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Common name
dieback (English, India), blotchy mottle (English, South Africa), vein phloem degeneration (English, Indonesia), huanglongbing (HLB) (Chinese), greening (English, South Africa), mottle leaf (English, Philippines), citrus greening disease (English), yellow shoot disease (English), likubin (English, Taiwan), Enverdecimiento (Spanish), yellow branch (English, South Africa)
Synonym
Candidatus Liberobacter asiaticus
Candidatus Liberobacter asiaticum
Similar species
Candidatus Liberibacter africanus, Candidatus Liberibacter americanus
Summary
Huanglongbing (HLB) or citrus greening disease is a destructive disease of citrus caused by gram-negative phloem-restricted bacteria belonging to the genus Candidatus Liberibacter. The genus comprises three known species: Candidatus Liberibacter asiaticus, occurring in Asian countries and, to a lesser extent, in Brazil and the USA (Florida), Candidatus Liberibacter africanus, recorded from African countries, and Candidatus Liberibacter americanus present in Brazil and Florida. It is thought that each Liberibacter species evolved in the continent after which it is named. HLB is transmitted between trees by the psyllids Trioza erytreae in Africa and Diaphorina citri in Asia and America. HLB affects all commercial citrus varieties, causing mottling of leaves, stunting of growth and formation of small, deformed fruit which fail to colour properly. HLB can destroy citrus groves within 5 to 8 years. Apart from prevention there are no control measures currently available, causing HLB to often be described as the most destructive and serious disease of citrus.
Species Description
The disease known commonly as huanglongbing (HLB) is caused by gram-negative bacteria with a double-membrane cell envelope in the genus Candidatus Liberibacter. There are three known species which cause HLB in different regions of the world: Candidatus Liberibacter asiaticus, Candidatus Liberibacter africanus and Candidatus Liberibacter americanus. None of the Candidatus species of Liberibacter have been cultured despite efforts by researchers (Li et al. 2008), hence the term Candidatus which indicates an organism that has not been cultured and is characterized on the basis of DNA properties (Murray and Schleifer 1994 in Bove and Ayres 2007). However a very recent study by Sechel et al (2009) reports the successful cultivation of all three species of the genus

The three known species of Liberibacter cause essentially the same symptoms wherever HLB occurs. Bove (2006) reports that “ Infected trees show a blotchy mottle condition of the leaves that results in the development of yellow shoots, the early and very characteristic symptom of the disease. Trees are stunted, declining and bear a few, small-sized, and deformed (lop-sided) fruits, that are poorly coloured (greening) and with coloration starting at the peduncular end (colour inversion).” However there are no specific symptoms of HLB that can be used as a diagnostic (Bove 2006). Time from infection to appearance of symptoms ranges from less than a year to several years depending on season, environmental conditions, tree age, host species/cultivar and health of tree (Jepson 2008).

For these reasons additional techniques are required for detection. Electron microscopy (EM) has been used in the past for detection of HLB. Detection is based on the location of HLB in the sieve tubes, and the presence of a cell wall; features which no other citrus-infecting bacteria possess (Bove 2006). However there are no morphological differences to distinguish between the Liberibacter species which cause HLB.

The African and Asian form can be distinguished based on serological methods or by temperature sensitivity, as Candidatus Liberibacter africanus is heat sensitive, while Candidatus Liberibacter asiaticus is heat tolerant (Garnier et al. 1991; Gao et al. 1993 in Bove 2006). Candidatus Liberibacter americanus is also heat tolerant (Das et al. 2007). Other qualitative methods used for detection or identification of HLB pathogens include biological indexing (Roistacher 1991 in Li et al. 2008b), chemifluoresence (Schwarz 1968 in Li et al. 2008b) and enzyme-linked immunosorbent assay (Garnier and Bove 1993 in Li et al. 2008b). Gottwald et al. (2007) report that “PCR is now the main confirmatory test and is routinely used in many areas and particularly in Florida and Brazil both for diagnostics and as a prelude to disease management.” Two PCR systems are commonly used; based on the 16S rRNA gene and the ß operon (Bove and Ayres 2007).

For high quality images and descriptions please see Gottwald et al. (2007): Citrus Huanglongbing: The Pathogen and Its Impact.

