Decline of citrus trees in Pakistan
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Extent of the decline
In his 1970 FAO report, Chapot mentioned that a relatively large number of trees were declining and showed dieback. In 1987, Bové encountered the same problem in all the citrus areas visited, on mandarin (Fig. 215) as well as on sweet orange trees (Fig. 216). Thus it appears that the decline affecting citrus is not new, even though it may appear so when it affects young trees that grew well at first, and that begin to show symptoms only after three or four years. This is the case in the Sahiwal Horticultural Research Station (SHRS). Four-year-old Bloodred (Figs 216 and 217) and Musambi sweet orange trees, planted in the field in 1982-83, began to show decline after the winter of 1985-86.
Symptoms of decline included: overall pale green-yellowish colour of foliage; mature leaf drop and replacement of normal-sized leaves by small ones; a high proportion of small leaves, at least at some periods of the year (compare left and right halves of the tree in Figure 217); upright position of small leaves along shoots; zinc-deficiency symptoms on the small leaves but without green islands on an overall yellow blade; mild leaf mottle on old leaves; dieback; and stunting. The above trees were four years old at the time of examination. Older trees at SHRS showed the same decline. The disease is in no way restricted to local varieties such as Bloodred and Musambi sweet oranges, as symptoms were observed, for instance, on Sanguinelli trees introduced from California to SHRS in 1977.
Cases of decline with similar symptoms, i.e. greening-like symptoms, were also observed in commercial orchards in the Sahiwal-Okara district. In one orchard, Pineapple sweet orange trees on rough lemon planted in 1979 presented the typical decline syndrome: leaf drop resulting in many small, but few normal-sized, leaves. In this orchard, Catara noticed greening-like trees in January 1987 and was able to detect, by electron microscopy, greening organisms in the fruit axis of a Maltese (Vaniglia) sweet orange (Grimaldi and Catara, personal communication).
Severe decline was also noticed in the Renala Kurd district on ten-year-old Valencia late sweet orange trees on rough lemon rootstock. Trees with many small leaves were again seen. The declining trees in this orchard looked, more than anywhere else, like greening-affected trees, even though leaf mottle was not much more pronounced than elsewhere. However, one of the declining trees showed severe inverse stem pitting and bark pinholing. In this orchard, there were many empty spaces indicating that several trees had died. From the age of the remaining normal or declining trees it was evident that the trees had reached a fair development before they became affected.
Many cases of declining sweet orange trees have been observed at the Tarnab Agricultural Research Institute near Peshawar, NWFP. It was in this experiment station that, in 1976, Cochran noticed symptoms of greening in the variety collection. He also found many nursery trees infected. In the meantime, in 1981, a new collection of 25 sweet orange varieties on sour orange rootstock was planted with material from SHRS. Most of the trees are stunted and in a severe state of decline. As these trees are on sour orange, CTV may be involved in the decline. Indeed, CTV was detected by electron microscopy in samples of a Vaniglia sweet orange tree. The greening organism was not detected in this tree, but was positively identified by electron microscopy in two sour orange seedlings. These results clearly indicate that greening is present in the Peshawar area, as is D. citri, the psyllid vector of the greening bacterium (Fig. 210). Cochran (1976) had also noticed that D. citri was abundant in the variety orchard, in the nursery and on ornamental sour orange hedges.
Not only sweet orange, but also mandarin trees are affected by the decline problem. At the Tarnab Agricultural Research Institute, both Kinnow and Feutrell's early mandarin trees were affected. The symptoms are similar to those on sweet orange trees: leaf drop, small-sized leaves, some zinc deficiency and leaf mottle, and dieback. Similar declining Kinnow mandarin trees were seen at the Faisalabad Agricultural Research Station. Too much irrigation by flooding and excessive ploughing for clean cultivation could be part of the decline problem, but greening is most likely to be the principal cause. Indeed, Catara was able to detect the greening organism at the Faisalabad Research Station in samples of rough lemon leaves with yellow midveins (Grimaldi and Catara, personal communication). The seriousness of the decline problem on mandarin trees is best illustrated by Figure 215, showing a commercial Kinnow mandarin orchard near Lahore with many declining, dieback-affected, greening-like trees.
