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Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease (2010)

Chapter: Appendix K: Huanglongbing Research Milestones (1956–2009)

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Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
×

Appendix K
Huanglongbing Research Milestones (1956–2009)

Year(s)

Milestone

Principal Investigator(s) or Author(s)

Publication/Journal

1956

Infectious nature of huanglongbing disease (HLB) was demonstrated.

Lin Kung Hsiang

Acta Phytopathologica Sinica 2:1-42

1957

This is the only known report on Lin Kung Hsiang’s work to have appeared in the western world soon after the publication of Lin’s work in 1956 (See: Lin, K.H., 1956). Unfortunately, Ciccarone’s report remained essentially unknown too.

Ciccarone

Revista di Agrumicoltura 2: 45-50.

1965

Graft and insect vector (Trioza erytreae) transmissibility of greening was demonstrated.

McClean and Oberholzer

South Africa Journal of Agricultural Science 8:253-276; 297-298

1967

Transmission of HLB by the Asian citrus psyllid (ACP) was demonstrated.

Martinez and Wallace

Plant Disease Reporter 51:692-695

Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
×

Year(s)

Milestone

Principal Investigator(s) or Author(s)

Publication/Journal

1967

With the use of psyllid to transmit the HLB pathogen, it was confirmed that trees with "citrus dieback" symptoms were positive for HLB.

Capoor et al

Indian Journal of Agricultural Sciences 37(6):572-576

1968

Citrus dieback in India is reported to have many similarities with greening disease of South Africa. The similarities with huanglongbing in China could not have been mentioned because Lin’s work on HLB was still not known out of China.

Fraser and Singh

Proceedings of 4th Conference, IOCV:141-144, University of California, Division of Agricultural Sciences, Riverside, CA.

1968

Localized pockets of necrotic phloem were found scattered throughout vascular system of mature leaves in greening-affected sweet orange shoots in South Africa. Leaf mottle associated with HLB are thought to be caused by the reaction to the blockage of the translocation stream.

Schneider

Phytopathology 58:1155-1160

1969

HLB in Africa was found to be heat-sensitive and occurs only in areas below 30-32°C. Trioza erytreae, the African psyllid vector, was also found to thrive only in cool environments.

Catling

Journal of Entomology Society South Africa 32:209-223;

1970

"Mycoplasma-like organism" observed in citrus phloem tissue infected with HLB through electron microscopy.

Laflèche and Bové

Comptes Rendus de L'Academie des Sciences, Paris, 270:1915-1917

1970

These are the first two reports on bacterial structures associated with HLB, a disease until then considered to be caused by a virus. The structures were restricted to the phloem sieve tubes and were thought to be mycoplasmas, i.e bacteria lacking a cell wall. They were observed not only with South Africa greening, but also with Reunion and Indian greening. They were shown only a few months later to be not mycoplasma-like (see Saglio et. al., 1971).

Laflèche and Bové

Fruits 25: 455-465 C.R. Acad. Sci. Paris 270:1915-17

1971

HLB bacterium seen in citrus with "likubin" disease.

Chen et al

Phytopathology 61:598

Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
×

Year(s)

Milestone

Principal Investigator(s) or Author(s)

Publication/Journal

1971

Citrus stubborn disease is also associated with sieve tube-restricted bacterial structures. These structures could be cultured and shown to be mycoplasma-like, surrounded by a 70 A° thick cell envelope, which lacked a cell wall and was composed only of a unit membrane. Compared to the stubborn mycoplasma-like structures, those associated with greening had a 200A° thick envelope and therefore could not be mycoplasma-like. The 200A° envelope was characteristic not only of South African greening, but also of the disease in Reunion, the Philippines, and India.

Saglio et al.

Physiologie Végétale 9: 569-82.

1971

As greening was found to be associated with bacteria, antibiotics, such as tetracyclines, were injected into affected trees in an effort to control the disease.

Schwarz and van Vuuren

Plant Disease Reporter 55: 747-750.

1973

HLB bacterium seen in citrus with "likubin" disease.

Tanaka and Doi

International Citrus Congress, Murcia-Valencia, pp. 352-353

1973

HLB bacterium seen in T. erytreae.

Moll and Martin

Phytophylactica 5:41-44

1973

HLB bacterium seen in D. citri (seen in salivary glands).

Chen et al.

Phytopathology 63(1):194-195

1973

HLB bacterium seen in citrus with "mottle leaf" disease.

Tanaka and Doi

International Citrus Congress, Murcia-Valencia, pp. 352-353

1974

First demonstration under phytotron conditions that African HLB was heat-sensitive (no symptom development at 32°C), while Asian HLB (from India, the Philippines) was heat tolerant (good symptom development at 32°C).

Bové et al.

Proceedings of 6th Conference, IOCV:12-15, University of California, Division of Agricultural Sciences, Riverside, CA.

Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
×

Year(s)

Milestone

Principal Investigator(s) or Author(s)

Publication/Journal

1974

The cell envelope of the organism associated with greening was found to resemble that of a Gram-negative bacterium. However, the presence of peptidoglycan, a characteristic component of the bacterial cell wall, could not be demonstrated.

Moll and Martin

Proceedings of Conference Les Mycoplasmes/Mycoplasmas, INSERM 33: 89-96

1976

The African citrus psyllid vector, Trioza erytreae, is not only vector of the African HLB bacterium, but can also transmit the Asian HLB bacterium.

Massonié, Garnier, and Bové

Proceedings of 7th Conference (1976) IOCV: 18-20, University of California, Division of Agricultural Sciences, Riverside, CA.

1977

Through electron microscopy, the HLB causal organism was shown to possess a cytoplasmic membrane and a bacterial cell wall.

Garnier and Bové

Fruits 32:749-752

1980

Greenhouse-grown HLB-affected citrus plants having absorbed penicillin through the roots grew better, produced more roots and larger symptomless shoots and leaves than untreated controls. In contrast, Penicillin had no effect on Stubborn-affected citrus plants. A beneficial effect was also noted when penicillin was injected into the trunk of field-grown HLB-affected sweet orange trees in Reunion Island. Tetracycline had a beneficial effect on HLB-affected citrus as well as on stubborn-affected citrus. In view of the mode of action of penicillin (inhibits late step in peptidoglycan biosynthesis) and tetracycline (inhibits protein biosynthesis), these results strongly suggested that the bacterium associated with greening contained peptidoglycan, the characteristic component of the bacterial cell wall, indicating that the greening organism is a walled bacterium.

Aubert and Bové; Bové et al.

Proceedings of 8th Conference, (1980) IOCV: 103-108; 91-102 University of California, Division of Agricultural Sciences, Riverside, CA.

Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
×

Year(s)

Milestone

Principal Investigator(s) or Author(s)

Publication/Journal

1980

First successful biological control of Trioza erytreae and Diaphorina citri, the two psyllid vectors of HLB, in Reunion Island.

Etienne and Aubert

Proceedings of 8th Conference, (1980) IOCV: 118-121 University of California, Division of Agricultural Sciences, Riverside, CA.

1983

First transmission of HLB from citrus to periwinkle through dodder. In periwinkle, like in citrus (see: Bové et al., 1974), the Asian HLB bacterium was found to be heat tolerant, while the African HLB bacterium was heat sensitive, showing that the temperature effect was due to the bacterium and not to the host. These observations were the first indications that the two bacteria were biologically different.

