Reciprocal crosstalk between jasmonate and salicylate defence-signalling pathways modulates plant volatile emission and herbivore host-selection behaviour

Wei, Jianing; Loon, Joop J. A. van; Gols, Rieta; Menzel, Tila R.; Li, Na; Kang, Le; Dicke, Marcel

doi:10.1093/jxb/eru181

Cited by 92 publications

(76 citation statements)

References 55 publications

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“…The PLS‐DA extension of the SIMCA P + 12.0 software program (Umetrics AB, Umeå, Sweden) revealed which volatile compounds were important for the separation of volatile blends emitted by differently treated plants (Wei et al . ). In addition, the variable importance in the projection (VIP) was calculated.…”

Section: Methodsmentioning

confidence: 97%

Manipulating two olfactory cues causes a biological control beetle to shift to non‐target plant species

et al. 2017

Journal of Ecology

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1. Olfactory cues can determine the host preferences of herbivorous insects, but their role in host shifting is unclear. Host specificity and the potential for host shifts are important criteria for screening and post-release evaluation of biological control agents for invasive plants. However, the role of olfactory cues in mediating host shifts in biological control agents is not well understood. 2. To investigate the role of olfactory cues in host selection of a reportedly monophagous flea beetle (Agasicles hygrophila), an important biocontrol agent for invasive alligator weed (Alternanthera philoxeroides), we extracted and analyzed the volatiles produced by the host plant A. philoxeroides and the non-host plants A. sessilis, Beta vulgaris, and Amaranthus Accepted Article This article is protected by copyright. All rights reserved. mangostanus. Moreover, we used electrophysiologcial techniques, behavioural bioassays and field trials to test the antennal responses and behavioural preferences of A. hygrophila to combinations of different plant volatiles and treatments, and pure compounds in different dosages and combinations. 3. We show that A. hygrophila female beetles indeed use olfactory cues to select plants for feeding and oviposition and that the survivorship of larvae on the second preferred non-host plant A. sessilis, a close relative of the first preferred host plant A. philoxeroides, was over 75% in a field trail. Although female beetles responded to many volatile compounds from host and non-host plants, (E)-4,8-dimethyl-1,3,7- nonatriene (DMNT) positively encouraged the beetle’s feeding and oviposition preferences, whereas (Z)-3-hexenol displayed repellent effect. Remarkably, complementation assays with (Z)-3-hexenol on host plant or DMNT on non-host plants significantly shifted A. hygrophila host preferences to non-host plants and resulted in oviposition and egg hatching on the non-host plant A. sessilis in field trials. 4. Synthesis. We demonstrate an olfactory mechanism by which a specialized herbivorous beetle uses the ratio of two common plant volatiles, DMNT and (Z)-3-hexenol, to discriminate between its host and non-host plants in nature. This study highlights an important mechanism by which olfactory cues could lead to undesired host range expansion in biocontrol agent, thus representing an important warning of the potential for a host shift and development of invasiveness in a common biocontrol agent, the flea beetle

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Section: Methodsmentioning

confidence: 97%

Manipulating two olfactory cues causes a biological control beetle to shift to non‐target plant species

et al. 2017

Journal of Ecology

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“…Furthermore, the variable importance in the projection (VIP) was calculated. Variables with VIP > 1 are the most influential for the model (Wei et al ., ). The levels of volatiles released from locusts were normalized to nanogram per hour per 10 locusts in absorbent trapping and to nanogram per half‐hour per locust in SPME studies.…”

Section: Methodsmentioning

confidence: 99%

Composition and emission dynamics of migratory locust volatiles in response to changes in developmental stages and population density

