citrus huanglongbing (greening) disease (citrus greening)
- Taxonomic Tree
- Notes on Taxonomy and Nomenclature
- Distribution Table
- Risk of Introduction
- Hosts/Species Affected
- Host Plants and Other Plants Affected
- Growth Stages
- List of Symptoms/Signs
- Biology and Ecology
- Means of Movement and Dispersal
- Plant Trade
- Vectors and Intermediate Hosts
- Economic Impact
- Detection and Inspection
- Similarities to Other Species/Conditions
- Prevention and Control
- Distribution Maps
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PicturesTop of page
IdentityTop of page
Preferred Scientific Name
- citrus huanglongbing (greening) disease
Preferred Common Name
- citrus greening
Other Scientific Names
- African greening
- Asian greening
- Candidatus Liberibacter africanus
- Candidatus Liberibacter asiaticus
- Candidatus Liberobacter africanum Monique Garnier
- Candidatus Liberobacter asiaticum Monique Garnier
- citrus greening bacterium
- greening bacterium
- huanglongbing bacterium
- Liberibacter africanus subsp capensis (Candidatus)
- Liberibacter americanus (Candidatus)
- Liberobacter africanum
- Liberobacter africanum [Candidatus] Monique Garnier
- Liberobacter asiaticum
- Liberobacter asiaticum [Candidatus] Monique Garnier
- South American greening
International Common Names
- English: blotchy mottle disease of Citrus; greening; leaf mottling of Citrus; yellow branch disease; yellow shoot
- Spanish: enverdecimiento de los cítricos
- French: greening; virescence des agrumes
Local Common Names
- India: citrus dieback
- Indonesia: citrus vein phloem degeneration (CVPD)
- Philippines: blotchy mottle; mottle leaf disease
- Taiwan: likubin
Taxonomic TreeTop of page
- Domain: Bacteria
- Phylum: Proteobacteria
- Class: Alphaproteobacteria
- Order: Rhizobiales
- Family: Phyllobacteriaceae
- Genus: citrus huanglongbing (greening) disease
Notes on Taxonomy and NomenclatureTop of page
Citrus huanglongbing (yellow shoot disease) has been known in China for more than 100 years (Zhao, 1981). In 1929, a disease with similar symptoms appeared in South Africa and was named 'yellow branch' in Western Transvaal and 'greening' in Eastern Transvaal (Oberholzer et al., 1965). The agent associated with the disease was transmitted by graft-inoculation from citrus to citrus for the first time by Lin in China in 1956 (Lin, 1956). This work remained unknown outside China; McLean and Oberholzer (1965a) demonstrated independently that South African greening was graft-transmissible. Because 'huanglongbing' was the name used in the paper describing graft-transmission of the agent for the first time, it has priority over other names and has been unanimously adopted as the official name of the disease by the International Organization of Citrus Virologists (IOCV) (at the 12th Congress of IOCV, Fuzhou, China, 1995).
In the 1960s, the agent was shown to be transmitted by two insects: the African citrus psyllid Trioza erytreae in Africa (McLean and Oberholzer, 1965b) and the Asian citrus psyllid Diaphorina citri in Asia (Salibe and Cortez, 1966; Capoor et al., 1967; Martinez and Wallace, 1967).
Vector- and graft-transmissions of the huanglongbing agent (Ha) were obtained at a time when the nature of the Ha was still unknown. Laflèche and Bové (1970) were the first to show that greening was characterized by the presence of a microorganism, not a virus, in the sieve-tubes of affected plants, and they described this microorganism as mycoplasma-like. However, shortly after, the citrus stubborn agent was discovered and found to be a mycoplasma (later named Spiroplasma citri). EM comparisons between the Ha and the stubborn mycoplasma showed the Ha to be different from a mycoplasma (Saglio et al., 1971). In particular, while the stubborn mycoplasma, like all other mycoplasmas, was only surrounded by a 10-nm-thick cytoplasmic membrane, and had no cell wall, the Ha had a 25-nm-thick envelope, much too wide to be a single membrane envelope of a mycoplasma. Since then, much work has confirmed this view and shown the Ha to be a bacterium with a peptidoglycan-containing membranous cell wall, similar to that of Gram-negative bacteria (Garnier et al., 1976, 1984a, 1984b; Garnier and Bové, 1977, 1978). The bacterial nature of the Ha explains why penicillin treatments of infected plants result in symptom remission in the greenhouse (Bové et al., 1980) and in the field (Aubert and Bové, 1980).
As soon as the bacterial nature of the Ha was established, several groups tried to culture the organism. In 1984, Garnett (1984) claimed isolation and characterization of the Ha from South Africa. She cultured a Gram-negative bacterium from South African Ha-infected citrus leaf midribs. In view of the interest raised by this claim, several laboratories throughout the world tried to repeat the results. So far, all attempts to reproduce this work have failed (Garnier and Bové, 1983; Manicom, 1984; Garnier et al., 1987; da Graça, 1991). From these negative results and the fact that no experimental evidence has so far been produced to show that the bacterium cultured by Garnett is in fact the Ha, it is clear that the Ha has yet to be obtained in culture.