Finally, there were declining grapefruit trees on rough lemon rootstock, which were planted in 1977, at SHRS. They began to show symptoms of decline in 1984, two years before the sweet orange trees. The symptoms were stubborn-, or greening-like: small, cupped leaves, with some mottle and small fruit with aborted seeds. One tree (Marsh JBC 430, sample 19) was found to be infected with CTV.
Cause of decline (dieback) in Pakistan
Arguments for greening as the cause of citrus decline in Pakistan.
Arguments based on symptomatology and symptom development. Both the symptoms of decline and their development in sweet orange and mandarin trees in Pakistan are similar to those of citrus greening disease, i.e. dieback, in India. In 1976, Cochran diagnosed greening on the basis of the following symptoms and facts:
D. citri, the psyllid vector of the greening BLO, is present in Pakistan throughout the citrus-growing areas of the NWFP and the Punjab. The psyllid population peaks in March and April after the spring flush of growth, with a second peak in the autumn.
The sour orange leaves in which the greening BLO was detected by electron microscopy came from seedling plants. Since the greening BLO is not transmitted through seeds, infection of these sour orange seedlings must have been by the psyllid vector. Numerous D. citri psyllids were seen feeding on citrus and sour orange leaves when the leaves were collected for electron microscopy.
The greening BLO and its vector D. citri are both present in the Indian provinces bordering Pakistan, so it is not surprising that they are present in the latter country. Greening is very widespread in India (see Table 42), and the citrus psyllid is very common in almost all parts of the country, becoming a serious pest of citrus during spring and early summer in western and central India and some parts of the north. Populations decline with the onset of the hot season and the monsoon, but reappear during autumn flushes. Populations are low during winter months in northern India (Raychaudhuri, Nariani and Ahlawat, 1977).
Arguments against greening being the cause of citrus decline.
Leaf symptoms. The consultant did not see strong, typical symptoms of leaf mottle, though this may have been on account of the time of year when the survey was carried out (April). Leaf mottle is often seen on mature leaves and, as mentioned several times above, at the time of the survey affected trees had few mature leaves as these had fallen off.
Even though leaves of affected trees showed zinc-deficiency symptoms, the type of symptom related to zinc deficiency - dark green spots on a yellow leaf - was rare.
Difficulty in detecting the greening BLO. The greening BLO could only be detected in sour orange leaves in the Peshawar district. Many other leaf samples from NWFP and the Punjab were examined by electron microscopy, but no greening organisms could be seen, in spite of the large number of sections scanned. Similarly, Grimaldi and Catara (personal communication) also state that "the number of affected samples was rather low and only one or two adjacent phloematic sieve tubes appeared infected".
The difficulty in detecting the greening BLO could be due to the lack of adequate plant material at the time of the survey. As stated above, leaves with typical mottle or with green spots on yellow leaf blades were rare and these are the leaves in which the greening BLO is best detected by electron microscopy. Also, in April most of the fruit had already been picked. Fruit axes, which are very good samples for detection of the greening BLO, were therefore unavailable.
Conclusion. The greening BLO is present in Pakistan, and decline of citrus in Pakistan is probably due to the greening BLO.
The results of this survey, as well as those of Grimaldi and Catara (personal communication), prove that citrus greening disease is present in Pakistan, as is the psyllid vector, D. citri. Does this mean that greening is responsible for the general decline of citrus in Pakistan? The answer to this question would be an unambiguous "yes", if the greening BLO had been detected more frequently in samples from affected trees. Since this is not the case, the answer, at this time, can only be "probably yes". In other words, it is very likely that the decline of citrus in Pakistan is essentially due to greening. The arguments in favour of this conclusion have more weight in the author's opinion than those against. However, additional work must be done to show more consistently the presence of the greening BLO in decline-affected trees.
Additional causes of decline. Even if greening is probably the major cause of citrus decline in Pakistan, other causes can also result in decline and dieback of citrus.
CTV infection is however not the cause of decline in the case of sweet orange trees grafted on rough lemon, since this rootstock is tolerant of CTV. In such cases, and in spite of CTV infection, greening is the most probable reason for decline. This situation is similar to that in India, where tristeza is widespread and was once wrongly thought to cause decline.
