Huanglongbing: a destructive, newly-emerging, century-old disease of citrus [Asia; South Africa; Brazil; Florida]

A detailed account is given of the history, aetiology, biology, epidemiology, detection, geographical distribution, and control of huanglongbing (HLB), a destructive disease of citrus that represents a major threat to the world citrus industry, and is slowly invading new citrusgrowing areas. HLB, whose name in Chinese means “yellow dragon disease”, was first reported from southern China in 1919 and is now known to occur in next to 40 different Asian, African, Oceanian, South and North American countries. The agent is a phloem-restricted, non cultured, Gram-negative bacterium causing crippling diseases denoted “greening “ in South Africa, “mottle leaf” in the Philippines, “dieback” in India, “vein phloem degeneration” in Indonesia. The HLB bacterium belongs to the genus Candidatus Liberibacter, three species of which are currently known, Candidatus Liberibacter asiaticus, occurring in Asian countries and, to a lesser extent, in Brazil and the USA (Florida), Candidatus Liberibacter africanus with its subspecies “capensis”, recorded from African countries, and Candidatus Liberibacter americanus present in Brazil. The suggestion is that each liberibacter species has evolved in the continent after which it is named. 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). HLB can be transmitted by grafting from citrus to citrus and by dodder to periwinkle. The psyllids Trioza erytreae and Diaphorina citri are natural vectors. Two different types of HLB are known: the heat-sensitive African form transmitted by T. erytreae, which develops at temperatures of 22-25°C, and the heat-tolerant Asian form, transmitted by D. citri, which stands temperatures well above 30°C. Although the HLB pathogen can be identified by electron microscopy, other laboratory methods are used for routine detection. ELISA with monoclonal antibodies is not recommended. Better systems are dot blot hybridization with a DNA probe, and various PCR formats (one-step, nested, multiplex) using species-specific primers based on 16S rRNA or rplKAJL-rpoBC operon sequences. Because no curative methods of HLB are available, control is preventive and largely based on inoculum elimination by removal of infected trees and chemical treatments against vectors. Strict quarantine measures must be implemented to impair further international spread of HLB agents and their vectors.

[1]  P. Cronjé,et al.  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'. , 2000, International journal of systematic and evolutionary microbiology.

[2]  M. Chen Citrus Likubin Pathogens in Salivary Glands of Diaphorina citri , 1973 .

[3]  Y. Ahlawat,et al.  Detection of the Asian Strains of the Greening BLO by DNA-DNA Hybridization in Indian Orchard Trees and Malaysian Diaphorina citri Psyllids , 1993 .

[4]  A. Hernández Trioza erytreae (Del Guercio 1918): nueva plaga de los cítricos en Canarias , 2003 .

[5]  H. Catling The bionomics of the South African citrus psylla Trioza erytreae (Del Guercio) (Homoptera: Psyllidae). 4. The influence of predators. , 1970 .

[6]  J. Bové,et al.  PCR detection of the two 'Candidatus' Liberobacter species associated with greening disease of citrus. , 1996, Molecular and cellular probes.

[7]  J. Bové,et al.  Influence of temperature on symptoms of California stubborn, South Africa greening, India citrus decline and Philippines leaf mottling diseases. , 1974 .

[8]  J. Bové,et al.  The phloem-limited bacterium of greening disease of citrus is a member of the alpha subdivision of the Proteobacteria. , 1994, International journal of systematic bacteriology.

[9]  X. Y. Zhao Citrus yellow shoot disease (Huanglongbing) in China - a review. , 1982 .

[10]  J. Bové,et al.  Penicillin and tetracycline treatments of greening disease-affected citrus plants in the glasshouse, and the bacterial nature of the procaryote associated with greening [Spiroplasma citri]. , 1980 .

[11]  J. Bové,et al.  Transmission de la bactérie associée à la forme africaine de la maladie du "Greening" par le psylle asiatique Diaphorina citri Kuwayama , 1986 .

