Virus and virus-like diseases
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Severe symptoms of cachexia-xyloporosis were observed on the Citrus macrophylla rootstocks of stunted Jaffa (Figs 299 to 301) and Balady sweet orange trees at the Hamraniyah Experiment Station. In addition to cachexia symptoms, the Balady sweet orange scions showed symptoms of gummy bark above the bud-union line.
Balady and Jaffa sweet orange trees on C. macrophylla turn out to be good indicator plants for cachexia detection in the field. The infected (but tolerant) sweet orange buds were grafted on healthy (but susceptible) C. macrophylla rootstock seedlings, and the symptoms subsequently showed up on the rootstock.
Similarly, exocortis can be detected in the field when exocortis-tolerant scions (sweet orange, mandarin, grapefruit, lemon or lime) are grafted on susceptible rootstock such as Poncirus trifoliata, citranges, Rangpur lime or citron. This is particularly the case at the Hamraniyah Experiment Station where bark-scaling symptoms of exocortis were observed on the Carrizo citrange rootstocks of old-line Jaffa sweet orange trees. It is very likely that many more old-line citrus cultivars are infected with the exocortis viroid(s) in the UAE than elsewhere in the world.
The above old-line Jaffa sweet orange trees were part of a rootstock experiment. But an old-line cultivar of unknown health status should never be used for rootstock experiments. This is well illustrated here where the Jaffa sweet orange trees on C macrophylla developed cachexia, and those on Carrizo citrange, exocortis. The experiment is worthless as a rootstock trial, but useful to demonstrate that the old-line Jaffa sweet orange cultivar is infected with the viroids of cachexia and exocortis.
At the Dibba Fruit Farm, many Balady sweet orange trees showed typical symptoms of bud-union crease of the type shown in Figure 135, with gum in the bark and a line of necrotic wood at the bud-union.
Symptoms of stubborn were observed on Washington navel sweet orange trees at the Fujairah Experiment Station, in the Hossein Bin Rahama orchard (Kalba area) where the trees were of Syrian origin, at the Hamraniyah Experiment Station, and on Balady sweet orange trees in the Masafi area. Symptoms included palmate leaves with yellow, pinched-in tips (Fig. 302), fruits with aborted seeds and/or thin albedo at the stylar end and thick albedo at the peduncular end (Figs 303 and 304).
No efforts were made to isolate Spiroplasma citri, the causal agent of stubborn, from the symptomatic sweet orange trees. However, the spiroplasma could be seen by electron microscopy in the leaves of a symptomatic periwinkle (Catharanthus roseus) plant (Fig. 305) collected in an ornamental periwinkle bed in Dubai harbour. Infection of periwinkle plants indicates that natural transmission of the spiroplasma occurs. The leafhoppers Neoaliturus haematoceps and Neoaliturus tenellus are the major vectors of S. citri. Their principal host plant is Salsola kali (Chenopodiaceae). This plant occurs along the seashores of the UAE, and it is important to determine whether it harbours the two leafhoppers.
WBDL is caused by an MLO (Bové et al., 1988; Garnier, Zreik and Bové, 1991). As stated above, the disease was restricted to Oman until 1989 when its symptoms were observed for the first time in the UAE. Taher collected lime shoots from witches' brooms at the Ibrahim Abdul Rahman and Naser Mukhtar farms in the Fujairah area, the Mohamed Salem El Rayes farm and another farm in the Hatta area. All four samples contained an MLO, as found by electron microscopy, and gave strongly positive reactions when examined by immunofluorescence using WBDL-MLO specific MAs. Leaves from normal lime trees gave negative reactions.
These results show that WBDL is no longer restricted to Oman but has now appeared in the UAE, not only along the coast at Fujairah immediately north of the area where WBDL is most severe in Oman, but also inland in the Hatta area, again immediately north of the border. In view of the rapid spread of WBDL in Oman, it is to be expected that other regions in the UAE will soon show signs of the disease. The vector of the disease in both countries must be determined as soon as possible.
The witches' brooms of WBDL are highly typical (see Fig. 140). Another type of witches' broom was occasionally observed, not only in the UAE (Fig. 306) but also in Oman, and it should not be confused with WBDL witches' brooms. While a WBDL-affected lime tree shows progressively more and more witches' brooms, trees with a witches' broom of the type shown in Figure 306 seem to carry only one such witches' broom' and when it is removed they do not produce new ones. The cause of this type of witches' broom is not known, but it does not seem to be infectious. Still other types of witches' brooms exist, such as those induced by the fungus Sphaeropsis tumefaciens Hedges in Yemen. Stubborn affected trees may also develop witches' brooms, but these are not as typical as those of WBDL.
