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Title: Induced release of a plant-defense volatile 'deceptively' attracts insect vectors to plants infected with a bacterial pathogen

item MANN, RAJINDER - University Of Florida
item ALI, JARED - University Of Florida
item HERMANN, SARA - University Of Florida
item TIWARI, SIDDHARTH - University Of Florida
item PELZ-STELINSKI, KIRSTEN - University Of Florida
item Alborn, Hans
item STELINSKI, LUKASZ - University Of Florida

Submitted to: PLoS Pathogens
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/13/2012
Publication Date: 3/15/2012
Citation: Mann, R.S., Ali, J.G., Hermann, S.L., Tiwari, S., Pelz-Stelinski, K., Alborn, H.T., Stelinski, L.L. 2012. Induced release of a plant-defense volatile 'deceptively' attracts insect vectors to plants infected with a bacterial pathogen. PLoS Pathogens. 8(3):e1002610. doi: 10.1371/journal.ppat.1002610.

Interpretive Summary: Scientists at University of Florida, Entomology and Nematology Department, Citrus Research and Education Center, Lake Alfred FL in collaboration with a scientist at the United States Department of Agriculture, Agricultural Research Center, Center for Medical, Agricultural, and Veterinary Entomology, Gainesville, FL discovered that Candidatus Liberibacter asiaticus, a fastidious, phloem-limited bacterium responsible for causing huanglongbing disease of citrus, induced citrus plants to release methyl salicylate attracting its psyllid vector, Diaphorina citri. After this initial preference for diseased plants, the insect vectors subsequently disperse to healthy plants as their final location of prolonged settling which probably is due to sub-optimal nutritional content of infected plants. The duration of initial infected plant feeding is long enough for the vectors to acquire the pathogen before dispersing. The psyllid behavior was not influenced by whether or not they were carriers of the pathogen and was similar under both light and dark conditions. In addition, feeding on citrus by D. citri adults also induce the release of methyl salicylate. This suggests the bacterial plant pathogen utilizes a cue, used by its vector to reveal location of conspecifics on host plants, to successfully promote its own proliferation.

Technical Abstract: 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 uninfected counterparts. Las-infected plants were more attractive to D. citri adults than uninfected plants initially; however after feeding, psyllids subsequently dispersed to uninfected rather than infected plants as their final settling point. Experiments with Las-infected and uninfected plants under complete darkness yielded similar results to those recorded under light. The behavior of psyllids in response to infected versus uninfected plants was not influenced by whether or not they were carriers of the pathogen. Quantification of volatile release from either uninfected or 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 uninfected plants. Methyl salicylate was attractive to psyllids, while methyl anthranilate did not affect their behavior. 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. Infected plants were characterized by lower levels of nitrogen, phosphorus, sulfur, zinc, and iron and higher levels of potassium and boron. Collectively, our results suggest that the 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 experimentally that this pathogen-mediated manipulation of vector behavior may facilitate spread of disease.