Garnier and Bové

Phytopathology 73: 1358-1363

1984

The HLB-associated bacterium was shown to possess a cell wall of the Gram-negative type with an outer cell wall membrane and a peptidoglycan layer, thus establishing the Gram negative nature of the HLB-associated bacterium.

Garnier, Danel and Bové

Annales de l'Institut Pasteur. Microbiologie 135(1): 169-179; Proceedings of 9th Conference, IOCV: 115-124 University of California, Division of Agricultural Sciences, Riverside, CA.

1986

The ACP vector, Diaphorina citri, is not only vector of the Asian HLB bacterium, but can also transmit the African HLB bacterium. Since Trioza erytreae can also transmit the two bacteria (see: Massonié et al., 1976), each psyllid can transmit each one of the two bacteria.

Lallemand, Fos, and Bové

Fruits 41: 341-343

1991

First extensive review on citrus greening disease was published.

Da Graça

Annual Review of Phytopathology 29:109-36

Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
×

Year(s)

Milestone

Principal Investigator(s) or Author(s)

Publication/Journal

1992

By random cloning of total DNA from periwinkle plants affected by Indian HLB, the first genome fragments of the HLB-associated bacterium were obtained: In-2.6, In-1.0, and In-0.6. Sequencing showed In-2.6 to be the nusG-rplKAJL-rpoBC gene cluster (beta operon), and In-1.0 coded for a bacteriophage DNA polymerase. In-2.6, used as a hybridization probe, detected all Asian HLB strains but not the South African strain.

Villechanoux et al.

Current Microbiology 24: 89-95; Current Microbiology 26: 161-166.

1993

Monoclonal antibodies specific for HLB bacteria were produced.

Gao et al.

Proceedings of 12th Conference, (1993) IOCV: 244-249, University of California, Division of Agricultural Sciences, Riverside, CA

1994

On the basis of 16SrDNA sequence analyses, the HLB-associated bacterium was confirmed to be a Gram negative bacterium, belonging to a new genus, Candidatus Liberobacter, in the alpha subdivision of the Proteobacteria. “Candidatus” indicated that the HLB-bacterium was not available in culture. Two liberobacter species were characterized by molecular, biological, and serological methods: Candidatus Liberobacter africanum (CLaf) in Africa and Candidatus Liberobacter asiaticum (CLas) in Asia.

Jagoueix, Bove, and Garnier

International Journal of Systematic Bacteriology 44: 397-86

1993

Transmission of HLB to tobacco by dodder was demonstrated.

Garnier and Bové

Proceedings of 8th Conference, (1993) IOCV: 212-219, University of California, Division of Agricultural Sciences, Riverside, CA

1995

Part of the rplKAJL-rpoBC operon of the African liberobacter was obtained as a 1.7 kb fragment (As-1.7). As-1.7, used as a probe, detected the African HLB strains, but not the Asian strains.

Planet et al.

Current Microbiology 30: 137-141

Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
×

Year(s)

Milestone

Principal Investigator(s) or Author(s)

Publication/Journal

1996

First PCR detection of the Asian and African liberibacters by amplification of 16S rDNA.

Jagoueix, Bove, and Garnier

Molecular and Cellular Probes 10: 43-50.

1996

Already known to harbor both the African and the Asian psyllid vectors of HLB, Reunion and Mauritius islands were also shown to carry both the African and the Asian liberibacters.

Garnier et al.

Proceedings of 13th Conference, IOCV: 392-394, University of California, Division of Agricultural Sciences, Riverside, CA

1997

Confirmation that CLas and CLaf are two different bacterial species based on the 16S/23S rRNA intergenic regions.

Jagoueix et al.

International Journal of Systematic Bacteriology 47(1):224-227

1997

Petroleum spray oil was tested against the ACP in Guangzhou, China; It was found that petroleum oil was as effective as an organophosphate pesticide and an insect growth regulator in controlling psylla nymphs.

Rae et al.

International Journal of Pest Management 43(1):71-75

1999

Random Amplified Polymorphic DNA (RAPD) was used to identify additional genomic sequences of the HLB liberibacters. In particular, the omp (outer membrane protein) gene was obtained.

Hocquellet, Bove, and Garnier

Hocquellet, A., Bové, J.M., and Garnier, M. 1999. Isolation of DNA from the uncultured “Candidatus Liberobacter” species associated with citrus huanglongbing by RAPD.

1999

A PCR detection method based on the amplification of ribosomal protein genes, which allows direct identification of the liberibacter species by the size of the amplified DNA, was developed.

Hocquellet et al.

Molecular and Cellular Probes 13(5):373-379

Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
×

Year(s)

Milestone

Principal Investigator(s) or Author(s)

Publication/Journal

2000

The Asian psyllid vector of HLB, Diaphorina citri, was captured for the first time in southern Iran in 1997 during a mission on Witches' Broom Disease of Lime.

Bové et al.

Proceedings of 14th Conference, IOCV: 207-212 University of California, Division of Agricultural Sciences, Riverside, CA

2000

Following a 1999 proposal in prokaryote nomenclature, “Liberobacter”, “africanum”, and “asiaticum were respectively renamed “Liberibacter”, “africanus”, and “asiaticus”. A new liberibacter was detected in an ornamental rutaceous tree, Calodendron capense, in South Africa. The liberibacter was identified as a subspecies of Ca. L. africanus and named “Ca. L. africanus subsp. Capensis”.

Garnier et al.

International Journal of Systematic and Evolutionary Microbiology 50: 2119-2125.

2000

The HLB causal agent was shown to replicate in Chinese box orange (Severinia buxifolia) and wood apple (Limonia acidissima) but not in common jasmine orange (Murraya paniculata var. paniculata) and curry leaf (Murraya euchrestifolia).

Hung et al.

Journal of Phytopathology-Phytopathologische Zeitschrift 148(6):321-326

2000

This study was conducted to determine the effect of temperature on the biology and life table parameters of the ACP. Findings include the following: 1) Average number of eggs produced per female significantly increased with increasing temperature; maximum number of eggs was produced at 28°C; 2) Population reared at 28°C had the highest intrinsic rate of increased and net reproductive rate and the shortest population doubling time and mean generation time compared with populations reared at 15-25°C; 3) The optimum range of temperature for D. citri population growth was found to be 25-28°C.

Liu and Tsai

Annals of Applied Biology 137(3):201-206

Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
×

Year(s)

Milestone

Principal Investigator(s) or Author(s)

Publication/Journal

2000

The endosymbiotic microbiota of the citrus psyllid was investigated using PCR and RFLP. The whole DNA of D. citri was found to contain sequences that are similar to that of mycetocyte symbionts of other psyllids, Oxalobacter and Herbaspirillum, Arsenophonous spp., Liberobacter spp. and Wolbachia spp.

Subandiyah et al.

Zoological Science 17:983-989

2000

Taylor's power law and Iwao's patchiness regression models indicated that D. citri populations were aggregated.

Tsai et al.

Florida Entomologist 83(4):446-459

2001

The ability of D. citri and its two parasitoids, Tamarixia radiata and Diaphorencyrtus aligarhensis to survive at different relative humidities and temperatures was studied. This study showed that D. citri survived longer than the parasitoids at all conditions tested, indicating a lower net water loss rate.

