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1.  Induced Release of a Plant-Defense Volatile ‘Deceptively’ Attracts Insect Vectors to Plants Infected with a Bacterial Pathogen 
PLoS Pathogens  2012;8(3):e1002610.
Transmission of plant pathogens by insect vectors is a complex biological process involving interactions between the plant, insect, and pathogen. Pathogen-induced plant responses can include changes in volatile and nonvolatile secondary metabolites as well as major plant nutrients. Experiments were conducted to understand how a plant pathogenic bacterium, Candidatus Liberibacter asiaticus (Las), affects host preference behavior of its psyllid (Diaphorina citri Kuwayama) vector. D. citri were attracted to volatiles from pathogen-infected plants more than to those from non-infected counterparts. Las-infected plants were more attractive to D. citri adults than non-infected plants initially; however after feeding, psyllids subsequently dispersed to non-infected rather than infected plants as their preferred settling point. Experiments with Las-infected and non-infected plants under complete darkness yielded similar results to those recorded under light. The behavior of psyllids in response to infected versus non-infected plants was not influenced by whether or not they were carriers of the pathogen. Quantification of volatile release from non-infected and infected plants supported the hypothesis that odorants mediate psyllid preference. Significantly more methyl salicylate, yet less methyl anthranilate and D-limonene, was released by infected than non-infected plants. Methyl salicylate was attractive to psyllids, while methyl anthranilate did not affect their behavior. Feeding on citrus by D. citri adults also induced release of methyl salicylate, suggesting that it may be a cue revealing location of conspecifics on host plants. Infected plants were characterized by lower levels of nitrogen, phosphorus, sulfur, zinc, and iron, as well as, higher levels of potassium and boron than non-infected plants. Collectively, our results suggest that host selection behavior of D. citri may be modified by bacterial infection of plants, which alters release of specific headspace volatiles and plant nutritional contents. Furthermore, we show in a laboratory setting that this apparent pathogen-mediated manipulation of vector behavior may facilitate pathogen spread.
Author Summary
In this investigation, we experimentally demonstrate specific mechanisms through which a bacterial plant pathogen induces plant responses that modify behavior of its insect vector. Candidatus Liberibacter asiaticus, a fastidious, phloem-limited bacterium responsible for causing huanglongbing disease of citrus, induced release of a specific volatile chemical, methyl salicylate, which increased attractiveness of infected plants to its insect vector, Diaphorina citri, and caused vectors to initially prefer infected plants. However, the insect vectors subsequently dispersed to non-infected plants as their preferred location of prolonged settling because of likely sub-optimal nutritional content of infected plants. The duration of initial feeding on infected plants was sufficiently long for the vectors to acquire the pathogen before they dispersed to non-infected plants, suggesting that the bacterial pathogen manipulates behavior of its insect vector to promote its own proliferation. The behavior of psyllids in response to infected versus non-infected plants was not influenced by whether or not they were carriers of the pathogen and was similar under both light and dark conditions. Feeding on citrus by D. citri adults also induced the release of methyl salicylate, suggesting that it may be a cue revealing location of conspecifics on host plants.
PMCID: PMC3310815  PMID: 22457628
2.  Sexual Transmission of a Plant Pathogenic Bacterium, Candidatus Liberibacter asiaticus, between Conspecific Insect Vectors during Mating 
PLoS ONE  2011;6(12):e29197.
Candidatus Liberibacter asiaticus is a fastidious, phloem-inhabiting, gram-negative bacterium transmitted by Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Psyllidae). The bacterium is the presumed causal agent of huanglongbing (HLB), one of the most destructive and economically important diseases of citrus. We investigated whether Las is transmitted between infected and uninfected D. citri adults during courtship. Our results indicate that Las was sexually transmitted from Las-infected male D. citri to uninfected females at a low rate (<4%) during mating. Sexual transmission was not observed following mating of infected females and uninfected males or among adult pairs of the same sex. Las was detected in genitalia of both sexes and also in eggs of infected females. A latent period of 7 days or more was required to detect the bacterium in recipient females. Rod shaped as well as spherical structures resembling Las were observed in ovaries of Las-infected females with transmission electron microscopy, but were absent in ovaries from uninfected D. citri females. The size of the rod shaped structures varied from 0.39 to 0.67 µm in length and 0.19 to 0.39 µm in width. The spherical structures measured from 0.61 to 0.80 µm in diameter. This investigation provides convincing evidence that a plant pathogenic bacterium is sexually transmitted from male to female insects during courtship and established evidence that bacteria persist in reproductive organs. Moreover, these findings provide an alternative sexually horizontal mechanism for the spread of Las within populations of D. citri, even in the absence of infected host trees.
PMCID: PMC3244449  PMID: 22216209
3.  Stable Isotope Analysis Reveals Detrital Resource Base Sources of the Tree Hole Mosquito, Aedes triseriatus 
Ecological entomology  2010;35(5):586-593.
1. Detritus that forms the basis for mosquito production in tree hole ecosystems can vary in type and timing of input. We investigated the contributions of plant- and animal-derived detritus to the biomass of Aedes triseriatus (Say) pupae and adults by using stable isotope (15N and 13C) techniques in lab experiments and field collections.
2. Lab-reared mosquito isotope values reflected their detrital resource base, providing a clear distinction between mosquitoes reared on plant or animal detritus.
3. Isotope values from field-collected pupae were intermediate between what would be expected if a single (either plant or animal) detrital source dominated the resource base. However, mosquito isotope values clustered most closely with plant-derived values, and a mixed feeding model analysis indicated tree floral parts contributed approximately 80% of mosquito biomass. The mixed model also indicated that animal detritus contributed approximately 30% of mosquito tissue nitrogen.
4. Pupae collected later in the season generally had isotope values that were consistent with an increased contribution from animal detritus, suggesting this resource became more nutritionally important for mosquitoes as plant inputs declined over the summer.
PMCID: PMC2995505  PMID: 21132121
Aedes triseriatus; tree hole; stable isotope; 13C; 15N; detritus
4.  Beetle (Coleoptera: Scirtidae) Facilitation of Larval Mosquito Growth in Tree Hole Habitats is Linked to Multitrophic Microbial Interactions 
Microbial Ecology  2011;62(3):690-703.
Container-breeding mosquitoes, such as Aedes triseriatus, ingest biofilms and filter water column microorganisms directly to obtain the bulk of their nutrition. Scirtid beetles often co-occur with A. triseriatus and may facilitate the production of mosquito adults under low-resource conditions. Using molecular genetic techniques and quantitative assays, we observed changes in the dynamics and composition of bacterial and fungal communities present on leaf detritus and in the water column when scirtid beetles co-occur with A. triseriatus. Data from terminal restriction fragment polymorphism analysis indicated scirtid presence alters the structure of fungal communities in the water column but not leaf-associated fungal communities. Similar changes in leaf and water bacterial communities occurred in response to mosquito presence. In addition, we observed increased processing of leaf detritus, higher leaf-associated enzyme activity, higher bacterial productivity, and higher leaf-associated fungal biomass when scirtid beetles were present. Such shifts suggest beetle feeding facilitates mosquito production indirectly through the microbial community rather than directly through an increase in available fine particulate organic matter.
PMCID: PMC3175047  PMID: 21607876

Results 1-4 (4)