Incidence of virus and virus-like diseases

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Tristeza

Citrus tristeza virus in satsuma trees from Japan at Mahdasht. CTV was introduced at Mahdasht, near Sari, in the Caspian Sea area (see Map 6) with the importation from Japan of satsuma trees grafted on P. trifoliata. Forty thousand budded trees were imported and planted in the Mahdasht orchard in 1968, and 15 000 more in 1970.

Since tristeza is endemic in Japan, practically all of the 55000 trees were likely to be infected with CTV. Work by Iranian experts has shown that this is indeed so. CTV was detected in the trees by indexing on small-fruited acid lime as well as by ELISA and immunosorbent electron microscopy (Ebrahimi, personal communication; Minassian, 1983a; Minassian and Ghorbani, 1983). In one experiment, over 400 citrus trees from different areas in the Caspian Sea region were indexed by ELISA; in the Mahdasht orchard, 90 to 100 percent of the Japanese satsuma trees showed positive reactions (Minassian, 1983a).

Field inspection of the trees in Mahdasht, as well as ELISA and electron microscopy carried out at Bordeaux to detect CTV in samples collected at Mahdasht, have shown that five categories of satsuma trees can be identified.

Group A comprises old, healthy-looking, vigorous satsuma trees on P. trifoliata rootstock and infected with CTV. These are the budded trees imported from Japan in 1968 and 1970. They show no symptoms of tristeza in spite of their infection as they are grafted on P. trifoliata, a rootstock tolerant of CTV.

Group B consists of old, healthy-looking, vigorous satsuma trees on sour orange rootstock, and free of CTV. These are some of the satsuma trees that were present in the orchard before the trees were imported from Japan.

Group C is made up of small, stunted satsuma trees on sour orange rootstock which show pinholing on the rootstock below the bud-union line (see Fig. 145). They are infected with CTV, probably from the use of CTV-infected buds taken from trees imported from Japan, i.e. trees of Group A. They are stunted because they are susceptible to CTV when grafted on sour orange.

The fourth category, Group D, is that of relatively young, normal, satsuma trees on sour orange rootstock with no pinholing. They are free of CTV, as the buds from which these trees were propagated very probably came from CTV-free trees, such as those of Group B.

None of the above are likely to have been infected through natural transmission of CTV. There is, however, a fifth category of satsuma trees where natural transmission cannot be ruled out.

Group E is composed of large, declining satsuma trees on sour orange rootstock. They show pinholing and are found, by ELISA and electron microscopy (Fig. 31), to be infected with CTV. These trees differ from those in Group C. Whereas those in Group C are small and severely stunted, having probably been infected with CTV throughout their life - which explains why they have never produced good growth - trees of Group E were undoubtedly well developed before they began to decline. This means that they were not infected with tristeza early in their life, but became infected later, probably by natural infection.

Natural spread of CTV in the Mahdasht orchard. CTV is insect-transmitted and it is known that its insect vectors are aphids. The major aphid vector is the black Asian citrus aphid, T. citricida, which is responsible for the spread of CTV in South America, South and West Africa, Australia, India and the Far East. T. citricida is not present in the Mediterranean area or the Near East. It has never been reported in Iran. However, other aphid species can also transmit CTV: Aphis gossypii in California, Florida, India, Israel and Spain; Aphis citricola in Florida, India, Israel and Spain; Toxoptera aurantii in Florida, India and Spain; and Myzus persicae, Aphis craccivora Koch and Dactynotus jaceae L. in India.

