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Chapter 6: Short description of major citrus diseases in the near east
Viroid and viroid-like diseases
Virus and virus-like diseases
Diseases involving phloem restricted prokaryotic
agents
Fungal
diseases
Bacterial diseases: Citrus canker
Bibliography
Viroid and viroid-like diseases
Cachexia and exocortis are diseases caused by viroid RNA molecules (see Tables 2 and 3, p. 11-12). Gummy bark is included in this chapter because its symptoms on sweet orange are similar to those of cachexia on mandarin. The possibly viroid nature of gummy bark is under investigation. Grapefruit trees affected by the new]y discovered Kassala disease show gum impregnation of the grapefruit bark similar to that of cachexia in mandarin and gummy bark in sweet orange. Unlike gummy bark and cachexia, Kassala disease has not yet been shown to be graft-transmissible. Its possibly viroid nature is also being investigated.
Cachexia
Xyloporosis was first described as a disease affecting sweet lime rootstocks in the country then known as Palestine (Reichert and Perlberger, 1934). In 1950, a disease with symptoms resembling those of xyloporosis, but affecting Orlando tangelo, was described under the name of cachexia in Florida (Childs, 1950) and shown to be caused by a graft-transmissible agent. Later, both diseases were considered to be caused by the same agent, and the expression "cachexia-xyloporosis" came into common usage. The terms cachexia and xyloporosis have been widely used as synonyms, but this view has recently been challenged (Roistacher, 1988).
The agent of cachexia is of a viroid nature (Semancik et al., 1988) (see Tables 2 and 3) and induces pitting of the woody cylinder (stem pitting) and bark gumming in mandarin, tangelo, sweet lime, Citrus macrophylla and some other citrus types (see Tables 5 to 8, p. 21-27). Bark gumming shows up when the trunk of an affected tree is scratched with a knife to remove the outer layers of bark at the bud-union area (Figs 38, 40, 42, 49 and 52). Removal of a piece of bark across the bud-union line is required to see pits in the stem (Figs 38, 41, 44 and 54). If the tree is affected by cachexia, the cambial face of the piece of bark will show pegs matching the pits in the stem (Figs 39, 41, 43, 45 and 55).
In addition, the presence of gum can be seen within the bark (Figs 39, 41, 43 and 45). Symptoms range from the severe in Orlando, Wekiwa and Seminole tangelos, Clementine and Parson's Special mandarin, Murcott and Ellendale tangors (C. sinensis x C. reticulata), to the undetectable in sweet orange, sour orange, grapefruit and trifoliate orange. Symptoms occur on the trunk of infected trees, above or below (Fig. 57) the bud-union according to the position of the susceptible variety. In severe cases, bark cracking (Figs 47, 52, 55 and 57) and pinholing (Figs 51 and 53) are observed.
Since the cachexia-xyloporosis viroid is perpetuated by the use of infected budwood and no insect vector is known, it can be eliminated from new plantings by the use of healthy propagation material. Parson's Special mandarin on a vigorous rootstock is used for indexing (Roistacher, Blue and Calavan, 1973) (Figs 58 and 59).
Gummy bark of sweet orange
This is a graft-transmissible disease which affects sweet orange trees in some Mediterranean countries and most countries of the Near East region (Nour-Eldin, 1956, 1968). The disease is suspected to be of a viroid nature. Diseased trees are usually stunted, and when the bark of the trunk above bud-union is scraped it shows gum deposits (Figs 60 to 62, 66, 69, 70 and 73). Removal of a piece of bark across the bud-union is required to see stem pitting (Figs 64 and 66). Symptoms of gummy bark on sweet orange resemble those Of cachexia-xyloporosis on mandarin, but the cachexia agent fails to induce any symptoms on sweet orange and the gummy bark agent does not cause symptoms on mandarin. Rough lemon is also susceptible to the gummy bark agent (Nour-Eldin, 1981). Sweet orange trees on rough lemon exhibiting gummy bark symptoms in sweet orange scion also show bark pegging and gumming, and stem pitting on the rootstock, as well as bud-union crease (Figs 74, 75 and 77). The amount of gum in the sweet orange bark above bud-union can be considerable and, in such cases, bark scaling is observed (Figs 68 and 69). No vector is known. Propagations from only healthy trees are recommended for preventing the introduction of the problem into new orchards.