No symptoms of greening were seen in the orchards surveyed. Only one suspect case was encountered in the Hamraniyah Experiment Station in Kinnow and Feutrell mandarin trees imported from Pakistan in 1979. A decline apparently caused by the greening bacterium affects citrus, including mandarin, in Pakistan. As citrus tristeza virus (CTV) has also been detected in several trees in Pakistan, it is not advisable to introduce citrus from that country.
At the Hamraniyah Experiment Station, the Kinnow mandarin trees were in a severe state of decline (Fig. 307) and the Feutrell mandarin trees were less affected. It was advised that all the trees of Pakistani origin be eliminated.
Lime trees are very susceptible to tristeza and are excellent indicator plants for CTV detection. They show specific vein clearing and characteristic stem pitting. None of these symptoms were observed on the many lime trees surveyed. This indicates that no spread of CTV has occurred in the UAE, even though some of the disease's aphid vectors are present in the country, namely, Aphis gossypii, Aphis.spiraecola and Myzus persicae. The most efficient aphid vector of CTV, Toxoptera citricida, is absent from the UAE. However, under certain circumstances A. gossypii, which is present, can be a fairly efficient vector. Tristeza must be kept out of the UAE by reinforcing restrictions on citrus importations from abroad. Introduction of CTV through citrus material and its subsequent spread by aphid vectors would be highly detrimental to the major citrus cultivar grown in the UAE - lime. The disease would also affect all trees grafted on sour orange rootstock.
Citrus canker is a serious disorder. It produces lesions on leaves, twigs and fruit. The causal agent is the bacterium Xanthomonas campestris pv. citri. Several pathotypes of the bacterium are known. Pathotype A (Asiatic canker) affects essentially lime and grapefruit. This is the type present in the UAE as well as in Oman. The first symptoms in the UAE were observed in 1984 in the Dhaid area. Twenty-seven farms were affected, with a total of 5 000 trees, of which 200 showed canker lesions. The trees were not eradicated, but pruned to remove affected parts and sprayed with copper oxychloride. In the Masafi area, three- to four-year-old seedling lime trees were also affected; they were pulled out and burnt. At Kayathi (Abu Dhabi Emirate) and Ahwir (Dubai Emirate) canker lesions were seen on mandarin. The trees were pruned and sprayed.
No lesions of citrus canker were seen during the 1987 survey, indicating that control of the disease by pruning and spray treatments with copper oxychloride three times a year (in February, March and April) is relatively efficient. It is, however, unfortunate that no efforts were made to eradicate the disease when it first appeared in 1984.
More than 10 000 lime trees from private nurseries in the Masafi area are sold each year to Oman. Despite phytosanitary certificates, canker could be introduced to Oman with these trees and thus represents a serious threat to the, as yet, canker-free lime industry in the Tihama.
At the Hamraniyah Experiment Station, mal secco-like symptoms, first noted in the early 1980s, affect Eureka lemon trees on Citrus volkameriana rootstock (Fig. 308). The lemon line comes from California. The cause of this disorder was not discovered. Shoots lose their leaves and show dieback only at the tip. There is a clear-cut borderline between the dead brownish bark of the dieback-affected shoot tip and the still live green bark. In the case of mal secco there is no such distinct zone between dead and live bark. Leaves show necrotic zones (Fig. 309) from which Alternaria spp. can be isolated. The shoots also have a rubbery consistency. In India, Ahlawat (personal communication) has described rubbery wood on lemon trees as a new MLO disease.
Several cases of severe sunburn were observed at the Hamraniyah Experiment Station on fruit of Orlando tangelo, Marsh and Ruby blood (Fig. 310) grapefruits, Lisbon lemon and citron, and on leaves of Balady and Jaffa sweet oranges. [Ed. note At the same station cases of Rio Grande gummosis were observed in March 1993.]
Sweet orange shoots with palmate or cordate leaves, caused by excessive heat, were observed in several cases. When in addition such leaves show yellowish tips (Fig. 302), infection with the stubborn agent must be suspected.
Two diseases present in the UAE are of major concern: WBDL and citrus canker. The first symptoms of WBDL were seen in the UAE only in 1989. [Ed. note. In February 1993 the disease had reached catastrophic proportions in all regions of the UAE.] It is to be expected that the number of affected trees will increase over the coming years. Control of the disease must be based on control of its putative insect vectors, leafhoppers or psyllids. Identification of the vectors must receive first priority, not only in the UAE, but also in Oman.
