Liberibacter africanus
(African greening)

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Picture	Title	Caption	Copyright
Title Symptoms Caption Liberibacter africanus (African greening); greening symptoms on plant Copyright ©Esther Arengo	Symptoms	Liberibacter africanus (African greening); greening symptoms on plant	©Esther Arengo
Title Symptoms Caption Liberibacter africanus (African greening); greening symptoms on plant Copyright ©Esther Arengo	Symptoms	Liberibacter africanus (African greening); greening symptoms on plant	©Esther Arengo

Identity

Preferred Scientific Name

• Liberibacter africanus Jagoueix et al., 1994

Preferred Common Name

• African greening

Other Scientific Names

• Ca. Liberibacter africanus
• Ca. Liberobacter africanum
• Ca. Liberobacter africanus
• Candidatus Liberibacter africanus Garnier et al., 2000
• Candidatus Liberobacter africanum Jagouiex et al., 1994
• Candidatus Liberobacter africanus
• Liberibacter africanus subsp. africanus
• Liberibacter africanus subsp. capensis Garnier et al., 2000
• Liberobacter africanum
• Liberobacter africanus

International Common Names

• English: greening; greening of citrus; huanglongbing; yellow branch
• Spanish: enverdecimiento de los cítricos
• French: greening des agrumes; virescence des agrumes

EPPO code

• LIBEAF (Liberobacter africanum)

Summary of Invasiveness

Taxonomic Tree

• Domain: Bacteria
•     Phylum: Proteobacteria
•         Class: Alphaproteobacteria
•             Order: Rhizobiales
•                 Family: Phyllobacteriaceae
•                     Genus: Candidatus Liberibacter
•                         Species: Liberibacter africanus

Notes on Taxonomy and Nomenclature

Description

The bacteria causing huanglongbing are restricted to the sieve tubes of the phloem vessels. Electron microscopy studies reveal that they possess the characteristic double membrane cell envelope of the liberibacters (Garnier et al., 1984; Texeira et al., 2005; Kim et al., 2009). Thin-section EM examination reveals elongated sinuous rods with an uneven diameter of 0.15-0.25 µm. Round forms of larger diameter can also be observed in degenerating cells. Similar particles are observed in the haemolymph and salivary glands of the two insect vectors.

Distribution Table

The 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.

Habitat

Calodendrum capense, the host of L. africanus subsp. capense, is native to the southern African region. The description of L. africanus subsp. capense was from two locations, one on an ornamental tree bordering an orchard, which displayed the blotchy mottle symptom characteristic of HLB (Garnier et al., 2000).

Habitat List

Hosts/Species Affected

All citrus species appear to be susceptible to L. africanus; however, it is primarily a disease of sweet orange (Citrus sinensis) with Valencia showing more pronounced symptoms than navels. It is also particularly severe on mandarins (C. reticulata) and tangelos (C. reticulata x sinensis) but less so on lemon (C. limon). The least affected species is the acid lime (C. aurantifolia) (da Graca, 1991).

Transmission to Catharanthus roseus, which shows distinct yellowing symptoms, is via the parasitic plant dodder, not the insect vector (Garnier and Bové, 1978).

To date, the African form of the disease has only been detected in Citrus species for L. africanus and Calodendrum capense for L. africanus subsp. capensis.

Host Plants and Other Plants Affected

Growth Stages

Symptoms

The first symptom of huanglongbing is usually the appearance of a yellow shoot on a tree (hence the name huanglongbing, which literally means ‘yellow dragon disease’). Progressive yellowing of the entire canopy follows: leaves turn pale yellow, show symptoms of zinc or manganese deficiency, or display blotchy mottling, and are reduced in size. Blotchy mottle is the most characteristic symptom, but is not specific to huanglongbing. Stubborn disease (Spiroplasma citri), severe forms of Citrus tristeza virus (CTV), species of Phytophthora, waterlogging and the use of marcots can produce similar blotchy mottle patterns. Symptoms of zinc deficiency are also associated with the early stages of citrus blight (a disease of unconfirmed aetiology). However, huanglongbing bacteria do not induce the xylem dysfunction and wilting observed in blighted trees.