Gummy bark has never been reported from North or South America and, until recently, the disease was thought to be of little concern. However, its prevalence in the Near East countries shows it to be of major importance.
Kassala disease
This disease of grapefruit trees was seen for the first time in Kassala in the Sudan by Bové in 1987. The affected trees show gum impregnations in the bark and mild stem pitting (Figs 80 to 82). The symptoms resemble those of cachexia on mandarin or those of gummy bark on sweet orange. However, the amount of gum in the bark seems to be smaller, even though bark gumming can extend up to 2 m above bud-union. The disease was seen on Foster and Marsh seedless grapefruit trees in many parts of the Sudan. Cases were also seen in southern Yemen. Kassala disease has not yet been shown to be graft-transmissible. However, its putative viroid nature is under investigation.
Exocortis
Exocortis disease is caused by a viroid or complex of viroids (Duran-Vila et al., 1988) and has been reported from practically all citrus-growing areas of the world (see Tables 2 and 3). The disease affects Poncirus trifoliata and most of its hybrids, especially the citranges, as well as Rangpur lime, Palestine sweet lime, some citrons and lemons and a number of other citrus varieties. It is symptom-less in many varieties, such as sweet and sour oranges, grapefruits, mandarins and rough lemon (see Tables 5 to 8). Therefore its symptoms are only manifested when exocortis viroid-infected budwood taken from symptomless carriers is used for propagation on susceptible rootstocks. Symptoms of exocortis include stunting of trees, bark splitting and scaling of the rootstock portion of the tree (Figs 83, 85 to 87). The time for bark scaling to appear usually ranges from four to eight years on trees budded on P. trifoliata or Rangpur lime rootstocks. Bark symptoms of exocortis, including yellowing of the bark of young branches, also appear when susceptible varieties such as P. trifoliata (Figs 319 to 321) and citron (Figs 88 and 89) are used as scion and rootstock become infected.
No insect vector is known for exocortis, but the viroid is transmissible via sap to citrus and non-citrus herbaceous hosts, and it is quite resistant to heat, drying and some chemicals (Garnsey and Weathers, 1972). Etrog citron and lemons are apparently effective sources of contamination of cutting instruments. Decontamination of budding knives and other tools by the use of household bleach or other solutions containing 5 percent sodium hypochlorite is recommended to prevent the spread of the disease in nurseries and commercial orchards. Mechanical transmission of exocortis in the field also seems to be affected by the nature of the donor and host plants. Infected Etrog citron plants of certain selections, e.g. "60-13" or "861-S1", develop leaf epinasty and are used as indicators for exocortis (Fig. 90).
The disease known as exocortis and characterized by tree stunting, bark scaling and shoot blotching of P. trifoliata is induced by the well-known CEV. Additional viroids have been identified in various field trees, in which they occur as mixtures of two to six different viroid groups. Those of groups 1, 111 and IV are believed to be responsible for mild forms of the exocortis disease. The cachexia viroid is part of group II. (See also Tables 2 and 3.)
Diseases with psorosis young leaf symptoms
Psorosis young leaf symptoms were first described in the case of scaly bark psorosis (psorosis A) (Fawcett, 1933). They range from pure vein flecking (Fig. 91) to a mixture of vein flecking and oak-leaf pattern (Figs 92 to 96).
The symptoms are induced by several graft-transmissible agents, namely those of scaly bark psorosis (psorosis A and B), ringspot, concave gum-blind pocket, impietratura and cristacortis, and are thus shared by several diseases. The well-characterized crinkly leaf and infectious variegation viruses (Ilarvirus group) are also able to induce these symptoms. Leaf flecking is sometimes considered specific to scaly bark psorosis, while oak-leaf pattern is thought to be characteristic of concave gum-blind pocket. In Corsica, no such specificities could be observed. Here even sources of budwood producing only leaf flecking or oak-leaf pattern in California induced both symptoms on young leaves. Similar observations have been made in Spain (Moreno, personal communication).
The psorosis young leaf symptoms fade as the leaf matures and require cool temperatures for expression. The trunk symptoms associated with scaly bark psorosis and concave gum-blind pocket usually require at least two or three years for expression. On the contrary, the psorosis young leaf symptoms show up very early on young trees, a long time before the trunk symptoms appear. In such cases, the leaf symptoms only indicate that the trees are infected with any one of the above disease agents. They do not permit identification of the agent involved.