These aphid species are generally considered less efficient CTV vectors than T. citricida. However, in Israel, A. gossypii was found to be an efficient vector of one strain of CTV (Bar-Joseph and Loebenstein, 1973). In California, the transmission rate of CTV by A. gossypii was very low in the 1950s, but recently it was found that this aphid has become a very efficient vector of several CTV isolates, probably because the virus has undergone mutations that make it readily transmissible by A. gossypii (Roistacher et al., 1980). In Spain also, one isolate of CTV was transmitted with high efficiency by A. gossypii but with low efficiency by A. citricola and T. aurantii (Hermoso de Mendoza, Ballester-Olmos and Pina Lorca, 1984). M. persicae, Aphis fabae, A. craccivora, Aphis nerii and Hyalopterus pruni failed to transmit CTV. Interestingly enough, CTV could be detected by ELISA not only in the three aphid species that transmitted the virus but also in the five species that did not. This indicates that different aphid species can acquire CTV, regardless of their ability to transmit the virus to healthy plants (Hermoso de Mendoza, Ballester-Olmos and Pina Lorca, 1984). Finally, CTV strains in Florida (Norman and Grant, 1956) and India (Capoor and Rao, 1967) are also efficiently transmitted by A. gossypii.

To summarize, it appears that in countries where T. citricida is absent, A. gossypii can be an efficient vector of CTV and, more precisely, of certain CTV isolates. A. citricola is a less efficient vector, but is frequently abundant on citrus and may be more important as a vector of CTV than laboratory transmission tests indicate.

The following known aphid vectors of CTV are present in Iran: A. gossypii, A. citricola, T. aurantii, A. craccivora and M. persicae. In the northern province of Mazandaran, where the CTV-infected satsuma trees occur, A. gossypii is present (Ghorbani, 1983), but the two most common aphid species are T. aurantii and A. citricola (Minassian, 1983b). Hence, potential vectors for CTV transmission exist in the Caspian Sea region.

On the basis both of the trees of Group E and of the presence of potential CTV aphid vectors, it has to be concluded that natural transmission of CTV has occurred in Mahdasht.

However, judging from the symptom expression in trees, natural transmission seems to have occurred fairly recently. Also, the rate of transmission still seems to be low, judging by the absence of tristeza symptoms and lack of decline in the many trees on sour orange rootstock in the Mahdasht orchard.

The low level of natural transmission is probably due to the fact that T. aurantii and A. citricola are the predominant aphid species in the Caspian Sea area. These species are inefficient vectors of CTV compared with A. gossypii, which, under certain circumstances, can be an efficient vector. Also, it is not clear how easily aphids other than T. citricida carry CTV from satsuma to satsuma and other citrus species.

In the Izmir region of Turkey, along the Aegean coast, many satsuma trees are grown on P. trifoliata, and some are infected with CTV. In one orchard, ELISA showed 41 of 641 trees (6.4 percent) to be infected (C. Bové, personal communication). However, natural transmission has not yet been reported. In Morocco, eight trees on sour orange rootstock, including five satsuma Owari trees, were infected with CTV in the Marrakech Experiment Station, yet none of the many neighbouring trees became infected in the long period before the trees were pulled out (Cassin, 1963).

Sour orange is the only citrus rootstock used in the Caspian Sea region, and infection of trees on this rootstock with CTV would result in tristeza decline. No decline was observed by Bové during his short survey of the area in November 1985, or by the many citrus experts (Ebrahimi, Habashi, Rahimian and others) in daily contact with citrus in Mazandaran province.

It has, however, been reported that a few trees were found positive for CTV by ELISA (Minassian, 1983a), namely two mandarin trees from orchards in the vicinity of the Mahdasht orchard, as well as three trees in the Khorram-Abad citrus collection. Regarding the trees in the citrus collection in Khorram-Abad, Habashi collected samples from ten satsuma trees on sour orange rootstock. The samples were then analysed by ELISA in Bordeaux. One of the samples gave a weakly positive reaction.

In conclusion, if natural spread of CTV from the heavily CTV-infected Mahdasht orchard has occurred, its intensity still seemed to be very low (November 1985).

Recommendations.