As the huanglongbing bacterium is not available in culture, molecular techniques have been used alone to characterize the organism. This work was facilitated by using the herbaceous host plant Catharanthus roseus (Garnier and Bové, 1983), in which the Ha reaches much higher titres than it does in citrus.
Using polymerase chain reaction (PCR), the 16S ribosomal DNAs (rDNAs) of an Asian strain (Poona strain, India) and an African strain (Nelspruit strain, South Africa) of the Ha were amplified from the total DNAs of infected C. roseus plants, cloned and sequenced (Jagoueix et al., 1994). Comparisons of the 16S rDNA sequences of the two Ha with sequences of 16S rDNAs obtained from the GenBank data base have shown that the two Ha belong to the alpha subdivision of the class Proteobacteria. This subdivision is a diverse group of Gram-negative bacteria that includes both plant pathogens/symbionts and human pathogens (Stackebrandt et al., 1988). The organisms in this group live in intimate association with eukaryotic cells and, in many cases, have acquired the ability to grow within an arthropod vector. The Ha fits this description: it grows in a specialized niche in its eukaryotic plant host (the phloem sieve-tubes) and is transmitted by two arthropod vectors (citrus psyllids), in which it multiplies both in the haemolymph and in the cells of the salivary glands.
Even though the closest relatives of the Ha are members of the alpha-2 subgroup, the Ha does not belong to this subgroup - it also has nucleotide signatures of the alpha-1 and alpha-3 subgroups. The Ha probably represents the first member of a new subgroup in the alpha subdivision. According to the proposal of Murray and Schleifer (1994) for the designation of putative taxa of prokaryotes, including non-culturable bacteria, the Ha has been assigned to the Candidatus genus Liberobacter (Jagoueix et al., 1994), later to be renamed Candidatus Liberibacter (Garnier et al., 2000).
The genome of the Ha contains the well-known eubacterial nusG-rplKAJL-rpoBC gene cluster (Villechanoux et al., 1993). The product of nusG is involved in transcription antitermination; rplKAJL codes for ribosomal proteins L11, L1, L10 and L12, and rpoBC, for the ß and ß' submits of RNA polymerase. A DNA fragment of this gene cluster from the Asian Poona (India) strain of the Liberibacter was cloned and sequenced. This fragment (In 2.6) was 2667 nucleotides long and comprised the 3' half of rplK, the entire rplA, rplJ and rplL genes, and the 5' half of rpoB. Using primers designed from In 2.6, a similar fragment (As 1.7) measuring 1676 nucleotides was obtained by PCR for the African Nelspruit Liberibacter strain (Planet et al., 1995). As 1.7 contains the 3' half of rplA, the entire rplJ and rplL genes, and the 5' half of rpoB. The percentage of homology between the nucleotide sequence of In 2.6 and As 1.7 is 74.2%. Because these DNA fragments code for highly conserved proteins (ribosomal proteins) it is likely that the percentage of homology of the total DNA of the two Liberibacter strains is <70% indicating that the African Liberibacter and the Asian Liberibacter represent two different species. Following the proposal of Murray and Schleifer (1994), the huanglongbing Liberibacter from India has received the designation Candidatus Liberibacter asiaticum, and the Liberibacter from South Africa, the designation Candidatus Liberibacter africanum (Jagoueix et al., 1994). The names of the HLB bacteria were then changed to 'Candidatus Liberibacter asiaticus, and 'Candidatus Liberibacter africanus' under the International Code of Nomenclature of Bacteria (Garnier et al., 2000).
In 1995 a new strain of African greening was detected in Calodendrum capense from South Africa. The new species was characterized by sequencing the 16S rDNA, the intergenic 16S/23S region and part of the rplKAJL-rpoBC operon. Comparisons with the equivalent genes showed that it differed from the two previously described Liberibacter species. When immunoflourescent reactions with monoclonal antibodies, produced from the Asian and African liberibacters, were carried out with the new strain the only antibodies reacting with infected C. capense leaf midrib sections were those specific for 'Candidatus Liberibacter africanus'. Results from the 16S rDNA sequence and phylogenetic analysis as well as the results from the serology, the C. capense Liberibacter appears to be more closely related to 'Candidatus Liberibacter africanus' than 'Candidatus Liberibacter asiaticus'. However, the intergenic 16S-23S region was closer to that of 'Candidatus Liberibacter asiaticus'. A name for the new Liberibacter, 'Candidatus Liberibacter africanus subsp. capensis was proposed as it can be easily distinguished from the 'Candidatus Liberibacter africanus' species infecting Citrus by RFLP analysis of the amplified DNA or using the specific oligonucleotide CAL1 (Garnier et al., 2000).
