Modeling huanglongbing transmission within a citrus tree

Chiyaka, Christinah; Singer, Burton H.; Halbert, Susan E.; Morris, J. Glenn; Bruggen, A.H.C. van

doi:10.1073/pnas.1208326109

Cited by 100 publications

(81 citation statements)

References 31 publications

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“…Recent work by Chiyaka et al (22) has also incorporated seasonal forcing into a model for HLB spread within trees. Chiyaka et al also modeled the dynamics of vector infection on a single tree.…”

Section: Discussionmentioning

confidence: 99%

Bayesian inference for an emerging arboreal epidemic in the presence of control

Parry

Gibson

Parnell

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

102

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The spread of Huanglongbing through citrus groves is used as a case study for modeling an emerging epidemic in the presence of a control. Specifically, the spread of the disease is modeled as a susceptible-exposed-infectious-detected-removed epidemic, where the exposure and infectious times are not observed, detection times are censored, removal times are known, and the disease is spreading through a heterogeneous host population with trees of different age and susceptibility. We show that it is possible to characterize the disease transmission process under these conditions. Two innovations in our work are (i) accounting for control measures via time dependence of the infectious process and (ii) including seasonal and host age effects in the model of the latent period. By estimating parameters in different subregions of a large commercially cultivated orchard, we establish a temporal pattern of invasion, host age dependence of the dispersal parameters, and a close to linear relationship between primary and secondary infectious rates. The model can be used to simulate Huanglongbing epidemics to assess economic costs and potential benefits of putative control scenarios.

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Section: Discussionmentioning

confidence: 99%

Bayesian inference for an emerging arboreal epidemic in the presence of control

Parry

Gibson

Parnell

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

102

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“…Liberibacter asiaticus" to citrus plants by infected D. citri insects is among the critical parameters that facilitate HLB prevalence and spread (3,(10)(11)(12). It is expected that D. citri insects heavily infected with "Ca.…”

Section: Discussionmentioning

confidence: 99%

“…Liberibacter asiaticus"-infected D. citri insects are primarily responsible for infection and spread of HLB among citrus plants, monitoring and investigation of the infection dynamics of "Ca. Liberibacter asiaticus" in field populations of D. citri are of pivotal importance (9)(10)(11)(12). Furthermore, infection densities of "Ca.…”

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confidence: 99%

Infection Density Dynamics of the Citrus Greening Bacterium “Candidatus Liberibacter asiaticus” in Field Populations of the Psyllid Diaphorina citri and Its Relevance to the Efficiency of Pathogen Transmission to Citrus Plants

Ukuda-Hosokawa

Sadoyama

Kishaba

et al. 2015

Appl Environ Microbiol

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h Huanglongbing, or citrus greening, is a devastating disease of citrus plants recently spreading worldwide, which is caused by an uncultivable bacterial pathogen, "Candidatus Liberibacter asiaticus," and vectored by a phloem-sucking insect, Diaphorina citri. We investigated the infection density dynamics of "Ca. Liberibacter asiaticus" in field populations of D. citri with experiments using field-collected insects to address how "Ca. Liberibacter asiaticus" infection density in the vector insect is relevant to pathogen transmission to citrus plants. Of 500 insects continuously collected from "Ca. Liberibacter asiaticus"-infected citrus trees with pathological symptoms in the spring and autumn of 2009, 497 (99.4%) were "Ca. Liberibacter asiaticus" positive. The infections were systemic across head-thorax and abdomen, ranging from 10 3 to 10 7 bacteria per insect. In spring, the infection densities were low in March, at ϳ10 3 bacteria per insect, increasing up to 10 6 to 10 7 bacteria per insect in April and May, and decreasing to 10 5 to 10 6 bacteria per insect in late May, whereas the infection densities were constantly ϳ10 6 to 10 7 bacteria per insect in autumn. Statistical analysis suggested that several factors, such as insect sex, host trees, and collection dates, may be correlated with "Ca. Liberibacter asiaticus" infection densities in field D. citri populations. Inoculation experiments with citrus seedlings using field-collected "Ca. Liberibacter asiaticus"-infected insects suggested that (i) "Ca. Liberibacter asiaticus"-transmitting insects tend to exhibit higher infection densities than do nontransmitting insects, (ii) a threshold level (ϳ10 6 bacteria per insect) of "Ca. Liberibacter asiaticus" density in D. citri is required for successful transmission to citrus plants, and (iii) D. citri attaining the threshold infection level transmits "Ca. Liberibacter asiaticus" to citrus plants in a stochastic manner. These findings provide valuable insights into understanding, predicting, and controlling this notorious citrus pathogen. H uanglongbing (HLB), or citrus greening, is one of the most serious diseases of citrus plants in many countries across Asia, Africa, and North and South America (1-5). This disease is caused by the phloem-inhabiting, noncultivable, and insect-vectored bacterial pathogens "Candidatus Liberibacter asiaticus" (Asia, North America, and Brazil), "Ca. Liberibacter africanus" (Africa), and "Ca. Liberibacter americanus" (Brazil) (6-8).The Asian citrus psyllid Diaphorina citri Kuwayama (Hemiptera: Liviidae) is the principal vector of "Ca. Liberibacter asiaticus" in Asia, North America, and Brazil (1-5). On the grounds that "Ca. Liberibacter asiaticus"-infected D. citri insects are primarily responsible for infection and spread of HLB among citrus plants, monitoring and investigation of the infection dynamics of "Ca. Liberibacter asiaticus" in field populations of D. citri are of pivotal importance (9-12). Furthermore, infection densities of "Ca. Liberibacter asiaticus" within vector in...

