Candidatus Liberibacter africanus (African greening)
Index
- Pictures
- Identity
- Summary of Invasiveness
- Taxonomic Tree
- Notes on Taxonomy and Nomenclature
- Description
- Distribution Table
- Habitat
- Habitat List
- Hosts/Species Affected
- Host Plants and Other Plants Affected
- Growth Stages
- Symptoms
- List of Symptoms/Signs
- Biology and Ecology
- Notes on Natural Enemies
- Means of Movement and Dispersal
- Pathway Causes
- Pathway Vectors
- Plant Trade
- Vectors and Intermediate Hosts
- Impact Summary
- Impact
- Risk and Impact Factors
- Diagnosis
- Detection and Inspection
- Similarities to Other Species/Conditions
- Prevention and Control
- References
- Contributors
- Distribution Maps
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Top of pagePreferred Scientific Name
- Candidatus Liberibacter africanus (Garnier et al. 2000)
Preferred Common Name
- African greening
Other Scientific Names
- Candidatus Liberibacter africanus Garnier et al., 2000
- Candidatus Liberobacter africanum Jagoueix et al., 1994
- Candidatus Liberobacter africanus
- Liberibacter africanus subsp. africanus
- Liberobacter africanum
- Liberobacter africanus
International Common Names
- English: blotchy mottle of citrus; greening; greening of citrus; huanglongbing; yellow branch
- Spanish: enverdecimiento de los cítricos
- French: greening des agrumes; virescence des agrumes
EPPO code
- LIBEAF
Summary of Invasiveness
Top of pageCandidatus Liberibacter africanus is not considered as invasive as Candidatus Liberibacter asiaticus, however, the species and its vector appear on several alert lists including the EPPO A1 list of Regulated Quarantine Plant Pests. African greening occurs mostly in cooler, moist, elevated production regions (Schwarz, 1967) and symptom expression is temperature dependant, occurring under relatively cool conditions (20-24°C optimum) (Garnier and Bové, 1993). This suggests that Ca. L. africanus is temperature sensitive. This temperature sensitivity coincides with the temperature sensitivity of its natural vector, Trioza erytreae. Temperatures above 30°C, together with relative humidity (RH) below 25%, are lethal to certain life stages of the vector (Catling, 1969). The combined sensitivity of the pathogen and the vector limit the spread of the disease to climatically favourable regions.
Taxonomic Tree
Top of page- Domain: Bacteria
- Phylum: Proteobacteria
- Class: Alphaproteobacteria
- Order: Rhizobiales
- Family: Phyllobacteriaceae
- Genus: Candidatus Liberibacter
- Species: Candidatus Liberibacter africanus
Notes on Taxonomy and Nomenclature
Top of pageFive sub-species of Ca. L. africanus were identified from indigenous rutaceous trees in South Africa i.e., Ca. L. africanus subsp. capensis (Garnier et al., 2000); Ca. L. africanus subsp. clausenae; Ca. L. africanus subsp. vepridis; Ca. L. africanus subsp. zanthoxyli (Roberts et al., 2015) and Ca. L. africanus subsp. tecleae (Roberts and Pietersen, 2017). Sub-species designations were assigned due to close sequence identity to Ca. L. africanus in partial sequences of the 16S ribosomal DNA, rplA/rplJ and omp protein gene regions as well as biological separation of hosts (Roberts et al., 2015; Roberts and Pietersen, 2017). Candidatus Liberibacter africanus subsp. clausenae was subsequently identified from citrus in East Africa (Roberts et al., 2017). The other Ca. L. africanus subspecies have not been detected in citrus.
Description
Top of pageThe bacteria associated with African greening are restricted to the sieve tubes of the phloem vessels. Electron microscopy (EM) studies reveal that they possess the characteristic double membrane cell envelope of the Candidatus Liberibacters (Garnier et al., 1984; Kim et al., 2009). Thin-section EM examination reveals elongated sinuous rods of uneven diameter between 0.15 and 0.25 µm. Round forms of larger diameter can also be observed in degenerating cells. Similar particles were observed in the haemolymph and salivary glands of the insect vector, Trioza erytreae (Moll and Martin, 1973).
Distribution Table
Top of pageThe distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.