McFarland and Hoy

Florida Entomologist 84(2): 227-233

2002

Psyllid population levels on orange jasmine were found to be positively related to the availability of new shoot flushes, which were in turn related to the weekly minimum temperature and rainfall. The study indicated that continuous flushes produced by orange jasmine could play an important role in maintaining high populations of psyllids when new shoot flushes are not available in citrus groves.

Tsai et al.

Florida Entomologist 85(3):446-451

2004

First report of CLas associated with HLB in Brazil.

Colleta-Filho et al.

Plant Disease 88:1382.

2004

Using PCR, it was determined that Liberibacter asiaticus persists in the Asian citrus psyllid vector but it is not transovarially transmitted.

Hung et al.

Plant Pathology 53(1):96-102

Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
×

Year(s)

Milestone

Principal Investigator(s) or Author(s)

Publication/Journal

2004

Results from a laboratory and spray booth study indicated that nymphal and adult D. citri and a mite complex can be controlled by high concentrations of sucrose octanoate, a synthetic analog of natural sugar esters found in leaf trichomes of wild tobacco (Nicotiana gossei Domin).

McKenzie and Puterka

Journal of Economic Entomology 97(3):970-975

2004

Coccinellid beetles were found to be the most important biological control agents of high-density populations in central Florida and that intraguild predation causes >95% mortality of immature stages of Tamarixia radiata.

Michaud

Biological Control 29(2):260-269

2004

A rearing method was developed for ACP and its parasitoids, Tamarixia radiata and Diaphorencyrtus aligerhensis.

Skelley and Hoy

Biological Control 29(1):14-23

2005

Omp (outer membrane protein gene)-based PCR-RFLP analysis was shown to be a simple method for detecting and differentiating CLas isolates. The phylogeny tree based on the omp gene sequences of the African and Asian liberibacters was very similar to the tree based on the 16S rDNA sequences.

Bastianel et al.

Applied Environmental Microbiology 71:6473-6478.

2005

Murraya paniculata, the preferred host of the Asian HLB psyllid vector, was also found to be a host of the two HLB bacteria present in São Paulo State, CLam and CLas.

Lopes, Martins, and Frare

Summa Phytopathologica 31: 48-49.; Fitopatologia Brasileira 31: 303.

2005

Discovery and first report of a new liberibacter species associated with HLB in São Paulo State, Brazil: Candidatus Liberibacter americanus. The new liberibacter was also detected in Diaphorina citri, suggesting that the Asian psyllid vector in Brazil was transmitting not only CLas, but also CLam.

Texeira et al.

Plant Disease 89: 107; International Journal of Systematic and Evolutionary Microbiology 55: 1857-1862; Proceedings of 16th Conference, IOCV: 325-340 University of California, Division of Agricultural Sciences, Riverside, CA

Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
×

Year(s)

Milestone

Principal Investigator(s) or Author(s)

Publication/Journal

2005

Development of PCR techniques for the detection of CLam and CLas in citrus and psyllids.

Texeira et al.

Molecular and Cellular Probes, 19; 173-179; Proceedings of 16th Conference, IOCV: 432-438 University of California, Division of Agricultural Sciences, Riverside, CA

2005; 2007

CLas was detected in Wampee (Clausena lansium Skeels) using nested PCR.

Ding et al.; Deng et al.

Journal of Plant Pathology 87(3):207-212; Plant Health Progress 2007

2005

Detection of HLB pathogen through loop-mediated isothermal amplification (LAMP) was demonstrated; The LAMP method, which does not use a thermocycler and electrophoresis apparatus, is deemed useful for under-equipped laboratories.

Okuda et al.

Plant Disease 89(7):705-711

2005

Coccinellid species found to have potential important role as predators of the psyllid in Puerto Rico.

Pluke et al.

Florida Entomologist 88(2):123-128

2005

Third bacterial species was detected and identified as another causal organism of HLB in Brazil. The name Ca. Liberibacter americanus was proposed for this HLB pathogen. Detection of CLam in D. citri indicated that this is also the vector for this liberibacter species.

Teixeira et al.

Molecular and Cellular Probes 19(3):173-179; International Journal of Systematic and Evolutionary Microbiology 551857-1862 Part 5

2005

In greenhouse trials, a neem-based biopesticide containing 4.5% azadirachtin was found to reduce psyllid nymph populations; however, no mortality was observed in psyllid adults that were exposed to 11-180 ppm azadirachtin.

Weathersbee and McKenzie

Florida Entomologist 88(4):401-407

2006

Guava intercropping was observed to reduce ACP/HLB incidence in Vietnam

Beattie et al.

Unpublished

Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
×

Year(s)

Milestone

Principal Investigator(s) or Author(s)

Publication/Journal

2006

The first extensive review on HLB following arrival of the disease in America was published.

Bové

Journal of Plant Pathology 88: 7-37.

2006

TaqMan real-time PCR using 16S rDNA-based TaqMan primerprobe sets specific to the different Ca. L. spp. was developed. Used successfully in the confirmation of HLB caused by Ca. L. asiaticus in FL.

Li et al.

Journal of Microbiological Methods 66(1):104-115

2006

Conventional PCR and two real-time PCR (RTi-PCR) methods were developed and compared according to their sensitivity and specificity for detecting CLas. The SYBR Green I (SGI) RTi-PCR was found to be most sensitive; the TaqMan RTi-PCR assay was rapid and had the greatest specificity. Mottled leaves yielded highest positive rate, indicating that leaf mottling was the most reliable symptom for field surveys.

Wang et al.

Plant Pathology 55(5):630-638

2006

First demonstration that Diaphorina citri transmits CLam in São Paulo State, Brazil.

Yamamoto et al.

Page 96 in: Proceedings of the Huanglongbing Greening International Workshop, Ribeirão Preto, SP, Brazil.

2007

This study showed that maximum and minimum temperatures are more important than mean temperature in determining winter survival of D. citri; D. citri will be able to survive winter in areas with mean daily minimum and maximum temperatures of 5° and 12.5 °C.

Ashihara

Japanese Journal of Applied Entomology and Zoology 51(4): 281-287

2007

Polymorphic microsatellite markers were developed from microsatellite-enriched DNA libraries and mined from an expressed sequence tags library of D. citri. Microsatellite loci can provide means for assessing overall genetic variation and migration patterns for D. citri.

Boykin et al.

Molecular Ecology Notes 71202-1204

Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
×

Year(s)

Milestone

Principal Investigator(s) or Author(s)

Publication/Journal

2007

It was found that yellow sticky card traps and blue sticky card traps were equally effective in detecting the presence of D. citri adults in trees while CC traps (red, blue, black, white, yellow, and dark green bases) and multi-lure traps captured few adults and provided poor detection of adult psyllids. Tap sampling was found to be an easy way to conduct and provided relatively good detection of trees infested by adults, based on the level of infestation in the two groves that were sampled in this study. Stem tap sampling provides information on the presence and relative abundance of adult D. citri in one visit to a block of trees while sticky trap sampling requires two visits.

Hall et al.

Florida Entomologist 90(2):327-334

2007

A sampling procedure was devised to estimate flush abundance. It was found, based on Taylor's power law coefficients, that over all sample weeks, flush shoots were randomly distributed within the young grapefruit trees and only weakly aggregated within the block of mature orange trees. Projections indicated that a sampling plan of 40 trees (one sample per tree) would provide density estimates that are acceptable enough for general estimates at mean densities of one or more shoots per sample.

