Invasive Species Compendium

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Datasheet

Candidatus Liberibacter africanus
(African greening)

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Datasheet

Candidatus Liberibacter africanus (African greening)

Summary

  • Last modified
  • 16 November 2021
  • Datasheet Type(s)
  • Invasive Species
  • Pest
  • Preferred Scientific Name
  • Candidatus Liberibacter africanus
  • Preferred Common Name
  • African greening
  • Taxonomic Tree
  • Domain: Bacteria
  •   Phylum: Proteobacteria
  •     Class: Alphaproteobacteria
  •       Order: Rhizobiales
  •         Family: Phyllobacteriaceae
  • Summary of Invasiveness
  • Candidatus 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 Pest...

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Pictures

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PictureTitleCaptionCopyright
Candidatus Liberibacter africanus infected branch of a citrus tree showing leaves with Zn deficiency. South Africa.
TitleFoliar Symptoms
CaptionCandidatus Liberibacter africanus infected branch of a citrus tree showing leaves with Zn deficiency. South Africa.
Copyright©Citrus Research International
Candidatus Liberibacter africanus infected branch of a citrus tree showing leaves with Zn deficiency. South Africa.
Foliar SymptomsCandidatus Liberibacter africanus infected branch of a citrus tree showing leaves with Zn deficiency. South Africa.©Citrus Research International
Candidatus Liberibacter africanus infected branch of a citrus tree showing foliar blotchy mottle. South Africa.
TitleFoliar Symptoms
CaptionCandidatus Liberibacter africanus infected branch of a citrus tree showing foliar blotchy mottle. South Africa.
Copyright©Citrus Research International
Candidatus Liberibacter africanus infected branch of a citrus tree showing foliar blotchy mottle. South Africa.
Foliar SymptomsCandidatus Liberibacter africanus infected branch of a citrus tree showing foliar blotchy mottle. South Africa.©Citrus Research International
Candidatus Liberibacter africanus infected branch of a citrus tree showing foliar blotchy mottle, yellow leaf veins and twig die-back. South Africa.
TitleFoliar Symptoms
CaptionCandidatus Liberibacter africanus infected branch of a citrus tree showing foliar blotchy mottle, yellow leaf veins and twig die-back. South Africa.
Copyright©Citrus Research International
Candidatus Liberibacter africanus infected branch of a citrus tree showing foliar blotchy mottle, yellow leaf veins and twig die-back. South Africa.
Foliar SymptomsCandidatus Liberibacter africanus infected branch of a citrus tree showing foliar blotchy mottle, yellow leaf veins and twig die-back. South Africa.©Citrus Research International
Candidatus Liberibacter africanus infected branch of a citrus tree showing yellow leaf veins. South Africa.
TitleFoliar Symptoms
CaptionCandidatus Liberibacter africanus infected branch of a citrus tree showing yellow leaf veins. South Africa.
Copyright©Citrus Research International
Candidatus Liberibacter africanus infected branch of a citrus tree showing yellow leaf veins. South Africa.
Foliar SymptomsCandidatus Liberibacter africanus infected branch of a citrus tree showing yellow leaf veins. South Africa.©Citrus Research International
Candidatus Liberibacter africanus infected citrus tree showing African greening symptoms including sparse foliage, shoots with upright growth manner and fruit showing ripening colour inversion. South Africa.
TitleSymptomatic Tree
CaptionCandidatus Liberibacter africanus infected citrus tree showing African greening symptoms including sparse foliage, shoots with upright growth manner and fruit showing ripening colour inversion. South Africa.
Copyright©Citrus Research International
Candidatus Liberibacter africanus infected citrus tree showing African greening symptoms including sparse foliage, shoots with upright growth manner and fruit showing ripening colour inversion. South Africa.
Symptomatic TreeCandidatus Liberibacter africanus infected citrus tree showing African greening symptoms including sparse foliage, shoots with upright growth manner and fruit showing ripening colour inversion. South Africa.©Citrus Research International
Candidatus Liberibacter africanus infected citrus fruit with ripening colour inversion and a leaf displaying blotchy mottle. South Africa.
TitleFruit and foliar symptoms
CaptionCandidatus Liberibacter africanus infected citrus fruit with ripening colour inversion and a leaf displaying blotchy mottle. South Africa.
Copyright©Citrus Research International
Candidatus Liberibacter africanus infected citrus fruit with ripening colour inversion and a leaf displaying blotchy mottle. South Africa.
Fruit and foliar symptomsCandidatus Liberibacter africanus infected citrus fruit with ripening colour inversion and a leaf displaying blotchy mottle. South Africa.©Citrus Research International
Candidatus Liberibacter africanus infected citrus fruit (right), which is smaller and shows ripening colour inversion compered to a healthy fruit (left). South Africa.
TitleFruit symptom
CaptionCandidatus Liberibacter africanus infected citrus fruit (right), which is smaller and shows ripening colour inversion compered to a healthy fruit (left). South Africa.
Copyright©Citrus Research International
Candidatus Liberibacter africanus infected citrus fruit (right), which is smaller and shows ripening colour inversion compered to a healthy fruit (left). South Africa.
Fruit symptomCandidatus Liberibacter africanus infected citrus fruit (right), which is smaller and shows ripening colour inversion compered to a healthy fruit (left). South Africa.©Citrus Research International
Severe citrus fruit from associated with African greening on citrus. South Africa.
TitleFruit drop symptom
CaptionSevere citrus fruit from associated with African greening on citrus. South Africa.
Copyright©Citrus Research International
Severe citrus fruit from associated with African greening on citrus. South Africa.
Fruit drop symptomSevere citrus fruit from associated with African greening on citrus. South Africa.©Citrus Research International
Candidatus Liberibacter africanus (African greening); greening symptoms on plant
TitleSymptoms
CaptionCandidatus Liberibacter africanus (African greening); greening symptoms on plant
Copyright©Esther Arengo
Candidatus Liberibacter africanus (African greening); greening symptoms on plant
SymptomsCandidatus Liberibacter africanus (African greening); greening symptoms on plant©Esther Arengo
Candidatus Liberibacter africanus (African greening); greening symptoms on plant
TitleSymptoms
CaptionCandidatus Liberibacter africanus (African greening); greening symptoms on plant
Copyright©Esther Arengo
Candidatus Liberibacter africanus (African greening); greening symptoms on plant
SymptomsCandidatus Liberibacter africanus (African greening); greening symptoms on plant©Esther Arengo