Last updated: 23 May 2022Continent/Country/Region | Distribution | Last Reported | Origin | First Reported | Invasive | Reference | Notes |
---|---|---|---|---|---|---|---|
Africa |
|||||||
Angola | Present, Localized | Collected from a commercial farm near Calulo and in a nursery in Luanda. | |||||
Burundi | Present | ||||||
Cameroon | Present | ||||||
Central African Republic | Present | ||||||
Comoros | Present | ||||||
Eswatini | Present | ||||||
Ethiopia | Present | ||||||
Kenya | Present | ||||||
Madagascar | Present | ||||||
Malawi | Present | ||||||
Mauritius | Present | ||||||
Nigeria | Present | ||||||
Réunion | Present | ||||||
Rwanda | Present | ||||||
Saint Helena | Present, Widespread | ||||||
Somalia | Present | ||||||
South Africa | Present, Localized | ||||||
Tanzania | Present, Localized | ||||||
Uganda | Present | ||||||
Zimbabwe | Present, Localized | ||||||
Asia |
|||||||
Saudi Arabia | Present, Localized | Introduced | Invasive | ||||
Yemen | Present, Localized | Invasive | |||||
Europe |
|||||||
Belgium | Absent | ||||||
Netherlands | Absent, Confirmed absent by survey | ||||||
Slovenia | Absent | ||||||
Spain | Absent, Confirmed absent by survey |
Habitat
Top of pageCandidatus L. africanus has not been identified on indigenous rutaceous species. However, Ca. L. africanus subspecies clausenae, was originally identified from Clausena anisata (horsewood) in South Africa (Roberts et al., 2015). C. anisata is widespread in tropical Africa, from Guinea and Sierra Leone, eastwards to Ethiopia and Sudan and southward to the Eastern and Western Cape Provinces of South Africa, but not in arid regions. It also occurs in tropical Asia and South-East Asia and is cultivated in Malaysia and Indonesia (https://uses.plantnet-project.org/en/Clausena_anisata_(PROTA)#). To date, Ca. L. africanus subspecies clausenae has only been reported in C. anisata in South Africa and in citrus in Uganda, Kenya, Tanzania and Ethiopia (Roberts et al., 2015, 2017; Ajene et al., 2020).
Habitat List
Top of pageCategory | Sub-Category | Habitat | Presence | Status |
---|---|---|---|---|
Terrestrial | Managed | Cultivated / agricultural land | Present, no further details | Harmful (pest or invasive) |
Terrestrial | Managed | Protected agriculture (e.g. glasshouse production) | Secondary/tolerated habitat | Harmful (pest or invasive) |
Terrestrial | Managed | Managed forests, plantations and orchards | Secondary/tolerated habitat | Harmful (pest or invasive) |
Hosts/Species Affected
Top of pageAll citrus and Fortunella species, as well as Poncirus trifoliata (including hybrids) are susceptible to Ca. L. africanus. The least affected citrus species is the acid lime (Citrus aurantifolia) (da Graça, 1991).
Transmission to Catharanthus roseus (periwinkle), which showed distinct yellowing symptoms, was transmitted via the parasitic plant dodder, not the insect vector (Garnier and Bové, 1978).
Candidatus L. africanus subsp. clausenae was originally identified from Clausena anisata (horsewood) (Roberts et al., 2015) and subsequently from Citrus (Roberts et al., 2017).