Regarding citrus canker, it is now too late for eradication of the disease agent, and control of the bacterium must be maintained by spraying programmes.
Diseases such as cachexia, exocortis and gummy bark, which have no insect vectors, can be excluded from new citrus orchards by using only citrus budwood certified free of infectious diseases, and by avoiding mechanical transmission by pruning tools.
Stubborn disease is present in the UAE. Natural transmission of the causal agent, S. citri, occurs, as periwinkle plants infected with the spiroplasma have been found in nature, but at this time the importance of S. citri transmission to citrus remains unknown. A search for the two major leafhopper vectors of S. citri, N. haematoceps and N. tenellus, especially on their preferred host plant' S. kali, should be initiated. Identification of the vector of WBDL and a search for S. citri leafhopper vectors could be part of the same programme.
Greening and its two psyllid vectors are not present in the UAE. They do, however' occur in southwestern Saudi Arabia and in northern Yemen. No foci of tristeza have been found in the UAE, or elsewhere in the Arabian Peninsula, even though aphid vectors of tristeza virus occur in the region. It is essential to keep greening and tristeza out of the UAE. This implies rigid restrictions on the importation of citrus plant material from areas where the diseases are known to be present, such as
Pakistan, India and Asia in general. Movement of citrus material between the UAE and Oman should be rigidly restricted. Citrus canker could be introduced with nursery trees from the UAE into the as yet canker-free Tihama region of Oman. Conversely, the danger of introducing more sources of WBDL from Oman to the UAE with nursery trees is real.
Many beautiful citrus trees are growing in the UAE. It is enough to cite lime trees at Hamraniyah, Kalba (Fig. 311) and Fujairah, lemon trees at Dhaid (Fig. 312) and Dibba and grapefruit trees at Dibba (Fig. 313). The potential of the UAE for citrus production should be maintained by proper control of virus and virus-like diseases.
Bové, J.M., Garnier, M., Mjeni, A.M. & Khayrallah, A. 1988. Witches' broom disease of small-fruited acid lime trees in Oman: first MLO disease of citrus. In Proc. 10th Conf: IOCV, p. 307-309. Riverside, Univ. Calif.
Garnier, M., Zreik, L. & Bové, J.M. 1991. Witches' broom, a lethal mycoplasmal disease of lime trees in the Sultanate of Oman and the United Arab Emirates. Plant Dis., 75(6): 546-551.
Chapter 25: Yemen
While carrying out a survey for virus and virus-like diseases of citrus in Saudi Arabia in November 1981 on behalf of FAO, Bové discovered the presence of citrus greening disease in the southwestern part of the country. The geographical extent of the disease was further determined during two additional surveys in Saudi Arabia in April 1982 and December 1983. The 1982 mission also included northern Yemen (previously the Yemen Arab Republic) and the 1983 inspection covered northern Yemen again and also took in southern Yemen (previously the People's Democratic Republic of Yemen).
These surveys established that citrus greening disease as well as its insect vector, the psyllid Diaphorina citri, were present in Saudi Arabia from Jeddah to the border with northern Yemen. Since the disease was found not only at the fairly high altitudes of the southwestern plateau of the Arabian Peninsula, but also at the low altitudes of the coastal plains of Saudi Arabia, and since the vector was identified as the Asian psyllid D. citri, it was concluded that the form of greening present in Saudi Arabia was the heat-tolerant Asian form.
The 1982 and 1983 surveys showed that greening disease was also present in northern Yemen, but only at altitudes of I 000 m and more, not on the coastal Tihama plain. The form of greening present in northern Yemen is very probably the heat-sensitive African form, since the insect vector is the African psyllid, Trioza erytreae, and the disease, as well as the psyllid, only occurs on cool elevated areas, not on the coastal plains or in hot oases such as Marib and Harib (see Map 19).
Finally, during the 1983 survey it was found that the two psyllids, D. citri and T. erytreae, occur together in the Abha area of Saudi Arabia, only 100 km north of the border with Yemen. This shows that T. erytreae probably introduced into Yemen from Ethiopia - is moving northwards, while D. citri probably introduced into the Mecca area with pilgrims from the Indian subcontinent or Southeast Asia -is moving southwards. The psyllids have "met" at Abha, only slightly north of the border between Saudi Arabia and Yemen.