Symptoms of huanglongbing (HLB) were reported in Sao Paulo state in Brazil in 2004. Leaves with blotchy mottle symptoms characteristic of HLB were tested using PCR primers specific for the HLB 16S rRNA; however, the majority of samples tested negative for HLB. Using primers, universal for prokaryotic 16S rRNA evidence of infection by a bacterium was obtained. Sequence analysis and phylogeny studies were then used to determine that the amplified gene possessed the oligonucleotide and secondary loop structures of the alpha-Proteobacteria which includes the liberibacters, the group to which the HLB pathogens belong. Gene sequence similarities of 98.4 and 96.0% to 'Ca. L. asiaticus' and 'Ca. L. africanus', respectively, were obtained this lower similarity was reflected in the phylogenetic tree where the new bacterium did not cluster with the other HLB liberibacters, but in a separate branch. Sequence similarity of the 16S/23S intergenic region between the new bacterium and 'Ca. L. asiaticus' and 'Ca. L. africanus' were 66.0 and 79.5%, respectively. As sequence similarity with Liberibacter species does not vary greatly, this confirmed that the new bacterium is a novel species for which the name 'Candidatus Liberibacter americanus' is proposed (Texeira et al., 2005a).
DescriptionTop of page The huanglongbing bacteria are restricted to the phloem sieve tubes and possess a characteristic double-membrane cell envelope (Garnier et al., 1984). 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.
DistributionTop of page
The geographical distribution of Liberibacter asiaticus and L. africanus has been studied by DNA-DNA hybridization with probe In 2.6 specific for L. asiaticum and As 1.7 specific for L. africanus, as well as by PCR followed by XbaI restriction of the amplified DNA (see Diagnostic Methods). Only L. asiaticus was found in isolates from the 12 Asian countries studied, i.e. India, Nepal, Sri Lanka, Myanmar, Vietnam, Cambodia, Malaysia, Indonesia, Thailand, the Philippines, Taiwan, Japan, the Arabian Peninsula and China. Only L. africanus was found in samples from South Africa and Zimbabwe (Garnier and Bové, 1996; Colleta-Filho et al., 2004). Both L. asiaticus and L. africanus were present in Reunion and Mauritius, sometimes co-existing in the same tree (Garnier et al., 1996).
The occurrence of Liberibacter in additional countries is based on electron microscopy (EM), a technique which cannot distinguish between L. asiaticus and L. africanus (Bové and Garnier, 1994; Garnier and Bové, 1996). It is, however, very likely that the Liberibacter seen by EM in citrus from the following Asian countries is L. asiaticus: Japan, Bangladesh, Pakistan and Saudi Arabia; in these countries the vector is the Asian psyllid Diaphorina citri. Similarly, the Liberibacter involved in the following African countries is very probably L. africanus: Yemen, Burundi, Cameroon, Kenya, Malawi, Rwanda and Somalia; in these countries the vector is the African psyllid Trioza erytreae. At the border region between northern Yemen and south-western Saudi Arabia, both the African and Asian psyllids were found in the same orchards, the African psyllid coming from Yemen and the Asian psyllid from Saudi Arabia (Bové and Garnier, 1984).
In the following countries the presence of huanglongbing is based on symptomatology: Swaziland, Tanzania and Madagascar (Bové and Garnier, 1994). The vector present is the African psyllid.
The Mediterranean region and West Asia (from eastern Mediterranean to Afghanistan) are free from huanglongbing psyllid vectors and huanglongbing liberibacters, except Madeira where the African psyllid T. erytreae has been recently reported (EPPO/CABI, 1996). Also, D. citri has been observed in Iran just next to the border with Pakistan (M Garnier, INRA, France, personal communication, 1998).
Huanglongbing now occurs in the USA and Brazil and high populations of the Asian psyllid D. citri occur in Argentina, Brazil and Honduras, and Abaco and Grand Bahama island, The Cayman islands, US Virgin islands, the Dominican Republic, Cuba and Puerto Rico and probably other South and central American and Carribean countries (Halbert and Nunez, 2004). D. citri has reached Guadeloupe (Etienne et al., 1998), Florida (Hoy, 1998), Venezuela (Cermeli et al., 2000), Mexico (da Graca and Korsten, 2004) and Texas (French et al., 2001) and has recently been reported in Barbados (IPPC, 2014). Australia is free from the disease and its psyllid vectors; no liberibacters could be detected by EM and PCR in leaves with so-called greening-like symptoms (M Garnier and P Barkley, INRA, France, unpublished data; Weinert et al., 2004). Huanglongbing and D. citri are present in Papua New Guinea (Weinert et al., 2004).
See also CABI/EPPO (1998, No. 261) and CABI/EPPO (1998, No. 262).