Host Plants and Other Plants Affected
Top of pagePlant name | Family | Context | References |
---|---|---|---|
Calodendrum capense (cape chestnut) | Rutaceae | Main | |
Catharanthus roseus (Madagascar periwinkle) | Apocynaceae | Other | |
Citrus | Rutaceae | Main | |
Citrus aurantiifolia (lime) | Rutaceae | Main | |
Citrus limon (lemon) | Rutaceae | Main | |
Citrus nobilis (tangor) | Rutaceae | Main | |
Citrus reticulata (mandarin) | Rutaceae | Main | |
Citrus sinensis (sweet orange) | Rutaceae | Main | Shimwela et al. (2016); Ajene et al. (2020) |
Citrus x paradisi (grapefruit) | Rutaceae | Main | |
Clausena anisata (horsewood) | Rutaceae | Wild host | |
Fortunella (kumquats) | Rutaceae | Main | |
Poncirus trifoliata (Trifoliate orange) | Rutaceae | Main |
Symptoms
Top of pageSymptoms of African greening were extensively detailed by Oberholzer et al. (1965) and McClean and Schwarz (1970). Symptoms are varied and dependent on the host cultivar, time of infection and various environmental factors. New growth may display shoots that are yellow or pale green with small leaves growing upright and gradually become leathery. Leaf veins on these shoots become a prominent yellowish colour and leaves of infected branches are frequently smaller. Possibly the most characteristic foliar symptom is a blotchy mottle, observed on older leaves of infected trees, but this symptom is not specific to greening and is observed with other citrus diseases. Other foliar symptoms are similar to those observed with elemental deficiencies, particularly zinc, but also manganese, iron, calcium, sulphur and boron. Symptoms similar to deficiencies are not only specific to greening and can be associated with the early stages of other citrus diseases.
Young trees are stunted when infected at an early stage and show severe leaf drop with twig dieback, rendering sparsely foliated trees. This decline is accompanied by out-of-season growth flushes and blossoming as well as abnormal premature fruit drop. Root systems of severely affected trees are poorly developed with a reduction of fibrous roots. African greening differs from the Asian form of the disease in that only a section or a branch of a tree may be infected and display symptoms, whereas the rest of the tree exhibits normal growth and yields normal fruit.
Fruit of diseased trees are often small, lopsided and may develop high shoulders at the peduncle end. Seedy varieties contain aborted or undeveloped seed. Uneven fruit colour development is associated with the disease where the shaded sides of the fruits frequently remain green, hence the origin of the name greening. Additionally, a ripening colour inversion can occur where the stylar end remains green and the peduncle end colours prematurely. Another diagnostic feature is the ‘silver thumb print’. Pressure exerted on the fruit with a finger leaves a greyish-white imprint on the rind. Affected fruit are acidic with low Brix/acid ratios, low juice percentage and low soluble solids. These fruit have a bitter and salty taste which impacts juice quality and marketability of the fruit.
List of Symptoms/Signs
Top of pageSign | Life Stages | Type |
---|---|---|
Fruit / abnormal patterns | ||
Fruit / abnormal shape | ||
Fruit / discoloration | ||
Fruit / premature drop | ||
Fruit / reduced size | ||
Growing point / dieback | ||
Growing point / discoloration | ||
Growing point / dwarfing; stunting | ||
Leaves / abnormal colours | ||
Leaves / abnormal forms | ||
Leaves / abnormal leaf fall | ||
Leaves / abnormal patterns | ||
Leaves / yellowed or dead | ||
Seeds / shrivelled | ||
Whole plant / discoloration | ||
Whole plant / dwarfing | ||
Whole plant / early senescence |
Biology and Ecology
Top of pageThe disease is vectored and is graft transmissible (McClean and Oberholzer, 1965; McClean and Schwarz, 1970).
Three Candidatus Liberibacter species have been identified on citrus including Ca. L. asiaticus (Asian origin), Ca. L. americanus (American origin) and Ca. L. africanus (African origin). The African form is less severe than the Asian form and is normally found at higher altitudes, above 600-900 m above sea level. Its distribution is restricted to cooler, moist regions, together with its natural vector, the African citrus triozid, Trioza erytreae (Schwarz, 1967; Catling and Green, 1972; da Graça and Korsten, 2004). Ca. L. africanus, is heat sensitive as symptoms are produced under relatively cool conditions (20-24°C optimum) (Garnier and Bové, 1993). Symptom expression is generally restricted to temperatures below 27°C (da Graça and Korsten, 2004). Extended periods of high temperatures suppress symptom development but do not suppress infection of citrus (USDA, 2012). This temperature sensitivity is similar to that of T. erytreae. Temperatures above 30°C, together with relative humidity (RH) below 25%, are lethal to certain life stages such as eggs and first-instar nymphs. T. erytreae survives short periods of high temperatures or low RH, but these extreme climatic conditions become lethal to young life stages when occurring together (Catling, 1969; Catling and Green, 1972).
