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Herbivore-induced plant volatiles mediate defense regulation in maize leaves but not in maize roots.

ABSTRACT: Plant leaves that are exposed to herbivore-induced plant volatiles (HIPVs) respond by increasing their defenses, a phenomenon referred to as priming. Whether this phenomenon also occurs in the roots is unknown. Using maize plants, Zea mays, whose leaves respond strongly to leaf HIPVs, we measured the impact of belowground HIPVs, emanating from roots infested by the banded cucumber beetle, Diabrotica balteata, on constitutive and herbivore-induced levels of defense-related gene expression, phytohormones, volatile and non-volatile primary and secondary metabolites, growth and herbivore resistance in roots of neighbouring plants. HIPV exposure did not increase constitutive or induced levels of any of the measured root traits. Furthermore, HIPV exposure did not reduce the performance or survival of D. balteata on maize or its ancestor teosinte. Cross-exposure experiments between HIPVs from roots and leaves revealed that maize roots, in contrast to maize leaves, neither emit nor respond strongly to defense-regulating HIPVs. Together, these results demonstrate that volatile-mediated defense regulation is restricted to the leaves of maize. This finding is in line with the lower diffusibility of volatiles in the soil and the availability of other, potentially more efficient, information conduits below ground.

SUBMITTER: van Doan C

PROVIDER: S-EPMC8360093 | biostudies-literature | 2021 Aug

REPOSITORIES: biostudies-literature

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Herbivore-induced plant volatiles mediate defense regulation in maize leaves but not in maize roots.

van Doan Cong C Züst Tobias T Maurer Corina C Zhang Xi X Machado Ricardo A R RAR Mateo Pierre P Ye Meng M Schimmel Bernardus C J BCJ Glauser Gaétan G Robert Christelle A M CAM

Plant, cell & environment 20210406 8

Plant leaves that are exposed to herbivore-induced plant volatiles (HIPVs) respond by increasing their defenses, a phenomenon referred to as priming. Whether this phenomenon also occurs in the roots is unknown. Using maize plants, Zea mays, whose leaves respond strongly to leaf HIPVs, we measured the impact of belowground HIPVs, emanating from roots infested by the banded cucumber beetle, Diabrotica balteata, on constitutive and herbivore-induced levels of defense-related gene expression, phytoh ...[more]

PMID: 33748996

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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:Maize (Zea mays) emits volatile terpenes in response to insect feeding and egg deposition to defend itself against harmful pests. However, maize cultivars differ strongly in their ability to produce the defense signal. To further understand the agroecological role and underlying genetic mechanisms for variation in terpene emission among maize cultivars, we studied the production of an important signaling component (E)-caryophyllene in a South American maize landrace Braz1006 possessing stemborer Chilo partellus egg inducible defense trait, in comparison with the European maize line Delprim and North American inbred line B73. The (E)-caryophyllene production level and transcript abundance of TPS23, terpene synthase responsible for (E)-caryophyllene formation, were compared between Braz1006, Delprim, and B73 after mimicked herbivory. Braz1006-TPS23 was heterologously expressed in E. coli, and amino acid sequences were determined. Furthermore, electrophysiological and behavioral responses of a key parasitic wasp Cotesia sesamiae to C. partellus egg-induced Braz1006 volatiles were determined using coupled gas chromatography electroantennography and olfactometer bioassay studies. After elicitor treatment, Braz1006 released eightfold higher (E)-caryophyllene than Delprim, whereas no (E)-caryophyllene was detected in B73. The superior (E)-caryophyllene production by Braz1006 was positively correlated with high transcript levels of TPS23 in the landrace compared to Delprim. TPS23 alleles from Braz1006 showed dissimilarities at different sequence positions with Delprim and B73 and encodes an active enzyme. Cotesia sesamiae was attracted to egg-induced volatiles from Braz1006 and synthetic (E)-caryophyllene. The variation in (E)-caryophyllene emission between Braz1006 and Delprim is positively correlated with induced levels of TPS23 transcripts. The enhanced TPS23 activity and corresponding (E)-caryophyllene production by the maize landrace could be attributed to the differences in amino acid sequence with the other maize lines. This study suggested that the same analogous genes could have contrasting expression patterns in different maize genetic backgrounds. The current findings provide valuable insight not only into genetic mechanisms underlying variation in defense signal production but also the prospect of introgressing the novel defense traits into elite maize varieties for effective and ecologically sound protection of crops against damaging insect pests.

Project description:Host plant defenses are known to cascade up food chains to influence herbivores and their natural enemies, but how herbivore and predator traits and identity mediate such tri-trophic dynamics is largely unknown. We assessed the influence of plant defense on aphid and coccinellid performance in laboratory trials with low- vs. high-glucosinolate varieties of Brassica napus, a dietary specialist (Brevicoryne brassicae) and generalist (Myzus persicae) aphid, and five species of aphidophagous coccinellids. The performance of the specialist and generalist aphids was similar and unaffected by variation in plant defense. Aphid glucosinolate concentration and resistance to predators differed by aphid species and host plant defense, and these effects acted independently. With respect to aphid species, the dietary generalist aphid (vs. specialist) had 14% lower glucosinolate concentration and coccinellid predators ate three-fold more aphids. With respect to host plant variety, the high-glucosinolate plants (vs. low) increased aphid glucosinolate concentration by 21%, but had relatively weak effects on predation by coccinellids and these effects varied among coccinellid species. In turn, coccinellid performance was influenced by the interactive effects of plant defense and aphid species, as the cascading, indirect effect of plant defense was greater when feeding upon the specialist than generalist aphid. When feeding upon specialist aphids, low- (vs. high-) glucosinolate plants increased coccinellid mass gain by 78% and accelerated development by 14%. In contrast, when feeding upon generalist aphids, low- (vs. high-) glucosinolate plants increased coccinellid mass gain by only 11% and had no detectable effect on development time. These interactive effects of plant defense and aphid diet breadth on predator performance also varied among coccinellid species; the indirect negative effects of plant defenses on predator performance was consistent among the five predators when transmitted via the dietary specialist aphid, but these effects varied substantially among predators-in both the magnitude and direction-when transmitted via the dietary generalist aphid. Accordingly, the cascading effect of plant defense on predators was stronger in magnitude and more consistent among predator taxa when transmitted by the specialist than generalist herbivore. Overall, these findings support a central role of herbivore diet breadth in mediating both the strength and contingency of tri-trophic interactions.

Dataset Information

Herbivore-induced plant volatiles mediate defense regulation in maize leaves but not in maize roots.

Publications

Herbivore-induced plant volatiles mediate defense regulation in maize leaves but not in maize roots.

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