Distribution TableTop of page
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.
|Continent/Country/Region||Distribution||Last Reported||Origin||First Reported||Invasive||Reference||Notes|
|Bangladesh||Present||Catling et al., 1978|
|Bhutan||Present||EPPO, 2011||Candidatus Liberibacter asiaticus|
|Cambodia||Present||Garnier and Bové, 1998|
|-Fujian||Present||Lin and Lin, 1956|
|-Guangdong||Present||Lin and Lin, 1956|
|-Guangxi||Present||Lin and Lin, 1956|
|-Hainan||Present||Lin and Lin, 1956|
|-Hong Kong||Present, few occurrences||EPPO, 2011||Candidatus Liberibacter asiaticus|
|-Hunan||Present||EPPO, 2011||Candidatus Liberibacter asiaticus|
|-Jiangxi||Present||Lin and Lin, 1956|
|-Sichuan||Present||EPPO, 2011||Candidatus Liberibacter asiaticus|
|-Yunnan||Present||EPPO, 2011||Candidatus Liberibacter asiaticus|
|-Zhejiang||Present||Lin and Lin, 1956|
|East Timor||Widespread||Weinert et al., 2004|
|-Andhra Pradesh||Present||Bové et al., 1993|
|-Arunachal Pradesh||Present||EPPO, 2011||Candidatus Liberibacter asiaticus|
|-Bihar||Present||EPPO, 2011||Candidatus Liberibacter asiaticus|
|-Delhi||Present||Bové et al., 1993|
|-Gujarat||Present||EPPO, 2011||Candidatus Liberibacter asiaticus|
|-Haryana||Present||EPPO, 2011||Candidatus Liberibacter asiaticus|
|-Himachal Pradesh||Present||EPPO, 2011||Candidatus Liberibacter asiaticus|
|-Indian Punjab||Present||Ahlawat, 1997|
|-Jammu and Kashmir||Present||EPPO, 2011||Candidatus Liberibacter asiaticus|
|-Karnataka||Present||Bové et al., 1993|
|-Kerala||Present||EPPO, 2011||Candidatus Liberibacter asiaticus|
|-Madhya Pradesh||Present||EPPO, 2011||Candidatus Liberibacter asiaticus|
|-Maharashtra||Present||Bové et al., 1993|
|-Manipur||Present||EPPO, 2011||Candidatus Liberibacter asiaticus|
|-Meghalaya||Present||EPPO, 2011||Candidatus Liberibacter asiaticus|
|-Odisha||Present||Bové et al., 1993|
|-Rajasthan||Present||Bové et al., 1993|
|-Sikkim||Present||EPPO, 2011||Candidatus Liberibacter asiaticus|
|-Tamil Nadu||Present||EPPO, 2011||Candidatus Liberibacter asiaticus|
|-Uttar Pradesh||Present||Bové et al., 1993|
|-West Bengal||Present||EPPO, 2011||Candidatus Liberibacter asiaticus|
|Indonesia||Present||Present based on regional distribution.|
|-Irian Jaya||Present||Davis et al., 2000|
|-Java||Present||Aubert et al., 1985|
|-Kalimantan||Present||Aubert et al., 1985|
|-Sulawesi||Present||Aubert et al., 1985|
|-Sumatra||Present||Aubert et al., 1985|
|Iran||Restricted distribution||EPPO, 2011; Mohkami et al., 2011; Salehi et al., 2012||Candidatus Liberibacter asiaticus|
|Japan||Present||Present based on regional distribution.|
|-Kyushu||Restricted distribution||EPPO, 2011||Candidatus Liberibacter asiaticus|
|-Ryukyu Archipelago||Present||Miyakawa and Tsuno, 1989|
|Laos||Present||Garnier and Bové, 1998|
|-Peninsular Malaysia||Present||Garnier and Bové, 1996|
|-Sarawak||Present||Bové et al., 1993|
|Myanmar||Present||Garnier and Bové, 1998|
|Nepal||Widespread||Regmi et al., 1996|
|Pakistan||Present||Garnier and Bové, 1996|
|Philippines||Widespread||Garnier and Bové, 1996|
|Saudi Arabia||Restricted distribution||Bové and Garnier, 1984|
|Sri Lanka||Present||EPPO, 2011||Candidatus Liberibacter asiaticus|
|Taiwan||Widespread||Matsumoto et al., 1961|
|Vietnam||Restricted distribution||Bové et al., 1996|
|Yemen||Restricted distribution||Bové and Garnier, 1984|
|Burundi||Present||Aubert et al., 1988|
|Cameroon||Present||Aubert et al., 1988|
|Central African Republic||Present||Aubert et al., 1988|
|Ethiopia||Present||Aubert et al., 1988|
|Kenya||Present||Introduced||1972||Invasive||Garnier et al., 1996; IPPC-Secretariat, 2005|
|Madagascar||Present||Bové and Garnier, 1994|
|Malawi||Present||Aubert et al., 1988|
|Mauritius||Present||Garnier et al., 1996|
|Réunion||Present||Etienne and Aubert, 1980|
|Rwanda||Present||Aubert et al., 1988|
|South Africa||Restricted distribution||Korsten et al., 1996|
|Swaziland||Present||Bové and Garnier, 1994|
|Tanzania||Restricted distribution||Bové and Garnier, 1994|
|Zimbabwe||Restricted distribution||Garnier and Bové, 1996|
|Mexico||Restricted distribution||NAPPO, 2010|
|-California||Present||California Department of Food and Agriculture, 2012; NAPPO, 2012; Kumagai et al., 2013|
|-Louisiana||Present, few occurrences||EPPO, 2011||Candidatus Liberibacter asiaticus|
|-South Carolina||Present, few occurrences||EPPO, 2011||Candidatus Liberibacter asiaticus|
|-Texas||Present||NAPPO, 2012; Alabi et al., 2014||Candidatus Liberibacter asiaticus|
Central America and Caribbean
|Belize||Present||Manjunath et al., 2010|
|Costa Rica||Restricted distribution||EPPO, 2011||Candidatus Liberibacter asiaticus|