Notes on Natural Enemies
Top of pageThe vector, Trioza erytreae, has natural predators and parasites (Catling, 1970; van den Berg et al., 1987). The parasitoid wasp Tamarixia dryi (=Tetrastichus dryi) is widespread in Africa and is the most common and effective parasitoid of T. erytreae (van den Berg and Greenland, 2000).
Means of Movement and Dispersal
Top of pageVector Transmission:
African greening is transmitted by the African citrus triozid, Trioza erytreae (McLean and Oberholzer, 1965). Experimentally, Ca. L. africanus was transmitted by Diaphorina citri, the Asian citrus psyllid (Lallemand et al., 1986). Dispersal of the pathogen can occur through normal range expansion of the vector from infected regions to new areas or infected insects can be hitchhikers on transported host plants.
Movement of plants and propagation material (budwood):
Movement of infected plants or budwood for propagation purposes is a primary means of dispersal of the disease.
No seed transmission:
Citrus Liberibacters have been shown not to be seed transmitted (Albrecht and Bowman, 2009; Hartung et al., 2010). Fruit is not a means of dispersal.
Pathway Causes
Top of pageCause | Notes | Long Distance | Local | References |
---|---|---|---|---|
Hitchhiker | Infected vectors on leaf debris and hosts plants | Yes | Yes | |
Horticulture | Infected plants or propagation material (budwood) | Yes | Yes | |
Industrial purposes | Fruit juicing / oil extraction – fruit and seed (not pathways) | |||
Live food or feed trade | Fruit and seed (not pathways) | |||
Nursery trade | Propagation and sale of infected/infested plants | Yes | Yes | |
Off-site preservation | Genetic resource interchange within and between collaborating countries/ research organisations | Yes | Yes | |
People sharing resources | Informal sharing or trading of host plants/propagation material infected/infested with the pathogen and/or vector | Yes | Yes | |
Research | Introduction of infected plants or vectors at trial sites or research facilities | Yes | Yes | |
Smuggling | Tourists - illegal introduction of infected/infested plants/propagation material (budwood) | Yes | Yes |
Pathway Vectors
Top of pageVector | Notes | Long Distance | Local | References |
---|---|---|---|---|
Germplasm | Research or cultivar introductions | Yes | Yes | |
Land vehicles | Only insofar as plants / budwood is transported by vehicles | Yes | Yes | |
Plants or parts of plants | Yes | Yes |
Plant Trade
Top of pagePlant parts liable to carry the pest in trade/transport | Pest stages | Borne internally | Borne externally | Visibility of pest or symptoms |
---|---|---|---|---|
Seedlings/Micropropagated plants | Yes | Pest or symptoms usually invisible | ||
Stems (above ground)/Shoots/Trunks/Branches | Yes | Pest or symptoms usually invisible |
Plant parts not known to carry the pest in trade/transport |
---|
Bark |
Bulbs/Tubers/Corms/Rhizomes |
Fruits (inc. pods) |
Leaves |
True seeds (inc. grain) |
Vectors and Intermediate Hosts
Top of pageVector | Source | Reference | Group | Distribution |
---|---|---|---|---|
Trioza erytreae | CABI/EPPO (1998) | Insect |
Impact Summary
Top of pageCategory | Impact |
---|---|
Animal/plant collections | None |
Animal/plant products | Negative |
Biodiversity (generally) | None |
Crop production | Negative |
Environment (generally) | None |
Fisheries / aquaculture | None |
Forestry production | None |
Human health | None |
Livestock production | None |
Native fauna | None |
Native flora | None |
Rare/protected species | None |
Tourism | None |
Trade/international relations | Negative |
Transport/travel | None |
Impact
Top of pageCrop losses of 30-100% have been reported in South Africa during the periods 1932-1936 and 1939-1946 (da Graça and Korsten, 2004). By the mid-1970s, it was estimated that 4 million of the 11 million citrus trees in South Africa were infected (Buitendag and von Broembsen, 1993). The disease can be effectively managed in affected production regions, unlike huanglongbing (see Prevention and Control). The crop losses reported reflect the potential harm in areas with conducive climate in combination with failure to effectively manage the disease.