Many commercial citrus varieties exhibit psorosis young leaf symptoms (see Table 7): sweet orange, mandarin, grapefruit, etc. Seedlings of sweet orange, mandarin or dweet tangor are used as indicator plants. The symptoms to be observed are those shown in Figs 91 to 96. Inoculated indicator seedlings should be kept in a cool greenhouse (18-25°C).
The psorosis complex: psorosis A (scaly bark psorosis), psorosis B and ringspot
Psorosis A. The agent of psorosis A or scaly bark psorosis is easily graft-transmissible and induces psorosis young leaf symptoms (vein flecking and/or oak-leaf patterns) as well as bark scaling on the trunk and major branches of susceptible varieties such as sweet orange (Figs 99 to 101), grapefruit and mandarin (see Table 7). Varieties such as sour orange and lemon (see Table 8), which remain free of bark scaling, do however show young leaf symptoms.
Wallace (1978) described the development of bark scaling as follows. Lesions first appear as very small, pimply eruptions, followed by scaling of the bark in dry, irregular flakes. On older, active lesions, the bark breaks away in fairly extensive sections at the margins and new bark forms within the lesion area. There is a continuous cracking and sloughing of dead tissue. Bark lesions usually develop first on the trunk and primary limbs. Initially, there may be a single lesion, but sometimes several lesions begin at about the same time. Gum deposits are sometimes evident under the scales and gum may exude, but gum is not a consistent accompaniment. Lesions may encircle small branches, large limbs and even the trunk, causing parts above the encircled area to deteriorate. Advanced decline is experienced when bark scaling has become severe, affecting large areas and encircling the trunk.
Most sources of psorosis A induce shock symptoms on sweet orange, dweet tangor and small-fruited acid lime seedlings. The shock reaction is defined as the sudden wilting and necrosis of young shoots which develop after inoculation.
Scaly bark psorosis exists worldwide and has caused considerable damage. No insect vectors are known and mechanical transmission in the field has not been observed. The disease can be eliminated easily by the use of disease-free propagative material.
Psorosis B. Psorosis B is a severe form of psorosis A in which bark lesions are rampant and expand rapidly, with sloughing of large strips of bark (Fawcett, 1933; Fawcett and Bitancourt, 1943). Twigs develop gum-impregnated lesions. Symptoms are observed on mature leaves (Fig. 97) and include ringspots and/or large irregular chlorotic patterns with the lower leaf surface showing brownish gum-impregnated eruptions. Psorosis B occurs in the field, but it can also be induced experimentally when a psorosis A lesion is used as inoculum to graft-inoculate young sweet orange seedlings. Bark blistering and scaling quickly develop on the seedling stem and psorosis B mature leaf symptoms appear. These severe reactions do not appear on sweet orange seedlings previously inoculated with psorosis A non-lesion bark. This challenge inoculation can be used to identify the agent present in non-lesion bark as that of psorosis A.
When severe bark scaling is observed in the orchard, it is not always easy to determine whether one is dealing with psorosis A or psorosis B. However, the presence of symptoms on mature leaves with gum-impregnated eruptions on the lower leaf surface (Fig. 97) is indicative of psorosis B.
The agent of psorosis B can be mechanically transmitted from citron to non-rutaceous, herbaceous plants and back to citron. Graft transmission from the mechanically infected citron back to sweet orange results in psorosis B symptoms.
Ringspot. In the United States of America and Argentina, many isolates of CRSV are associated with bark scaling of sweet orange and grapefruit. In several aspects this bark scaling resembles that of psorosis B. More generally, CRSV and the agent of psorosis B have the same host range and induce essentially the same symptoms, including psorosis B mature leaf symptoms. The two agents are mechanically transmissible to a number of herbaceous hosts and cause diagnostic local lesions on Chenopodium quinoa. Recently, several psorosis A isolates have been shown to induce the same type of lesions on C. quinoa. Furthermore, CRSV shows cross-protection against the agent of psorosis B. Interestingly, the original isolate of CRSV described by Wallace and Drake (1968) did not protect against psorosis B. Therefore, citrus ringspot as described by Timmer and Garnsey (1980) and psorosis B as described by Fawcett and Bitancourt (1943) are considered synonymous by Timmer and Garnsey.