|Cuba||Widespread||EPPO, 2011||Candidatus Liberibacter asiaticus|
|Dominican Republic||Restricted distribution||IPPC, 2009|
|French West Indies||Present||Cellier et al., 2014|
|Guadeloupe||Present||2012||Cellier et al., 2014|
|Honduras||Present, few occurrences|
|Martinique||Present||2013||Cellier et al., 2014|
|Puerto Rico||Restricted distribution|
|United States Virgin Islands||Present||NAPPO, 2010||Candidatus Liberibacter asiaticus|
|Argentina||Present, few occurrences|
|-Minas Gerais||Present||EPPO, 2011||Candidatus Liberibacter asiaticus|
|-Parana||Present||EPPO, 2011||Candidatus Liberibacter asiaticus|
|-Sao Paulo||Widespread||Invasive||Coletta-Filho et al., 2004|
|Paraguay||Present||Leite et al., 2013||Candidatus Liberibacter asiaticus.|
|Venezuela||Present||IPPC, 2018||Present: subject to official control.|
|Netherlands||Absent, confirmed by survey||NPPO of the Netherlands, 2013|
|Papua New Guinea||Restricted distribution||Weinert et al., 2004; Davis et al., 2005|
Risk of IntroductionTop of page
The major phytosanitary risk is presented by the introduction of Liberibacter-infected citrus budwood or trees into regions still free from the disease but where the psyllid vectors occur. This is the case for the major parts of the Cape region in South Africa where Trioza erytreae is present, and the many Latin American countries where Diaphorina citri occurs.
Also, there is a danger of introducing both the huanglongbing agent and the psyllid vector(s) into regions where they are absent, especially the Mediterranean region and western Asia. The presence of T. erytreae in Madeira and of D. citri in Florida (USA), Guadeloupe and Iran is alarming. Restriction of movement of plant material from infected to non-infected regions applies not only to citrus fruit trees but also to rutaceous ornamentals. The detection of the huanglongbing pathogens, particulary L. asiaticus, generally seem to follow the introduction of the vector to a new area, e.g. Brazil and Florida.
Hosts/Species AffectedTop of page
Huanglongbing is a disease of rutaceous plants. It severely affects sweet orange, mandarin and tangelo trees but many other species show more or less pronounced symptoms of the disease. Mexican lime (Citrus aurantifolia) is less susceptible than sweet orange and mandarin even though it is a preferred host of the vector Diaphorina citri (Bové and Garnier, 1984).
Several wild rutaceous species are hosts of the psyllid vectors. In South Africa, Toddalia lanceolata, a host of Trioza erytreae, was infected by Liberibacter africanus (Korsten et al., 1996) and, recently, Calodendrum capense, an ornamental rutaceous tree, was infected by a Liberibacter characterized as a subspecies of L. africanus (Garnier et al., 1998). A name for the new Liberibacter, 'Candidatus Liberibacter africanus subsp. capensis' was proposed. To date this strain of the Liberibacter has not been detected in citrus (Garnier et al., 2000). In Asia, the ornamental rutaceous shrub, Murraya paniculata, is also a preferred host of D. citri. In Mauritius, however, it has tested negative for Liberibacter infection by DNA hybridization and PCR. A strain of Liberibacter, thought to be 'Candidatus Liberibacter americanus', has been identified in M. paniculata in Brazil (Coletta-Filho et al., 2005).
Both L. africanus and L. asiaticus can be transmitted by dodder (Cuscuta campestris) from citrus to Catharanthus roseus in which the liberibacters reach higher titres than in citrus (Garnier and Bové, 1983). Subsequently, transmission from C. roseus to C. roseus is achieved by graft inoculation. L. asiaticus has also been dodder-transmitted from C. roseus to tobacco (Nicotiana tabacum var. xanthi NC). Infected tobacco plants show severe symptoms even though the Liberibacter titre is low (M Garnier, INRA, France, unpublished data).
The African psyllid vector T. erytreae and the Asian psyllid vector D. citri are natural hosts of L. africanus and L. asiaticus, respectively. However, it has been shown experimentally that T. erytreae is a host and a vector of L. asiaticus and D. citri, a host and a vector of L. africanus (Massonié et al., 1976; Lallemand et al., 1986). Whether this is also true in nature in regions where the two liberibacters and the two psyllids are known to occur concomitantly, is not yet established. T. erytreae also feeds on C. capense, the host of 'Candidatus Liberibacter africanus subsp. capensis; however, it has not been proven to be a vector of the Liberibacter strain. D. citri is the vector of 'Candidatus Liberibacter americanus' (Texeira et al., 2005).