Risk and Impact Factors
Top of page- Invasive in its native range
- Has a broad native range
- Abundant in its native range
- Host damage
- Negatively impacts agriculture
- Negatively impacts livelihoods
- Negatively impacts trade/international relations
Diagnosis
Top of pageA diagnostic protocol for the detection of Candidatus Liberibacter africanus, Ca. Liberibacter americanus and Ca. Liberibacter asiaticus in their host species and for detection in their experimental and natural vectors, Diaphorina citri and Trioza erytreae was published by EPPO (2014). The protocol involves detection based on the disease symptoms and molecular tests (PCR), as well as reporting and documentation.
PCR diagnostics were updated to avoid misdiagnosis of subspecies of Ca. Liberibacter africanus (Roberts et al., 2017).
Detection and Inspection
Top of pageAfrican greening symptoms are difficult to recognize as they often resemble those of other citrus disorders and nutrient deficiencies. If suspected, the presence of the disease should be confirmed by PCR.
Similarities to Other Species/Conditions
Top of pageDisease symptoms are almost identical to and can be confused with those of the other species of Candidatus Liberibacter. Mixed infections of two of the strains have been reported (Roberts et al., 2017).
Leaf symptoms can resemble nutrient deficiencies, particularly those of zinc and iron (Oberholzer et al., 1965; McClean and Schwarz, 1970). Symptoms may include yellowing and interveinal chlorosis. Nutrient deficiencies however tend to present uniformly across the canopy on similar aged shoots, whereas greening symptoms first appear on single shoots or branches. Symptoms of zinc deficiency are also similar to the early stages of citrus blight, a disease of unconfirmed aetiology (Brlansky, 2000). However, greening is not associated with xylem dysfunction and wilting observed in blighted trees.
Blotchy mottle is the most characteristic symptom of greening, but is not specific to this disease. Stubborn disease (Spiroplasma citri) and Australian citrus dieback, a disease of unknown aetiology, also induce blotchy mottle. Australian citrus dieback is further associated with other typical greening symptoms such as yellowing, reduced fruit size and dieback (Broadbent et al., 1976). Stubborn disease similarly displays symptoms such as small, lop-sided fruit, with colour inversion, aborted seeds and out-of-season flowering which can be confused with greening disease (Bové and Garnier, 2000).
Other diseases that may confuse diagnosis include severe infections of Citrus tristeza virus (CTV) which display twig and branch dieback, sparse foliage and small leaves, with various deficiencies and small sized fruit, as well as root rot, caused by Phytophthora spp., which can cause leaf yellowing, leaf drop and dieback, often sectorially.
Prevention and Control
Top of pageDue to the variable regulations around (de)registration of pesticides, your national list of registered pesticides or relevant authority should be consulted to determine which products are legally allowed for use in your country when considering chemical control. Pesticides should always be used in a lawful manner, consistent with the product's label.
Phytosanitary Methods
In areas where the disease is not present, effective quarantine measures such as exclusion are essential to prevent the introduction of the Candidatus Liberibacter pathogen or the vector. Exclusion means importation of disease-free propagation material from covered insect-free nurseries or pest free regions/areas/countries. Furthermore, the possibility exists that the vector can spread through natural range expansion and simultaneously introduce the pathogen to unaffected regions. Regular scouting to detect disease outbreaks and monitoring for insect vectors is needed for early implementation of control interventions (da Graca and Korsten, 2004).
Disease-free nursery trees should be used to establish orchards and infected, abandoned or unproductive trees should be removed. Branches can be removed from trees if sectorial infections are observed to reduce the inoculum pressure (Buitendag and von Broembsen, 1993).
Biological Control
In the absence of hyperparasitoids, the parasitic wasp Tamarixia dryi (=Tetrastichus dryi) significantly reduced populations of Trioza erytreae on the Indian Ocean island of Reunion, leaving a greatly limited population of the vector (Aubert and Quilici, 1984).
Chemical Control
There are no chemical controls that specifically target the bacterium. Several antibiotics have been trialled to treat the tree via trunk injection methods. However, this was not sustained as a commercial treatment because the method proved expensive, remission was temporary, treated trees were inclined to produce small fruit, there were phytotoxic effects at the injection site and high levels of residues were found in the fruit of treated trees. Treatment then turned to control of the vector (Buitendag and von Broembsen, 1993).