The search for greening in northern Yemen in 1983 showed the disease and its vector, T. erytreae, to be present and well established in the Al Baida area, which is very close to the former border between northern and southern Yemen. Therefore, an attempt was made in 1983 to visit the Mukayras area in the south, only a few kilometres from Al Baida. However, Mukayras proved impossible to reach and the 1983 survey in southern Yemen was thus restricted to the Lawdar-Mudia area and the Say'un-Tarim area in Wadi Hadramawt. A second attempt to get to Mukayras was successful in April 1987. The survey included orchards in the Lawdar-Mudia as well as the Zinjibar-Gaar area, and the Jawl-Madrum district, near Al Musaymir.
MAP 19 Yemen
The major results of the surveys in southern Yemen confirmed the presence of T. erytreae in the Mukayras area and the importance of gummy bark disease throughout the areas visited.
The 1982 and 1983 surveys for virus and virus-like diseases of citrus in northern Yemen were carried out essentially to determine whether or not citrus greening disease was present in the country. Concern that greening might be present arose from the fact that in 1982 Bové discovered the disease in the southwestern part of Saudi Arabia, as described in Chapter 18. The 1982 and 1983 surveys showed that greening was also present in northern Yemen.
Ta'izz region (April 1982 and December 1983 surveys). The first place where evidence for greening was found was the citrus collection at the Agricultural Research Station (Aussfera farm) at Ta'izz. This collection (Fig. 181) was established in 1974 with plant material from Italy. In April 1982, most of the sweet orange trees showed severe symptoms of greening: sparse foliage, yellow, mottled leaves (Fig. 184); lopsided fruits of all sizes and off-season flowering. In addition, typical T. erytreae-induced galls were present on the leaves. The occurrence of the psyllid T. erytreae was confirmed the same day by the entomologist in charge, who was trying to control the psyllid population by dimethoate sprays. In fact, nymphs or galls of T. erytreae could be seen on leaves of sweet orange, lemon (Figs 192 and 193), sour orange and mandarin. Confirmation that the symptoms observed were those of greening came from electron microscopy observations carried out in Bordeaux on leaf midveins and fruit axes from symptomatic trees. In all cases the BLO associated with greening was detected (Fig. 3).
Advice was given in April 1982 to eradicate the badly infected citrus collection by pulling out the trees, but this was not done. On his second visit to Ta'izz in December 1983, Bové was surprised to see that the trees had been severely pruned (Fig. 182) rather than removed. This treatment resulted in the growth of many young, tender shoots (Fig. 182), on which psyllids were feeding, becoming infected at the same time with the greening pathogen. This heavy pruning contributed to enhanced transmission of the disease agent. Evidence that this was the case was observed in the three-year-old Washington navel sweet orange block, adjacent to the infected citrus collection. Several of the young trees were already stunted and showed symptoms of greening (Fig. 183). Electron microscopy showed the trees to be infected by the greening BLO. In another nearby block, young small-fruited acid lime trees were similarly stunted and showed severe leaf mottle as well as psyllid-induced galls on the leaves. They also carried the greening BLO.
An extensive survey was carried out in December 1983 south of Ta'izz, in the Barakani area, where sweet orange and mandarin trees were known to have been dying since the 1970s. Indeed, no such trees could be found in the whole area, in spite of an extensive search. It was learnt subsequently that over 1 000 declining sweet orange trees had been pulled out in 1979. However, many small fruited acid lime trees were seen, some of which were 15 years old. Practically all of them had clear-cut symptoms of greening (Figs 185 to 187). Some of the leaves showed T. erytreae-induced galls or bumps (Fig. 187). Electron microscopy detected the greening BLO in the leaves of all four lime trees examined. These observations demonstrate that greening disease affects most of the lime trees in the Barakani area. A 20-year-old sweet lime seedling tree also carried greening. The decline of sweet orange and mandarin that occurred in the 1970s is therefore most probably due to greening, as sweet orange and mandarin are much more susceptible to greening than small-fruited acid lime. A situation similar to that in the Barakani area also occurs on a much larger scale in the southwestern part of Saudi Arabia, where sweet orange and mandarin trees have disappeared, and only acid lime trees now survive. In both situations, the lime trees are still growing relatively well because they are only moderately susceptible to greening and are not affected by tristeza. Indeed, no evidence for tristeza could be seen on the many trees observed: there was no vein clearing or stem pitting.