Host Plants and Other Plants AffectedTop of page
|Calodendrum capense (cape chestnut)||Rutaceae||Wild host|
|Citrus aurantiifolia (lime)||Rutaceae||Other|
|Citrus limon (lemon)||Rutaceae||Other|
|Citrus reticulata (mandarin)||Rutaceae||Main|
|Citrus reticulata x paradisi (tangelo)||Rutaceae||Main|
|Citrus sinensis (navel orange)||Rutaceae||Main|
|Clausena (wampee)||Rutaceae||Wild host|
|Fortunella (kumquats)||Rutaceae||Wild host|
|Limonia acidissima (elephant apple)||Rutaceae||Wild host|
|Murraya paniculata (orange jessamine)||Rutaceae||Wild host|
Growth StagesTop of page Flowering stage, Fruiting stage, Seedling stage, Vegetative growing stage
SymptomsTop of page
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). Huanglongbing bacteria, however, do not induce the xylem dysfunction and wilting observed in blighted trees. Dual infection of trees with HLB and CTV is common with reports suggesting that these trees have more severe symptoms (Huang et al., 1980).
Chronically infected trees are sparsely foliated and show extensive twig dieback. The fruits are often small, lopsided and 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/SignsTop of page
|Fruit / abnormal patterns|
|Fruit / abnormal shape|
|Fruit / premature drop|
|Fruit / reduced size|
|Growing point / dieback|
|Inflorescence / premature ripening|
|Leaves / abnormal patterns|
|Leaves / yellowed or dead|
|Roots / reduced root system|
|Seeds / discolorations|
|Seeds / distortion|
|Seeds / empty grains|
|Stems / dieback|
|Whole plant / dwarfing|
|Whole plant / early senescence|
|Whole plant / plant dead; dieback|
Biology and EcologyTop of page
In South Africa, Kenya, Ethiopia, Madagascar and Yemen, huanglongbing occurs only in cool climatic conditions, at elevations above 600-1000 m. The psyllid vector is Trioza erytreae. In contrast, in the Indian Subcontinent, Asia and Saudi Arabia, the disease also occurs at low elevations with a hot climate. The psyllid vector is Diaphorina citri. These observations, confirmed by experiments under phytotron conditions (Bové et al., 1974), suggest that there are two forms of huanglongbing: the African heat-sensitive form caused by Liberibacter africanus, and the Asian heat-tolerant form caused by L. asiaticus. That these temperature effects are due to the respective liberibacters has been demonstrated in Catharanthus roseus: in plants infected by L. africanus, the disease is heat sensitive (no symptoms above 25-30°C), while in L. asiaticus-infected plants, the disease is heat tolerant (symptoms also above 30°C). The distinction between heat-tolerant and heat-sensitive forms of huanglongbing was the first indication that different strains of the agent occur, and that African strains are quite different from Asian strains. These early observations are now easily understood on the basis of two recognized Liberibacter species: L. africanus and L. asiaticus. No data are available on the climatic conditions necessary for the survival of L. americanus; however, it does occur in the same areas as L. asiaticus (Texeira et al., 2004), suggesting similar climatic requirements.
Means of Movement and DispersalTop of page
Huanglongbing was shown to be transmitted by two insects: the African citrus psyllid, Trioza erytreae, in Africa (McLean and Oberholzer, 1965b) and the Asian citrus psyllid, Diaphorina citri, in Asia (Capoor et al., 1967; Martinez and Wallace, 1967).
Plant TradeTop of page
|Plant parts liable to carry the pest in trade/transport||Pest stages||Borne internally||Borne externally||Visibility of pest or symptoms|
|Bark||Yes||Pest or symptoms usually visible to the naked eye|
|Flowers/Inflorescences/Cones/Calyx||Yes||Pest or symptoms usually visible to the naked eye|
|Fruits (inc. pods)||Yes||Pest or symptoms usually visible to the naked eye|
|Growing medium accompanying plants||Yes||Pest or symptoms usually invisible|
|Leaves||Yes||Pest or symptoms usually visible to the naked eye|
|Roots||Yes||Pest or symptoms usually visible to the naked eye|
|Seedlings/Micropropagated plants||Yes||Yes||Pest or symptoms usually invisible|
|Stems (above ground)/Shoots/Trunks/Branches||Yes||Pest or symptoms usually visible to the naked eye|
|True seeds (inc. grain)||Yes||Pest or symptoms usually visible to the naked eye|
|Wood||Yes||Pest or symptoms usually invisible|
|Plant parts not known to carry the pest in trade/transport|
Vectors and Intermediate HostsTop of page
ImpactTop of page
HLB has been regarded as one of the most important threats to global commercial and sustainable citrus production. It is estimated that globally more than 60 million trees had been destroyed by the disease by the early 1990s (Aubert, 1993). In Saudi Arabia, all sweet oranges and mandarin trees had declined by 1986 leaving only limes (Aubert, 1993). In Indonesia alone, HLB has resulted in the destruction of 3 million trees (Tirtawadja, 1980).