The extent of tristeza virus infection
CTV was detected at several sites in Pakistan.
Sahiwal Horticultural Research Station (SHRS). Typical symptoms of vein clearing (Fig. 128) were seen on leaves of a large, small-fruited acid (Kagzi) lime tree on rough lemon rootstock. Vein clearing of lime leaves is specific to CTV infection and, indeed, the presence of the virus in this tree was confirmed by ELISA and electron microscopy. The tree had been propagated by grafting a bud from a lime seedling on a rough lemon rootstock seedling. As CTV is not transmitted through seeds, infection must be the result of insect transmission of the virus. Indeed, aphid vectors of CTV are known to be present in Pakistan (see below). If so, other trees, including mandarin, sweet orange and grapefruit, at SHRS must also be infected, though if they are grafted on CTV-tolerant rootstocks (rough lemon, citranges, etc.) their infection can only be detected by indexing on Kagzi lime indicator plants, by ELISA or by electron microscopy. Bundles of CTV virions were indeed seen by electron microscopy in leaves of a Marsh JBC 430 grapefruit tree. This tree showed no stem pitting, suggesting that the strain of CTV involved is one of those milder strains that do not induce stem pitting symptoms on grapefruit.
Similarly, the above CTV-infected lime tree showed no stem pitting. The lack of this symptom, as well as the large size of the tree, suggests that infection with CTV is either relatively recent or that the strain of CTV involved is mild.
Okara district (northeast of Sahiwal - Mian Muhammad Shafi citrus orchards, Burj Jiwe Khan). A declining, greening-like Bloodred sweet orange tree, examined by electron microscopy for the presence of the greening BLO, was found to be infected with CTV.
Similarly, in the same orchard, Grimaldi and Catara (personal communication) observed CTV virions in a fruit axis from a declining Pineapple sweet orange tree on rough lemon rootstock. In spite of their infection with CTV, these trees do not decline because of CTV since sweet orange trees on rough lemon rootstock are tolerant to CTV. Greening is probably the cause of the decline. Many more trees in this orchard may be infected with CTV.
Peshawar district (Tarnab Agricultural Research Institute). Many of the trees in the sweet orange collection, which are grafted on sour orange rootstock and were planted in 1981, are stunted. A stunted Vaniglia sweet orange tree was chosen as a representative tree and electron microscopy showed it to be infected with CTV. Since sour orange is a CTV-susceptible rootstock, infection by CTV of the Vaniglia sweet orange tree, and probably of other trees in the collection, explains the stunted condition of these trees. The trees in the collection were propagated with plant material from SHRS. Since CTV is now known to be present at SHRS, CTV-infection of the above Vaniglia tree (and probably of other sweet orange trees) could be due to the use of CTV-infected buds from Sahiwal.
However, there is also the possibility that the tree(s) in the Tarnab collection became infected by insect transmission of CTV. Indeed, another tree was found to be infected with CTV, namely a sour orange tree growing along a roadside. This tree is probably an ungrafted seedling tree and, if so, infection of the tree with CTV must have been through insect transmission.
At the time of writing, tristeza is not known to be present in the Peshawar district, where sour orange is the only rootstock used. It is urgent that the CTV-susceptible sour orange rootstock be replaced by CTV-tolerant stocks, such as rough lemon.
Insect vectors of CTV in Pakistan
Toxoptera citricida, the black tropical citrus aphid and the most efficient vector of CTV, is not present in the NWFP or the Punjab. However other aphid vectors of CTV are present. Aphis gossypii, the cotton aphid, is an efficient vector of several strains of CTV, but is usually not abundant on citrus. Toxoptera aurantii, also present in Pakistan and abundant on citrus, is able to transmit CTV under experimental conditions, but is probably not a significant vector. Myzus persicae occurs as well, and is a vector in India.
CTV and its vectors in India
Table 42 shows that CTV is widespread in almost all the citrus-growing areas of India. In several provinces severe strains of CTV are present. These strains are defined by Ahlawat and Raychaudhuri (1988) as those which induce vein clearing as well as stem pitting in Kagzi (Mexican) lime indicator seedlings. Mild strains cause only vein clearing. Some strains produce stunting and chlorosis in seedlings of sour orange, acid lemon or grapefruit.