Ironically, the budwood for the sweet orange and mandarin trees that have died or were pulled out in the Barakani area came through the extension services from the Agricultural Research Station in Ta'izz. It is quite possible that greening was introduced into the Barakani area with budwood from the Ta'izz station, where greening is well established.
Al Baida region (December 1983 survey). Dinahem area, Nasser Al Kahr Shuft orchard The orchard comprises about 100 12-year-old Valencia late sweet orange trees. The planting material came from Aden (where greening has never been reported). The trees showed severe T. erytreae damage, but symptoms of greening occurred only on some branches, suggesting that the disease was of recent introduction. Symptoms of greening were seen on the leaves (zinc-deficiency pattern, mottle and yellow midveins), and on the fruit (Figs 194 and 195). The greening BLO was detected by electron microscopy (Fig. 5).
No psyllid damage or greening symptoms could be seen on three-year-old navel and Valencia late sweet orange trees of Egyptian origin in three nearby orchards, indicating again that introduction of greening and its vector is relatively recent.
Zaher area, Homegani orchard. Severe greening was seen on an eight-year-old sweet orange tree that was introduced from Ta'izz. Electron microscopy detected the greening BLO in the tree (Fig. 6).
T. erytreae-induced galls and symptoms of greening were seen on 20 three-year-old acid lime trees.
In summary, in the Al Baida region, T. erytreae and greening are present. Their introduction into this relatively isolated area must have occurred recently, probably in the late 1970s. Eradication of the relatively few affected trees was advised.
In 1985 when northern and southern Yemen were still separate countries, it was not possible to go from Al Baida in the north to nearby Mukayras in the south. Bové was, however, given the opportunity to reach Mukayras in April 1987 via Aden and Lawdar. As expected, he observed the presence of T. erytreae on leaves of sour orange (Figs 189 and 190) and small-fruited acid lime (see the section on southern Yemen below). These observations indicate that the whole Al Baida-Mukayras area is infected.
Hammam Ali region (April 1982 survey). T. erytreae-induced galls were seen on leaves of sweet orange, Clementine (Fig. 191) and mandarin. Eggs and nymphs of the psyllid were abundant on young sweet orange leaves. Greening symptoms were seen on certain branches. The disease is probably of recent introduction.
Wadi Dahr, San'a region (December 1983 survey). In the Hassan Al Buchari orchard, severe T. erytreae damage was observed on leaves of lemon, small-fruited acid lime and sweet orange. The greening BLO was detected by electron microscopy of yellow, mottled sweet orange leaves (Fig. 4). Leaves of a nearby fig tree had many galls. These were due to Trioza buxtoni, not T. erytreae.
Other regions. No evidence for the presence of greening and its psyllid vector, T. erytreae, was found in the Tihama or Marib-Harib areas.
Other virus and virus-like diseases
Marib-Harib region (December 1983 survey). The Marib region contains many fine sweet orange and mandarin trees and seems well suited to citrus production. Unfortunately, trees were not propagated from certified bud-wood and show symptoms of several transmissible diseases of citrus. Psorosis young leaf symptoms (Figs 94 and 96) were observed in every orchard on practically all sweet orange trees. Such symptoms are associated with several diseases (scaly bark psorosis, concave gum, cristacortis, impietratura and infectious variegation). In Marib, they seem to be more particularly associated with concave gum. Indeed, severe concave gum was frequently observed (Figs 103 and 104). In one orchard (Mohamed Eberi Saad) young sweet orange trees showed conspicuous psorosis young leaf symptoms, but were too young to show trunk symptoms. However, the 15-year-old mother trees from which they had been propagated showed very severe symptoms of concave gum (Fig. 103) as well as psorosis young leaf symptoms. This indicates that the symptoms shown by the young sweet orange trees are, in this case, due to the concave gum agent, and that this agent has been transmitted from the mother trees to the progeny trees.
In several orchards, the trunks of young trees were covered with soil (Fig. 224). This inadvisable practice favours phytophthora gummosis on the susceptible sweet orange and lemon scions, and the disease was indeed observed on several lemon trees. Some lemon trees also showed symptoms resembling mal secco. The causal fungus, Deuterophoma tracheiphila Petri is believed to be present in northern Yemen, and the German plant protection group in northern Yemen has reported mal secco in Hammam Ali (though Bové did not observe it there). It is important to confirm or refute the presence of mal secco in Yemen.