Hall and Albrigo

HortScience 42(2):364-368

2007

It was found that 1) a 3% (wt:vol) suspension of kaolin-based hydrophilic particle film (Surround WP) in water was not acutely toxic to eggs, older nymphs or adults, 2) presence of dried particle on leaves hampered the ability of adults to grasp and walk on citrus leaves, 3) numbers of eggs and nymphs per flush shoot were reduced by 85% and 78%, respectively, in trees treated with particle film. However, the suppressive effects of Surround treatment were degraded by rain.

Hall et al.

Journal of Economic Entomology 100(3):847-854

Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
×

Year(s)

Milestone

Principal Investigator(s) or Author(s)

Publication/Journal

2007

TaqMan real-time PCR was found to be 10 to 100-fold more sensitive than conventional PCR and LAMP; It can be used as a tool for early detection of HLB and identification of CLas before symptom development.

Li et al.

Plant Disease 91(1):51-58

2007

Removing HLB-affected branches from symptomatic trees (“pruning”), in an effort to decrease the sources of HLB inoculum, has been found ineffective in São Paulo State to control HLB and should not replace removal of the whole trees.

Lopes et al.

European Journal of Plant Pathology 119: 463-468.

2007

This study determined the duration and viability of the egg and nymphal stages, sex ratio, fecundity, and longevity of D. citri on three hosts (orange jasmine, Rangpur lime, and Sunki mandarin). D. citri lower temperature threshold and thermal constant values for the egg, nymphal, and biological cycle were determined.

Nava et al.

Journal of Applied Entomology 13(1):709-715

2007

The reproductive biology and behavior of D. citri was studied; Emergence patterns of males and females were found to be similar, with no evidence for protandry or protogyny. Both males and females reached reproductive maturity by 2-3 days post eclosion. Oviposition generally began within 1 day after mating, but was longer when females mated at 2d of age. Mating on orange jasmine was observed almost exclusively on flush shoots during daylight hours, with no obvious peak of daily mating activity. Mating activity may be constrained during scotophase partly due to cooler temperatures and lack of light.

Wenninger and Hall

Florida Entomologist 90(4):715-722

2007

First report of dodder transmission of HLB from naturally infected Murraya paniculata to citrus.

Zhou et al.

FCPRAC; Plant Disease 91(2):227-227

Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
×

Year(s)

Milestone

Principal Investigator(s) or Author(s)

Publication/Journal

2008

First study of transcriptional profiling in citrus in response to liberibacter infection using microarray technology. Results indicate that gene expression changes involved a variety of different processes including cell defense, transport, cellular organization, photosynthesis, and carbon metabolism. Pathogen-induced accumulation of transcripts for phloem-specific lectin PP2-like protein was noted.

Albretch and Bowman

Plant Science 175(3):291-306

2008

Factors involved in HLB management in 20 citrus farms in São Paulo State over a period of four years (2004 to 2008) have been identified and explain success or failure of HLB control.

Belasque et al.

International Research Conference, Huanglongbing, Dec. 1-5 , Orlando, FL

2008

It was determined that the HLB bacterium may be translocated into the external parts of the embryo during seed development but this infection typically disappears during early growth and thus unlikely to result in seedlings that have HLB disease symptoms or that can serve as sources of inoculum.

Bowman

Manuscript submitted for publication; FCPRAC Annual Report 2008

2008

Transformation of citrus with AMP (antimicrobial peptide) D4E1 (synthetic derivative of cecropin) and the garlic leaf lectin, ASAL, was carried out. Transformation is complete and transformants with the AMP are now being grown in the greenhouse for testing against HLB and canker.

Bowman

FCPRAC Annual Report 2008

2008

Laboratory trials showed that Silwet L-77 and Kinetic (organosilicone adjuvants) alone and petroleum oil and copper hydroxide alone, or in combination with the adjuvants, had low residual and acute toxicity to T. radiata (parasitoid of D. citri) and appear to be compatible with biocontrol using T. radiata.

Cocco and Hoy

Florida Entomologist 91(4):610-620

2008

On the basis of PCR data, co-cultivation of CLas with Actinobacteria was reported. No pure cultures of liberibacters could be obtained.

Davis et al.

Plant Disease 92: 1547-1550

Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
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Principal Investigator(s) or Author(s)

Publication/Journal

2008

A transient-expression vector based on Citrus tristeza virus (CTV) that provides systemic expression of foreign genes in citrus was built. The CTV-based vector is being developed as an interim measure to protect citrus trees. It has continually expressed foreign genes in citrus for six years so far. 27 of 30 citrus trees that have been infected with the vector for 4-6 years still contain the intact foreign gene. Based on this observation, it is believed that a very high percentage of the trees would retain the peptide for ten years or more.

Dawson

FCPRAC Annual Report 2008

2008

It was determined that the non-tRNA gene regions of the 16S-23S ITS and the 23S-5S rRNA ITS of CLas did not share any similarity to any known non-Liberibacter DNA sequences and could be used for the specific and efficient detection of CLas.

Deng et al.

Molecular and Cellular Probes 22(5-6):338-340

2008

Differences in the microbial community composition of HLBinfected and recovered plants and Las-infected and non-infected psyllids were detected with the use of 16S rDNA-based molecular techniques and traditional culturing methods. Species of bacteria that support the multiplication of Las bacterium on agar media plates were tentatively identified as Aerations altamirensis, Phycibacter jejuensis and Agrococcus versicolor based on their 16S r DNA analyses. RFLP and library-based assays of the partial RNA operon (~3.3kb) of Las bacteria indicated the genetic diversity in the Las bacteria that are present in plants that displayed different disease phenotypes. Subsequent sequence analysis indicated that all these variations belonged to single nucleotide polymorphisms (SNPs) and the SNPs varied from population to population.

Duan

FCPRAC Annual Report 2008

2008

Transmission of HLB from citrus to tomato plants via dodder was confirmed.

Gabriel and Duan

FCPRAC Annual Report 2008

Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
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Principal Investigator(s) or Author(s)

Publication/Journal

2008

More than 265 transgenic plants from independent transformation events with six different anti-bacterial constructs were regenerated, including many sweet orange and grapefruit, several with a phloemlimited promoter. All are being micro-grafted for subsequent HLB challenge. The first transgenic grapefruit plants containing the LIMA construct, challenged (greenhouse) with HLB over a year ago, remain RT-PCR negative with no symptoms, while the grafted HLB inoculum budsticks remain RT-PCR positive; this encouraging result suggests that LIMA may provide resistance or at least substantially delay disease.

Gmitter

FCPRAC Annual Report 2008

2008

Development of promoters that will prevent expression of foreign genes in fruit; demonstrated the feasibility of engineering zinc finger-based proteins to regulate the expression (up to 77% inhibition) of genes used currently to produce antibacterial proteins.

Gurley

FCPRAC Annual Report 2008

2008

It was found that in Florida, D. citri was most consistently present and more abundant at the study sites in the months of May, June, and July. Results of this study also indicate that large infestations could occur anytime of the year depending on environmental conditions and flush availability.

Hall et al.

Environmental Entomology 37(4):914-924

2008

The latency period of Liberibacter in adult D. citri was determined to be 8-16 weeks

Hall

FCPRAC Annual Report 2008

Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
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Milestone

Principal Investigator(s) or Author(s)

Publication/Journal

2008

Experiments with Diaphorencyrtus aligarhensis (parasitoid of ACP) imported from China showed that this strain is ideally suited for mass rearing and release into Florida as a biological control agent. Choice and no choice tests indicated that this parasitoid will parasitize 2nd thru 4th instar nymphs only and will host feed on 1st thru 4th instars of immature psyllids. Y-tube experiments show the parasitoids are not attracted to various uninfested host plants but are attracted to ACP-infested plants, psyllid nymphs and honeydew/wax waste products from nymphal feeding.