Identity

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Preferred 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

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Candidatus 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

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

Notes on Taxonomy and Nomenclature

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Five 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

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The 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

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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.

Last updated: 23 May 2022
Continent/Country/Region Distribution Last Reported Origin First Reported Invasive Reference Notes

Africa

AngolaPresent, LocalizedCollected from a commercial farm near Calulo and in a nursery in Luanda.
BurundiPresent
CameroonPresent
Central African RepublicPresent
ComorosPresent
EswatiniPresent
EthiopiaPresent
KenyaPresent
MadagascarPresent
MalawiPresent
MauritiusPresent
NigeriaPresent
RéunionPresent
RwandaPresent
Saint HelenaPresent, Widespread
SomaliaPresent
South AfricaPresent, Localized
TanzaniaPresent, Localized
UgandaPresent
ZimbabwePresent, Localized

Asia

Saudi ArabiaPresent, LocalizedIntroducedInvasive
YemenPresent, LocalizedInvasive

Europe

BelgiumAbsent
NetherlandsAbsent, Confirmed absent by survey
SloveniaAbsent
SpainAbsent, Confirmed absent by survey

Habitat

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Candidatus 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

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CategorySub-CategoryHabitatPresenceStatus
Terrestrial ManagedCultivated / agricultural land Present, no further details Harmful (pest or invasive)
Terrestrial ManagedProtected agriculture (e.g. glasshouse production) Secondary/tolerated habitat Harmful (pest or invasive)
Terrestrial ManagedManaged forests, plantations and orchards Secondary/tolerated habitat Harmful (pest or invasive)

Hosts/Species Affected

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All 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).

Growth Stages

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Flowering stage, Fruiting stage, Seedling stage, Vegetative growing stage

Symptoms

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Symptoms 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

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SignLife StagesType
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

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The 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

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The 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

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Vector 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

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CauseNotesLong DistanceLocalReferences
HitchhikerInfected vectors on leaf debris and hosts plants Yes Yes
HorticultureInfected plants or propagation material (budwood) Yes Yes
Industrial purposesFruit juicing / oil extraction – fruit and seed (not pathways)
Live food or feed tradeFruit and seed (not pathways)
Nursery tradePropagation 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 resourcesInformal sharing or trading of host plants/propagation material infected/infested with the pathogen and/or vector Yes Yes
ResearchIntroduction of infected plants or vectors at trial sites or research facilities Yes Yes
SmugglingTourists - illegal introduction of infected/infested plants/propagation material (budwood) Yes Yes

Pathway Vectors

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VectorNotesLong DistanceLocalReferences
GermplasmResearch or cultivar introductions Yes Yes
Land vehiclesOnly insofar as plants / budwood is transported by vehicles Yes Yes
Plants or parts of plants Yes Yes

Plant Trade

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Plant parts liable to carry the pest in trade/transportPest stagesBorne internallyBorne externallyVisibility 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

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VectorSourceReferenceGroupDistribution
Trioza erytreaeCABI/EPPO (1998)Insect

Impact Summary

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CategoryImpact
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

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Crop 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

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Invasiveness
  • Invasive in its native range
  • Has a broad native range
  • Abundant in its native range
Impact outcomes
  • Host damage
  • Negatively impacts agriculture
  • Negatively impacts livelihoods
  • Negatively impacts trade/international relations