• The Mahdasht orchard, which is so widely contaminated with CTV, must be destroyed and all the trees pulled out. This applies not only to the satsuma trees, but also to trees of sweet orange, Clementine, etc. regardless of whether rootstocks are P. trifoliata or sour orange. As wounded or sectioned citrus roots have the ability to produce shoots, care must be taken to remove all such shoots that could develop from roots left behind after the trees have been pulled out. These drastic measures must be taken for the following reasons:

• Natural spread of CTV seems to have already occurred, but the extent of transmission still seems to be low. The level of natural transmission could increase very quickly under various conditions if the large source of virus inoculum, the Mahdasht orchard, is not removed. Such conditions could be a high aphid population in the spring on young shoots following a severe frost in the winter; mutations of the virus into new strains readily transmissible by the aphids; or occurrence of CTV in citrus other than satsuma, from which spread by aphids would be more efficient.
• The CTV-infected satsuma trees on P. trifoliata are good-looking trees since they are on tolerant rootstocks. Hence, there is always the danger that inexperienced persons will collect budwood on these trees and propagate it, acting, in this way, as true vectors of the disease.
• CTV might eventually infect not only the Caspian Sea citrus area, but also other Iranian citrus regions.

• Prohibit for at least five years the use of P. trifoliata as a citrus rootstock and continue to use sour orange. Indeed, if some spread of CTV has occurred and eventually continues, trees on sour orange that have become infected will decline. They will be easy to spot and can be pulled out. The trees in the neighbourhood of the infected tree can be indexed by ELISA and, if found positive, removed. Hence, a focus of infection can be eradicated. If, however, P. trifoliata is the rootstock, the infected trees cannot be spotted; not only will the infection centres not be removed, but they will increase in size.
• Make frequent surveys to spot any tree on sour orange rootstock that might be showing early symptoms of decline.
• Use ELISA to screen suspect trees for CTV, or to identify trees that are tolerant of tristeza. Trees tolerant of tristeza are, for instance, trees grafted on root-stocks such as P. trifoliata and seedling trees of sweet orange and mandarins. The Caspian Sea province has many local seedling sweet orange trees. Make sure, by using ELISA, that none of these trees carry CTV.

Unfortunately, as of November 1992, the Mahdasht orchard had not been destroyed.

Stubborn

Citrus stubborn disease is caused by the helical mycoplasma S. citri (Saglio et al., 1973) (see Figs 22 to 24). The disease is widespread throughout the Mediterranean citrus areas and the Near East (Cyprus, Egypt, Iraq, Israel, Lebanon, the Syrian Arab Republic and Turkey). It used to be one of the major problems of citrus in California and Arizona.

Stubborn in Iran. The presence of stubborn disease in Iran has been suspected for a long time. Until the 1970s, diagnosis of the disease was based solely on symptomatology, and it is a well-known fact that stubborn diagnosis from visual symptoms is not easy. In Iran, the diagnosis seemed to be even more difficult since excessive summer heat was thought to mimic stubborn symptoms (Cochran and Samadi, 1976). For these reasons, the incidence of the disease in Iran has been reported variously as rare (Wallace, 1973) to nearly universal (Chapot, 1970, 1975). Cochran and Samadi (1976) were probably the first to confirm field diagnosis of stubborn in Iran by graft transmission of the disease agent to indicator seedlings. They transmitted stubborn from a symptomatic Gillette navel sweet orange tree from an orchard in Jiroft (southeastern Iran) to Pineapple sweet orange seedlings under greenhouse conditions.

Since the discovery and characterization of S. citri in the 1970s, stubborn can be diagnosed by detection techniques such as culture of the spiroplasma (Bové, Whitcomb and McCoy, 1983) and ELISA (Saillard and Bové, 1983).

The first S. citri isolate from Iran was cultured in Bordeaux from a sample collected in Iran by Newcomb in 1974. Since then, Rahimian, in Iran, was able to culture S. citri from citrus trees in many areas of southern and southeastern Iran (Table 30). He isolated S. citri from grapefruit and sweet orange trees, and also from Cleopatra mandarin and rough lemon trees (Rahimian, 1983).

Fruit samples were collected by Bové during his survey and taken to Bordeaux for S. citri screening by culture. Table 31 shows that S. citri could be cultured from sweet oranges collected at the Kotra, Khorram Abad and Ramsar experiment stations in the Caspian Sea area. These results prove the presence of stubborn disease in Mazandaran province. S. citri could also be detected in sweet oranges from Jiroft as well as in sweet oranges and grapefruits from the Khafr area (Fars province).

In conclusion, stubborn disease is present in practically all citrus-growing areas of Iran (see Map 2 on p. 70).