In the Harib region, two interesting cases were observed in the Al Sagifa Abduraba Golan orchard, one on sweet orange trees, the other on mandarin trees. Several sweet orange trees on unrecorded rootstocks were declining. The trees showed bud-union crease, conspicuous stem pitting with corresponding bark pegging on the rootstock (Figs 76 and 77) and gum impregnation of the sweet orange scion bark (Fig. 78). The presence of gum in the sweet orange bark is characteristic of gummy bark. The other symptoms observed on these trees (bud-union crease and stem pitting on rootstock) could also be due to the gummy bark agent if the rootstock were rough lemon. This is very probably the case, since a shoot growing out of a root from an affected tree (Fig. 76) was identified as rough lemon on the basis of its leaves. Hence, the declining sweet orange trees are affected by gummy bark and show the symptoms of this disease both on the sweet orange scions and the rootstocks, identified as rough lemon. Some of the trees are also affected by concave gum.
The second case involved Willowleaf mandarin trees. Practically all showed symptoms of cachexia: heavy gum impregnation of the mandarin bark (Fig. 262, right) and stem pitting with corresponding bark pegging on the mandarin scion (Fig. 262). The unrecorded rootstock also showed stem pitting and mild bark gumming below the bud-union. The rootstock is again probably rough lemon, since rough lemon has been identified in this orchard (see above). If so, the symptoms observed on the rootstock are those of gummy bark. These mandarin trees are thus affected by two diseases: cachexia as seen on the scion, and gummy bark as seen on the rough lemon rootstock.
The above two cases illustrate how difficult it is to diagnose certain diseases accurately when the nature of the rootstock is not recorded. The farmers' attention must be drawn to the importance of recording the major characteristics of their trees: origin of budwood, age of trees at date of planting, name of scion cultivar and name of the rootstock cultivar.
In summary, the major diseases observed in the Marib-Harib region are concave gum, psorosis young leaf symptoms and gummy bark on sweet orange trees, and cachexia and gummy bark on mandarin trees. As the trees are old-line trees, they are probably also infected with the exocortis viroid, but this can only be determined by indexing. No evidence of tristeza and greening was seen. No psyllids or psyllid galls were found. Contrary to a 1983 report, no symptoms of cristacortis were observed. The Marib-Harib region is well suited to citrus, but new citrus projects must make use of only certified budwood so as to avoid the many diseases whose symptoms are seen in today's orchards.
Hammam Ali (April 1982 survey). Hammam Ali is among the regions that harbour T. erytreae, the vector of citrus greening disease. Early symptoms of greening were seen there, as noted earlier.
In addition, very strong and typical symptoms of cristacortis were seen on many mandarin trees on sour orange rootstock, which were also affected by cachexia. Cristacortis stem pitting and corresponding bark pegging were seen on the sour orange trunk (Figs 109 and 112). Cachexia was diagnosed by the presence of gum in the mandarin bark (Fig. 112). An additional symptom of cachexia is stem pitting. Figure 112 clearly shows the difference between the conoid type of pitting associated with the strain of cachexia involved here and the cristacortis stem pitting, in which the pits occur as distinct, deep and narrow, longitudinal depressions (Fig. 110).
Ibb (April 1982 and December 1983 surveys). In April 1982, no evidence for the presence of T. erytreae was seen. In December 1983, however, galls of the psyllid were seen on many leaves of lemon, sour orange and sweet orange trees.
The most widespread symptom observed in April 1982 was the psorosis young leaf symptom. This symptom (see Figs 91 to 97) must be observed at the right time of the year, when the leaves are still young and soft and the temperature is cool. April seems to be a good period for this in the highlands of Yemen, and, indeed, psorosis young leaf symptoms (see Fig. 97) were seen on all navel sweet orange trees on sour orange rootstock imported from Egypt.
Typical symptoms of cristacortis were observed in 1983 on the sour orange rootstocks of lemon trees of Egyptian origin (Figs 114 and 115). Cristacortis is one of the diseases in which psorosis young leaf symptoms occur.
In December 1983, severe symptoms of phytophthora gummosis were observed on the scions of lemon trees grafted on sour orange (Figs 229 and 230). This is a typical case. Phytophthora gummosis developed because the trees were planted too deep, with their bud-union buried below soil level, and trees began to show phytophthora lesions above soil level. When soil was removed from around the trunks, the lesions were seen to extend all the way down to the bud-union line (Fig. 230). Figures 229 and 230 show how circular soil levees have been built around the trees to protect them from irrigation water.