Hall

FCPRAC Annual Report 2008

2008

First description of a non-citrus liberibacter transmitted by the tomato/potato psyllid, Bactericera cockerelli. The new liberibacter has no association with HLB.

Hansen et al.

Applied and Environmental Microbiology 74: 5862-5865.

2008

Two PCR primer sets (16S and a pair of 10F, 489R) were chosen to detect novel endosymbiont bacterial 16s rDNA sequences within the ACP. Sequence homology results found 40 of the 47 were 100% homologous to a Syncytium endosymbiont of D. citri (accession number EF433792) and seven were 100% homologous to Wolbachia of D. citri (accession number EF433793). The 2.5 kb of PCR product with 10F, 489R primer pairs contained six major types of sequences. These methods identified the presence of eight different bacterial homologs: Carbazole degrading bacterium, Janthinobacterium sp. IC161, an ammonia-oxidizing bacterium, Nitrosospira multiformis ATCC25196, known as a biodegradation bacterium, Acinetobacter sp. and an alkane degrading bacterium, Alkanindiges. These data provide evidence that Asian citrus psyllids are supported by a rich bacterial fauna of many endosymbiotic and gut fauna bacteria of various types, all of which have important interactions between each other and may interact with CLas when it occurs in psyllids.

Hunter

FCPRAC Annual Report 2008

Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
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Principal Investigator(s) or Author(s)

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2008

This study that evaluated nine different commercially available media for their suitability to culture psyllid cells. The most efficient medium determined so far is the SF900-III-supplemented. It was found that a combination of this media plus 10% Fetal bovine serum can support psyllid cells for over three months.

Hunter

FCPRAC Annual Report 2008

2008

Primary cell lines successfully established using D. citri embryos.

Keyhani

FCPRAC Annual Report 2008

2008

This study showed that standard curve established with DNA extracted from naturally-infected field-grown plants was more accurate than the standard curve constructed from plasmids containing the amplification targets as cloned inserts. A universal standard curve was established for the quantification of the pathogen in various citrus tissues of different citrus species planted in different geographic locations.

Li et al.

Plant Disease 92(6):854-861

2008

330 symptomatic and symptomless leaf samples were collected from HLB orchards in Guangdong, Guangxi, Fujian, Jiangxi, Zhejiang, Hunan, Yuannan and Guizhou provinces of China. While Ca. L. asiaticus was detected in 96 samples, Ca. L. americanus was found in only one sample, a sample from Hunan. If this result is confirmed, it will be the first time that Ca. L. americanus has been detected out of Brazil. Also, so far the American liberibacter as well as the Asian liberibacter have never been detected in Africa.

Lou et al.

Program and Abstracts book, 11th International Citrus Congress, p. 232, abstract P333.

2008

Morphological and genetic data was found to support the identification of the fungus that killed adult D. citri in a FL citrus grove in 2005 as Isaria fumosorosea (=Paecilomyces fumoroseus). Completion of Koch's Postulates established the pathogenicity of the fungus to D. citri.

Meyer et al.

Journal of Invertebrate Pathology 99(1):96-102

Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
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Milestone

Principal Investigator(s) or Author(s)

Publication/Journal

2008

Micronized fluorescent powder found to be effective for marking ACP; does not affect survival and can be used for ca. 5 weeks in the field.

Nakata

Applied Entomology and Zoology 43 (1):33-36

2008

The external morphology of the antennal sensilla of male and female psyllids were examined using scanning electron microscopy and the putative functions of the identified sensilla were determined using transmission electron microscopy techniques.

Onagbola et al.

Micron 39(8):1184-1191

2008

Aldicarb application (5.6 kg/ha) to the bed side of mature citrus trees 2-3 months before spring growth can suppress ACP through spring without direct effects on principal psyllid natural enemies. This practice is now widely adopted by the industry.

Qureshi and Stansly

Pest Management Science 64(11):1159-1169; FCPRAC Annual Report 2008

2008

A volatile (dimethyl disulfide or DMDS) was discovered for the first time from guava leaves. DMDS is known to have potent repellency and insecticidal properties against other insects.

Rouseff et al.

FCPRAC Annual Report 2008; Journal of Agricultural and Food Chemistry 56(19):8905-8910

2008

A study performed in 34 grapefruit and 6 sweet orange orchards from March to August in Southern Texas showed that densities of D. citri eggs, nymphs and adults were significantly higher in sweet orange than in grapefruit and that the number of D. citri immatures were significantly

higher in the southern quadrant of the trees. The spatial distribution pattern was analyzed using Iowa's patchiness regression and Taylor's power law models. According to projections, a sampling plan consisting of 10 trees and 8 flush shoots per tree would provide acceptable density estimates of the three developmental stages of D. citri that can be used for population studies and for making management decisions.

Setamou et al.

Journal of Economic Entomology 101(4):1478-1487

Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
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Principal Investigator(s) or Author(s)

Publication/Journal

2008

Lab and field trials demonstrated that an organosilicone adjuvant (Silwet L-77 or Kinetic) added to one-fourth or one-half the lowest label rate for imidacloprid killed as many eggs, nymphs as the lowest label rate of imidacloprid but did not control adults as well as the lowest label rate.

Srinivasan et al.

Florida Entomologist 91 (1) 87-100

2008

This study demonstrated that aerial applications of broad-spectrum insecticides such as Imidan® (Phosmet) provided satisfactory control but that more selective insecticides such as Provado® (imidacloprid) and Delegate® (spinetoram) require better coverage obtained from ground applications. Resulting recommendations have been adopted by citrus and agrochemical industries.

Stansly and Qureshi

FCPRAC Annual Report 2008

2008

This study provided 1) direct proof that unmanaged citrus groves serve as reservoirs of psyllids that infest nearby commercial groves; and 2) direct proof of rapid short range psyllid movement which suggests that lack of control in a nearby grove can lead to rapid reinfestation in intensely-managed groves.

Stelinski

Unpublished; FCPRAC Annual Report 2008

2008

CLas was found to be distributed in bark tissue, leaf midrib, roots, and different floral and fruit parts, but not in the endosperm and embryo of infected fruits. HLB pathogen was found to be unevenly distributed in planta, with a relatively high concentration in fruit peduncles.

Tatineni et al.

Phytopathology 98(5):592-599

2008

The tufB-secE-nusG-rplKAJL-rpoB gene cluster of CLas could be obtained and sequenced, and compared to the gene cluster of CLaf and CLas. These comparisons confirmed that CLam represented a distinct liberibacter species. Liberibacter speciation dating was also evaluated. The time of divergence between CLaf and CLas was estimated at 147 million years (Myr) and the splitting between CLam and the asiaticus/africanus branch would have occurred 309 Myr ago.

Teixeira et al.

International Journal of Systematic and Evolutionary Microbiology. 58: 1414-1421.

Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
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Principal Investigator(s) or Author(s)

Publication/Journal

2008

Occurrence of CLam was examined in 822 leaf samples from a single HLB- affected sweet orange tree by two conventional PCR techniques and a newly developed real time (RTi) PCR, also used for quantification of the liberibacter in the leaves. Even though RTi-PCR detected as few as 10 liberibacters per gram of leaf tissue (l/g), no liberibacters could be detected in any of the many leaf samples from a symptomless branch, while in blotchy mottle leaves from symptomatic branches of the same tree, the liberibacter titer reached values as high as 107 l/g. Nested PCR was almost as sensitive as RTi-PCR.

Teixeira et al.

Molecular and Cellular Probes 22: 139-150.

2008

PCR and RTi-PCR were used to detect/quantify CLam in citrus; the study showed that the pathogen was unevenly distributed in HLB infected citrus trees.

Teixeira et al.

Molecular and Cellular Probes 22(3):139-150

2008

A phytoplasma of group IX is associated with citrus HLB symptoms in São Paulo State, Brazil.

Teixeira et al.

Phytopathology 98(9):977-984

2008

Sweet orange trees showing characteristic leaf and fruit symptoms of HLB in São Paulo State, but testing negative for all known liberibacters, were found to be infected with a phytoplasma of group 16Sr IX, closely related to the Pigeon pea witches’ broom phytoplasma. The phytoplasma could be detected easily in citrus by PCR using universal or specific primers. The HLB-associated phytoplasma could also be detected in Crotalaria junceae plants (grown in between rows of citrus trees for improvement of soil conditions) and showing typical witches’ (Wulff et al., unpublished). The insect vector transmitting the phytoplasma to citrus trees, probably from the infected Crotalaria plants, has not yet been identified.

Teixeira et al.

Phytopathology 98: 977-984.

Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
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Year(s)

Milestone

Principal Investigator(s) or Author(s)

Publication/Journal

2008

Isothermal and chimeric primer-initiated amplification of nucleic acids combined with cycling probe technology (cycleave ICAN) was found to shorten the time for large-scale detection of HLB.

Urasaki et al.

Journal of General Plant Pathology 74(2):151-155

2008

Behavioral evidence was found for a female-produced volatile sex attractant pheromone in D. citri.

Wenninger et al.

FCPRAC; Entomologia Experimentalis et Applicata 128 (3):450-459

2008

It was demonstrated that D. citri females require multiple matings over time to achieve high reproductive output, but oviposition is constrained by the presence of males.

Wenninger and Hall

Physiological Entomology 33(4):316-321

2009

Laboratory trials showed the effect of temperature on the toxicity of selected organophosphates, carbamate, avermectin, pyrethroid, and neonicotinoid insecticides against adult D. citri. Data collected can be used when selecting insecticides depending on the prevailing environmental temperature.

Boina et al.

Journal of Economic Entomology 102 (2):685-691

2009

Updated review on HLB at the web site of IOCV (International Organization of Citrus Virologists) with 152 color illustrations on most aspects of HLB.

Bové

Bové, J.M. 2009. Citrus Diseases, Huanglongbing, Text and Image Gallery. http://www.ivia.es/iocv

2009

A phytoplasma related to Ca. Phytoplasma asteri was detected in citrus showing HLB symptoms in Guangdong, China.

Chen et al.

Phytopathology 99(3):236-242

2009

A complete circular genome has been obtained by metagenomics, using the DNA extracted from a single CLas-infected psyllid. The 1.23 Mb genome has an average 36.5% GC content. Many characteristics derived from the annotation are reported. The authors indicate that this is the first genome sequence of an uncultured α-proteobacterium that is both an intracellular plant pathogen and insect symbiont.

Duan et al.

Molecular Plant-Microbe Interactions 22: 1011-1020.

Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
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Principal Investigator(s) or Author(s)

Publication/Journal

2009

First report of HLB in the southern and southwestern parts of Iran. The Asian psyllid vector was detected in the area in 1997 (see Bové et al., 2000).

Faghihi et al.

Plant Pathology 58: 793.

2009

Microarray analysis indicated that HLB infection significantly affected the expression of 624 genes whose encoded proteins fell into the following categories: sugar metabolism, plant defense, phytohormone, cell wall metabolism and 14 other categories. Anatomical examination indicated that HLB bacterium infection caused phloem disruption, sucrose accumulation, and plugged sieve pores. It was determined that HLB-associated blockage resulted from plugged sieve pores and not due to HLB bacterial aggregates since CLas does not form aggregates in citrus.

Kim et al.

Phytopathology 99(1):50-57

2009

Systematic quantification of the distribution of CLas genomes in tissues of six citrus species using a quantitative polymerase chain reaction assay was performed. The study showed the ubiquitous presence of CLas in symptomatic citrus trees and the variation in distribution between individual trees and among samples of different tissues from the same trees.

Li et al.

Phytopathology 99(2):139-144

Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
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Publication/Journal

2009

While the new liberibacter described by Hansen et al.; see Hansen et al., 2008) as Candidatus Liberibacter psyllaurus was characterized from the tomato/potato psyllid, Bactericera cockerelli, the liberibacter described by Liefting et al. (2009a, b) as Candidatus Liberibacter solanacearum was characterized from tomato and other solanaceous plants. The two liberibacters represent one and the same organism: Ca. L. psyllaurus refers to the agent in the psyllid vector, Ca. L. solanacearum refers to the agent in plants. It is the agent associated with potato Zebra chip disease (PZCD) and the PZCD psyllid vector. It has been shown that the citrus liberibacter, CLas, can experimentally infect, and induce disease in at least two solanaceous plants: tobacco (Garnier and Bové, 1993) and tomato (Duan et al., 2008). It might be expected that, similarly, Ca. L. solanacearum will be shown to infect, and induce symptoms in citrus.

Liefting et al.; Lin et al.

Plant Disease 93: 208-214; International Journal of Systematic and Evolutionary Microbiology 59: 2274-2276; Journal of Plant Pathology 91: 215-219.

2009

Percentages of transmission by graft inoculation were from 54.7 to 88.0% for Ca. L. asiaticus and 10.0 to 45.2% for Ca. L. americanus. Average bacterial titers in field trees were 6.67 log cells per gram of leaf midrib for CLas and 5.74 for CLam. The titer of CLas in field trees being higher than that of CLam, transmission of the former by the psyllid vector might be more efficient than that of the latter and explain why newly infected trees are more frequently infected with CLas than with CLam.

Lopes et al.

Phytopathology 99: 301-306.

2009

While CLas, not yet affected at 35°C, was confirmed to be heat tolerant, CLam, affected at 32°C, was found to be heat sensitive. Thus two of the citrus liberibacters are heat sensitive: CLaf and CLam.

Lopes et al.

Plant Disease 93: 257-262.

Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
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2009

Phylochip analysis indicated that 47 orders of bacteria in 15 phyla were present in citus leaf midribs while cloning and sequencing indicated 20 orders of bacteria in 8 phyla. Phylochip arrays indicated that nine taxa were significantly more abundant in symptomatic midribs than in asymptomatic midribs.

Sagaram et al.

Applied and Environmental Microbiology 75(6):1566-1574

2009

CLam found to be less heat tolerant than CLas.

Lopes et al.

Plant Disease 93(3):257-262

2009

Cultivation of all three citrus liberibacter species has been reported. Confirmation in several laboratories is attempted.

Sechler et al.

Phytopathology 99:480-486.

2009

This study provides evidence that D. citri uses olfactory and visual cues in orientation to host plants which indicates the possibility of using plant volatiles to monitor and manage ACP.

Wenninger et al.