In Argentina, a form of psorosis-like bark scaling is spreading naturally (Beñateña and Portillo, 1984). This is also happening in Texas (Timmer and Garnsey, 1980) and Florida, but to a much lesser extent. An aphid vector is suspected in Argentina, but this needs confirmation. It seems clear, however, that the transmitted agent in both North and South America is CRSV, even though, in Argentina it is called psorosis.
In the Mediterranean and the Near East countries, ringspot patterns can be observed on sweet orange fruits and leaves in the absence of bark scaling, suggesting that this type of ringspot is not caused by CRSV. This shows that more than one agent may induce ringspot patterns in citrus. (See the section on ringspot diseases in this chapter.)
Final elucidation of the relationships between psorosis A and psorosis B or ringspot requires that the agents involved in this so-called psorosis complex be identified and characterized. This work is in progress.
Concave gum-blind pocket
The symptoms of concave gum-blind pocket were first described in California (Fawcett, 1936; Fawcett and Bitancourt, 1943), but the disease exists worldwide. The term "concave gum" refers to conspicuous broad concavities of various sizes on trunk or limbs (Figs 102 to 106), with concentric gum deposits present in the layers of wood beneath. Gum-filled layers may alternate with normal layers and gum may exude through a crack in the bark at certain seasons. Washington navel sweet orange and Orlando tangelo are especially good producers of gum.
The term "blind pocket" refers to relatively large, longitudinal depressions of trunk or limbs with the two lateral sides of the depressions coming close together (Fig. 102). Gum is rarely forced to the surface. Concave gum and blind pocket often occur together on the same tree (Fig. 102) and are thought to be due to a single agent. Psorosis young leaf symptoms are also characteristically associated with the disease.
Cristacortis is another disease in which depressions appear on the trunk and limbs, but these are much smaller than those of concave gum-blind pocket and the pits in the stem correspond to matching pegs on the cambial face of the bark. No stem pitting-bark pegging is associated with the depressions or concavities of concave gum-blind pocket. For a full description of cristacortis, see the section below.
Severe symptoms of concave gum-blind pocket can be seen on mandarin, tangelo and sweet orange trees. Symptoms can be so severe that the trunks are completely deformed. Sour orange is tolerant. See Tables 5 to 8 for further host range data.
No vectors are known. Seed transmission of an agent inducing psorosis young leaf symptoms in P. trifoliata and Troyer and Carrizo citranges has been reported and could be the agent of concave gum-blind pocket.
Infectious variegation-crinkly leaf
The agent of infectious variegation-crinkly leaf (Fawcett and Klotz, 1939) is an ilarvirus (Uyeda and Mink, 1983) (see Table 1, p. 10). It was one of the first citrus viruses to be mechanically transmitted (Grant and Corbett, 1961) and purified (Corbett and Grant, 1967; Davino and Garnsey, 1984) (see Table 9, p. 33). CLRV (Garnsey, 1975) is serologically related. Symptoms affect leaves and fruit of lemon, sour orange, sweet orange, grapefruit, citron, satsuma, etc. In the case of the more severe infectious variegation virus, leaves are variegated, somewhat crinkled and distorted, irregular in outline and narrow. They can also be boat-shaped. With the milder crinkly leaf virus, the major leaf symptoms are crinkling (Fig. 107), warping and pocketing. Leaf size is normal or even larger than normal and there is little or no variegation. Both strains of the virus cause chlorotic pinpoint spotting. Crinkly leaf virus and, especially, infectious variegation virus may cause lemons to be small, coarse, bumpy and misshapen. Infectious variegation virus has a marked effect on lemons, satsumas, oranges (Fig. 108), grapefruits, etc.
Under field conditions in Corsica, it is difficult to tell the two diseases apart by the leaf symptoms only. On experimentally inoculated Hamlin sweet orange, Wase satsuma and Eureka lemon trees, leaf symptoms are similar to those of the crinkly leaf (Fig. 107) rather than the variegation type. However, only infectious variegation virus induces fruit symptoms on sweet orange and satsuma, although both viruses induce symptoms on lemon fruits.
The virus is present in most Mediterranean countries, the United States of America, Argentina and Australia. Lemon seedlings are good indicator plants. Cowpea (Vigna sinensis) can be used for mechanical inoculation. Immunosera are available for serological detection.