Crop losses from HLB of 30-100% have been reported in Africa (da Graca and Korsten, 2004). A survey was conducted during 1994 to determine the importance of citrus huanglongbing in South Africa (E Juckers and L Korsten, University of Pretoria, South Africa, personal communication). Results indicate that in comparison with a previous survey (Schwarz, 1967), the disease has continued to spread throughout the citrus industry. However, the severity of the disease has been greatly reduced in areas where control strategies are rigorously applied (see Prevention and Control). In huanglongbing-affected areas, lower psyllid populations were observed in the 1994 survey than in 1967, due to effective insect control. However, higher psyllid populations were found in Southern Natal and Eastern Cape where the disease is not present. Several orchards were affected by huanglongbing in the Western Cape (Paarl, Stellenbosch, Vemmershoek) in 1996.
In the Philippines, citrus culture has been drastically limited by huanglongbing. Similarly, in certain areas of Indonesia, the incidence of the disease is high. In northern Bali for instance, almost 100% of mandarin trees planted in 1990-91 were severely affected in 1996. In India, the disease is widespread (Bové et al., 1993; Varma et al., 1993). In the Pokhara Valley of Nepal, a major mandarin-growing area, trees show huanglongbing symptoms before they are 10 years old. The trees are replaced and the disease reoccurs on new trees. This cycle of replanting has occurred several times since the disease was introduced from India in the 1960s (Regmi et al., 1996). In southwestern Saudi Arabia, practically all mandarin and sweet orange trees were destroyed by the disease, but the more tolerant Mexican lime (Citrus aurantifolia) trees managed to survive despite heavy infestation with Diaphorina citri (Bové and Garnier, 1984).
The introduction of L. asiaticus and the discovery of L. americanus in Brazil has resulted in the removal of hundreds of thousands of trees from citrus orchards in Brazil. The eradication of L. asiaticus from Florida, USA, is not considered possible.
Economic ImpactTop of page
Reduced citrus production resulting in both lower incomes and less food available (IPPC-Secretariat, 2005).
DiagnosisTop of page
32P-labelled In 2.6 and As 1.7 can be used as probes in Southern or dot-blot hybridizations. At high stringency, In 2.6 hybridizes only with Liberibacter asiaticus while As 1.7 reacts only with L. africanus (Villechanoux et al., 1992; Planet et al., 1995). For these hybridizations, DNA is extracted from 2 g of citrus leaf midribs by the CTAB (cetyltrimethylammonium bromide) method of Murray and Thompson (1980). Dot-blot hybridization is carried out as described in Villechanoux et al. (1992). DNA hybridization with probes In 2.6 or As 1.7 can also be applied to the identification of liberibacters in individual psyllid vectors. The anaesthetized insects are crushed with a glassrod on a Nylon N+ membrane (1 insect per cm²) to yield a so-called 'crush-blot', and the membrane, after DNA denaturation, is hybridized with the probe (Bové et al., 1993).
The two Candidatus Liberibacter species can also be identified by PCR-amplification of their 16S rDNA followed by restriction enzyme (XbaI) analysis of the amplified DNA (Jagoueix et al., 1996). Forward primer OI-1 was defined from the 16S rDNA sequence of L. asiaticus (Poona strain, India) and forward primer OA-1, from the 16S rDNA of L. africanum (Nelspruit strain, South Africa). OA-1 is identical to OI-1 except for three base changes. Reverse primer OI-2c corresponds to identical sequences on the two Liberibacter 16S rDNAs. The primer pair OI-1/OI-2c is able to amplify the two Liberibacter species; a band of amplified DNA is obtained with as little as 0.1 ng of template DNA. The pair OA-1/OI-2c preferentially amplifies L. africanum. In both cases, amplicons close to 1160 bp are obtained. When both Liberibacter species are known or suspected to be present, it is recommended to use the two forward primers OI-1 plus OA-1 in the same PCR reaction mixture. Off the shelf DNA extraction kits, including the Sigma REDExtract-N-AmpTM Plant PCR Kit, Sigma, Missouri, USA and the Qiagen DNeasy® Plant Mini Kit, can also be used to extract DNA for PCR reactions (D Hailstones, personal communication, 2005).
The amplicon from the 16S rDNA of L. asiaticus contains one Xba1 site and yields 2 fragments (640 bp and 520 bp) upon Xba1 hydrolysis. The amplicon from the 16S rDNA of L. africanum has two Xba1 sites and yields three fragments (520 bp, 500 bp and 130 bp). Thus Xba1 treatment of the amplicons permits easy distinction between the two Liberibacter species. Details for template DNA preparation (Wizard extracts), PCR detection and identification of the two Liberibacter species has been published (Jagoueix et al. 1996). The PCR technique can also be applied to the psyllid insect vectors.