Notes
Although HLB is currently attributed to Candidatus Liberbacter spp. it is possible that other plant pathogens contribute to this disease. Because Ca. Li. spp. are unable to be cultured, Koch’s postulates which confirm the causal agent of a disease, cannot be fulfilled. Furthermore PCR results from citrus showing symptoms sometimes yield negative results. While the common explanation is that the bacterial titer is below detection limits, it may be that another pathogen is involved. A survey conducted in 2006-2007 in China sampled citrus showing HLB symptoms. A phytoplasma, termed HLB-associated phytoplasma, was associated with HLB symptoms more than was Ca. L. asiaticus. 29.1% of samples were detected with phytoplasma only; compared to just 14.2% detected with just Ca. L. asiaticus. This study indicates that phytoplasma may have a role in HLB but “more data, particularly those from controlled experiments, are needed to better establish the association of phytoplasma with HLB” (Chen et al. 2009).
Lifecycle Stages
Candidatus Liberibacters are gram-negative bacteria with a double-membrane cell envelope found in the sieve tube elements of phloem. The bacteria are transmitted by psyllids as they feed. Candidatus Liberibacter asiaticus and Candidatus Liberibacter americanus are transmitted by the adults of the citrus psyllid Diaphorina citri Kuwayana. Ca. L. africanus is transmitted by the adult psyllid Trioza erytreae Del Guercio. The bacteria can be acquired by the insects in the nymphal stages and may be transmitted throughout the lifespan of the psyllid (Jepson 2008). The bacteria have been detected in the haemolymph and salivary glands of both psyllid vectors. D. citri has been demonstrated to retain the bacteria for 12 weeks, indicaitng that the bacteria may be replicating in the insect (Hung et al. 2004 in Manjunath et al. 2008). There is a remote possibilityt that Candidatus Liberibacter asiaticus bacteria are transmitted transovarially [transmission from parent to offspring] (Manjunath et al. 2008).
Uses
Due to their devastating effects on citrus trees and their efficient transmission by the psyllid vectors, ‘Ca. L. africanus’ and Ca. L. asiaticus’ have been classified by the US Government as ‘select agents’ with potential for bioterrorism (Teixeira et al. 2005)
Habitat Description
The disease known commonly as huanglongbing (HLB) is caused by gram-negative bacteria with a double-membrane cell envelope in the genus Candidatus Liberibacter. There are three known species which cause HLB in different regions of the world: Candidatus Liberibacter asiaticus, Candidatus Liberibacter africanus and Candidatus Liberibacter americanus. None of the Candidatus species of Liberibacter have been cultured despite efforts by researchers (Li et al. 2008), hence the term Candidatus which indicates an organism that has not been cultured and is characterized on the basis of DNA properties (Murray and Schleifer 1994 in Bove and Ayres 2007). However a very recent study by Sechel et al (2009) reports the successful cultivation of all three species of the genus

The three known species of Liberibacter cause essentially the same symptoms wherever HLB occurs. Bove (2006) reports that “ Infected trees show a blotchy mottle condition of the leaves that results in the development of yellow shoots, the early and very characteristic symptom of the disease. Trees are stunted, declining and bear a few, small-sized, and deformed (lop-sided) fruits, that are poorly coloured (greening) and with coloration starting at the peduncular end (colour inversion).” However there are no specific symptoms of HLB that can be used as a diagnostic (Bove 2006). Time from infection to appearance of symptoms ranges from less than a year to several years depending on season, environmental conditions, tree age, host species/cultivar and health of tree (Jepson 2008).

For these reasons additional techniques are required for detection. Electron microscopy (EM) has been used in the past for detection of HLB. Detection is based on the location of HLB in the sieve tubes, and the presence of a cell wall; features which no other citrus-infecting bacteria possess (Bove 2006). However there are no morphological differences to distinguish between the Liberibacter species which cause HLB.

The African and Asian form can be distinguished based on serological methods or by temperature sensitivity, as Candidatus Liberibacter africanus is heat sensitive, while Candidatus Liberibacter asiaticus is heat tolerant (Garnier et al. 1991; Gao et al. 1993 in Bove 2006). Candidatus Liberibacter americanus is also heat tolerant (Das et al. 2007). Other qualitative methods used for detection or identification of HLB pathogens include biological indexing (Roistacher 1991 in Li et al. 2008b), chemifluoresence (Schwarz 1968 in Li et al. 2008b) and enzyme-linked immunosorbent assay (Garnier and Bove 1993 in Li et al. 2008b). Gottwald et al. (2007) report that “PCR is now the main confirmatory test and is routinely used in many areas and particularly in Florida and Brazil both for diagnostics and as a prelude to disease management.” Two PCR systems are commonly used; based on the 16S rRNA gene and the ß operon (Bove and Ayres 2007).