This reaction, called seedling yellows, is used experimentally to detect severe isolates of the virus. As shown in Table 42, certain citrus regions of India possess CTV strains that cause seedling yellows (Ahlawat and Ray-chaudhuri, 1988).
The presence of severe strains of CTV as well as of strains producing seedling yellows is related to the presence of T. citricida (see Table 42).
Ahlawat and Raychaudhuri (1988) have shown that severe strains of CTV and seedling yellows strains are restricted to places where T. citricida occurs. Elsewhere, A. gossypii, Aphis craccivora, M. persicae and Dactynotus jaceae are the vectors, but they are less efficient.
As shown in Table 42, the Indian provinces that border Pakistan are free of T. citricida, as well as of seedling yellows and severe strains of CTV.
The same situation seems to be true in Pakistan, where T. citricida does not occur and where no stem pitting was seen on CTV-infected Kagzi lime and grapefruit trees, suggesting that the CTV strains involved in these cases were mild. However, more work must be done to identify the type of CTV strains present in Pakistan.
CTV is present in NWFP and the Punjab. From the absence of T. citricida, it can be deduced that probably only relatively mild strains of CTV occur and the absence of stem pitting on CTV-infected Kagzi lime and grapefruit trees supports this conclusion. The mild strains present in Pakistan are, however, capable of inducing decline of citrus trees (except lemon) when grafted on sour orange rootstock, as shown by the stunted, CTV-infected, Vaniglia sweet orange tree and probably many other trees in the collection block of the Tarnab Agricultural Research Institute. Therefore, sour orange must be replaced by CTV-tolerant rootstocks such as rough lemon.
During his survey, the author examined many Kagzi (Mexican) lime trees for symptoms of CTV infection (vein clearing and stem pitting). Vein clearing was seen on only one occasion -at SHRS (see Fig. 128). This suggests that aphid vector transmission of CTV is still rare. The results of the survey have shown that CTV was discovered in three of 20 trees that were examined, not because tristeza was suspected but because greening was thought to be involved. This is quite a high percentage (15 percent) of infection. More randomly selected trees must be analysed to determine more precisely the percentage of CTV infection. In any case, the number of CTV-infected trees appears higher than first thought. The origin of the infection probably derives from the propagation of CTV-infected buds, rather than active aphid transmission (see above).
The commercial citrus species (sweet orange, mandarin, grapefruit and lemon) do not show symptoms of exocortis. They are symptomless carriers of the exacortis agent, a complex of various viroids. Hence, when grafted on exocortis-susceptible rootstocks such as P. trifoliata, citranges, Rangpur lime, sweet lime or citron, they infect these rootstocks which, after a period of time, show symptoms of exocortis, namely, bark scaling (see Figs 83 to 87) and/or stunting.
Sour orange and rough lemon are also symptomless carriers of the exacortis viroids, so, contrary to the above susceptible rootstocks, do not show symptoms of the disease. Therefore, exocortis infection cannot be detected by visual examination of scion-rootstock combinations such as sweet orange, mandarin or grapefruit on sour orange or rough lemon rootstock. Indexing is required to diagnose exocortis in these symptomless trees. The indicator plant for exocortis indexing is Etrog citron selection 861-51 (see Fig. 90).
In Pakistan, sour orange in the NWFP and rough lemon in the Punjab are the major rootstocks - hence no symptoms of exocortis could be seen in commercial orchards. It is, however, highly probable that many sweet orange, mandarin, grapefruit and lemon cultivars carry the exocortis agent. Indeed, in citrus experiment stations where exocortis-susceptible rootstocks have been tried, exacortis disease is frequently observed in rootstock experiments in which scion varieties of unknown health status have been used.