et al. 2016

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Chemical communication plays an important role in density-dependent phase change in locusts. However, the volatile components and emission patterns of the migratory locust, Locusta migratoria, are largely unknown. In this study, we identified the chemical compositions and emission dynamics of locust volatiles from the body and feces and associated them with developmental stages, sexes and phase changes. The migratory locust shares a number of volatile components with the desert locust (Schistocerca gregaria), but the emission dynamics of the two locust species are significantly different. The body odors of the gregarious nymphs in the migratory locust consisted of phenylacetonitrile (PAN), benzaldehyde, guaiacol, phenol, aliphatic acids and 2,3-butanediol, and PAN was the dominant volatile. Volatiles from the fecal pellets of the nymphs primarily consist of guaiacol and phenol. Principal component analysis (PCA) showed significant differences in the volatile profiles between gregarious and solitary locusts. PAN and 4-vinylanisole concentrations were significantly higher in gregarious individuals than in solitary locusts. Gregarious mature males released significantly higher amounts of PAN and 4-vinylanisole during adulthood than mature females and immature adults of both sexes. Furthermore, PAN and 4-vinylanisole were completely lost in gregarious nymphs during the solitarization process, but were obtained by solitary nymphs during gregarization. The amounts of benzaldehyde, guaiacol and phenol only unidirectionally decreased from solitary to crowded treatment. Aliphatic aldehydes (C7 to C10), which were previously reported as locust volatiles, are now identified as environmental contaminants. Therefore, our results illustrate the precise odor profiles of migratory locusts during developmental stages, sexes and phase change. However, the function and role of PAN and other aromatic compounds during phase transition need further investigation.

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“…However, levels of 525 the phytohormone SA, which has been considered an her-526 bivore repellent in many previous studies (Erb et al 2012), 527 were not significantly different between N. tenuis-punc-528 tured plants and intact plants. Wei et al (2014) demon-529 strated that there are antagonistic effects of SA-mediated 530 responses on JA-mediated responses and vice versa. In 531 addition, the dose and timing of phytohormone levels may 532 affect the behavioral responses of an herbivore.…”

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Defensive plant responses induced by Nesidiocoris tenuis (Hemiptera: Miridae) on tomato plants

et al. 2015

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8 Abstract In the last decade, biological control programs 9 for greenhouse tomatoes and other crops have been suc-10 cessfully implemented using zoophytophagous plant bugs 11 (Miridae), which can feed on both plant tissues and insect 12 prey. It is well known that plants respond to herbivore 13 attacks by releasing volatile compounds through diverse 14 pathways triggered by phytohormones. These herbivore-15 induced plant volatiles can alert neighboring plants, repel 16 or attract herbivores, and attract natural enemies of these 17 herbivores. Nevertheless, the possible benefits of induced 18 plant responses by zoophytophagous predators that could 19 add to their usefulness as biocontrol agents have not been 20 studied until now. Here we show that the zoophytophagous 21 predator Nesidiocoris tenuis activated abscisic acid and 22 jasmonic acid (JA) signaling pathways in tomato plants, 23 which made them less attractive to the whitefly Bemisia 24 tabaci, a major tomato pest worldwide, and more attractive 25 to the whitefly parasitoid, Encarsia formosa. We also found 26 that intact tomato plants exposed to volatiles from N. ten-27 uis-punctured plants activated the JA pathway, and as a 28 consequence, E. formosa was also attracted to these intact 29 plants with activated defense systems. Thus, our results 30 demonstrate that N. tenuis not only benefits tomato plants 31 directly by entomophagy but also indirectly by phyto-32 phagy, which induces a physiological response in the 33 tomato plant. 38We have proved that the zoophytophagous predator Nesi-39 diocoris tenuis induces plant benefits directly by its ento-40 mophagy and also indirectly by its phytophagy, which 41 induces the attraction of a whitefly parasitoid (Encarsia 42 formosa) and antixenosis to the whitefly Bemisia tabaci. 43 Furthermore, N. tenuis-punctured plants induce plant 44 defenses in intact plants that result in attraction of E. for-45 mosa. Our results might be one reasonable explanation for 46 the great success achieved by N. tenuis as a key biocontrol 47 agent in tomatoes.

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Reciprocal crosstalk between jasmonate and salicylate defence-signalling pathways modulates plant volatile emission and herbivore host-selection behaviour

Abstract: SummaryLow-dose crosstalk between jasmonic acid and salicylic acid signalling pathways results in a dynamic plant phenotype in terms of plant volatile emission and behavioural responses of an herbivorous spider mite.

Cited by 92 publications

References 55 publications

Manipulating two olfactory cues causes a biological control beetle to shift to non‐target plant species

Manipulating two olfactory cues causes a biological control beetle to shift to non‐target plant species

Composition and emission dynamics of migratory locust volatiles in response to changes in developmental stages and population density

Defensive plant responses induced by Nesidiocoris tenuis (Hemiptera: Miridae) on tomato plants

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