequently observed disease in the Near East region. Other fungal diseases are Rio Grande gummosis, especially severe in Somalia, and mal secco which is affecting many trees in the Mediterranean area.
Citrus canker, a bacterial disease known to be present in the Indian subcontinent, has unfortunately appeared in Oman, Saudi Arabia, the United Arab Emirates and Yemen. It is very unfortunate that the disease was not promptly eradicated in these countries. There is still some hope that it can be eradicated in the Salalah area of Oman.
Movement of citrus plants must be controlled by all means possible so as to avoid, for instance, the introduction of tristeza virus and citrus canker into Oman, with plants imported irresponsibly from India by incompetent nurseries. Bové was able to spot such a consignment of plants, infected with both tristeza and canker, within 48 hours of their release from customs. Had these trees not been destroyed immediately, the lime orchards of Oman would have begun to die not only from WBDL, but also from tristeza and canker. This shows how important it is to control importation of citrus plants and to establish effective quarantine control measures.
It is hoped that the information presented in this review will result in increased production and better-quality citrus fruit.
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