[12]  J. Etienne,et al.  Biological Control of Psyllid Vectors of Greening Disease on Reunion Island , 1980 .

[13]  J. Bové,et al.  Transmission of Indian citrus decline by Trioza erytreae (Del Guercio), the vector of South African greening. , 1976 .

[14]  S. Goodison,et al.  16S ribosomal DNA amplification for phylogenetic study , 1991, Journal of bacteriology.

[15]  J. Bové,et al.  Detection of the Asian Huanglongbing (Greening) Liberobacter in Nepal by DNA-DNA Hybridization , 1996 .

[16]  J. Bové,et al.  Production of Monoclonal Antibodies Recognizing Most Asian Strains of the Greening BLO by in Vitro Immunization With an Antigenic Protein Purified From the BLO , 1993 .

[17]  C. Roistacher The Economics of Living with Citrus Diseases: Huanglongbing (Greening) in Thailand , 1996 .

[18]  M. Garnier,et al.  Structure trilamellaire des deux membranes qui entourent les organismes procaryotes associés à la maladie du "greening" des agrumes , 1977 .

[19]  R. D. Tripathi,et al.  Chromium and manganese uptake by Hydrilla verticillata (l.f.) royle : Amelioration of chromium toxicity by manganese! , 1993 .

[20]  J. Fletcher,et al.  Association of a Phloem-Limited Bacterium with Yellow Vine Disease in Cucurbits. , 1998, Plant disease.

[21]  O. Reinking Diseases of Economic Plants in Southern China. , 1919 .

[22]  E. Kitajima,et al.  First Report of a Huanglongbing-Like Disease of Citrus in Sao Paulo State, Brazil and Association of a New Liberibacter Species, "Candidatus Liberibacter americanus", with the Disease. , 2005, Plant disease.

[23]  T. Miyakawa,et al.  Occurrence of Citrus Greening Disease in the Southern Islands of Japan , 1989 .

[24]  L. Korsten,et al.  Huanglongbing (Greening) Detection in South Africa , 1996 .

[25]  K. Schleifer,et al.  Taxonomic notes: a proposal for recording the properties of putative taxa of procaryotes. , 1994, International journal of systematic bacteriology.

[26]  P. C. J. Obergolzer,et al.  Greening Disease of Sweet Orange in South Africa , 1965 .

[27]  J V Graca,et al.  Citrus greening disease. , 1991 .

[28]  J. Bové,et al.  UC Riverside International Organization of Citrus Virologists Conference Proceedings ( 1957-2010 ) Title Distribution of the Huanglongbing ( Greening ) Liberobacter Species in Fifteen African and Asian Countries Permalink , 2007 .

[29]  J. Bové,et al.  Witches' broom disease of lime (WBDL). , 2003 .

[30]  H. Catling The bionomics of the South African citrus psylla, Trioza erytreae (Del Guercio) (Homoptera: Psyllidae) I. The influence of the flushing rhythm of citrus and factors which regulate flushing , 1969 .

[31]  J. Bové,et al.  La lutte contre la maladie du "Greening" des agrumes a l'île de la Réunion. Résultats et perspectives , 1980 .

[32]  L. Korsten,et al.  Presence of " Candidatus Liberibacter africanus" in the Western Cape Province of South Africa , 2000 .

[33]  J. Bové,et al.  Spiroplasma citri and the organism associated with likubin: comparison of their envelope systems. , 1976 .

[34]  Y. Ahlawat,et al.  Detection of Greening BLO by Electron Microscopy, DNA Hybridization in Citrus Leaves with and without Mottle from Various Regions in India , 1993 .

[35]  F. Laigret,et al.  The genome of the non-cultured, bacterial-like organism associated with citrus greening disease contains thenusG-rplKAJL-rpoBC gene cluster and the gene for a bacteriophage type DNA polymerase , 1993, Current Microbiology.