Cristacortis
The cristacortis disease was first described by Vogel and Bové (1964) in Corsica on Tarocco sweet orange trees grafted on sour orange rootstock, and shown to be a distinct disease (Vogel and Bové, 1968, 1972). Previously, trees with cristacortis symptoms were thought to be affected by xyloporosis or concave gum-blind pocket. The disease is widespread throughout Mediterranean countries and certain islands (Corsica, Sardinia). In northern Yemen (Figs 109 to 115), the disease was probably introduced from Italy via Ethiopia. Susceptible species are numerous and include tangelo, sour orange, sweet orange, mandarin, satsuma, grapefruit, rough lemon and sweet lime (see Table 7). Only one of many isolates is able to induce symptoms on lemon. Small-fruited acid lime is among tolerant varieties (see Table 8).
On leaves, symptoms are vein flecking and oak-leaf patterns (psorosis young leaf symptoms). Symptoms also affect trunk, limbs and shoots, and are typically vertical or lengthwise depressions or pockets (Figs 109 and 114) due to pits in the wood (Figs 110, 112, 113 and 115) with corresponding pegs on cambial side of bark (Figs 111, 113 and 115). With certain species, such as tangelos, gum-like material stains the tissues at the top of the peg and bottom of the pit. Young pits in the wood can occur without accompanying external depressions, and depressions, even severe ones, disappear with time as a consequence of radial growth. Traces of previous depressions and pitting remain buried in the wood, and can be seen in cross-sections as radially oriented clear lines perpendicular to the wood layers. These radial traces of previous pits are of diagnostic value and distinguish cristacortis from concave gum-blind pocket in which the stain beneath the concave depressions follows the concentric wood layers. Although old depressions disappear, new pits and pegs can develop anywhere on the tree.
Cristacortis is probably the only disease inducing stem pitting on sour orange. The presence of stem pitting on the sour orange stock, in addition to stem pitting on the scion, is valuable for diagnosis.
The cristacortis agent is easily graft-transmitted. Leaf and trunk symptoms can be induced by placing pollen from infected trees under the bark of Orlando tangelo seedlings (Vogel and Bové, 1980). However, natural spread of cristacortis by pollen has never been observed.
Impietratura
Impietratura, a disorder that affects citrus fruit, is considered to be of a viral nature, based on graft transmissibility (Ruggieri, 1955, 1961). The disease has been found in most citrus-growing countries of the Mediterranean basin: Algeria, Cyprus, France (Corsica), Greece, Israel, Italy, Lebanon, the Libyan Arab Jamahiriya, Morocco, Portugal, Spain, the Syrian Arab Republic, Tunisia and Turkey. Its symptoms have also been seen in Saudi Arabia, Somalia and the Islamic Republic of Iran. Trees affected by impietratura display leaf vein clearing and oak-leaf patterns (psorosis young leaf symptoms) and characteristic fruit symptoms, though not all fruits on diseased trees are affected. Affected fruits are small, malformed and hardened, hence the Italian name of the disease impietratura, meaning that the fruits become as hard as a stone. Affected fruits have characteristic gum pockets in the albedo (Figs 116 and 117) resulting in protuberances on the fruit surface. However, it should be remembered that boron deficiency also induces gum pockets in the albedo. During ripening, affected areas appear green (Fig. 1 16). Protuberances can disappear as fruits approach maturity and affected areas may remain depressed. Among susceptible varieties are bergamot, Clementine, grapefruit, lemon, rough lemon, sour orange, sweet orange and Citrus volkameriana (see Table 7). Citron, on the other hand, is tolerant (see Table 8).
Impietratura causes heavy losses to citrus growers because of off-season fruit drop, and because affected fruits are not suitable for commercial export. In some instances, as much as 80 percent of the fruit from impietratura-infected trees is unmarketable as fresh fruit and has to be processed for juice, if not discarded. Finally, infected trees do not show symptoms regularly each year. A tree with badly affected fruit this year might well produce normal fruit the following year. The reasons for this behaviour are not known.
Satsuma dwarf
The agent of satsuma dwarf is a well-characterized, isometric RNA virus (26 nm in diameter) with two nucleocapsid components (see Table 1). The disease is widespread in Japan where it was first described by Yamada and Sawamura (1952). It has since been reported from China and the Korean peninsula. In Turkey, about 2 percent of the satsuma trees on P. trifoliata grown in the Izmir region, and probably of Japanese origin, are affected by satsuma dwarf. In addition they carry tristeza virus. There is probably also a similar situation in the former Yugoslavia and Albania. Satsuma trees affected by satsuma dwarf are stunted and look bare because the shoots are short (short internodes) and the leaves small. The typical symptom is mature, boat-shaped leaves (Fig. 118). In cultivars other than satsuma, symptoms are mild or absent.