Warazan nursery, Al Rahida region (April 1982 survey). It is a pity that the budwood used in this well-kept nursery came from uncertified, old-line mother trees. Indeed, every navel sweet orange budling of Egyptian origin showed psorosis young leaf symptoms whether the plants were still in plastic bags or already planted in the field. Seedlings of several rootstock cultivars other than sour orange, such as rough lemon, Troyer citrange and Cleopatra mandarin, were growing in shaded seed-beds. It is not advisable to graft uncertified budwood from the above sweet orange trees on these seedlings, especially Troyer citrange, as problems may be encountered with diseases such as exocortis.
Citrus trees imported from a commercial nursery in Rome (Italy) were also seen. They were not certified free of transmissible diseases.
No symptoms of tristeza (leaf vein clearing) were seen on the many small-fruited acid lime seedlings, and no signs of T. erytreae were seen in the nursery, though the psyllid is probably present in the area.
Agricultural Research Station, Aussfera farm, Ta'izz (April 1982 and December 1983 surveys). On this farm Bové found evidence of citrus greening disease for the first time in Yemen.
Psorosis young leaf symptoms were again seen on navel sweet orange trees from Egypt. Trees had also been imported from India and Japan. Coorg mandarin trees on different rootstocks came from Bangalore, and sweet orange budlings from Japan. Both India and Japan are known to be infected with CTV as well as the citrus canker bacterium. Introduction of citrus from such countries should be strictly prohibited, even for agricultural experiment stations. It is highly likely that citrus canker was introduced into Yemen by citrus trees from India.
Typical stem-pitting symptoms of cristacortis were seen on sweet orange trees of Italian origin.
Mauza farm, Wadi Safia region (April 1982 survey). Mauza is southwest of Ta'izz and close to the coastal Tihama. Its low altitude (200 m) explains why no T. erytreae psyllids or greening symptoms were seen. However, many other citrus disorders were observed in this old citrus farm on sweet orange, mandarin and lemon trees over 20 years of age.
Typical symptoms of gummy bark (gum impregnation of bark) were observed above the bud-union lines of sweet orange trees grafted on sour orange rootstock. The tolerant rootstocks showed no symptoms. An interesting case of gummy bark was observed on sweet orange trees that were top-grafted with mandarin. The sweet orange part of the mandarin trees was present in between the sour orange rootstocks and the mandarin tops. Severe gummy bark symptoms were present only on the susceptible sweet orange middle section (Fig. 79).
Some of the sweet orange trees with gummy bark also had characteristic symptoms of Rio Grande gummosis. Old, inactive lesions with exposed wood at the centre (Fig. 242) indicate that Rio Grande gummosis is not a disease of recent appearance in Mauza.
Typical cristacortis stem pitting was present on some of the sweet orange trees (Fig. 113) and suggests that trees are of Italian origin. Shell bark (Fig. 258) was seen on an old-line lemon tree on sour orange rootstock.
Garouba Citrus Project, Bait al Faqih region, Tihama (1982 survey.) With 50 000 nursery trees, this is the largest citrus project in Yemen and extends over 5 ha. It was started with the help of USAID in 1978-79. Budwood for the various field blocks comes from the United States of America and Spain and was certified free of transmissible diseases. Indeed, no symptoms of such diseases were seen. Because of the low altitude - less than 200 m - and the hot climate, T. erytreae is absent. Unfortunately, however, citrus canker has been detected and is a severe blow to the whole project.
Jaraba Citrus Project, Bajil region, Tihama (1982 survey). As in Garouba, the hot climate associated with the low altitude prevents the occurrence of T. erytreae, but citrus canker has been introduced with citrus trees from India. Such trees were seen growing in the open field. No symptoms of tristeza were seen on four-year-old small-fruited acid lime trees.