[36]  S. Vautrin,et al.  Association with the Syndrome "Basses Richesses" of Sugar Beet of a Phytoplasma and a Bacterium-Like Organism Transmitted by a Pentastiridius sp. , 2002, Phytopathology.

[37]  D. Singh,et al.  Citrus Dieback in India—the Contribution of Greening Virus , 1968 .

[38]  S. P. Capoor,et al.  Diaphorina citri Kuway., a vector of the greening disease of Citrus in India. , 1967 .

[39]  J. C. Autrey,et al.  Both Huanglongbing (Greening) Liberobacter Species Are Present in Mauritius and Reunion , 1996 .

[40]  Martín,et al.  Electron microscope evidence that citrus psylla {Trioza erytreae) is a vector of greening disease in South Africa , 1973 .

[41]  A. P. D. McClean,et al.  Greening or blotchy-mottle disease of Citrus. , 1970 .

[42]  J. Bové,et al.  Study of the Greening Organism (GO) with Monoclonal Antibodies: Serological Identification, Morphology, Serotypes, and Purification of the GO , 1991 .

[43]  J. Bové,et al.  Diversity of “Candidatus Liberibacter asiaticus,” Based on the omp Gene Sequence , 2005, Applied and Environmental Microbiology.

[44]  J. Bové,et al.  Mycoplasmes dans les agrumes atteints de "Greening", de "Stubborn" ou de maladies similaires , 1970 .

[45]  M. Garnier,et al.  Le greening, une sérieuse menace pour les productions agrumicoles de l'archipel indonésien. Perspectives de lutte , 1985 .

[46]  E. Calavan,et al.  Occurrence of mycoplasmalike bodies in phloem of stubborn-infected citrus seedlings. , 1970 .

[47]  P. Saglio,et al.  Stubborn and Greening: A Review, 1969-1972 , 1974 .

[48]  J. Bové,et al.  Presence of citrus greening disease in Bangladesh and a new method for rapid diagnosis. , 1978 .

[49]  Y. Doi,et al.  Mycoplasma- or PLT Group-like Microorganisms Found in the Phloem Elements of Plants Infected with Mulberry Dwarf, Potato Witches' Broom, Aster Yellows, or Paulownia Witches' Broom , 1967 .

[50]  J. Bové,et al.  Citrus Greening Disease and the Greening Bacterium , 1993 .

[51]  M. Chen Mycoplasmalike Bodies Associated with Likubin-Diseased Ponkan Citrus , 1971 .

[52]  J. M. Wallace,et al.  Citrus leaf-mottle-yellows disease in the Philippines and transmission of the causal virus by a Psyllid, Diaphorina citri. , 1967 .

[53]  Michael J. Davis,et al.  Association of a bacterium and not a phytoplasma with papaya bunchy top disease. , 1996 .

[54]  T. Hung,et al.  Identification of Alternative Hosts of the Fastidious Bacterium Causing Citrus Greening Disease , 2000 .

[55]  J. Bové,et al.  Huanglongbing (Greening) in Vietnam: Detection of Liberobacter asiaticum by DNA-Hybridization with Probe in 2.6 and PCR-Amplification of 16S Ribosomal DNA , 1996 .

[56]  S. Halbert,et al.  ASIAN CITRUS PSYLLIDS (STERNORRHYNCHA: PSYLLIDAE) AND GREENING DISEASE OF CITRUS: A LITERATURE REVIEW AND ASSESSMENT OF RISK IN FLORIDA , 2004 .

[57]  H. Catling Distribution of the Psyllid vectors of Citrus greening disease, with notes on the biology and bionomics of Diaphorina citri. , 1970 .

[58]  L. Korsten,et al.  Citrus Huanglongbing: Review, Present status and Future Strategies , 2004 .

[59]  J. Bové,et al.  Detection and identification of the two Candidatus Liberobacter species associated with citrus huanglongbing by PCR amplification of ribosomal protein genes of the beta operon. , 1999, Molecular and cellular probes.