FCPRAC Annual Report 2008; Environmental Entomology 38(1):225-234

2009

Vibrational communication between male and female psyllids was studied. Findings include: 1) both sexes produced simple, low amplitude vibrational signals at multiples of 17-250 Hz, ranging in duration from 140 to 700 ms; 2) vibrational frequency in males were significantly negatively correlated with mass; 3) latent period for initialization of calling was significantly shorter for males exposed to clean air, suggesting that in the absence of olfactory cues, psyllids might be more inclined to use acoustic signals to communicate with conspecifics.

Wenninger et al.

Annals of the Entomological Society of America 102(3):547-555

2009

The size of the CLam genome was determined by pulse field gel electrophoresis, using Lam-infected periwinkle plants for bacterial enrichment. The genome size was found to be ~1.31 Mbp, a value close to 1.23 Mbp as found by Duan et al., 2009. The data also suggest the genome to be circular and to contain three ribosomal operons.

Wulff et al.

International Journal of Systematic and Evolutionary Microbiology 59: 1984-1991.

Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
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2009

Two field trials have been established in Florida to evaluate the resistance of transgenic citrus to citrus canker and citrus greening. The transgenic citrus tested carry the following genes: 1) gene encoding for a plant-based anti-microbial peptide and 2) a proprietary gene with the trademark “Disease Block”. No field resistance data have been generated as of December 2009 but preliminary laboratory data for the transgenic citrus in both trials indicate efficacy against citrus greening.

M. Irey

http://www.aphis.usda.gov/biotechnology/status.shtml

http://www.isb.vt.edu/cfdocs/fieldtests1.cfm

FCPRAC 2009 Progress Reports

2009

Results from this study indicate that D. citri which complete their development on CLas(+) plants are more likely to acquire the pathogen compared to those individuals that feed on Las(+) plants as adults only. Therefore, the presence of CLas(+) trees on which psyllids can complete development is an important factor in the overall spread of HLB within a grove. Results from preliminary tests suggest that there appears to be some seasonality to the abundance of Las positive psyllids with one period of increase occurring in the late fall/early winter and a second smaller peak occurring in the spring.

Brlansky

FCPRAC Progress Report (January, 2009)

2009

Results from this study provided (further) evidence that distribution of the greening-associated pathogen varies widely within symptomatic, PCR-positive citrus trees and thus illustrates the importance of obtaining multiple samples from trees where an infection is suspected. Using real-time PCR, it was determined that 80% of stumps had one or more sprouts that were CLas positive. This work confirms the importance of controlling sprouts from citrus stumps in order to minimize the spread of HLB within and between citrus groves.

Brlansky and Davis

FCPRAC Progress Report (January, 2009); Proceeding of the International Research Conference on Huanglongbing. Orlando, FL

Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
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2009

The response of 32 different citrus varieties or relatives to HLB was studied. The effect of HLB on the plants was differentiated most dramatically by the rate of continuing growth. Although some trees developed distinctive symptoms on leaves, growth was inhibited only marginally, while with other trees when leaves became chlorotic, growth ceased. Sweet orange, grapefruit, tangelo, and some mandarins were extremely sensitive. Preliminary results in terms of most severe symptoms and reduced growth are: Valencia > Hamlin > Rhode Red Valencia > Pineapple for sweet orange; for grapefruit Duncan = Marsh > Rio Red.

Dawson

FCPRAC Progress Report (January, 2009)

See also Folimonova, S.Y., Robertson, C.J., Garnsey, S.M., Gowda, S., and Dawson, W.O. 2009. Examination of the responses of different genotypes of citrus to huanglongbing (citrus greening) under different conditions. Phytopathology 99(12):1346-1354

2009

DNA from highly infected citrus was sequenced. To date, we have 55 million bases from a 454 run with an average read length of 235 bases. We also have 255 million bases from a Solexa sequencer at Oregon State University. An additional 8 billion bases should be available within 2 weeks from a SOLiD sequencer at UF. All of these data will be assembled with expertise from the University of Florida and Oregon State University. Several assembly programs are being tested for this purpose. These data are expected to provide a significant amount of citrus genome data as well as the citrus greening genome. We are attempting to use these data to fill gaps in the sequencing results of other groups.

Dawson

FCPRAC Progress Report (January, 2009)

2009

Development and validation of a novel and efficient adaptor-based genomic subtractive enrichment protocol, which enables the nearly complete removal of host DNA and maximizes the likelihood of cloning only bacterial sequences from the extremely low titer of the bacterium present in infected tissues.

Gmitter

FCPRAC Progress Report (January, 2009)

Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
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2009

The first transgenic grapefruit plants containing the LIMA construct were inoculated with HLB 18 months ago and remain RT-PCR negative with no symptoms, while the grafted HLB inoculum budsticks remain RT-PCR positive; this result suggests that LIMA may provide resistance or at least substantially delay disease. Citrus genes involved in systemic acquired resistance (SAR) have been identified and cloned, and several have already been engineered into transgenic plants, and are being tested against HLB and canker.

Gmitter

FCPRAC Progress Report (January, 2009)

2009

A sweet orange genome "re-sequencing project", using next-gen sequencing (454 of Roche Diagnostics) was initiated and is underway. This project is in concert with the ICGC sequencing initiative plans to use next-generation sequencing technologies on several diploid genomes, as an added resource to the Sanger haploid sequencing project conducted in parallel. Sequence reads already available have been aligned to 23 previously sequenced BAC clones, revealing excellent agreement between the previous Sanger sequence and the currently produced 454 sequence data.

Gmitter

FCPRAC Progress Report (January, 2009)

2009

It is estimated that for every tree that shows symptoms of HLB, there are on the average 13 trees (range is 2-52) that are infected but are asymptomatic. Latency of HLB is estimated to be from 6 to 36 months.

Gottwald

FCPRAC Progress Report (April, 2009)

Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
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Principal Investigator(s) or Author(s)

Publication/Journal

2009

A new strain of Diaphorencyrtus aligarhensis (parasitoid of ACP) was imported from China and is currently being reared and released to help reduce or eliminate ACP populations. Before release, temperature and relative humidity experiments, as well as parasitism rate experiments were conducted. Choice and no choice tests have shown that this parasitoid will parasitize 2nd thru 4th instar nymphs only and will host feed on 1st thru 4th instars of immature psyllids. Results from these experiments show that this strain is ideally suited for mass rearing and release into Florida as a biological control agent.

Hall

FCPRAC Progress Report (January, 2009)

2009

In this study, it was noted that fall and winter appear to be time periods when percentages of infected psyllids may be consistently the highest.

Hall

FCPRAC Progress Report (January, 2009)

2009

cDNA psyllid libraries were produced, which resulted in 17,000 expressed sequence tags. The libraries were from adult, testes, and midgut tissues. These results aided efforts to identify the microbial fauna of the Asian citrus psyllid, enabling genetic promoters to be designed for further analyses. Eight sequences suggest there is an as yet unidentified phage within the psyllids. Sequences from a new Reovirus were identified and characterized. Sequences from a new Wolbachia species were produced. The internal anatomy of the psyllid was identified for tissue collection in anticipation of future cDNA library constructions. An inbred psyllid population was created F7 to produce the needed genomic material for a psyllid genome effort. Several classes of cathepsins were identified, as well as a new FK506-binding protein; these proteins have important functions in body formation, digestion, and in egg/embryo metabolism, plus cell maintenance. Approximately 60 proteins and all other sequences have been published in the public database, at NCBI for use by the research community.