The virus has been mechanically transmitted to many herbaceous plants (see Table 9). In Japan, local natural spread, apparently by a soil-borne vector, has been observed. Symptomless infection occurs in a windbreak tree, China laurestine (Viburnum odoratissimum), which markedly enhances natural transmission (Koizumi et al., 1988).
Antibodies against SDV are available and are used in ELISA to detect the virus. Indexing can also be done by mechanical inoculation to white sesame.
Yellow vein clearing
Yellow vein clearing (Figs 119 to 122) is a new, as yet unidentified, disorder that was first seen on lemon leaves in Pakistan. The disease is described and compared with known disorders in Chapter 17.
Ringspot diseases
Several agents probably induce ringspot patterns in citrus, but the most studied agent is CRSV. Two filamentous RNA nucleocapsids, one short and one long, have been detected and both are required for infectivity. CRSV and psorosis B are considered synonymous (see the section above on psorosis), as their host range (see Table 7) and symptoms are essentially the same. Symptoms affect leaves and trunk, and sometimes fruit. Symptoms on young leaves are variable, but they usually include irregular yellow spots (Fig. 126), and some ring patterns (Fig. 124), which may coalesce and form mottled chlorotic areas (Fig. 123). Necrotic etching may also occur. The chlorotic patterns persist in mature leaves (psorosis B mature leaf symptoms). Trunk symptoms on sweet orange and grapefruit trees consist of psorosis B-type bark scaling. Furthermore, on soft stems up to 1 cm in diameter, yellowish blotches may appear and develop into necrotic lesions (stem lesions) encircling the stem and causing the parts above it to die. This reaction is different from the psorosis A shock reaction. Fruit may also exhibit ringspot symptoms (Figs 124 and 127).
Field trees may show the above symptoms. Leaf symptoms and stem lesions are best seen on experimentally graft-inoculated seedlings of sweet orange and grapefruit.
CRSV (or psorosis B) can be mechanically transmitted to citrus and to numerous herbaceous hosts. All isolates produce chlorotic to necrotic local lesions in C. quinoa but infection does not become systemic. For best results, fully expanded leaves of C. quinoa should be inoculated with fresh inoculum prepared from a symptomatic young flush. Tatterleaf-citrange stunt virus also infects C. quinoa but, in contrast to CRSV, infection is systemic.
Ringspot is not always associated with bark scaling. For instance, in Greece, 30-year-old Navelina sweet orange trees showed ringspot patterns on leaves but no bark scaling. In Corsica, a 30-year-old Clementine tree without bark scaling was infected with a ringspot agent as shown by graft inoculation to Parson's Special mandarin and Etrog citron. In the Islamic Republic of Iran, ring pattern disease (Figs 123 and 124) occurs in the absence of bark scaling, especially on sweet orange. In Spain, two ringspot isolates not associated with bark scaling showed yellow spots and rings with sharp edges in old leaves, shoots and fruits. These isolates differed from the ringspot isolates associated with bark scaling in that they did not induce a shock reaction on inoculated seedlings, did not cross-protect against psorosis B, were not mechanically transmissible to C. quinoa, and did not have associated to them a 48 kDa protein usually present in psorosis A and B and other CRSV isolates. Whether the ringspot agents apparently not associated with bark scaling are isolates of CRSV remains to be seen.
Finally, the CRSV (psorosis B agent) is naturally spread in Argentina, perhaps by an aphid vector (Beñateña and Portillo, 1984). In Texas and Florida, natural transmission occurs, but to a much lesser extent than in Argentina (Timmer and Garnsey, 1980).
Tristeza
Tristeza is a very destructive virus disease which affects trees of sweet orange, mandarin, grapefruit and other cultivars - but not lemon -when they are grafted on sour orange and certain other rootstocks (see Tables 5 to 8). It occurs in most citrus-growing areas of the world and is naturally spread by aphids. It has been reported from Argentina, Australia, Brazil, China, Israel, Japan, Paraguay, Peru, the United States of America (California), Uruguay, Venezuela, Southeast Asia in general and most countries of sub-Saharan Africa. Tristeza has destroyed about 25 million trees in South America and about 3 million in California. The disease represents a very serious threat to citrus in the Mediterranean and Near East countries, one of the last areas still essentially free from the virus and planted extensively with the intolerant scion-sour orange combination. In Spain, large-scale spread of tristeza began in 1957 in the Alcira-Carcagente-Corbera district of the province of Valencia. Since then it has caused the death of about 15 million trees. More recently, tristeza was found to be spreading in Israel. In spite of an extensive eradication programme based on ELISA for CTV testing, the virus could not be eradicated and has produced severe damage in certain areas.