[60]  M. Garnier,et al.  Citrus Greening disease survey in East and West African countries south of Sahara , 1988 .

[61]  M. Salehi,et al.  Witches’ Broom Disease of Lime (WBDL)in Iran , 2000 .

[62]  J. Bové,et al.  Detection of several strains of the bacterium-like organism of citrus greening disease by DNA probes , 1992, Current Microbiology.

[63]  J. Bové,et al.  Aetiology of citrus greening disease. , 1984, Annales de microbiologie.

[64]  Susan E. Halbert,et al.  DISTRIBUTION OF THE ASIAN CITRUS PSYLLID, DIAPHORINA CITRI KUWAYAMA (RHYNCHOTA: PSYLLIDAE) IN THE CARIBBEAN BASIN , 2004 .

[65]  J. Bové,et al.  Detection and characterization of the African citrus greening Liberobacter by amplification, cloning, and sequencing of the rplKAJL-rpoBC operon , 1995, Current Microbiology.

[66]  C. H. Buitendag,et al.  Living with Citrus Greening in South Africa , 1993 .

[67]  J. Bové,et al.  Citrus huanglongbing in São Paulo State, Brazil: PCR detection of the 'Candidatus' Liberibacter species associated with the disease. , 2005, Molecular and cellular probes.

[68]  P. Oberholzer,et al.  Citrus psylla, a vector of the greening disease of sweet orange. , 1965 .

[69]  J. Bové,et al.  Production and evaluation of non-radioactive probes for the detection of the two 'Candidatus Liberobacter' species associated with citrus huanglongbing (greening). , 1997, Molecular and cellular probes.

[70]  J. Bové,et al.  Effect of Penicillin or Tetracycline Injections of Citrus Trees Affected by Greening Disease Under Field Conditions in Reunion Island , 1980 .

[71]  M. Takita,et al.  First Report of the Causal Agent of Huanglongbing ("Candidatus Liberibacter asiaticus") in Brazil. , 2004, Plant disease.

[72]  R. E. Cortez,et al.  Leaf Mottling—a Serious Virus Disease of Citrus in the Philippines , 1968 .

[73]  J. Bové,et al.  Comparison of the 16S/23S ribosomal intergenic regions of "Candidatus Liberobacter asiaticum" and "Candidatus Liberobacter africanum," the two species associated with citrus huanglongbing (greening) disease. , 1997, International journal of systematic bacteriology.

[74]  J. Bové,et al.  Spiroplasma citri gen. and sp. n.: A Mycoplasma-Like Organism Associated with “Stubborn” Disease of Citrus , 1973 .

[75]  P. Oberholzer,et al.  Greening disease of the sweet orange : evidence that it is caused by a transmissible virus. , 1965 .

[76]  T. Iwanami,et al.  Comparison of 16S rDNA and 16S/23S Intergenic Region Sequences Among Citrus Greening Organisms in Asia. , 2000, Plant disease.

[77]  J. Bové,et al.  The Greening Organism is a Gram Negative Bacterium , 1984 .

[78]  J. Bové,et al.  Transmission of the organism associated with citrus greening disease from sweet orange to periwinkle by dodder , 1983 .

[79]  J. Bové,et al.  Purification of the bacterium-like organism associated with greening disease of citrus by immunoaffinity chromatography and monoclonal antibodies , 1990, Current Microbiology.

[80]  J. Bové,et al.  Huanglongbing in Cambodia, Laos and Myanmar , 2000 .

[81]  J. Bové,et al.  Citrus Greening and Psylla Vectors of the Disease in the Arabian Peninsula , 1984 .

[82]  J. Bové,et al.  Phylogenetic characterization of the bacterium-like organism associated with marginal chlorosis of strawberry and proposition of a Candidatus taxon for the organism, 'Candidatus phlomobacter fragariae'. , 1998, International journal of systematic bacteriology.