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“…Las between the psyllid vector, D. citri, and young flush shoots on the trees. Treating a tree as a flush patch is a key feature of the model, an emphasis first put forth by Chiyaka et al (3). To relate the local transmission mechanism at flush shoots to the spread through a grove, we identify patches of flush and groups of psyllids with points on a 2D grid, representing a grove of citrus trees.…”

Section: Transmission Modelmentioning

confidence: 99%

Asymptomatic spread of huanglongbing and implications for disease control

Lee

Halbert

Dawson

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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185

132

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Huanglongbing (HLB) is a bacterial infection of citrus trees transmitted by the Asian citrus psyllid Diaphorina citri. Mitigation of HLB has focused on spraying of insecticides to reduce the psyllid population and removal of trees when they first show symptoms of the disease. These interventions have been only marginally effective, because symptoms of HLB do not appear on leaves for months to years after initial infection. Limited knowledge about disease spread during the asymptomatic phase is exemplified by the heretofore unknown length of time from initial infection of newly developing cluster of young leaves, called flush, by adult psyllids until the flush become infectious. We present experimental evidence showing that young flush become infectious within 15 d after receiving an inoculum of Candidatus Liberibacter asiaticus (bacteria). Using this critical fact, we specify a microsimulation model of asymptomatic disease spread and intensity in a grove of citrus trees. We apply a range of psyllid introduction scenarios to show that entire groves can become infected with up to 12,000 psyllids per tree in less than 1 y, before most of the trees show any symptoms. We also show that intervention strategies that reduce the psyllid population by 75% during the flushing periods can delay infection of a full grove, and thereby reduce the amount of insecticide used throughout a year. This result implies that psyllid surveillance and control, using a variety of recently available technologies, should be used from the initial detection of invasion and throughout the asymptomatic period.asymptomatic huanglongbing | latent period | transmission model | control strategies T he main symptoms of huanglongbing (HLB) in citrus trees are yellow shoots, leaves with blotchy mottle, and small lopsided fruits. Ultimately, infected branches die back and the tree dies. The putative causal agent of HLB is an alpha-proteobacterium, Candidatus Liberibacter asiaticus (Ca. Las), that resides within the phloem and is transmitted by the Asian citrus psyllid Diaphorina citri Kuwayama. The highest concentrations of Ca. Las in infected trees are in the stem and midribs of flush. The flush is a newly developing cluster of very young leaves on the expanding end of a terminal shoot. The bacterium multiplies in both the psyllids and the trees, but the psyllids are essential for the spread of the disease.The dominant control measure currently in use is the combination of insecticidal spraying to limit the psyllid populations and removal of infected trees, an inoculum source, when they are symptomatic. This strategy has had only marginal effect because symptoms appear anywhere from months to years after an initial infection, long after the trees have been active in the transmission process (1). Presymptomatic trees can serve as a source of inoculum for psyllids, but the length of time from initial infection of a tree until it is infective as a source of inoculum is known from experimental measurements only to within coarse bounds (within 60 d) (1). A...

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Modeling huanglongbing transmission within a citrus tree

Cited by 100 publications

References 31 publications

Bayesian inference for an emerging arboreal epidemic in the presence of control

Bayesian inference for an emerging arboreal epidemic in the presence of control

Infection Density Dynamics of the Citrus Greening Bacterium “Candidatus Liberibacter asiaticus” in Field Populations of the Psyllid Diaphorina citri and Its Relevance to the Efficiency of Pathogen Transmission to Citrus Plants

Asymptomatic spread of huanglongbing and implications for disease control

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