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 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.

Highlights

  • Transmission of plant pathogens by insect vectors is a complex biological process involving interactions between the plant, insect, and pathogen [1,2]

  • We experimentally demonstrate specific mechanisms through which a bacterial plant pathogen induces plant responses that modify behavior of its insect vector

  • 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

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Summary

Introduction

Transmission of plant pathogens by insect vectors is a complex biological process involving interactions between the plant, insect, and pathogen [1,2]. Candidatus Liberibacter asiaticus (Las) is a gram-negative, fastidious, phloem-limited bacterium that causes huanglongbing (HLB) disease in citrus [20] Based on their 16S rRNA gene sequence, three species of the pathogen have been identified to date: 1) Candidatus Liberibacter asiaticus (Las), 2) Candidatus Liberibacter africanus (Laf), and 3) Candidatus Liberibacter americanus (Lam) [22,23,24,25,26]. Las and Lam are transmitted by the Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Psyllidae); whereas, Laf is transmitted by the African citrus psyllid, Trioza erytreae (Del Guercio) (Hemiptera: Psyllidae) Both D. citri adults and nymphs are capable of transmitting Las after feeding on an infected plant for 30 minutes or longer [19,30,31,32]. The bacteria presumably multiply within the vector and are retained throughout the entire life cycle of the vector [33,34]

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