This is precisely the case in three of the four research stations visited. At the Tarnab Agricultural Research Institute (Peshawar district) the seven-year-old Bloodred sweet orange trees on Troyer citrange in the high density block are very small for their age and show severe symptoms of exocortis (bark scaling) on the citrange rootstock (Fig. 87). At the Sargodha Horticultural Research Substation, severe symptoms of exocortis were seen on the rootstock of Valencia late sweet orange trees on Carrizo citrange in the rootstock block. It is probably the same Valencia late sweet orange variety that has induced exocortis symptoms on Troyer, Carrizo and Yuma citranges in the block of Valencia late sweet orange trees on various rootstocks at SHRS. These results show that the Bloodred and Valencia late sweet orange scions used in these experiments were infected with the exocortis viroid(s) and probably with other pathogens too.
Rootstock and other experiments must only be carried out with budwood that has been shown by indexing to be free of viruses, viroids and virus-like agents. As stated above, visual examination of a candidate tree selected for budwood collection is totally inadequate as a means of establishing health status - good-looking, symptomless trees may be symptomless carriers of several infectious agents such as exocortis, cachexia, tristeza, etc.
The importance of these considerations is related to the problem of CTV. Control of tristeza implies, in particular, the replacement of the sour orange rootstock by CTV-tolerant rootstocks such as rough lemon, P. trifoliata, citranges, citrumellos, Rangpur lime and sweet orange. As indicated above, some of these are susceptible to exocortis (and/or cachexia). To reiterate, it is therefore imperative that citrus cultivars to be budded on these rootstocks be free of the agents of exocortis, cachexia and, preferably, all other citrus diseases. They must be indexed to determine their true health status.
Gummy bark of sweet orange and cachexia of Mandarin
The symptoms of gummy bark are seen on sweet orange and consist of gummy deposits in the bark. When the bark is scraped, circumferential reddish-brown, gum-impregnated streaks are visible (see Figs 60, 61 and 63). These symptoms are similar to those induced by the cachexia viroid in mandarin. In mild cases or early stages of gummy bark, the discoloration is near the bud-union. In severe cases or later stages, it can extend upwards for a metre or more. In addition to gum impregnation of the bark, the sweet orange wood can show some stem pitting (see Fig. 64) with corresponding pegs (see Fig. 65) on the cambial face of the bark.
Gummy bark-infected sweet orange trees on rough lemon rootstock develop bud-union constriction or crease. There are, however, cases of bud-union crease on rough lemon which are not due to the gummy bark agent.
The author has seen severe cases of gummy bark in the Islamic Republic of Iran, Iraq, Oman, Saudi Arabia, the Syrian Arab Republic, Turkey and southern Yemen. In Yemen, gummy bark-affected sweet orange trees on rough lemon rootstock showed not only sweet orange bark gumming and bud-union crease, but also, sometimes, severe stem pitting and bark pegging on the rootstock.
Two mild but clear-cut cases of gummy bark were found in Pakistan. At the Tarnab Agricultural Research Institute, gummy bark was seen on two sweet orange varieties, Akay Sekeri and Trablus, both of Turkish origin. Similarly, at SHRS, gummy bark affected two sweet orange varieties of Turkish origin, Kozan and, again, Trablus.
The cambial side of a piece of bark removed across the bud-union of a declining Kinnow mandarin tree (Sargodha district) showed mild pegging on the mandarin bark, and severe pegging on the rootstock bark. The tree indexed negatively for CTV. The rootstock is probably rough lemon (rough lemon sprouts occurred on neighbouring trees). The pegging on the rootstock bark is similar to that observed in Yemen on rough lemon rootstocks of gummy bark-affected sweet orange trees. Whether or not this pegging is due to the gummy bark agent should be further investigated by graft-transmission experiments. The mild pegging on the mandarin bark (see Fig. 55) suggests cachexia. Similar symptoms were noticed on several other Kinnow mandarin trees in the same orchard (Sargodha district, village 26 Nb, Nasar Ullah Khan Orchard), as well as on a Feutrell's early mandarin tree at the Faisalabad Research Station. In all of these cases, there were no gum deposits in the mandarin bark. The absence of such bark gumming makes it difficult to conclude unequivocally that the mild bark pegging (and the corresponding stem pitting) is due to cachexia. Graft-transmission experiments to Parson's Special mandarin, a variety highly susceptible to the cachexia viroid, or analysis using sPAGE (see Table 13, p. 47) are required to confirm the presence of cachexia.
