Citrus orchards are subject to various diseases, but not all of them cause economically important damages. Some of them are widespread throughout the world, others have an importance restricted to certain citrus areas, others are present only in particular weather conditions. Among these diseases there are some that are made evident in field
Table 4.3 Some diseases of citrus
Fungal diseases Armillaria mellea Elsinoe fawcettii Mycosphaerella citri Phoma tracheiphila
Phytophthora citrophthora and P. parasitica Septoria citri Bacterial diseases Pseudomonas syringae Xanthomonas campestris pv. citri
Armillaria root rot Scab
Greasy spot Mai secco
Phytophthora root rot, Foot rot, Brown rot Septoria spot
Blast and black pit Canker
(Table 4.3) and others in post-harvest (Table 4.4). For some of these a brief description will be done.
It is a fungal disease restrictedly spread in the Mediterranean Basin, around the Black Sea and in Asia Minor, whose causal agent is Phoma tracheiphila. It has been known since 1894, even though the causal agent has been defined afterwards. It attacks mainly lemon and citron trees, but it can infect all species of Citrus, Poncirus and Fortunella. Therefore not only scions but also rootstocks like sour orange, citrange, alemow are susceptible. It is the most serious disease affecting lemon trees in Italy (Salerno and Cutuli, 1992). Infections occur mainly during autumn-winter time with high relative humidity and with a suitable temperature for the growth of fungus at 20 °C approximately. The development of infection is favoured by a vigorous growth of the tree. The infected trees are subject to a more rapid decline if the infection is in the roots and less rapid if apical. The pathogen penetration can proceed through stomata, but it is mostly through wounds deriving from winds, hail storms, frosts and other causes. Through these wounds, the fungus reaches the xylem vessels of the tree from which it spreads systematically. The infection manifests itself with vein chlorosis of leaves, which dry up and can either drop or stay on the tree according to the virulence of the infection, and with reddish or orange colouration of the xylem, that with ageing tends to brown. Quick pruning operations are used to stop apical infections, while root ones are not under control. Chemical treatments, even though repeated, have a limited effect. Cultural operations which interfere with the disease directly or undirectly are exploited as strategy of control. Among these the immediate pruning out and consequent burning of diseased parts of tree are fundamental. The only efficacious means of control against this disease is the use of resistant varieties like Monachello lemon, whose fruit quality, however, is not good.
The best known species of Phytophthora in citrus orchard are: Phytophthora parasitica and P. citrophthora. These fungal species are widespread all over the world and they cause serious soilborne diseases in citrus. Trees are attacked in any age of their life.
In the nursery they provoke a decline of seeds in germinating stage or of seedlings and in field foot, rot and a decay of feeder roots. Fruits affected in field are subject to fruit drop and in packinghouse to brown rot. The fungus penetrates through wounds and develops provoking necrosis and abundant gum exudation of trunk and root decline. The infected trees show leaves with yellow veins. Means of spread are infested plants when they are transplanted in field, the tillage equipment, the irrigation and drainage water and the wind. The excessive soil moisture and air humidity, the low oxygenation of soil and temperatures are essential elements for mycelial growth. P. citrophthora has an optimum development between 24—28 °C while P. parasitica between 30-32 °C. Both the rootstocks and the different grafted species and varieties have a different susceptibility to infection. For instance among rootstocks, trifoliate orange and Swingle cit-rumelo are resistant, sour orange and Carrizo citrange are tolerant, sweet orange and grapefruit are susceptible (Castle etal., 1989). The main strategy is to control the elements which favour the development of the pathogen and to strengthen the resistance of the host. Prevention is the best way to avoid the onset of this disease. Grafting beyond 15 cm high from soil, the lack of stagnant water, an efficacious airing under the tree canopy, the avoidance of every kind of injury, are very important preventive devices. The use of chemical products must be considered as a complementary measure only when the infection has reached economic thresholds.