Greening and other virus and virus-like diseases in northern Yemen: conclusion
Greening. Greening and its psyllid vector, T. erytreae, were seen in Ta'izz and the Barakani area, Al Baida (as well as in the nearby Mukayras area in southern Yemen), Hammam Ali and San'a (Wadi Dahr). The disease and its vector were not seen in the Tihama, or the Marib-Harib region. In other words, the disease and its vector only occur in areas where citrus is present at an altitude above 700-1 000 m. In these relatively cool areas the heat-sensitive psyllid vector thrives well, whereas it does not withstand the hot climate of the Tihama and other low-lying areas (Marib and Harib). Similarly, greening was only observed in the areas where T. erytreae was present. This indicates that the form of greening present in northern Yemen is the heat-sensitive African form. It is most probable that greening and T. erytreae entered Yemen over the Bab al Mandab strait from neighbouring Ethiopia where the disease and its vector are known to be well established. After having spread throughout the highlands of Yemen moving northwards, the insect eventually entered Saudi Arabia where it has already reached the Najran, Fayfa and Abha areas. The latter harbours not only T. erytreae but also D. citri, the Asian psyllid vector of the greening BLO. While T. erytreae invades new favourable zones travelling northwards, D. citri is moving southwards from the Mecca area. It has now reached Abha and could one day enter Yemen. As D. citri and the Asian form of greening are both heat-tolerant, they could easily become established, not only in the cool highlands of Yemen, but also in the hot lowlands of the Tihama. They are therefore potentially a great threat to Yemen.
Other virus and virus-like diseases. Psorosis young leaf symptoms were frequently seen on sweet orange leaves in the following areas: Marib-Harib, Ibb, Ta'izz and Warazan. In the Marib area, psorosis young leaf symptoms were associated with concave gum. At Ibb and Warazan, they were observed on practically all sweet orange trees of Egyptian origin, showing that these trees were not propagated from virus-free budwood.
Typical cases of cristacortis were seen on sour orange or sweet orange in Hammam Ali, Ibb, Ta'izz and Mauza. Cristacortis is a widespread disease in the Mediterranean islands of Sicily and Sardinia (Italy) and Corsica (France). It is therefore interesting to see such numerous and typical cases of the disease in Yemen. The presence of cristacortis in the country is probably due to the importation of infected trees or budwood from Italy. Indeed, Italy is among the countries from which trees were and still are imported to Yemen. For instance, in April 1982, at the Ibb and Warazan nurseries, Bové saw many mandarin, sweet orange and lemon trees just imported from Eurogarden nurseries in Rome. Therefore, the cristacortis-affected mandarin trees in Figures 109 to 1 15 illustrate a situation where the nature of the disease gives an indication of the origin of the trees.
Cases of gummy bark on sweet orange were seen in Harib and Mauza. This disease was first described in Egypt and is widespread in the Near East. Southern Yemen contains many such cases.
Cachexia was present on practically all mandarin trees in Hammam Ali and Harib. In Harib, the mandarin scions showed cachexia symptoms and their rough lemon rootstock, symptoms of gummy bark.
Exocortis symptoms were not observed because the rootstocks used in northern Yemen, sour orange and rough lemon, are tolerant of the exocortis viroid. It is, however, more than likely that most of the old-line cultivars introduced from Italy, Egypt, southern Yemen or Saudi Arabia are infected with the exocortis viroid(s). Propagation of the budwood of these old lines on rootstocks such as Troyer citrange would most probably result in exocortis appearing on the rootstock.
No symptoms of tristeza were seen on the many small-fruited acid lime trees observed, indicating that tristeza virus is not spreading in northern Yemen. Suspect trees were seen occasionally, but they all indexed negative for tristeza by ELISA in Bordeaux.
Symptoms of three fungal diseases were observed: phytophthora gummosis in the Marib and Ibb regions; Rio Grande gummosis at Mauza; and a mal secco-like disorder in Marib. Presence of Phoma tracheiphila, the causal fungus of mal secco, must be confirmed. Phytophthora gummosis can be prevented by proper horticultural practices and Rio Grande gummosis by keeping pruning to a minimum and disinfecting wounds.
Citrus canker, a disease caused by the bacterium Xanthomonas campestris pv. citri, was detected in the Tihama in 1982. No symptoms were observed by Bové during his 1982 survey in the Tihama, because the affected trees had been eradicated. The disease has subsequently spread to the highlands and eradication is no longer feasible. Citrus canker was very probably introduced with citrus trees from India, where the disease is widespread.
No evidence of citrus canker was found by Bové during his 1983 and 1987 surveys in southern Yemen, and it is essential that citrus canker be kept out of this part of the country. To this end, severe restrictions must be imposed on the movement of citrus material from the infected northern part of Yemen to the as yet uninfected south.
The Tihama was thought to be a suitable region for growing citrus nursery trees, because it is free of greening, and T. erytreae, the vector of the disease, does not multiply there. Unfortunately, the presence of citrus canker has made this region much less attractive. If, however, citrus canker has now spread throughout northern Yemen, it is not really important, as far as citrus canker is concerned, where the nurseries are established and the Tihama might again be used for nurseries.
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