Chronically infected trees are sparsely foliated and show extensive twig dieback. The fruits are often small, lopsided, can have a sour or bitter taste (Jepson, 2009; ANR, 2010; USDA, 2012) and are poorly coloured (hence the origin of the name greening). They often contain aborted seeds. Similar fruit symptoms are also observed with CTV infection.

List of Symptoms/Signs

Biology and Ecology

Four forms of greening now exist worldwide. The South African form is least severe and is normally found at higher altitudes, above 900 m above sea level. Its distribution is more restricted than the other forms and it is transmitted by Trioza erytreae (da Graca and Korsten, 2004). It is temperature sensitive and is restricted to temperatures below 27°C (da Graca and Korsten, 2004). Extended periods of high temperatures suppress symptom development but do not suppress infection of citrus (USDA, 2012).

Notes on Natural Enemies

The vector Trioza erytreae is parasitized by Tetrastichus dryi in Africa, Reunion and Mauritius.

Means of Movement and Dispersal

Vector Transmission

In the 1960s, the agent was shown to be transmitted by two insects: the African citrus psyllid, Trioza erytreae, in Africa (McLean and Oberholzer, 1965) and the Asian citrus psyllid, Diaphorina citri, in Asia (Capoor et al., 1967; Martinez and Wallace, 1967). Experimentally, both species of psyllid have been shown to transmit both forms of the disease (Massonié et al., 1976; Lallemand et al., 1986).

Pathway Causes

Pathway Vectors

Plant Trade

Vectors and Intermediate Hosts

Impact Summary

Impact

Risk and Impact Factors

• Invasive in its native range
• Has a broad native range
• Abundant in its native range
• Highly adaptable to different environments
• Is a habitat generalist
• Tolerates, or benefits from, cultivation, browsing pressure, mutilation, fire etc
• Benefits from human association (i.e. it is a human commensal)
• Reproduces asexually
• Has high genetic variability

• Damaged ecosystem services
• Host damage
• Increases vulnerability to invasions
• Loss of medicinal resources
• Negatively impacts agriculture
• Negatively impacts livelihoods
• Reduced native biodiversity
• Threat to/ loss of endangered species
• Threat to/ loss of native species
• Negatively impacts trade/international relations

Diagnosis

A diagnostic protocol for Liberibacter africanus, Liberibacter americanus and Liberibacter asiaticus and for their detection in their psyllid vectors Diaphorina citri and Trioza erytreae has been published by EPPO (2014). The protocol involves detection based on the disease symptoms and molecular tests (PCR), and reporting and documentation.

For a description of the diagnostic tests for this species, see the datasheet on Citrus huanglongbing (greening) disease. 

Detection and Inspection

Similarities to Other Species/Conditions

Disease symptoms are almost identical and can be confused with those of the other strains of Liberibacter causing huanglongbing. Mixed infections of two of the strains have been reported (Coletta-Filho et al., 2005). Leaf symptoms also resemble nutrient deficiencies, particularly in zinc, calcium and nitrogen.

Blotchy mottle is the most characteristic symptom of huanglongbing, but is not specific to it. Stubborn disease (Spiroplasma citri), severe forms of Citrus tristeza virus (CTV), species of Phytophthora, waterlogging and the use of marcots can produce similar blotchy mottle patterns. Symptoms of zinc deficiency are also associated with the early stages of citrus blight (a disease of unconfirmed aetiology). However, huanglongbing bacteria do not induce the xylem dysfunction and wilting observed in blighted trees.
 

Prevention and Control

Due 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 are essential to prevent the introduction of the huanglongbing (HLB) organism or the vector. Furthermore, the possibility exists that the vector could be introduced 'naturally' or through alternative hosts (da Graca and Korsten, 2004).

Biological Control

In the absence of hyperparasitic wasps, the parasitic wasp Tetrastichus dryi significantly reduced populations of Trioza erytreae, the vector of HLB, on the Indian Ocean island of Reunion, leaving a strongly 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 strategy of the provision of certified greening-free nursery trees to commercial growers, a reduction of inoculum through an ongoing programme of removing plant parts showing greening symptoms and the implementation of effective measures to control the psylla vector, T. erytreae. This has brought about a distinct reduction in the incidence of greening-infected trees in commercial plantings in South Africa.