These are diseases, whose causal agent is Pseudomonas syringae, a bacterium present in endemic form in citrus orchards (Salerno and Cutuli, 1992). This bacterial disease appears in cold and humid weather conditions, concerning above all the twigs of grapefruit and orange trees, and the fruits, in particular of lemon trees, when these have been damaged by wind, hail storm or other shocks that provoke wounds. Blast lesions appear on wings or petioles of leaves, as black areas. The infected leaves dry up and may remain attached to twigs or drop. Black pit lesions appear on fruit. They originate as brown spots on the peel and gradually turn black. Damaged fruit is not suitable for trade. In order to contain the damages of this disease, good cultural practices should be adopted. Orchards should be protected with windbreaks, in order to reduce wind scars, plant vigour should be controlled in autumn-winter time and, if necessary, copper fungicides should be used (De Cicco etal., 1978).
Fungal attacks occur also after the fruit harvest. These infections are not neglected, either because they appear inside packinghouse, with losses for the dealer, or when they are on the market already, discrediting the product. The study of these fungal diseases is important for globalization of markets, for long distance transport needs and the necessity to reduce chemical treatments. A concise description of the symptoms induced on fruit by some of these diseases is made (Table 4.4).
The graft-transmissible pathogens of citrus are reported in Table 4.5 and some of them will be described below.
Table 4-4 Postharvest fungal diseases
Pénicillium digitatum Pénicillium italicum
Green mold Blue mold
Phytophthora citrophthora Brown rot and P. parasitica
There are no external characteristic symptoms. It mostly attacks the mandarin fruits. It reveals itself with the black rot of the central axis and of the segment area near it. The pulp undertakes an unpleasant bitter taste. At first the infected fruit shows some areas of the rind which are from yellowish brown to dark brown. Afterwards a white mold appears which later gains a characteristic gray colour. The rot of the fruit begins with a yellow cream spot, slightly depressed with the softening of the underlying tissue. The rotting fruit gives off an acid odour. At first the infected areas are covered with a white mold which turns green (P. digitatum) or blue (P. italicum). In the advanced stage of infection the fruit decays. The deterioration of the fruit starts with a slight brown discolouration of the rind. The attacked area assumes a firm, leathery appearance. In humid condition it develops a white mycelium. The fruit gives off a characteristic penetrating acid odour.
Table 4.5 Some graft-transmissible pathogens of citrus
Types of pathogen
Citrus variegation Ring spot-psorosis complex Tristeza Virus-like diseases Cristacortis Impietratura Viroid diseases Cachexia Exocortis Systemic prokaryote diseases
Stubborn Diseases caused by unknown agent Blight
Not characterized Virus
Not characterized Not characterized
Spiroplasma citri Not characterized
It is a very important pathogen of citrus for economic damages that it produces and it is liable to increasing spread in new areas. It is a virus, of which many strains have been detected with different virulence. The trees declined owing to this virus in Argentina, Australia, Brazil, Israel, Spain, South Africa, USA and other nations are millions. It infects many species and varieties of citrus. In citrus areas where sweet orange, grapefruit and mandarin were grafted on sour orange rootstock citrus growers were obliged to change this rootstock, because of its susceptibility. The infection manifests itself on sour orange with necrosis of phloem tissue below the bud union and depletion of starch levels. Moreover in the inner face of the bark there can be a thick pinholing or honeycombing. Some strains on lime, grapefruit and sweet orange provoke the stem-pitting and the seedling yellows on seedlings of lemon variety Eureka, grapefruit and sour orange. The symptoms are tree wilting, leaf chlorosis, and reduced fruit size, with final decline of the tree. Beside sour orange, other root-stocks are susceptible. The disease is transmitted by grafting and by several aphid species. Toxoptera citricidus is the most efficient vector among aphids. The effectiveness of transmission depends on aphid species, on strains, on the donor and on the receptor. Various screening tests are available for its identification. The typical biological test is graft-inoculation of Mexican lime seedlings, these react with specific symptoms. At the moment the enzyme-linked immunosorbent assay (ELISA) is the most widely used test because it's cheap and immediate. Spread of the disease can be prevented with quarantine, with eradication programmes, with use of tolerant rootstocks and with budwood sources certified free of tristeza.
