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

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          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.

          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.

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          Most cited references176

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          Defensive function of herbivore-induced plant volatile emissions in nature.

          Herbivore attack is known to increase the emission of volatiles, which attract predators to herbivore-damaged plants in the laboratory and agricultural systems. We quantified volatile emissions from Nicotiana attenuata plants growing in natural populations during attack by three species of leaf-feeding herbivores and mimicked the release of five commonly emitted volatiles individually. Three compounds (cis-3-hexen-1-ol, linalool, and cis-alpha-bergamotene) increased egg predation rates by a generalist predator; linalool and the complete blend decreased lepidopteran oviposition rates. As a consequence, a plant could reduce the number of herbivores by more than 90% by releasing volatiles. These results confirm that indirect defenses can operate in nature.
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            The Myriad Plant Responses to Herbivores.

            Walling (2000)
            Plant responses to herbivores are complex. Genes activated on herbivore attack are strongly correlated with the mode of herbivore feeding and the degree of tissue damage at the feeding site. Phloem-feeding whiteflies and aphids that produce little injury to plant foliage are perceived as pathogens and activate the salicylic acid (SA)-dependent and jasmonic acid (JA)/ethylene-dependent signaling pathways. Differential expression of plant genes in response to closely related insect species suggest that some elicitors generated by phloem-feeding insects are species-specific and are dependent on the herbivore's developmental stage. Other elicitors for defense-gene activation are likely to be more ubiquitous. Analogies to the pathogen-incompatible reactions are found. Chewing insects such as caterpillars and beetles and cell-content feeders such as mites and thrips cause more extensive tissue damage and activate wound-signaling pathways. Herbivore feeding is not equivalent to mechanical wounding. Wound responses are a part of the induced responses that accompany herbivore feeding. Herbivores induce direct defenses that interfere with herbivore feeding, growth and development, fecundity, and fertility. In addition, herbivores induce an array of volatiles that creates an indirect mechanism of defense. Volatile blends provide specific cues to attract herbivore parasites and predators to infested plants. The nature of the elicitors for volatile production is discussed.
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              Silverleaf whitefly induces salicylic acid defenses and suppresses effectual jasmonic acid defenses.

              The basal defenses important in curtailing the development of the phloem-feeding silverleaf whitefly (Bemisia tabaci type B; SLWF) on Arabidopsis (Arabidopsis thaliana) were investigated. Sentinel defense gene RNAs were monitored in SLWF-infested and control plants. Salicylic acid (SA)-responsive gene transcripts accumulated locally (PR1, BGL2, PR5, SID2, EDS5, PAD4) and systemically (PR1, BGL2, PR5) during SLWF nymph feeding. In contrast, jasmonic acid (JA)- and ethylene-dependent RNAs (PDF1.2, VSP1, HEL, THI2.1, FAD3, ERS1, ERF1) were repressed or not modulated in SLWF-infested leaves. To test for a role of SA and JA pathways in basal defense, SLWF development on mutant and transgenic lines that constitutively activate or impair defense pathways was determined. By monitoring the percentage of SLWF nymphs in each instar, we show that mutants that activate SA defenses (cim10) or impair JA defenses (coi1) accelerated SLWF nymphal development. Reciprocally, mutants that activate JA defenses (cev1) or impair SA defenses (npr1, NahG) slowed SLWF nymphal development. Furthermore, when npr1 plants, which do not activate downstream SA defenses, were treated with methyl jasmonate, a dramatic delay in nymph development was observed. Collectively, these results showed that SLWF-repressed, JA-regulated defenses were associated with basal defense to the SLWF.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Pathog
                PLoS Pathog
                plos
                plospath
                PLoS Pathogens
                Public Library of Science (San Francisco, USA )
                1553-7366
                1553-7374
                March 2012
                March 2012
                22 March 2012
                : 8
                : 3
                : e1002610
                Affiliations
                [1 ]University of Florida, Entomology and Nematology Department, Citrus Research and Education Center, Lake Alfred, Florida, United States of America
                [2 ]Center for Medical, Agricultural, and Veterinary Entomology, Agricultural Research Service, U.S. Department of Agriculture, Gainesville, Florida, United States of America
                University of Idaho, United States of America
                Author notes

                Conceived and designed the experiments: LLS RSM JGA. Performed the experiments: RSM JGA SLH. Analyzed the data: RSM JGA KSPS LLS. Contributed reagents/materials/analysis tools: RSM KSPS ST HTA LLS. Wrote the paper: RSM LLS KSPS JGA.

                Article
                PPATHOGENS-D-11-02137
                10.1371/journal.ppat.1002610
                3310815
                22457628
                12d9b43a-312d-4f22-87e2-81afb7470ede
                This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.
                History
                : 27 September 2011
                : 13 February 2012
                Page count
                Pages: 13
                Categories
                Research Article
                Agriculture
                Crops
                Pest Control
                Biology
                Ecology
                Plant Science
                Zoology

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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