For high quality images and descriptions please see Gottwald et al. (2007): Citrus Huanglongbing: The Pathogen and Its Impact.

Nutrition
Candidatus Liberibacter spp. are restricted to the sieve tube elements of the phloem. Kim et al. (2008) report that phloem is an ideal habitat for many pathogens due to the presence of rich nutrients in phloem sap.

Principal source:

Compiler: IUCN SSC Invasive Species Specialist Group (ISSG) with support from the Ministry of Agriculture and Forestry (MAF)- Biosecurity New Zealand

Review:

Publication date: 2009-11-20

Recommended citation: Global Invasive Species Database (2018) Species profile: Candidatus Liberibacter asiaticus. Downloaded from http://www.iucngisd.org/gisd/species.php?sc=1496 on 16-12-2018.

General Impacts
Of all citrus diseases HLB is often described as the most destructive and lethal (Bove 2006; Bove and Ayres 2007; Gottwald et al. 2007). Bove (2006) reports that “HLB symptoms are virtually the same wherever the disease occurs. Infected trees show a blotchy mottle condition of the leaves that results in the development of yellow shoots, the early and very characteristic symptom of the disease. Trees are stunted, declining and bear a few, small-sized, and deformed (lop-sided) fruits, that are poorly coloured (greening) and with coloration starting at the peduncular end (colour inversion).” The taste of the fruit is also affected. David Hall, an entomologist with USDA in Fort Pierce, Florida describes the taste as “jet fuel mixed with Vicks VapoRub” (Stokstad 2006).

Kim et al. (2008) analyzed citrus response to HLB infection. Microarray analysis of citrus revealed that infection affected the expression of 624 genes including those involved with sugar metabolism, plant defense, phytohormone and cell wall metabolism. Anatomical analyses showed that HLB infection caused phloem disruption, sucrose accumulation, and plugged sieve pores. Phloem disruption and blockage is likely to be caused by host responses rather than by HLB bacterial aggregations. Plugged sieve pores and upregulation of genes involved in sucrose biosynthesis is thought to cause accumulation of sucrose in leaves leading to nutrient deficiencies in sink organs, stunting of plant growth, fruit maturation and seed development (Kim et al. 2008).

HLB affects almost all citrus cultivars, and causes substantial economic losses to the citrus industry by shortening the lifespan of trees and making fruit inedible (Das et al. 2007). Gottwald et al. (2007) report that “almost 100 million trees have been affected and destroyed in many countries of South and Southeast Asia, Indonesia, Philippines, India, Arabian Peninsula, and South Africa, compromising the local citriculture (Aubert et al. 1985; Bove 1986; Halbert and Manjunath 2004; Toorawa 1998). Since 2004, more than 500 thousand trees were officially eliminated in Brazil due to HLB and it is estimated that an additional 300 to 400 thousand trees were unofficially eliminated by commercial citrus growers.”

Management Info
At present there are no curative methods to control HLB. Thus control measures focus largely on prevention of infection. Please follow this link for more on the management and control of Huanglongbing (Candidatus Liberibacter spp.)
Countries (or multi-country features) with distribution records for Candidatus Liberibacter asiaticus
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Informations on Candidatus Liberibacter asiaticus has been recorded for the following locations. Click on the name for additional informations.
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Impact information
Of all citrus diseases HLB is often described as the most destructive and lethal (Bove 2006; Bove and Ayres 2007; Gottwald et al. 2007). Bove (2006) reports that “HLB symptoms are virtually the same wherever the disease occurs. Infected trees show a blotchy mottle condition of the leaves that results in the development of yellow shoots, the early and very characteristic symptom of the disease. Trees are stunted, declining and bear a few, small-sized, and deformed (lop-sided) fruits, that are poorly coloured (greening) and with coloration starting at the peduncular end (colour inversion).” The taste of the fruit is also affected. David Hall, an entomologist with USDA in Fort Pierce, Florida describes the taste as “jet fuel mixed with Vicks VapoRub” (Stokstad 2006).

Kim et al. (2008) analyzed citrus response to HLB infection. Microarray analysis of citrus revealed that infection affected the expression of 624 genes including those involved with sugar metabolism, plant defense, phytohormone and cell wall metabolism. Anatomical analyses showed that HLB infection caused phloem disruption, sucrose accumulation, and plugged sieve pores. Phloem disruption and blockage is likely to be caused by host responses rather than by HLB bacterial aggregations. Plugged sieve pores and upregulation of genes involved in sucrose biosynthesis is thought to cause accumulation of sucrose in leaves leading to nutrient deficiencies in sink organs, stunting of plant growth, fruit maturation and seed development (Kim et al. 2008).