Symptoms of stubborn in Iran. As shown in Table 31, stubborn-affected sweet orange trees in Iran are characterized by poor crops, bushy growth, stunting, fruits of various sizes and ages, small spoon-shaped leaves, seed abortion, off-season blooming, closure of navel, etc. Symptoms were more severe in the hot Jiroft and Khafr areas than in the cool Caspian Sea areas, probably because stubborn expression is poor in cool climates.

Stubborn-affected trees in the Caspian Sea area (Kotra, Ramsar, Khorram Abad stations) drew attention because of their poor yield.

The most severe symptoms of stubborn were observed in the Khafr area on local sweet orange trees (Fig. 147) and on grapefruit trees of unknown origin or possibly from Jiroft. The grapefruit trees in one orchard (Resvan orchard at Bab Anar) were severely stunted, with very small fruit showing strong blue albedo (Fig. 169). DNA-DNA hybridization confirmed these trees to be infected with S. citri.

TABLE 30 Occurrence of citrus stubborn disease in Iran

Notes:
¹ Personal communication.
² Cochran and Samadi, 1976.

Conditions of excessive heat change the normal morphology of citrus leaves. Lateral veins tend to run parallel to leaf margins, yielding so-called "palmate" leaves (see Fig. 159). Midribs of leaves are sometimes shortened, giving cordate leaves or leaves with blunt ends. Leaf distortion may produce boat-shaped leaves. In all these cases, the leaf blades remain uniformly green (see Fig. 159), except for sunburns. These leaf modifications have been described in Iran by Cochran and Samadi (1976) and Reuther, Nauer and Roistacher (1979). The latter also reproduced the symptoms using healthy citrus material in growth chambers, showing that the symptoms are physiological rather than pathological in origin, and hence not due to stubborn. Work by Bové in Iraq (see Chapter 12) has clearly shown that stubborn-affected trees under high-temperature conditions tend to produce sucker-like shoots characterized by leaves with pinched-in, yellow tips (see Fig. 160); and often also with yellow edges. Hence, such leaves are not uniformly green (see Figs 160 and 161). Some of these leaves may show heat effects (see Fig. 160), but stubborn infection is revealed by the yellow tips or edges, not by palmate or cordate leaf morphology. In the Jiroft area and in the Khafr region where citrus grows under high temperatures in the summer, leaves showing only heat effects could be clearly distinguished from those affected by stubborn. It must be added that leaves with normal morphology, but with yellow tips and edges due to stubborn, can sometimes occur in the absence of excessive heat.

TABLE 31 Stubborn in sweet orange trees in certain regions of Iran in November 1985 as diagnosed by visual symptoms and/or Spiroplasma citri

S. citri strains imported from California and Morocco. S. citri is naturally transmitted in California by at least three leafhopper species, the most important being Neoaliturus tenellus (Caravan and Bové, 1989). It is highly probable that some of the many budwood sticks imported from California in 1963-64 and 1971 -72 were infected with S. citri, even though they were certified free of known diseases. This is understandable in view of the natural spread of the disease in California and the difficulty of indexing for stubborn disease. Evidence for the presence of S. citri in some of the citrus cultivars imported from California can be seen in Table 31. For instance, Salustiana sweet orange imported in 1971 is infected with S. citri not only in Khorram Abad and Ramsar stations but also at Minab and Jiroft. Similarly, the Valencia late sweet orange imported in 1963-64 and the Hamlin sweet orange imported in 1971 are infected at both Kotra and Ramsar experiment stations. Skaggs Bonanza navel orange imported in 1971 is infected at both Minab and Jiroft stations.

It is also very probable that some of the species imported from Morocco in 1972 were similarly infected with S. citri, as stubborn is known to be a major problem in Morocco. Budwood imported from other Mediterranean countries could also have been infected.