The symptoms of tristeza disease on susceptible scion-rootstock combinations include stunting and slow dieback (trees take two, three or more years to die) or quick decline with sudden wilting, defoliation and death of the tree (within a few months following infection). Trees showing the slow decline type of tristeza generally develop an overgrowth of the scion trunk just above the bud-union. These reactions result from the basic histological symptom, namely the collapse and death of sieve tubes in the sour orange phloem below the bud-union. When a strip of bark is removed across the bud-union of tristeza-affected trees on sour orange, exposed wood shows bristly pegs fitting into the pinholes of the cambial side of the bark (Fig. 129).
CTV, in addition to the typical tristeza disease, i.e. the disease of trees on sour orange, is also responsible for stem pitting, a disorder that occurs in susceptible varieties, independent of the rootstock (see Tables 5 to 8) (McClean, 1974b). Stem pitting refers to small or long depressions or grooves in the wood of shoots, branches and trunk, and its early stages may be observed by removing the bark. Generally, the pits in the outer wood have corresponding pegs or projections on the inner surface of the bark. Species or varieties most susceptible to stem pitting are acid limes, grapefruit, Citrus macrophylla, Citrus hystrix, and certain sweet orange varieties such as Pera in Brazil and Mediterranean sweet in South Africa (Salibe, 1977). Leaves of CTV-infected, small-fruited acid lime seedlings and other sensitive varieties show CTV-specific vein clearing (Fig. 128), a symptom which is of diagnostic value. The presence and intensity of vein clearing and/or stem pitting in a given variety depends on the CTV strain involved. Polyclonal and monoclonal antibodies against CTV are available and widely used for tristeza virus detection by ELISA.
A third abnormal condition related to the presence of tristeza virus is "seedling yellows", a reaction experimentally induced by tissue-graft inoculation of certain strains of the virus into young seedlings of sour orange, grapefruit, lemon and some citron (Wallace, 1957).
CTV is a member of the closterovirus group (Bar-Joseph, Garnsey and Gonsalves, 1979). It is a flexuous filament about 2 000 nm long and 12 nm in diameter (see Fig. 1). Many strains of this virus, varying in pathogenicity, are known to occur. CTV is transmitted by aphids (see Table 10, p. 34) in a semi-persistent mode (Bar-Joseph, Raccah and Loebenstein, 1977) (see Table 11, p. 38). Toxoptera citricida, known as the brown or black tropical aphid (see the drawing on p. 36), is an efficient vector of CTV, since a single insect moving from an infected to a healthy tree can transmit the virus. Much less efficient vectors, where movement of about 50 individuals is required for transmission, are the aphids Aphis gossypii, Aphis spiraecola, Toxoptera aurantii and Myzus persicae. T. citricida has not been found in the Mediterranean basin or the Near East, but it is present in parts of India, most countries of Southeast Asia, sub-Saharan Africa, Central and South America. This insect has the ability to adapt to various climatic conditions and to spread rapidly from country to country. Recently it entered Venezuela, resulting in the destruction of 400 000 trees within five years. It has also recently been found in Costa Rica, El Salvador and Nicaragua, showing a clear movement towards the Northern Hemisphere.
Another alarming discovery was that tristeza virus can mutate, causing changes that permit rapid spread by alternative aphids. In California, tristeza in its more severe seedling yellows form was found to spread rapidly when carried by A. gossypii (Roistacher et al., 1980). In Israel, it was shown that this same aphid could transmit tristeza virus strain VT at a rate averaging 40 percent, compared with a rate of less than 5 percent with two other strains (Bar-Joseph and Loebenstein, 1973). Favourable climatic conditions allowing the buildup of high aphid populations, as happened in Spain and Florida after freeze damage, may lead to the rapid dissemination of tristeza. Mechanical transmission under controlled laboratory conditions has recently been achieved (see Table 9).
Generally speaking, the citrus areas of the world may be currently divided into three categories in relation to tristeza.