At SHRS the cambial face of a piece of bark removed across the bud-union of a Palestine sweet lime tree on rough lemon rootstock showed conoid pegs on the sweet lime bark, with corresponding pits in the scion stem. These symptoms correspond to those first described by Reichert and Perlberger (1934) under the name xyloporosis on sweet lime used as rootstock or as unbudded seedling. It now appears that cachexia and xyloporosis are not synonymous and that the disease in sweet lime (xyloporosis) is probably not caused by the cachexia viroid (Roistacher, 1988).
In conclusion, gummy bark of sweet orange is of only minor importance in Pakistan. Interestingly, no typical symptoms of cachexia were seen on the many Kinnow and Feutrell's early mandarins examined. As can be seen from Table 41, cachexia does not seem to have been reported from India.
Sweet orange, grapefruit or lemon trees on sour orange or rough lemon rootstock are symptomless carriers of the cachexia pathogen. It is more than likely that old-line cultivars of these varieties are infected with the cachexia viroid. Indeed, at SHRS, in the Musambi sweet orange block on various rootstocks, trees on Sylhet mandarin showed cachexia-like symptoms on the rootstock. Mandarins are susceptible to the cachexia viroid. Indexing on Parson's Special mandarin is required to confirm the presence of the cachexia agent in the Musambi sweet orange cultivar.
Only cachexia viroid-free cultivars should be propagated, especially if cachexia viroid-susceptible rootstocks such as Rangpur lime or tangelos are to be used.
Bud-union crease of sweet orange trees on rough lemon rootstock
Several cases of bud-union crease were noticed on Bloodred, Musambi, Valencia late and Pineapple sweet orange trees on rough lemon rootstock. In the case of Bloodred and Musambi sweet oranges the symptoms correspond to those described by Nour-Eldin (1959) for Blood orange on rough lemon in Egypt, and by Bhutani, Bakhshi and Knorr (1972) for Bloodred and Musambi sweet oranges in India in old trees. The bud-union shows a pronounced bulge or protrusion with a rough, uneven surface, forming a prominent collar or fissure of eruptive bark encircling the trunk(Fig. 133).
With Valencia late and Pineapple sweet oranges, an irregular and almost continuous ring of gum-impregnated projections is present on the cambial face of the bark at the bud-union line, which fits in the crease in the wood. Bark breaks easily at the constricted bud-union line, revealing gum deposits at the union (Fig. 133).
According to McClean (1974), the symptoms shown by Bloodred and Musambi sweet oranges correspond to a severe form of the disease, while those seen on the other two sweet oranges represent a milder form. This author has provided evidence that the bud-union crease of sweet orange trees on rough lemon rootstock is caused by a graft-transmissible pathogen. The disease is controlled by using new-line sweet orange on rough lemon where old lines are found to make abnormal unions.
Leaf yellow vein clearing - An unidentified disorder of lemon trees
Figures 119 to 122 illustrate the symptoms of yellow vein clearing of lemon leaves in Pakistan. These are best seen with transmitted light. Under such conditions, parts of the lateral veins let the light pass through and appear as translucent yellow flecks or lines of varying length, though generally not involving the entire vein. The yellow flecks may extend laterally into the tissue adjacent to the veins. The midveins show little clearing even on leaves with severely affected lateral veins (Figs 120 and 121). These symptoms are markedly different from those of citrus yellow vein disease as described in California (Weathers, 1960, 1961), where the first symptom to appear is a bright yellowing of main veins and yellowing is usually continuous along the petiole, midrib and main lateral veins. Lemon develops much less severe California yellow vein symptoms than does West Indian lime -symptoms are generally restricted to an occasional young leaf. For these reasons, yellow vein clearing in Pakistan seems to be different from citrus yellow vein in California.
Symptoms of yellow vein clearing on lemon leaves somewhat resemble CTV-induced vein-clearing of acid lime leaves, but the vein clearing symptoms on lemon are yellow and much more pronounced than those due to CTV on lime (compare Figs 120 and 128). However, lemon is tolerant to CTV and, inversely, yellow vein clearing has never been seen on acid lime. The two diseases thus appear to be different.