HLB affects almost all citrus cultivars, and causes substantial economic losses to the citrus industry by shortening the lifespan of trees and making fruit inedible (Das et al. 2007). Gottwald et al. (2007) report that “almost 100 million trees have been affected and destroyed in many countries of South and Southeast Asia, Indonesia, Philippines, India, Arabian Peninsula, and South Africa, compromising the local citriculture (Aubert et al. 1985; Bove 1986; Halbert and Manjunath 2004; Toorawa 1998). Since 2004, more than 500 thousand trees were officially eliminated in Brazil due to HLB and it is estimated that an additional 300 to 400 thousand trees were unofficially eliminated by commercial citrus growers.”

Red List assessed species 0:
Management information
At present there are no curative methods to control HLB. Thus control measures focus largely on prevention of infection. Please follow this link for more on the management and control of Huanglongbing (Candidatus Liberibacter spp.)
Locations
MAURITIUS
REUNION
UNITED STATES
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Monitoring
Bibliography
28 references found for Candidatus Liberibacter asiaticus

Managment information
Beattie, G.A.C. & Barkley, P. 2009. Huanglongbing and its vectors: A pest specific contingency plan for the citrus and nursery garden industries, Volume 2.
da Graca, J.V. & Korsten, L. 2004. Citrus huanglongbing: review, present status and future strategies. In S.A.M.H. Naqvi (Ed.), Diseases of Fruits and Vegetables. Diagnosis and Management Volume 1 (pp. 229-245). Kluwer Academic Publishers.
Ding, F., Shuangxia, J., Hong, N., Zhong, Y., Cao, Q., Yi, G. & Wang, G. 2008. Vitrification�cryopreservation, an efficient method for eliminating Candidatus Liberobacter asiaticus, the citrus Huanglongbing pathogen, from in vitro adult shoot tips. Plant Cell Reports 27: 241-250.
Lopes, S.A., Frare, G.f., Yamamoto, P.T., Ayres, A.J. & Barbosa, J.C. 2007. Ineffectiveness of pruning to control citrus huanglongbing caused by Candidatus Liberibacter americanus. European Journal of Plant Pathology 119: 463-468.
Manjunath, K.L., Halbert, S.E., Ramadugu, C., Webb, S. & Lee, R.F. 2008. Detection of �Candidatus Liberibacter asiaticus� in Diaphorina citri and its importance in the management of citrus huanglongbing in Florida. Phytopathology 98:387-396.
McKenzie, C.L. & Puterka, G.J. 2004. Effect of sucrose octanoate on survival of nymphal and adult Diaphorina citri (Homoptera: Psyllidae). Journal of Economic Entomology 97(3): 970-975.
Nakata, T. 2008. Effectiveness of micronized fluorescent powder for marking citrus psyllid, Diaphorina citri. Applied Entomology and Zoology 43(1): 33-36.
Qureshi, J.A. & Stansly. 2008. Rate, placement and timing of aldicarb applications to control Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Psyllidae), in oranges. Pest Management Science 64: 1159-1169.
Urasaki, N., Kawano, S., Mukai, H., Uemori, T., Takeda, O. & Sano, T. 2008. Rapid and sensitive detection of ��Candidatus Liberibacter asiaticus�� by cycleave isothermal and chimeric primer-initiated amplification of nucleic acids. Journal of General Plant Pathology 74: 151-155.
General information
APHIS. 2005. U.S. Department of Agriculture and Florida Department of Agriculture confirm detection of citrus greening. USDA Press Release.
Bove, J.M. 2006. Huanglongbing: a destructive, newly-emerging century-old disease of citrus. Journal of Plant Pathology 88(1): 7-37.
Bove, J.M. & Ayres, A.J. 2007. Etiology of three recent diseases of citrus in Sao Paulo state: sudden death, variegated chlorosis and huanglongbing. IUBMB Life 59(4-5): 346-354.
Chen, J., Pu, X., Deng, X., Liu, S., Li, H. & Civerolo, E. 2009. A phytoplasma related to �Candidatus Phytoplasma asteri� detected in citrus showing huanglongbing (yellow shoot disease) symptoms in Guangdong, P. R. China. Phytopathology 99:236-242.