A PCR method based on the amplification of ribosomal protein genes has been developed. It allows direct distinction between the two Liberibacter species based on the difference in size of the amplified DNA (Hocquellet et al., 1998). Two methods for the PCR detection of L. americanus have been published (Coletta-Filho et al., 2005; Texeira et al., 2005b).
Monoclonal antibodies (MAs) have been produced against the Nelspruit strain of L. africanus (MAs 14A1, 10H8 and MG8) and two strains of L. asiaticus: the Poona strain from India (MAs 10A6, 2D12, 2B6, 2C11 and 1A5) and the Fuzhou strain from China (MAs 10F4, 5H10, 6G1, 11H6 and 12E12). These MAs are strain-specific and recognize essentially the strain used for immunization (Garnier et al., 1987, 1991; Gao et al., 1993). However, MA 1A6 directed against the Poona strain recognized all Asian strains tested except those from Fuzhou and did not react with African strains. MA 14A1 directed against the Nelspruit strain has been used in South Africa to detect L. africanus by immunofluorescence (IF). In one experiment, 16 of 18 citrus leaf samples testing positive by PCR and hybridization were also positive by IF; 2 were negative (Korsten et al., 1996). These results indicate that at least two serotypes of L. africanus occur in South Africa: one reacting with MA 14A1, the other giving no reaction.
Fourier transform infrared-attenuated total reflection (FTIR-ATR) spectroscopy is a new technology that has been used by USDA-ARS scientists to identify citrus greening-infected plant leaves with 95% accuracy. The system clearly discriminated HLB-infected leaves from healthy leaves; however, more work will be needed to discriminate HLB from other citrus diseases (USDA-ARS, 2011).
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.
Detection and InspectionTop of page
The disease is not easy to recognize in the field as there are no specific symptoms (see Symptoms). A yellowing tree canopy, blotchy mottled leaves and small lopsided fruits with aborted seeds provide the best indications of huanglongbing infection. Diagnosis should always be confirmed by identifying the bacterium by EM, DNA hybridization or PCR (see Diagnosis).
Similarities to Other Species/ConditionsTop of page
The symptoms of huanglongbing can be confused with stubborn disease (Spiroplasma citri), Citrus tristeza virus, species of Phytophthora, citrus blight (a disease of unconfirmed aetiology) and certain nutrient deficiencies. See Symptoms for more details.
Prevention and ControlTop of page
Biological control of the two psyllid vectors was achieved successfully in Reunion with hymenopteran psyllid parasites: Tamarixia radiata introduced from India against Diaphorina citri, and Tamarixia dryi, from South Africa, against Trioza erytreae (Aubert and Quilici, 1984; Aubert, 1987; Hoy and Nguyen, 2000). Control of the psyllids, together with destruction of Liberibacter-infected trees and use of Liberibacter-free material for replantings have led to the almost total elimination of huanglongbing in Reunion. Unfortunately, biological control of the psyllids cannot be achieved in most countries because the psyllid parasites are themselves hosts for parasitic insects. Care was taken not to introduce these hyperparasites into Reunion when biological control was initiated.
Research on the biological control of the vectors has also been carried out in Mauritius (Aubert, 1987).
Appropriate use of insecticides has resulted in good control of T. erytreae, the vector, in South Africa (da Graça, 1991).
For control of the liberibacters, injection of antibiotics and especially tetracycline into the trunk of affected sweet orange trees in South Africa has resulted in at least partial recovery of the trees. However, tetracycline is bacteriostatic not bacteriocidal and has to be injected repeatedly. It is also phytotoxic. Its use on a large scale might have adverse effects on the environment. For these reasons, its use has decreased in recent years. In Indonesia, a nation-wide, large-scale tetracycline injection programme has failed.
In areas where the disease is not present, the most effective means to control the disease is to prevent its introduction or that of the vectors through strict quarantine measures. Inclusion of the alternative hosts in this strategy is also important (da Graca and Korsten, 2004).
In South Africa, removal of infected branches or trees and neglected trees, use of Liberibacter-free planting material, and control of the psyllid vector are used to reduce the impact of the disease (Buitendag and von Broembsen, 1993). The African form of HLB can be eliminated from citrus plant material by exposure to extended periods of heat (Labuschagne and Kotze, 1984).
In China, successful control of huanglongbing has been achieved by promoting large-scale production of healthy nursery plants, organizing systematic and early removal of infected plants in existing orchards, and applying insecticide sprays at critical flushing periods (Ke and Fan, 1990).
In northern Bali, Indonesia, in 1986-1988, eradication of the disease by the large-scale destruction of 4 million infected trees, followed by replanting with healthy trees, was attempted. However, the attempt failed, as by 1993, 40% of these trees were infected and in 1996 more than 90% showed HLB symptoms (Aubert, 1993). Shoot-tip grafting is recommended for producing healthy citrus plants (Navarro et al., 1975).
Some isolates of Citrus tristeza virus are reported to protect trees from HLB infection (van Vuuren et al., 2000).
ReferencesTop of page
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