Natural transmission of S. citri in Iran. The main evidence for natural transmission of S. citri in Iran comes from the fact that local sweet orange cultivars, i.e. cultivars not imported from California or Mediterranean countries, have been found to be infected with S. citri, for instance in the Khafr area and at Jiroft (Table 31). Further evidence is provided by the fact that a nucellar line of Hamlin sweet orange was found to be infected with S. citri at the Ramsar experiment station (Table 31). This nucellar line was developed in Iran from seeds collected in the foundation grove in Orlando (Florida). Since stubborn has never been described in Florida and since S. citri is not transmitted through seed, the Hamlin nucellar trees must have become infected in Iran.

If natural transmission of S. citri occurs in Iran, it is quite possible that some of the citrus species imported from California in 1963-64 and 1971-72 were initially healthy, but became infected with S. citri in Iran.

Distribution of the two major vectors of S. citri in the citrus-growing areas of Iran. N. tenellus (see Fig. 35) is the major leafhopper vector of S. citri in California and Arizona (Caravan and Bové, 1989). In the Mediterranean area and the Near East, N. haematoceps (see Fig. 34) has recently been identified as an efficient vector of S. citri (Fos et al., 1986; Calavan and Bové, 1989). N. tenellus is also present in the Mediterranean area but, in view of its paucity, it probably does not play a major role. N. haematoceps seems to be the main vector.

In Iran, both N. tenellus and N. haematoceps occur, the latter being, however, the most abundant of the two. Their distribution is fairly well established as they are known to be vectors of curly top virus of sugar beets. Tables 32 and 33 list some of the locations where they have been found, showing that the leafhoppers occur in all citrus-growing areas. From a comparison of Tables 32 and 33, it is clear that N. tenellus is less widespread than N. haematoceps. Map 2 on p. 70 gives the major citrus-growing areas, the occurrence of stubborn and the distribution of N. haematoceps and N. tenellus in Iran. It shows a close relationship between their occurrence and the presence of stubborn in the citrus-growing areas.

Occurrence of major host plants of N. haematoceps and N. tenellus. The distribution of N. haematoceps and N. tenellus reflects the distribution of their host plants. Table 34 lists host plants of N. tenellus in California-Arizona and of N. haematoceps in the Mediterranean area. Three wild host plants seem to be of major importance: Salsola kali L. (syn. S. pestifer, S. iberica), Alhagi camelorum (syn. A. persarum) and Matthiola spp. (stock).

S. kali subsp. tragus (see Figs 36, 170 to 174, and Map 3 on p. 71) is very widespread (Freitag, personal communication). Its natural distribution area covers the Mediterranean zone and most of the Irano-Turanian regions. It has spread over all arid and semi-arid areas in the warm temperature zones. In Cyprus, Iran, Iraq, Morocco and the Syrian Arab Republic the subspecies is extremely common -particularly on disturbed habitats (ruderal sites in towns, villages, on road sides, etc.), on arable lands (irrigated and non-irrigated) and on the seashore - from the hot lowlands up to altitudes of more than 2 000 m, with the highest densities in the hot and arid to semi-arid lowlands (see also Chapters 7, 9, 12, 15 and 21). In southern Iran, Pakistan and India, S. kali is replaced by an allied species. Other closely related species and subspecies are found in Azerbaijan, in the lowlands from northeastern Iran to central Asia. These taxa, systematically close to S. kali subsp. tragus, are probably able to nourish the same leafhoppers as S. kali.

Another wild host plant of N. haematoceps known to be widespread throughout Iran is A. camelorum. In Syria and Corsica, ornamental (Matthiola incana L.) and wild (Matthiola sinuata R.Br.) stock plants are also good hosts for N. haematoceps.

Both N. tenellus and N. haematoceps are often called "sugar beet leafhoppers" as they are common on that crop and are vectors of sugar beet curly top virus. Sugar beet is grown widely in the Shiraz region, and N. haematoceps has been found equally widely.

Thus there are many plants in Iran, both wild and cultivated, able to support the development of the two leafhopper vectors of S. citri. It is believed that naturally infected, non-rutaceous plants are the main sources of inoculum on which the leafhoppers become infected with S. citri, hence the importance of these plant species. Matthiola spp., or stock, found to be a good host of N. haematoceps in Syria and Corsica, can be infected with S. citri by both N. tenellus and N. haematoceps. Hence, it could be a good candidate for the source of inoculum.