Das, A.K., Rao, C.N. & Singh, S. 2007. Presence of citrus greening (huanglongbing) disease and its psyllid vector in the North-Eastern region of India confirmed by PCR technique. Current Science 92(12): 1759-1763.
Davis, R.I. & Tsatsia, H. 2009. A survey for plant diseases caused by viruses and virus-like pathogens in the Solomon Islands. Australasian Plant Pathology 38: 193-201.
Garnier, M., Jagoueix-Eveillard, S., Cronje, P.R., Le Roux, H.F. & Bove, J.M. 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: 2119�2125.
Gottwald, T. R., da Gra�a, J. V., and Bassanezi, R. B. 2007. Citrus Huanglongbing: The pathogen and its impact. Online. Plant Health Progress doi:10.1094/PHP-2007-0906-01-RV.
Jepson, S.B. 2008. Citrus Greening Disease (Huanglongbing). Oregon State University.
Kim, J.S., Sagaram, U.S., Burns, J.K., Li, J.L. & Wang, N. 2009. Response of sweet orange (Citrus sinensis) to �Candidatus Liberibacter asiaticus� infection: Microscopy and microarray analyses. Phytopathology 99:50-57.
Li, W., Levy, L. & Hartung, J. S. 2009. Quantitative distribution of �Candidatus Liberibacter asiaticus� in citrus plants with citrus huanglongbing. Phytopathology 99:139-144.
Li, W., Li, D., Twieg, E., Hartung, J. S., & Levy, L. 2008. Optimized quantification of unculturable Candidatus Liberibacter spp. in host plants using real-time PCR. Plant Disease 92:854-861.
NAPPO. 2008. Confirmation of Huanglongbing or Citrus Greening ( Candidatus Liberibacter asiaticus ) in Louisiana � United States
Qureshi, J.A., Rogers, M.E., Hall, D.G. & Stansly, P.A. 2009. Incidence of invasive Diaphorina citri (Hemiptera: Psyllidae) and its introduced parasitoid Tamarixia radiata (Hymenoptera: Eulophidae) in Florida citrus. Journal of Economic Entomology 102(1): 247-256.
Sechler, A., Schuenzel, E.L., Cooke, P., Donnua, S., Thaveechai, N., Postnikova, E., Stone, A.L., Schneider, W.L., Damsteegt, V.D. & Schaad, N.W. 2009. Cultivation of �Candidatus Liberibacter asiaticus�, �Ca. L. africanus�, and �Ca. L. americanus� associated with huanglongbing. Phytopathology 99:480-486.
Stokstad, E. 2006. New disease endangers Florida�s already-suffering citrus trees. Science 312: 523-524.
Teixeira, D.C., Saillard, C., Eveillard, S., Danet, J.L., Costa, P.I., Ayres, A.J. & Bove, J. 2005. Candidatus Liberibacter americanus, associated with citrus huanglongbing (greening disease) in Sao Paulo State, Brazil. International Journal of Systematic and Evolutionary Microbiology 55: 1857�1862
Trivedi, P., Sagaram, U.S., Kim, J.S., Brlansky, R.H., Rogers, M.E., Stelinski, L.L., Oswalt, C. & Wang, N. 2009. Quantification of viable Candidatus Liberibacter asiaticus in hosts using quantitative PCR with the aid of ethidium monoazide (EMA). European Journal of Plant Pathology, in press.
Contact
The following 3 contacts offer information an advice on Candidatus Liberibacter asiaticus
Barkley,
Pat
Organization:
Technical Advisor,
Citrus Australia Ltd.,
Address:
PO Box 46, MULGOA 2745. NSW Australia.
Phone:
61 2 47 739864
Fax:
61 2 47 739874
Beattie,
Andrew
Dr. Beattie s area of expertise is with integrated control of citrus pests in Australia and Southeast Asia. Has been involved with huanglongbing and ACIAR (Australian Centre for International Agricultural Research) projects in Indonesia and Vietnam since 2000 and more recently a Department of Innovation project in China.
Organization:
University of Western Sydney, Australia,
Address:

Phone:
02 4570 1287
Fax:
02 4570 1314
Qureshi,
Jawwad A
My research focuses on the biology and ecology of the Asian citrus psyllid (ACP), Diaphorina citri and its natural enemies and on the biological and chemical methods of pest control to develop integrated strategies to reduce the incidence of psyllid and huanglongbing or citrus greening disease vectored by the psyllid.
Organization:
Southwest Florida Research and Education Center, Department of Entomology and Nematology, University of Florida
Address:
University of Florida /IFAS, 2686 SR 29N, Immokalee, FL 34142, USA
Phone:
239-658-3451
Fax:
239- 658-3469