IPM Programmes
Buitendag and von Broembsen (1993) recommended a three-pronged control strategy including the supply of certified greening-free nursery trees to commercial growers, the reduction of inoculum by the removal of infected trees or branches, and insecticide applications to control T. erytreae. The use of systemic insecticides with long residual action, applied prior to the spring flush and followed by shorter acting insecticides, is the primary method to effectively control the vector. This approach has brought about a distinct reduction in the incidence of greening-infected trees in commercial plantings in greening affected regions in South Africa.
References
Top of pageANR, 2010. Citrus bacterial canker disease and huanglongbing (citrus greening). Publication 8218. California, USA: University of California, Agriculture and Nature Resources. http://anrcatalog.ucdavis.edu
Aubert B, Quilici S, 1984. Biological control of the African and Asian citrus psyllids (Homoptera: Psylloidea), through eulophid and encyrtid parasites (Hymenoptera: Chalcidoidea) in Reunion Island. In: Garnsey SM, Timmer LW, Dodds JA, eds. Proceedings of the 9th Conference of the International of Citrus Virologists. University of California, Riverside, USA: IOCV, 100-108
Bové JM, Garnier, M, 2000. Graft-transmissible, systemic diseases, Stubborn. In: Compendium of citrus diseases, [ed. by Timmer LW, Garnsey SM, Graham JH]. Minnesota, USA: The American Phytopathological Society. 48-50.
Brlansky RH, 2000. Graft-transmissible, systemic diseases, Blight. In: Compendium of citrus diseases, [ed. by Timmer LW, Garnsey SM, Graham JH]. Minnesota, USA: The American Phytopathological Society. 65-66.
Buitendag CH, von Broembsen LA, 1993. Living with citrus greening in South Africa. In: Moreno P, da Grata JV, Timmer LW, eds. Proceedings of the 12th Conference of the International Organization of Citrus Virologists. University of California, Riverside, USA: IOCV, 269-273
Catling HD, Green GC, 1972. The Influence of weather on the survival and population fluctuations of Trioza erytreae (Del Guercio) - a vector of greening. In: Proceedings of the 5th Conference of the International Organization of Citrus Virologists [ed. by Price WC]. Gainesville, USA: University of Florida Press/IOCV. 58-64.
da Graça J, Korsten L, 2004 Citrus Huanglongbing: Review, present status and future strategies. In Navqui S, ed. Diseases of Fruits and Vegetables: Diagnosis and Management vol 1
da Graça JV, 1991. Citrus greening disease. Annual Review of Phytopathology, 29:109-136
Fourie, PH, Kirkman, W, Cook, G, Steyn, C, de Bruyn, R, Bester, R, et al, 2020. First report of ‘Candidatus Liberibacter africanus’ associated with African greening of citrus in Angola. Plant Disease, https://apsjournals.apsnet.org/doi/pdf/10.1094/PDIS-06-20-1392-PDN doi: 10.1094/PDIS-06-20-1392-PDN
Garnier M, Bové J, 1978. Transmission of the organism associated with the citrus greening disease from sweet orange to periwinkle by dodder. Phytopathology, 73: 1358-63
Garnier M, Bové JM, 1993. Citrus greening disease and the greening bacterium. In: Proceedings of the 12thConference of the International Organization of Citrus Virologists [ed. by Moreno P, da Graça JV, Timmer LW]. Riverside, USA: University of California/IOCV. 212-219.
Garnier M, Bové JM, 1996. Distribution of the Huanglongbing (greening) Liberobacter species in fifteen African and Asian countries. In: Proceedings of the 13th Conference of the International Organization of Citrus Virologists [ed. by da Graça JV, Lee RF, Yokomi RK]. Riverside, USA: University of California/IOCV. 388-391.
Garnier M, Danel N, Bové JM, 1984. Aetiology of citrus greening disease. Annales de l'Institut Pasteur, Microbiology, 135A:169-179
Garnier, M, Jagoueix, S, Toorawa, P, Grisoni, M, Mallesard, R, Dookun, A, Saumtally, S, Autrey, JC, Bové, JM, 1996. Both Huanglongbing (greening) Liberobacter species are present in Mauritius and Reunion. In: Proceedings of the 13th Conference of the International Organization of Citrus Virologists [ed. by da Graça JV, Lee RF, Yokomi RK]. Riverside, USA: University of California/IOCV. 392-394.
