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Can Herbivore-Induced Volatiles Protect Plants by Increasing the Herbivores' Susceptibility to Natural Pathogens?

ABSTRACT: In response to insect herbivory, plants mobilize various defenses. Defense responses include the release of herbivore-induced plant volatiles (HIPVs) that can serve as signals to alert undamaged tissues and to attract natural enemies of the herbivores. Some HIPVs can have a direct negative impact on herbivore survival, but it is not well understood by what mechanisms. Here, we tested the hypothesis that exposure to HIPVs renders insects more susceptible to natural pathogens. Exposure of the caterpillars of the noctuid Spodoptera exigua to indole and linalool, but not exposure to (Z)-3-hexenyl acetate, increased the susceptibility to Spodoptera exigua multiple nucleopolyhedrovirus (SeMNPV). We also found that exposure to indole, but not exposure to linalool or (Z)-3-hexenyl acetate, increased the pathogenicity of Bacillus thuringiensis Additional experiments revealed significant changes in microbiota composition after forty-eight hours of larval exposure to indole. Overall, these results provide evidence that certain HIPVs can strongly enhance the susceptibility of caterpillars to pathogens, possibly through effects on the insect gut microbiota. These findings suggest a novel mechanism by which HIPVs can protect plants from herbivorous insects.IMPORTANCE Multitrophic interactions involving insect pests, their natural enemies, microorganisms, and plant hosts are increasingly being recognized as relevant factors in pest management. In response to herbivory attacks, plants activate a wide range of defenses that aim to mitigate the damage. Attacked plants release herbivore-induced plant volatiles (HIPVs), which can act as priming signals for other plants and attract natural enemies of herbivores, and which may have a direct negative impact on herbivore survival. In the present work, we show that exposure of the insects to the induced volatiles could increase the insects' susceptibility to the entomopathogens naturally occurring in the plant environment. These findings suggest a novel role for plant volatiles by influencing insect interactions with natural pathogens, probably mediated by alterations in the insect microbiota composition. In addition, this work provides evidence for selectable plant traits (production of secondary metabolites) that can have an influence on the ecology of the pests and could be relevant in the improvement of pest management strategies using natural entomopathogens.

SUBMITTER: Gasmi L

PROVIDER: S-EPMC6293100 | biostudies-literature | 2019 Jan

REPOSITORIES: biostudies-literature

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Can Herbivore-Induced Volatiles Protect Plants by Increasing the Herbivores' Susceptibility to Natural Pathogens?

Gasmi Laila L Martínez-Solís María M Frattini Ada A Ye Meng M Collado María Carmen MC Turlings Ted C J TCJ Erb Matthias M Herrero Salvador S

Applied and environmental microbiology 20181213 1

In response to insect herbivory, plants mobilize various defenses. Defense responses include the release of herbivore-induced plant volatiles (HIPVs) that can serve as signals to alert undamaged tissues and to attract natural enemies of the herbivores. Some HIPVs can have a direct negative impact on herbivore survival, but it is not well understood by what mechanisms. Here, we tested the hypothesis that exposure to HIPVs renders insects more susceptible to natural pathogens. Exposure of the cate ...[more]

PMID: 30366995

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Project description:Predatory mites locate herbivorous mites, their prey, by the aid of herbivore-induced plant volatiles (HIPV). These HIPV differ with plant and/or herbivore species, and it is not well understood how predators cope with this variation. We hypothesized that predators are attracted to specific compounds in HIPV, and that they can identify these compounds in odor mixtures not previously experienced. To test this, we assessed the olfactory response of Phytoseiulus persimilis, a predatory mite that preys on the highly polyphagous herbivore Tetranychus urticae. The responses of the predatory mite to a dilution series of each of 30 structurally different compounds were tested. They mites responded to most of these compounds, but usually in an aversive way. Individual HIPV were no more attractive (or less repellent) than out-group compounds, i.e., volatiles not induced in plants fed upon by spider-mites. Only three samples were significantly attractive to the mites: octan-1-ol, not involved in indirect defense, and cis-3-hexen-1-ol and methyl salicylate, which are both induced by herbivory, but not specific for the herbivore that infests the plant. Attraction to individual compounds was low compared to the full HIPV blend from Lima bean. These results indicate that individual HIPV have no a priori meaning to the mites. Hence, there is no reason why they could profit from an ability to identify individual compounds in odor mixtures. Subsequent experiments confirmed that naive predatory mites do not prefer tomato HIPV, which included the attractive compound methyl salicylate, over the odor of an uninfested bean. However, upon associating each of these odors with food over a period of 15 min, both are preferred. The memory to this association wanes within 24 hr. We conclude that P. persimilis possesses a limited ability to identify individual spider mite-induced plant volatiles in odor mixtures. We suggest that predatory mites instead learn to respond to prey-associated mixtures of volatiles and, thus, to odor blends as a whole.

Project description:Anthropogenic nutrient inputs into native ecosystems cause fluctuations in resources that normally limit plant growth, which has important consequences for associated food webs. Such inputs from agricultural and urban habitats into nearby natural systems are increasing globally and can be highly variable, spanning the range from sporadic to continuous. Despite the global increase in anthropogenically-derived nutrient inputs into native ecosystems, the consequences of variation in subsidy duration on native plants and their associated food webs are poorly known. Specifically, while some studies have examined the effects of nutrient subsidies on native ecosystems for a single year (a nutrient pulse), repeated introductions of nutrients across multiple years (a nutrient press) better reflect the persistent nature of anthropogenic nutrient enrichment. We therefore contrasted the effects of a one-year nutrient pulse with a four-year nutrient press on arthropod consumers in two salt marshes. Salt marshes represent an ideal system to address the differential impacts of nutrient pulses and presses on ecosystem and community dynamics because human development and other anthropogenic activities lead to recurrent introductions of nutrients into these natural systems. We found that plant biomass and %N as well as arthropod density fell after the nutrient pulse ended but remained elevated throughout the nutrient press. Notably, higher trophic levels responded more strongly than lower trophic levels to fertilization, and the predator/prey ratio increased each year of the nutrient press, demonstrating that food web responses to anthropogenic nutrient enrichment can take years to fully manifest themselves. Vegetation at the two marshes also exhibited an apparent tradeoff between increasing %N and biomass in response to fertilization. Our research emphasizes the need for long-term, spatially diverse studies of nutrient enrichment in order to understand how variation in the duration of anthropogenic nutrient subsidies affects native ecosystems.

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Can Herbivore-Induced Volatiles Protect Plants by Increasing the Herbivores' Susceptibility to Natural Pathogens?

Publications

Can Herbivore-Induced Volatiles Protect Plants by Increasing the Herbivores' Susceptibility to Natural Pathogens?

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