Citrus ringspot, as described by Wallace and Drake (1968) and Desjardins, Drake and French (1969), on lemon, grapefruit, sour orange, etc. is characterized by strong symptoms of ringspot, with the ring effect sometimes extending along the veins. At times the first symptom to appear (especially on sour orange) is a distinct tristeza-type vein clearing which, however, later disappears or develops into rings or blotches. Ringspots have not been observed by the author in the case of yellow vein clearing.
Sometimes lemon leaves with yellow vein clearing are crinkled (Fig. 122). In the Peshawar district, many sour orange seedlings, planted closely together in a row to form a hedge, showed yellow vein clearing and, in addition, many leaves were crinkled, warped and bumpy with wavy edges. Citrus crinkly leaf virus (Fawcett and Klotz, 1939; Fraser, 1961) also induces leaf warping, pocketing, blistering and crinkling on lemon. Irregular, small, narrow leaves with chlorotic, variegated areas varying in degree of chlorosis are additional symptoms of the more severe infectious variegation strain. A virus resembling citrus crinkly leaf virus has been reported in India (Ahlawat and Sardar, 1976a; see also Tables 41 and 42). However, the infectious variegation-crinkly leaf virus does not seem to be involved in yellow vein clearing of lemon in Pakistan, as serum against the former virus did not react in ELISA with yellow vein clearing-affected lemon leaves (Catara, personal communication).
Yellow vein clearing seems to be widespread in Pakistan. The disorder was observed on sour orange near the Tarnab Agricultural Research Institute; in Sihala on lemon of an unidentified variety; in the Faisalabad Research Station and Renala Kurd on Eureka lemon; and on the following lemon varieties or selections at SHRS: Allen, Cascade and Cook Eureka; Frost Eureka; Frost Lisbon; and Foothill and Limoneira 8A Lisbon. This list is not exhaustive. The following additional lemon varieties have shown yellow vein clearing in Islamabad at the National Agricultural Research Centre (NARC): Corona Eureka; Caver's old line, Caver's new line, Monachello new line and Molla Mehmet (Catara, personal communication).
Catara further notes that lemon seedlings grown from seeds of a tree showing yellow vein clearing are symptomless. This observation indicates that yellow vein clearing is not a genetic disorder, but probably an infectious disease that is not seed-transmitted. In Islamabad (NARC), only one of three trees of the following lemon varieties showed symptoms: Frost Eureka, Caver's new line, Lisbon and Monachello new line; only one of two Molla Mehmet lemon trees had symptoms. Since the symptomatic and the symptomless trees grow side by side, yellow vein clearing cannot be the result of some special soil or environmental condition. This conclusion is strengthened by the fact that recently introduced nucellar varieties of lemon growing close to affected trees are symptomless. More generally, it seems quite reasonable to assume that all the Lisbon, Eureka and other lemon varieties and selections mentioned above, introduced from California to Pakistan, were free of yellow vein clearing when they arrived in Pakistan. Indeed, yellow vein clearing has never been seen in California lemon orchards, nor probably in other parts of the world. It thus seems that the lemon trees of Californian origin became infected in Pakistan. How this happened (by mechanical or insect transmission), the source of the initial inoculum, etc. remain to be discovered.
Host range studies have not yet been made. At present, only lemon and sour orange are known to be susceptible. Rough lemon is probably not, as rough lemon rootstock suckers from affected lemon trees are symptomless.
Near the Tarnab Agricultural Research Institute at Peshawar, along the roadside, there is a hedge of more than 100 sour orange seedlings, 30 of which are affected. These seedlings are not uniformly distributed along the hedge. Twenty affected seedlings are adjacent to each other (one group of 20); in addition, there are three groups of two, and one group of three affected seedlings; only one affected seedling was single. This pattern of distribution suggests plant-to-plant transmission. Mechanical transmission during pruning of the hedge would account for such a pattern. The high percentage of affected lemon trees in commercial orchards could also be explained partly, at least, by mechanical transmission during pruning operations, usually more severe with lemon than with other citrus species. However, propagation of the disorder by buds from infected trees is most probably the major means of dissemination in the nursery. Finally, the absence of symptoms on sweet orange and mandarin trees growing in blocks next to symptomatic blocks of lemon trees might indicate that these varieties are tolerant or immune. In any case, the nature of the disorder, whether graft-transmissible or not' the susceptibility' tolerance or immunity of citrus species to the putative pathogen' the host range of the eventual pathogen, its transmission by mechanical means or by insects, remain to be experimentally studied.