TABLE 32 Occurrence of Neoaliturus haematoceps in Iran

Source: Ergebnisse der entomologischen Expeditionen nach dem Iran, Homoptera. Acta Entomologica Musei Nalionalis Pragae, 40, 1981, p. 251-252.

TABLE 33 Occurence of Neoaliturus tenellus in Iran

Source: Ergebnisse der entomologischen Expeditionen nach dem Iran, Homoptera. Acta Entomologica Musei Nalionalis Pragae, 40, 1981, p. 253.

Stubborn in Iran: conclusion. The fact that local sweet orange varieties as well as a nucellar line are infected with 5. citri shows that natural transmission of S. citri occurs in the country. This is not surprising since the two major leafhopper vectors are present in, or close to, the major citrus areas of Iran. The distribution of the leafhopper vectors reflects the distribution of their major host plants. Some of these, such as S. kali and A. camelorum, are extremely common in Iran.

Up to now, natural transmission of S. citri in Iran was probably obscured by the fact that some citrus cultivars imported from California, and perhaps Morocco, were infected with S. citri. Hence, it was believed that the presence of stubborn in Iran was the result of budwood importation. It is, however, extremely likely that citrus stubborn disease existed in Iran prior to these introductions. Also, it is quite possible that S. citri-infected plants other than citrus have been present in Iran for many years, and perhaps even before citrus was cultured on a large scale. From now on, programmes to control stubborn (see Chapter 7) must take into account natural transmission of the disease.

Other virus and virus-like diseases

Cachexia -xyloporosis

Cachexia (see Figs 38 to 59) was seen on many satsuma trees in the Mahdasht orchard (Mazandaran province). Some of these trees carry a double infection: cachexia and tristeza. In the Ramsar Experiment Station, 60-year-old satsuma trees on sour orange rootstock showed mild cachexia symptoms (gum in the bark).

TABLE 34 Host plants of Neoaliturus haematoceps and M tenellus

Notes:
¹ From the following references Calavan and Bové, 1989: Fos et al, 1986; Frazier, 1953; Freitag, Frazier and Huffaker, 1955; Huffaker e, al, 1954: Nielson, 1975.
² From: Calavan and Bové, 1989: Huffaker et al, 1954; Nielson, 1975.

Cachexia has been reported previously in the Caspian Sea area, near Sari-Ouaem Shar and Tonekabon (Habashi, personal communication; Ebrahimi, 1985). Cachexia was also seen at the Isin Citrus Station, Hormozgan province, on "Bami" local mandarin trees.

It is not surprising to find cachexia in Iran. The disease is present worldwide and many old-line cultivars of mandarin, Clementine, satsuma and tangelo carry the disease. Importations of old lines from Egypt, Israel, Italy, Japan, Lebanon, Morocco, Turkey and the former USSR have probably introduced the disease into Iran. The pathogen is also present in many old-line cultivars of sweet orange, grapefruit and lemon, but these species are tolerant of cachexia, and only indexing on indicator plants such as Parson's Special mandarin (see Figs 58 and 59) or detection of the viroid RNA by sPAGE (see Chapter 7) will confirm the presence of the pathogen in these species.

The cachexia viroid is mechanically transmissible, but is not spread by vectors other than humans and can be readily eliminated from citrus by shoot-tip grafting.

Ring pattern disease

This disease is characterized by spectacular leaf patterns, including ringspots, chlorotic spots and line patterns, as shown in Figs 123 and 124. Sunken lines and ring patterns are conspicuous on fruits (see Fig. 124). The disease is concentrated in the area around Chalus-Now Shar in the Caspian Sea region, although symptoms were also seen on satsuma fruits in the Mahdasht orchard near Sari. The disease mainly affects satsuma, Clementine and local sweet orange trees, and also Palestine sweet lime. No symptoms have been seen on lemon and shaddock trees. Habashi, from the Virus Diseases and Pests Laboratory at Tonekabon, has graft-transmitted the disease to citrus seedlings including local sweet orange (Fig. 124). Shang she tangerine has been found to be a good indicator plant (Ebrahimi, Anvari and Shakholleslami, 1988).

