Induced Release of a Plant-Defense Volatile ‘Deceptively’ Attracts Insect Vectors to Plants Infected with a Bacterial Pathogen

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.

Host Manipulation by Parasites: Cases, Patterns, and Remaining Doubts

“…For example, Tomato spotted wilt virus augments the frequency of all feeding behaviors in infected males of its thrips vector (Stafford et al, 2011), and Candidatus Liberibacter asiaticus makes the odor of infected citrus plants initially more attractive for its psyllid vector but then, after virus acquisition, causes psyllids to disperse to non-infected plants (Mann et al, 2012). Similarly, Tomato yellow leaf curl virus enhances the attractiveness of infected tomato plants to virus-free whiteflies (B. tabaci), whereas infected whiteflies lose the capacity to distinguish between infected and healthy host plants (Fang et al, 2013).…”

“…Indeed, differing persistence times might be a major explanation for the observation that manipulation effects are more frequently reported for intermediate than for final hosts, at least as long as all hosts are animals (Holmes and Bethel, 1972). Plant pathogens, by contrast, require mobile vectors for their dispersal among their immobile final hosts and, therefore, frequently manipulate the quality of their host plant for the vectors (Belliure et al, 2010;Mauck et al, 2010Mauck et al, , 2014aLuan et al, 2013;Shi et al, 2013) as well as the feeding decisions that are taken by their vectors (Stafford et al, 2011;Ingwell et al, 2012;Mann et al, 2012;Fang et al, 2013;Rajabaskar et al, 2014). These changes can be very fine-tuned: for example, plant viruses with a persistent mode of transmission require vectors to feed for a prolonged period of time on infected hosts and, thus, usually tend to improve the quality of the host plants for the vectors.…”

New Synthesis: A Holobiontic View on Plant-Insect Interactions

“…Mann et al (2012) demonstrated that infected Citrus sinensis plants emitted higher amounts of methyl salicylate, but less methyl anthranilate and Dlimonene than plants not infected by Candidatus Liberibacter asiaticus bacteria. Psyllid bugs (Diaphorina citri) initially chose infected plants but subsequently-after they became carriers of the pathogen-moved to non-infected plants.…”

Biocontrol program targets Asian citrus psyllid in California's urban areas

“…The most important contributing factors to rapid spread of CLas by ACP are (A) the high dispersal potential of adult psyllids, which is facilitated by their good flight capabilities and small size, enabling them to be blown long distances by wind and go undetected on shipped plants and (B) rapid psyllid population growth, which results from short generation times and the high fecundity of females (Lewis-Rosenblum et al 2015). Additionally, uninfected psyllids are more attracted to CLas-infected trees than to uninfected trees, which may further facilitate rapid pathogen spread (Mann et al 2012). Thus, suppressing ACP populations is important for reducing CLas movement, which in turn maximizes orchard longevity and productivity.…”