Diagnosis

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A 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

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African 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

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Disease 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

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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 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

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Ajene, I. J., Khamis, F. M., Asch, B. van, Pietersen, G., Seid, N., Rwomushana, I., Ombura, F. L. O., Momanyi, G., Finyange, P., Rasowo, B. A., Tanga, C. M., Mohammed, S., Ekesi, S., 2020. Distribution of Candidatus Liberibacter species in eastern Africa, and the first report of Candidatus Liberibacter asiaticus in Kenya. Scientific Reports, 10(3), doi: 10.1038/s41598-020-60712-0

Ajene, I. J., Khamis, F., Mohammed, S., Adediji, A. O., Atiri, G. I., Kazeem, S. A., Ekesi, S., 2020. First report of 'Candidatus Liberibacter africanus' associated with citrus greening disease in Nigeria. Plant Disease, 104(5), 1535-1535. doi: 10.1094/PDIS-11-19-2380-PDN

Albrecht, U., Bowman, K. D., 2009. Candidatus Liberibacter asiaticus and Huanglongbing effects on citrus seeds and seedlings. HortScience, 44(7), 1967-1973. http://hortsci.ashspublications.org/

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

Berg, M. A. van den, Deacon, V. E., Fourie, C. J., Anderson, S. H., 1987. Predators of the citrus psylla, Trioza erytreae (Hemiptera: Triozidae), in the Lowveld and Rustenburg areas of Transvaal. Phytophylactica, 19(3), 285-289.

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.

Bové, J. M., 2006. Huanglongbing: a destructive, newly-emerging, century-old disease of citrus. Journal of Plant Pathology, 88(1), 7-37. http://www.agr.unipi.it/sipav/jpp/index.html

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.

Broadbent, P., Fraser, L. R., McGechan, J., 1976. Australian citrus dieback. In: Proceedings of the Seventh Conference of the International Organization of Citrus Virologists [Proceedings of the Seventh Conference of the International Organization of Citrus Virologists], [ed. by Calavan, E. C.]. Riverside, USA: Univ. California. 141-146.

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

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.

Catling, H. D., 1969. The bionomics of the South African citrus psylla, Trioza erytreae (Del Guercio) Homoptera : Psyllidae. 3. The influence of extremes of weather on survival. Journal of the Entomological Society of Southern Africa, 32(2), 273-290.

Catling, H. D., 1970. The bionomics of the South African citrus psylla Trioza erytreae (Del Guercio) (Homoptera: Psyllidae). 4. The influence of predators. Journal of the Entomological Society of Southern Africa, 33(2), 341-348.

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

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

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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

McClean, A. P. D., Schwarz, R. E., 1970. Greening or blotchy-mottle disease of citrus. Phytophylactica, 2(3), 177-194.

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Roberts, R., Cook, G., Grout, T. G., Khamis, F., Rwomushana, I., Nderitu, P. W., Seguni, Z., Materu, C. L., Steyn, C., Pietersen, G., Ekesi, S., Roux, H. F. le, 2017. Resolution of the identity of 'Candidatus Liberibacter' species from Huanglongbing-affected citrus in East Africa. Plant Disease, 101(8), 1481-1488. doi: 10.1094/PDIS-11-16-1655-RE

Roberts, R., Pietersen, G., 2017. A novel subspecies of 'Candidatus Liberibacter africanus' found on native Teclea gerrardii (family: Rutaceae) from South Africa. Antonie van Leeuwenhoek, 110(3), 437-444. doi: 10.1007/s10482-016-0799-x

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Distribution References

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Ajene I J, Khamis F, Mohammed S, Adediji A O, Atiri G I, Kazeem S A, Ekesi S, 2020. First report of 'Candidatus Liberibacter africanus' associated with citrus greening disease in Nigeria. Plant Disease. 104 (5), 1535-1535. DOI:10.1094/PDIS-11-19-2380-PDN

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Magomere T O, Obukosia S D, Mutitu E, Ngichabe C, Olubayo F, Shibairo S, 2009. Molecular characterization of 'Candidatus Liberibacter' species/strains causing huanglongbing disease of citrus in Kenya. EJB, Electronic Journal of Biotechnology. 12 (2), article 2. http://ejb.ucv.cl/content/vol12/issue2/full/2/index.html DOI:10.2225/vol12-issue2-fulltext-2

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Pietersen G, Arrebola E, Breytenbach J H J, Korsten L, Roux H F le, Grange H la, Lopes S A, Meyer J B, Pretorius M C, Schwerdtfeger M, Vuuren S P van, Yamamoto P, 2010. A survey for 'Candidatus Liberibacter' species in South Africa confirms the presence of only 'Ca. L. africanus' in commercial citrus. Plant Disease. 94 (2), 244-249. DOI:10.1094/PDIS-94-2-0244

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Contributors

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01/02/2021 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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