The disease does not seem to be naturally transmitted. The presence of ring pattern symptoms on 50-year-old local sweet orange seedling trees is explained by Iranian workers by the occurrence of root grafts between healthy and affected trees as a result of root cuts following soil ploughing. No symptoms of bark scaling are associated with ring pattern disease in Iran. The disease may be similar to syndromes described in California (Wallace and Drake, 1968), Sicily (Catara and Grasso, 1968), Spain (Planes and Marti, 1972), Greece (Keramidas, 1975) and Corsica (Vogel and Bové, 1980), where no bark symptoms accompany those on fruit and leaves. It differs from those in Florida and Texas (Timmer and Garnsey, 1980) and Argentina (Pujol and Benatena, 1965), where the disease seems to spread naturally and is associated with bark lesions. Mechanical transmission of ring pattern in Iran has not yet been carried out.

Ringspot virus can be easily eliminated by shoot-tip grafting (Arroyo, 1984) and the same should be true for the ring pattern agent.

Woody gall-vein enation

At the Minab Experiment Station (Hormozgan province) and at the Jiroft Development Organization (Kerman province), large collections of citrus have been planted on small-fruited acid lime rootstocks. Typical woody gall symptoms were observed by Bové on the lime rootstocks of Campbell, Frost (Fig. 130) and Olinda Valencia late sweet orange trees, as well as on Kinnow and Batangas mandarin trees. The trees did not seem to be greatly affected by the disease. The three orange and two mandarin cultivars were introduced in 1971-72 from the Willits and Newcomb nurseries in California and were supposed to be certified free of known virus and virus-like diseases of citrus.

It is surprising to find woody gall on these trees. It is known that the pathogen is naturally transmitted in a persistent manner (see Chapter 3) by the aphids T. citricida, M. persicae and A. gossypii, the latter two being present in Iran. It is unlikely, however, that natural transmission is responsible for the presence of woody gall in the trees, as the orchard is planted as single rows of each cultivar, and the disease is only seen on certain rows, i.e. on certain cultivars but not on others. This pattern of disease distribution does not fit insect transmission.

At Jiroft, woody gall was seen on Moro sweet orange trees, again imported from Willits and Newcomb. Finally, woody gall was seen on the Bakravi rootstock of a local mandarin tree in an orchard near Jiroft (Fig. 131). Interestingly, Bakravi is supposed to be a hybrid between mandarin and small-fruited acid lime. The lime parent is probably responsible for Bakravi being susceptible to woody gall.

Woody gall disease is accompanied by vein enation leaf symptoms on certain citrus species such as small-fruited acid lime and sour orange. Seedlings of these species can be used for indexing purposes. Enations begin to appear five to eight weeks after graft inoculation of bark from infected candidate trees. Galls also develop on lime seedlings but they appear several weeks after the enations. They develop more extensively on rough lemon and Citrus volkameriana seedlings. It would be interesting to index some of the woody gall-infected trees in Iran for vein enation development on lime seedlings.

In conclusion, the use of an unorthodox, woody gall-sensitive rootstock - namely small-fruited acid lime - has revealed infection with the woody gall virus in certain cultivars.

Exocortis

Exocortis, a viroid disease characterized by bark scaling in various rootstocks (P. trifoliata, citranges, Rangpur lime - see Table 7, p. 25), has been reported by Iranian workers in citrus orchards of the Caspian Sea region. At the Kotra Experiment Station, Ebrahimi showed Bové severe cases of exocortis on Sanguinella sweet orange trees grafted on P. trifoliata rootstock (Fig. 83). The Sanguinella sweet orange was imported in 1934 from Italy. The disease was similarly observed on the P. trifoliata rootstock of a Clementine tree, also of Mediterranean origin. In addition to bark scaling of the rootstock, these trees were severely stunted.