Category I. This includes areas in which practically all citrus trees are infected with the virus, or where the virus is spreading rapidly -the vector being T. citricida - namely Southeast Asia; Australia; Africa south of the Sahara; and most South American countries.
Category II. This includes areas not yet infected by the virus, but in which most trees are susceptible to the disease. T. citricida is not present. Mediterranean countries (except Spain and Israel) and Mexico and certain areas of the United States of America are in this category.
Sour orange is used extensively in these areas. Isolated declining trees have been found to be infected with the virus in this region, but no evidence of field spread has been observed except in Spain and Israel. T. citricida has not been reported here, but other aphids exist.
Category III. This includes citrus areas where the tristeza virus is known to be spreading but the vector is not T. citricida.
Vein enation-woody gall
The agent of vein enation-woody gall (CVEV) is probably a luteovirus (Da Graca and Maharaj, 1991). The virion is 28 nm in diameter (see Table I). CVEV induces two types of symptoms (Wallace and Drake, 1960): enations on the veins of citrus species such as small-fruited acid lime, sour orange and rough lemon, and galls on the stem or trunk of small-fruited acid lime (Fig. 130) Citrus volkameriana and rough lemon. In Iran, galls were also observed on Bakravi rootstocks, a hybrid of small-fruited acid lime and mandarin (Fig. 131). In the field, sour orange and small-fruited acid lime develop strong enations and galls are seen on rough lemon and small-fruited acid lime growing near thorns or in association with wounds. The pathogen is transmitted in a persistent mode by several aphid species, including T. citricida, M. persicae and A. gossypii (see Table 10). Symptoms of the disease occur in Australia, California, India, Japan, Peru and Spain. In the Near East the disease has been seen in Iran and Turkey, although it is relatively unimportant. From the point of view of interaction between viruses, there is a synergistic effect between vein enation virus and yellow vein virus, in that the symptoms induced by yellow vein virus are strikingly enhanced by co-infection with vein enation virus (Weathers, 1960, 1961). Also, it has been shown in Japan that CVEV protects against tristeza virus (Koizumi and Sasaki, 1980).
Bud-union crease
Bud-union crease is an abnormality characterized by an intermittent or continuous necrotic line in the wood at the union of certain scion-rootstock combinations (Figs 132 to 135). Corresponding pegs or projections on the inner surface of the bark are also present (Fig. 135). Sometimes gum impregnation occurs in the affected area (Figs 132 and 133) and bark breaks easily at the bud-union line (Fig. 133). Trees with the disorder often die while young or remain stunted. Some forms of bud-union crease result from genetic incompatibilities, while others have been shown to be graft-transmissible (McClean, 1974a). Common scion-rootstock combinations showing bud-union crease include Shamouti (a Palestine Jaffa), Bloodred, Musambi and Pera oranges on rough lemon rootstock; Pera orange on Volkameriana lemon; and Lisbon and Eureka lemon on trifoliate orange. McClean has shown that bud-union crease of Triumph grapefruit on rough lemon and of lemon on trifoliate orange are non-transmissible. In the case of Shamouti sweet orange on rough lemon rootstock, certain abnormal bud-unions could be reproduced by graft inoculation, but others may be due to seed transmission of the pathogen or represent true incompatibility. Graft-transmissible bud-union crease of Cadenera sweet orange and a navel clone on rough lemon has recently been described in Spain. The causal agent of this crease could be eliminated by shoot-tip grafting (Navarro et al., 1992). Bud-union crease is also seen in the case of gummy bark-affected sweet orange trees on rough lemon (Figs 74 and 75). A graft-transmissible agent inducing bud-union crease of Parson's Special mandarin on Citrus volkameriana has been reported (Vogel and Bové, 1988).
Rumple
Rumple affects lemons of certain clones of Lisbon and some other varieties (Knorr and Koo, 1969), and is known in Cyprus, Ethiopia, Italy, Lebanon, Spain, Turkey and the United States of America. The disorder appears in late summer, first as faint chlorotic speckles on the rind surface of the fruit, which then turns brownish-black and finally collapses. Large fruits develop a higher incidence of rumple than smaller ones. The number of affected fruits varies from year to year and from orchard to orchard. There are no apparent tree symptoms. Rumple is suspected to be of a viral nature but no definite proof has been presented. Careful selection of budwood from disease-free trees is recommended for propagation in order to avoid the problem in new plantings.