Sour orange bark pegging and gumming
At SHRS there is a block of Musambi sweet orange trees on various rootstocks, planted in 1982-83. Some trees on sour orange (Seville Kimb.) are severely stunted in comparison with trees on rough lemon. This suggests involvement of CTV. However, when one stunted tree was analysed for the presence of CTV by ELISA, no CTV was detected. When a piece of bark from this tree was removed from the trunk across the bud-union, the following symptoms were found: conspicuous stem pitting on the sour orange rootstock with brownish, gum-like material in some pits (Fig. 260); the scion stem was smooth and normal. The cambial face of the removed piece of bark showed pegging, pinholing and staining with gum-like material (Fig. 261) only on the rootstock bark. Two other stunted Musambi sweet orange trees on sour orange rootstock showed the same symptoms. Three normal-sized trees were also examined. Two had no symptoms, but one presented stem pitting and bark pegging on the rootstock similar to that of the stunted trees.
Stunting of the Musambi sweet orange tree on sour orange rootstock is probably related to the symptoms shown by the rootstock, even though one tree with such symptoms is not (yet) stunted. However, the cause of these symptoms is unclear. It is not CTV, for two reasons: ELISA for CTV was negative and the symptoms shown by the rootstock are not those of CTV on sour orange. In severe cases of CTV, the sour orange rootstock shows, below the bud-union, inverse stem pitting with corresponding bark pinholing, but no stem pitting, bark pegging or bark gumming. In fact, such symptoms have never been described on sour orange. The only agent known to induce stem pitting on sour orange is that of cristacortis. However, cristacortis stem pitting on sour orange is very different from the type shown in Figure 52. Therefore, if the symptomatic rootstock is sour orange, the agent responsible for the symptoms appears to be new. There is another possibility however, namely that mislabelling has occurred and the rootstock used is not sour orange. From symptoms shown, a cachexia-susceptible rootstock might be involved.
Witches' brooms of calamondin trees
Typical witches' brooms were seen on several calamondin trees in Lahore.
A serious disease known as witches' broom disease of lime trees has recently been described in Oman (Bové et al., 19X8; and above). Mycoplasma-like organisms (MLOs) are involved. The disease kills the affected trees in a few years and the causal agent is apparently transmitted by insect vectors. It was therefore important to examine leaves from the calamondin witches' broom by electron microscopy for the presence of MLOs. Fortunately, no MLOs were seen.
Witches' brooms are also formed on galls owing to infection by the fungus Sphaeropsis tumefaciens Pledges. However, no obvious galls or knots were seen on the above calamondin trees. Witches' brooms have also been described in the southern parts of Africa in relation to multiple sprouting disease (Schwarz, 1970). Finally, witches' brooms may be due to genetic factors. Experiments are needed to determine if the calamondin disorder is graft-transmissible.
The survey undertaken did not include citrus canker. However, as expected, the disease was found throughout the districts visited: on acid lime at Sargodha, Faisalabad and Sahiwal; on sweet orange at Tarnab, Faisalabad and Okara; and on grapefruit at Faisalabad.
Exportation of citrus from a country where citrus canker is present to citrus-growing countries free of citrus canker is prohibited.
As in many other countries, trees are often budded too low and they are planted too deep, with the bud-union line too close to the soil, if not buried. These inadequate practices favour the development of phytophthora gummosis or footrot.
In Pakistan, the practice of growing winter fodder such as Egyptian clover (Trifolium alexandrium) in citrus orchards and the subsequent irrigation required by such crops also favour phytophthora gummosis. Even in the absence of such crops, citrus seems to be over-irrigated.
In addition, clean cultivation is often presented as the ne plus ultra technique of soil management, and is often obtained by heavy discing. Such operations destroy the surface roots and result in compaction of the soil in the zone below the cultivated area. For these reasons, intensive cultivation is, in general, a destructive practice. It could be a contributory factor in the greening-induced decline of citrus.
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