Worldwide, many old-line cultivars are known to be infected with the exocortis agent. Sweet orange, mandarin, grapefruit and lemon being tolerant, infected cultivars of these species will induce exocortis symptoms only when grafted on susceptible rootstocks (see Table 7). On sour orange, a tolerant root stock, no symptoms will develop. Hence, the distribution of exocortis in Iran might be much wider than revealed by trees grafted on P. trifoliata. Indexing for exocortis on Etrog citron (selections 60-13, 861-S1) (see Fig. 90) is easy and fast, and will reveal infection of tolerant scion-rootstock combinations.

Finally, it must be remembered that the exocortis viroids are mechanically transmissible with knives, scissors, pruning tools, etc. which can carry the disease agent from infected trees to healthy ones. Therefore, the presence of infected nursery or orchard trees alongside healthy trees is a hazard and must be avoided, unless careful disinfection of tools with bleach (5 percent sodium hypochlorite solution) is carried out. The same is true for the cachexia viroids.

Impietratura

The impietratura pathogen induces gum pockets (see Figs 116 and 117) in the albedo of many commercial citrus species (see Table 7). On ripening fruits, affected areas remain green longer (see Fig. 116). On mature fruits, they are often sunken. Impietratura, a widespread Mediterranean disease, has been reported by Iranian workers at various locations of the Caspian Sea region. Bové was shown the disease at the Kotra Experiment Station on fruit from 19-year-old Washington navel trees introduced from Willits and New-comb in 1963-64. The imported citrus plant material being certified free of virus and virus-like diseases, the presence of impietratura on these trees is surprising.

The symptoms of impietratura were first recorded in 1930 in Israel, but they were thought to be due to a physiological disorder (Reichert and Hellinger, 1930), and the infectious nature of the disease was only established in 1961 (Ruggieri, 1961). In addition, indexing for impietratura is not easy when fruit symptoms are to be obtained. Only in 1970 was it reported that impietratura-infected trees also show flecking on young leaves (Bar-Joseph and Loebenstein, 1970), similar to that known as "psorosis young leaf symptoms". It is possible, therefore, that the citrus material imported from California in 1963-64 had not yet been specifically indexed for impietratura. Another possibility is that the seedlings used as rootstocks for the 1963-64 California citrus material were already infected with the impietratura agent by previous grafting with infected buds that did not take, but did transmit the impietratura agent.

Concave gum

Concave gum disease is characterized by broad, conspicuous concavities (see Figs 102 to 106) on trunk and limbs of susceptible species such as sweet orange, mandarin and tangelo (see Table 7). Gum accumulates between wood and bark, and oozes out through cracks in the bark, especially in species such as Washington navel sweet orange and Orlando tangelo. Gum-filled wood layers may alternate with normal layers and result in gum-stained rings, as seen on cross-sections of branches and limbs. In addition, so-called psorosis young leaf symptoms are characteristic of infected trees.

Concave gum disease was observed by Bové at the Kotra Experiment Station on Washington navel sweet orange trees introduced from Willits and Newcomb in 1963-64. The trees showed gum accumulation between bark and wood, and gum pockets in the wood.

As in the case of impietratura, the presence of concave gum symptoms on citrus imported from California is surprising. Concave gum is an old, well-known disease, and it is easy to index on the basis of psorosis young leaf symptoms. Here again, the most plausible explanation is the use of infected rootstock seedlings.

Scaly bark psorosis

Scaly bark psorosis (Psorosis A) affects sweet orange, grapefruit, mandarin and tangelo (see Table 7). It has been reported from the Caspian Sea area. Bové was shown a case on a 60-year-old "du Bey" sweet orange tree on sour orange rootstock at the Ramsar Experiment Station.

Cristacortis

Cristacortis results in stem pitting (see Figs 109 to 115) of sweet orange, sour orange, mandarin, etc. (see Table 7). It has been found by Rahimian in the Babol and Sari areas of the Caspian Sea region on blood orange and satsuma trees grafted on sour orange rootstock. Stem pitting was seen not only on the scion, in particular on young branches, but also on the sour orange rootstock, a characteristic symptom of the disease. The affected trees showed psorosis young leaf symptoms, which are also typical of cristacortis. Graft transmissions of psorosis young leaf symptoms have been obtained, but it was too early to see stem pitting on the graft-infected seedlings.

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