The disorder of citrus described as `greening' was first reported in 1947 from South Africa, although the disease has been known since 1929. Likubin has seriously affected citrus trees in Taiwan since 1951, while a similar disease known as `huang-lunpin' (yellow shoot) was reported in 1943 in Mainland China.
This virus-like disease, known locally as likubin in Taiwan, leaf mottle yellows in the Philippines, citrus dieback in India, and citrus vein phloem degeneration (CVPD) in Indonesia, has been devastating all citrus-growing areas in Asia except Japan, and is also widespread in South Africa.
The South African greening organism belongs to a heat sensitive form, which induces severe symptoms at cool temperatures (22-24Â°C). The Asian greening organism produces symptoms in either warm temperatures (27-32Â°C) or a cool climate, and is classified as a heat-tolerant form.
The Asian form of greening has been spread rapidly by Asian psylla, and is causing great damage to the citrus industry by shortening the lifespan of trees.
Although the disease syndrome differs to some extent according to citrus variety, common symptoms are yellowing of the veins and adjacent tissues, followed by yellowing or mottling of the entire leaf, occasionally with corking of the veins ( Fig. 1(751)).
This is following by premature defoliation, dieback of twigs, decay of feeder rootlets and lateral roots, decline in vigor, and ultimately, the death of the entire plant. Diseased leaves become hardened and curl outward, while young leaves developed after premature defoliation are small and slender, with symptoms of zinc deficiency ( Fig. 2(714)).
Trees affected with greening become stunted, bear multiple off-season flowers, most of which fall off, and produce small irregularly shaped fruit with a thick, pale peel ( Fig. 4(846)).
The fastidious bacteria (FB) which causes greening exists in sieve tubes ( Fig. 3(841)). Electron microscopy, using serial sections and a three-dimensional configuration can confirm the presence of mature forms of the pathogen, generally rigid rods measuring 350 _ 550 x 600 _ 1500 mm, surrounded by a two-layered envelope, 20 _ 25 nm thick. However, FB bodies are pleomorphic, and produce flexible elongated rods which grow into new organisms (100-250 x 500-2,500 nm), while when they are old they form spherical bodies 700 _ 800 nm in diameter with a thin cytoplasm. Multiplication is generally accomplished by budding, less frequently by binary fission or beading.
Identification of citrus greening is mainly based on the diagnostic symptoms in citrus trees described above, and electron microscopy of the pathogen bodies in phloem sections. Additional indexing can be done by inoculating grafts of more susceptible citrus varieties particularly sensitive to the pathogen, such as Ponkan mandarin seedlings or Tankan tangor seedlings, with the suspect buds, to test for the presence of the pathogen according to symptom expression.
Tissue-graft indexing is done by budding at least four buds from suspect trees onto indicator seedlings (2 buds/seedling) grown under warm conditions.
Propagation with infected buds is the main way the disease is spread. In the orchard, the Asian citrus pyslla , Diapholina citri kuwayama ( Fig. 5(756)) persistently transmits the pathogen. Transmission ability is affected by the biotype of the psyllid: the Taiwan biotype, for example, has a very low transmission rate of less than 1%. However, field transmission of the pathogen by the psyllid vector might be significant, since citrus trees are exposed to infection in the open for quite a long time.
The jasmine orange shrub ( Muraya puniculata), the most suitable host for psyllid propagation, does not serve as an intermediate host for the pathogen. The pathogen moves slowly through citrus trees, and in the early stage of infection tends to remain confined to the localized branches into which it has been introduced by the psyllid vector.
Control of citrus greening can be achieved by such integrated measures as eradicating infected plant material, introducing clean nursery seedlings, and eliminating the insect vectors. Treating affected trees with injections of antibiotics alleviates the symptoms, but does not cure the diseased plants. Prompt elimination of diseased trees is strongly advised.
It is of primary importance to propagate and plant pathogen-free seedlings derived from foundation stock obtained by heat therapy, shoot-tip grafting, health indexing, or nucellar lines.
The vector psylla are controlled by spraying insecticide (e.g. dimethoate) on citrus trees and jasmine orange shrubs when their leaves are sprouting.
The introduction and application of ectoparasites, such as Tetrastichus dryi and T. radiatus, can be used for effective biological control of the psyllid vectors.
Index of Images
Figure 1 Leaf Symptoms of Likubin-Affected Wentan Pummelo (Left), Showing Yellowing and Mottling of Leaves and Vein Corking, Compared to Healthy Leaf (Right)
Figure 2 Leaf Symptoms of Diseased Luchen Sweet Orange. from Left to Right: Young Leaves, Small in Size and Showing Symptoms of Zinc Deficiency (3 Leaves); Mature, Mottled Leaves Which Are Curling Outwards (2 Leaves); Healthy Leaf
Figure 3 The Fastidious Bacteria (FB) Which Causes Asian Greening Disease, Likubin. a. FB Bodies in Sieve Tube, Showing One Body Passing through the Sieve Pore (Arrow); B. Stereomicrograph Showing a Typical Mature FB Rigid Rod Budding from the Lateral Side (Arrow); C. Cross-Section of FB Body Showing Two-Layered Envelope 20 NM (Arrow) Bars = 200 NM
Figure 4 (Above) Diseased Twig with Yellow Leaves and Diseased Fruit of Tankan Tangor. (Left): The Fruit Is Small and Pale Green in Color. a Healthy Green Leaf and Normal Large Fruit Are Shown to the Right.
Figure 5 (below) the Asian Citrus Psylla Diaphorina Citri Kuwayama, Which Transmits the Asian Strain of the Greening Organism
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