According to Garnsey (1999) this complex includes citrus necrotic ringspot, naturally spread psorosis, psorosis A, and psorosis B isolates. In this complex, still not well understood, are probably involved different causal agents with various symptomatologies. The transmission of all isolates occurs with infected budwoods and the control is obtained by using certified budwoods ringspot-psorosis complex free.
This disease, existing in many countries, is caused by a viroid. Its effects occur in citrus orchard when infected material is grafted on susceptible rootstocks like trifoliate orange, some of its hybrids and Rangpur lime (Garnsey and Barkley, 1988). The trees attacked dwarf, rarely decline and the quality of the fruit is not affected. Many species and varieties of citrus and non citrus host are susceptible to exocortis infection. The infected trees of sweet orange, grapefruit and mandarin are asymptomatic when grafted on non susceptible rootstocks. The most obvious symptom of exocortis is bark scaling on the rootstock with consequent stunting of the whole tree. Bark scaling usually begins when citrus trees are from 4 to 8 years old (Garnsey and Barkley, 1988). The disease can be spread by grafting, but it may also be transmitted mechanically by cutting graft tools and pruning equipment. It is just in this way that many trees which were immune have been infected. An indexing method for exocortis utilizes the grafting of a suspected diseased budwood on a Etrog citron clone that reacts with symptoms of epinasty. At the moment there are other detection procedures based on extracts, developed for laboratory analysis, with particular means (Garnsey and Barkley, 1988). In order to get viroid-free budwoods, shoot tip grafting can be used, a form of micrografting of the meristematic apex of a donor plant on a seedling to produce shoots immune from the pathogen. Cutting tools treated with aqueous solution containing 2 per cent sodium hydroxide plus 2 per cent formalin or freshly made 5—10 per cent solution of household bleach are used to prevent viroid mechanical transmission.
It is caused by Spiroplasma citri, a systemic prokaryote organism, smaller than common bacteria and bigger than viruses, wall free. This disease is important in hot and humid areas. Infections are rarely lethal. Among the most susceptible citrus species and hybrids there are: orange, grapefruit, mandarin and hybrids of mandarin (Garnsey and Gumpf, 1988). The causal agent can also infect non citrus plants. The trees infected show dwarfishness and branches with shortened internodes, cupped leaves and chlorosis. Fruits are frequently lopsided or acorn-shaped and small sized, with their stem ends greenish and with seeds often aborted. Stubborn is graft-transmitted from infected trees. There is also a natural transmission with some species of leafhoppers. Identification is made by graft inoculation of highly sensitive citrus varieties, such as sweet orange Madam Vinous, under warm conditions. A definitive diagnostic method is to culture the causal agent on artificial media and confirm its identity by microscopy or by serological test (Garnsey and Gumpf, 1988). Control is achieved by the use of stubborn free budwoods obtained with the shoot tip grafting technique.
It is a disease whose causal agent has not been defined, even though some hypotheses have been proposed. It is known also as Young Tree Decline and Declinio. It is widespread in Australia, Brazil, South America, Florida, Hawaii, South Africa and has widely been studied (Marais, 1990). It occurs in the tree canopy with leaves and twigs wilting, water sprouts on the trunk and zinc deficiency symptoms. It is characterized by zinc accumulation in the bark and xylem of the trunks, in whose vessels there are amorphous plugs which cause lack of water absorption. The symptoms of blight are not totally different from those of decline caused by other agents. Among the most susceptible rootstocks there are: rough lemon, volkameriana, trifoliate orange and Rangpur lime. The infection from the blight affected tree to a sound tree is root graft transmitted, and not by apical grafting. Sour orange and sweet orange rootstocks are more tolerant, but they are not taken into consideration for their susceptibility to tristeza and phytophthora. The kind of soil, cultural practices and nutritional disorders have been related to the incidence of blight. Several means of control have been used, without reducing the incidence of the disease.
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