Hunter

FCPRAC Progress Report (January, 2009)

Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
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Year(s)

Milestone

Principal Investigator(s) or Author(s)

Publication/Journal

2009

D. citri embryos were used to establish a series of primary cell lines and conditions for routine establishment of stable and transferable primary cell lines have been developed. To date, four cells lines Dce 10, Dce 17 and Dce 19(cell patch), and Dce 19(total) have undergone their first passage. All four cultures displayed cell growth after first passage of the cells into fresh media. Two cell lines, Dce 19 and Dce 17 have undergone their second passage, with clumps of cells appearing to grow. The current time of growth before passage is 4-5 weeks. We have successfully accomplished our second passage for two cells lines and anticipate continuing the cultivation of the cells. It is anticipated that efforts to begin cryopreservation of some cell aliquots will begin soon. Cell morphology of the various lines remains heterogeneous with some cells forming large clumps before spreading in the tissue culture flasks and whereas others remain in suspension.

Keyhani

FCPRAC Progress Report (January, 2009)

2009

Completion of assembly and annotation of all the Rutaceae sequences (ESTs and mRNAs) available in public databases (GenBank) and sequences from various previous studies (cold acclimation, canker response, salicylic acid treatment). With this information a new microarray based on Agilent technology was designed. Microarrays have been manufactured and a simple experiment (of known results) has been designed to test them before their release to the scientific community.

Moore

FCPRAC Progress Report (January, 2009)

2009

The baseline susceptibility information (LC50s) for commonly used insecticides for psyllid control was determined. These insecticides include the following: fenpropathrin (Danitol 2.4EC), chlorpyrifos (Lorsban 4E), carbaryl (Sevin XLR), imidacloprid (Provado 1.6F), dimethoate (Dimethoate 4EC), zeta-cypermethrin (Mustang), phosmet (Imidan), thiamethoxam (Actara; expected to be labeled for use in FL citrus in 2009) and abamectin (Agri-mek 0.15EC).

Rogers

FCPRAC Progress Report (January, 2009)

Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
×

Year(s)

Milestone

Principal Investigator(s) or Author(s)

Publication/Journal

2009

Results from a laboratory study that tested the effect of spray droplet size on ACP control indicate that smaller droplet sizes result in greater mortality of all ACP life stages than larger ones suggesting that ULV sprays may give more effective control of ACP in the field. Tests conducted in the field showed that for insecticides that are known to be effective against ACP, low volume applications are as effective as standard airblast sprays for psyllid control. Dibrom, Micromite (nymph activity only), Malathion, Portal *(nymph activity only), Dimethoate, Provado 1.6 F, Mustang, Danitol, and Delegate are effective against ACP when applied as low volume sprays.

Salyani and Stelinski

FCPRAC Progress Report (January, 2009)

2009

In this study, it was noted that certain micro- and macro-element levels are significantly changed in greening infected trees. Data from this study also suggest that greening-induced nutritional changes may be detectable before the disease is detectable by PCR analysis

Spann

FCPRAC Progress Report (January, 2009)

Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
×

Year(s)

Milestone

Principal Investigator(s) or Author(s)

Publication/Journal

2009

Gamma-butyrolactone was identified as one of the behaviorally active compounds that likely comprise the pheromone of ACP. Testing in the laboratory has confirmed its behavioral activity to psyllids. This chemical is attractive to male psyllids and appears to repel females. Also, this chemical attracts the psyllid parasitoid, Tamarixia radiata. This information will be used to manipulate the parasitoids’ behavior to enhance mass rearing programs of this species, a prerequisite to its utilization as a biocontrol agent. Biologically active compound(s), which attract T. radiata, will be incorporated into an efficient attractant formulation. Such attractants may allow for monitoring T. radiata population densities, which will allow for tailoring spray programs such that peak parasitoid population densities can be avoided and conserved. Also, deployment of a potent attractant within groves. Alpha Scents has formulated gamma-butyrolactone into lures as well as an attract-and-kill formulation for direct psyllid control, which we will be evaluating this year as psyllid populations build up.

Stelinski

FCPRAC Progress Report (January, 2009)

2009

CLas was found to be present in bark tissue, leaf midrib, roots and different floral and fruit parts but not in the endosperm and embryo of infected fruit. Quantification analysis showed that CLas is not evenly distributed in planta and a relatively high concentration was found in fruit peduncles. A method for quantifying viable CLas cells was developed. This method (EMA-QPCR), which uses ethidium monoazide to differentiate between live and dead cells, could provide an accurate assessment of the amount of viable CLas cells in plant samples

Wang

FCPRAC Progress Report (January, 2009); see also Satyanarayana et al. (Phytopathology, 2008)

Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
×

Year(s)

Milestone

Principal Investigator(s) or Author(s)

Publication/Journal

2009

Microscopy analysis was performed to compare the phloem of HLB infected citrus and healthy control. It was observed that 1) there was significantly greater accumulation of starch in phloem parenchyma cells of infected leaves, 2) callose deposition occurred more frequently in infected midribs. With the use of transmission electron microscopy, it was observed that sieve pores of the midribs of infected plant were plugged with an amorphous substance. Collapse of sieve tubes and companion cells were also observed in HLB-infected midribs but not in healthy midribs. TEM observations also indicated that the HLB bacterium can pass through the sieve plate pore, which suggests that it is unlikely that the HLB bacterium physically caused phloem blockage because multiple bacterial cells were not aggregating. It is likely that the host response results in sieve pore plugging.

Wang

FCPRAC Progress Report (January, 2009).

2009

Microarray analysis (based on 33,879 expressed sequence tag sequences from several citrus species and hybrids) indicated that HLB infection significantly affected expression of 624 genes whose encoded proteins were categorized according to function. The upregulation of three key starch biosynthetic genes including ADPglucose pyrophosphorylase, starch synthase, granule-bound starch synthase and starch debranching enzyme likely contributed to accumulation of starch in HLB-affected leaves.

Wang

FCPRAC Progress Report (January, 2009). Co-author of Kim in Phytopathology article (2009)

Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
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Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
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Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
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Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
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Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
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Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
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Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
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Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
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Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
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Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
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Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
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Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
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Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
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Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
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Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
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Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
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Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
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Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
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Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
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Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
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Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
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Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
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Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
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Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
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Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
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Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
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Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
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Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
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Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
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Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
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Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
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Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
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Suggested Citation:"Appendix K: Huanglongbing Research Milestones (1956–2009)." National Research Council. 2010. Strategic Planning for the Florida Citrus Industry: Addressing Citrus Greening Disease. Washington, DC: The National Academies Press. doi: 10.17226/12880.
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Next: Appendix L: Witches' Broom Disease Outbreak in Brazil and Control Attempts: Success and Failure in Bahia, Brazil (1989–2009) »
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Citrus greening, a disease that reduces yield, compromises the flavor, color, and size of citrus fruit and eventually kills the citrus tree, is now present in all 34 Floridian citrus-producing counties. Caused by an insect-spread bacterial infection, the disease reduced citrus production in 2008 by several percent and continues to spread, threatening the existence of Florida's $9.3 billion citrus industry.

A successful citrus greening response will focus on earlier detection of diseased trees, so that these sources of new infections can be removed more quickly, and on new methods to control the insects that carry the bacteria. In the longerterm, technologies such as genomics could be used to develop new citrus strains that are resistant to both the bacteria and the insect.

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