Jepson SB, 2009. Citrus greening disease (Huanglongbing). OSU Plant Clinic. Corvallis, Oregon, USA: Oregon State University
Kalyebi, A., Aisu, G., Ramathani, I., Ogwang, J., McOwen, N., Russell, P., 2015. Detection and identification of etiological agents (Liberibacter spp.) associated with citrus greening disease in Uganda. Uganda Journal of Agricultural Sciences, 16(1), 43-54.
Lallemand, J, Fos, A, Bové, JM, 1986. (Transmission de la bacterie associé à la forme africaine de la maladie du “greening” par le psylle asiatique Diaphorina citri Kuwayama). Fruits, 41, 341-343.
Lin KH, 1956. Observations on yellow shoot on citrus. Etiological studies of yellow shoot of citrus. Acta Phytopathologica Sinica, 2:1-42
McClean APD, Oberholzer PCJ, 1965. Citrus psylla, a vector of the greening disease of sweet orange. South African Journal of Agricultural Science, 8:297-298
Oberholzer PCJ, von Staden DFA, Basson WJ, 1965. Greening disease of sweet orange in South Africa. In: Proceedings of the 3rd Conference of the International Organization of Citrus Virologists [ed. by Price WC]. Riverside, USA: University of California/IOCV. 213-219.
Texeira D, Saillard C, Eveillard S, Danet J, da Costa P, Ayres A, Bové J, 2005. ’Candidatus Liberibacter americanus’, associated with citrus Huanglongbing (greening disease) in São Paulo State, Brazil. International Journal of Systematic and Evolutionary Microbiology, 55:1875-1862
USDA, 2012.
van den Berg MA, Greenland J, 2000. Tamarixia dryi, parasitoid of the citrus psylla, Trioza erytreae: a review. African Plant Protection, 6, 25-28.
Distribution References
Aubert B, Garnier M, Cassin JC, Bertin Y, 1988. Citrus greening survey in East and West African countries south of the Sahara. [Proceedings of the 10th Conference of the International Organization of Citrus Virologists], [ed. by Garnsey SM, Timmer LW, Dodds JA]. University of California, Riverside, USA: IOCV. 231-237.
Bové JM, Garnier M, 1984. Citrus greening and psylla vectors of the disease in the Arabian Peninsula. [Proceedings of the 9th Conference of the International Organization of Citrus Virologists], [ed. by Garnsey SM, Timmer LW, Dodds JA]. Riverside, USA: University of California, IOCV. 109-114.
CABI, Undated. CABI Compendium: Status as determined by CABI editor. Wallingford, UK: CABI
Fourie PH, Kirkman W, Cook G, Steyn C, de Bruyn R, Bester R, et al, 2020. First report of ‘Candidatus Liberibacter africanus’ associated with African greening of citrus in Angola. Plant Disease. https://apsjournals.apsnet.org/doi/pdf/10.1094/PDIS-06-20-1392-PDN DOI:10.1094/PDIS-06-20-1392-PDN
Garnier M, Bové JM, 1996. Distribution of the Huanglongbing (greening) Liberobacter species in fifteen African and Asian countries. [Proceedings of the 13th Conference of the International Organization of Citrus Virologists], [ed. by Moreno P, da Grata JV, Timmer LW]. Riverside, USA: University of California, IOCV. 388-391.
Kalyebi A, Aisu G, Ramathani I, Ogwang J, McOwen N, Russell P, 2015. Detection and identification of etiological agents (Liberibacter spp.) associated with citrus greening disease in Uganda. In: Uganda Journal of Agricultural Sciences, 16 (1) 43-54.
Contributors
Top of page01/02/2021 Updated by:
Glynnis Cook, Citrus Research International, South Africa
Hans J. Maree, Citrus Research International and Genetics Department, Stellenbosch University, South Africa
M.C. Pretorius, Citrus Research International, South Africa
Wayne Kirkman, Citrus Research International, South Africa
Elma Carstens, Citrus Research International, South Africa
27/03/13 Updated by:
Esther Arengo, National Agricultural Research Laboratories, Uganda
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