References

ANR, 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

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

CABI/EPPO, 1998. Liberobacter africanum. [Distribution map]. Distribution Maps of Plant Diseases, October (Edition 1). Wallingford, UK: CAB International, Map 765

Capoor SP, Rao DG, Viswanath SM, 1967. Diaphorina citri, a vector of the greening disease of citrus in India. Indian Journal of Agricultural Science, 37:572-576

Coletta-Filho H, Takita M, Targon M, Machado M, 2005. Analysis of 16S rDNA sequences from citrus Huanglongbing bacteria reveal a different ’Ca. Liberibacter’ strain associated with citrus disease in São Paulo. Plant Disease, 89:848-852

da Graca 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 Graca JV, 1991. Citrus greening disease. Annual Review of Phytopathology, 29:109-136

EPPO, 2014. PM 7/121 (1) 'Candidatus Liberibacter africanus', 'Candidatus Liberibacter americanus' and 'Candidatus Liberibacter asiaticus'. Bulletin OEPP/EPPO Bulletin, 44(3):376-389. http://onlinelibrary.wiley.com/journal/10.1111/(ISSN)1365-2338

EPPO, 2014. PQR database. Paris, France: European and Mediterranean Plant Protection Organization. http://www.eppo.int/DATABASES/pqr/pqr.htm

Garnier M, Bove 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, Danel N, Bové JM, 1984. Aetiology of citrus greening disease. Annales de l'Institut Pasteur, Microbiology, 135A:169-179

Garnier M, Jagoueix-Eveillard S, Cronje PR, Roux HFle, BovT JM, 2000. Genomic characterization of a liberibacter present in an ornamental rutaceous tree, Calodendrum capense, in the Western Cape province of South Africa. Proposal of 'Candidatus Liberibacter africanus subsp. capensis'. International Journal of Systematic and Evolutionary Microbiology, 50(6):2119-2125; 20 ref

Jagoueix S, Bové JM, Garnier M, 1994. The phloem-limited bacterium of greening disease of citrus is a member of the subdivision of the Proteobacteria. International Journal of Systematic Bacteriology, 44(3):379-386

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.

Kim DG, Burks TF, Schumann AW, Zekri M, Zhao XH, Qin JW, 2009. Detection of citrus greening using microscopic imaging. Agricultural Engineering International, 11:Manuscript 1194. http://www.cigrjournal.org/index.php/Ejounral/article/viewFile/1194/1226

Lin KH, 1956. Observations on yellow shoot on citrus. Etiological studies of yellow shoot of citrus. Acta Phytopathologica Sinica, 2:1-42

Martinez AL, Wallace JM, 1967. Citrus leaf mottle-yellows disease in the Philippines and transmission of the causal virus by a psyllid, Diaphorina citri. Plant Disease Reporter, 51:692-695

Massonié G, Garnier M, Bové JM, 1976. Transmission of Indian citrus decline by Tryoza erytreae (Del G.), the vector of South African greening. In: Calavan EC, ed. Proceedings of the 7th Conference of the International Organization of Citrus Virologists. University of California, Riverside, USA: IOCV, 18-20

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

Texeira D, Saillard C, Eveillard S, Danet J, da Costa P, Ayres A, Bove 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.

Distribution References

CABI, EPPO, 1998. Liberobacter africanum. [Distribution map]. In: Distribution Maps of Plant Diseases, Wallingford, UK: CAB International. Map 765.

CABI, Undated. Compendium record. Wallingford, UK: CABI

CABI, Undated a. CABI Compendium: Status as determined by CABI editor. Wallingford, UK: CABI

EPPO, 2020. EPPO Global database. In: EPPO Global database, Paris, France: EPPO.

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

27/03/13 Updated by:

Esther Arengo, National Agricultural Research Laboratories, Uganda

Distribution Maps