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Belowground and aboveground herbivory differentially affect the transcriptome in roots and shoots of maize

2022-7-22, Ye, Wenfeng, Bustos Segura, Carlos, Degen, Thomas, Erb, Matthias, Turlings, Ted

Plants recognize and respond to feeding by herbivorous insects by upregulating their local and systemic defenses. While defense induction by aboveground herbivores has been well studied, far less is known about local and systemic defense responses against attacks by belowground herbivores. Here, we investigated and compared the responses of the maize transcriptome to belowground and aboveground mechanical damage and infestation by two well-adapted herbivores: the soil-dwelling western corn rootworm Diabrotica virgifera virgifera (Coleoptera: Chrysomelidae) and the leaf- chewing fall armyworm Spodoptera frugiperda (Lepidoptera: Noctuidae). In responses to both herbivores, maize plants were found to alter local transcription of genes involved in phytohormone signaling, primary and secondary metabolism. Induction by real herbivore damage was considerably stronger and modified the expression of more genes than mechanical damage. Feeding by the corn rootworm had a strong impact on the shoot transcriptome, including the activation of genes involved in defense and development. By contrast, feeding by the fall armyworm induced only few transcriptional changes in the roots. In conclusion, feeding by a leaf chewer and a root feeder differentially affects the local and systemic defense of maize plants. Besides revealing clear differences in how maize plants respond to feeding by these specialized herbivores, this study reveals several novel genes that may play key roles in plant–insect interactions and thus sets the stage for in depth research into the mechanism that can be exploited for improved crop protection.

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Volatiles produced by soil-borne endophytic bacteria increase plant pathogen resistance and affect tritrophic interactions

2014, D'Alessandro, Marco, Erb, Matthias, Ton, Jurriaan, Brandenburg, Anna, Karlen, Danielle, Zopfi, Jakob, Turlings, Ted

Volatile organic compounds (VOCs) released by soil microorganisms influence plant growth and pathogen resistance. Yet, very little is known about their influence on herbivores and higher trophic levels. We studied the origin and role of a major bacterial VOC, 2,3-butanediol (2,3-BD), on plant growth, pathogen and herbivore resistance, and the attraction of natural enemies in maize. One of the major contributors to 2,3-BD in the headspace of soil-grown maize seedlings was identified as Enterobacter aerogenes, an endophytic bacterium that colonizes the plants. The production of 2,3-BD by E.?aerogenes rendered maize plants more resistant against the Northern corn leaf blight fungus Setosphaeria turcica. On the contrary, E.?aerogenes-inoculated plants were less resistant against the caterpillar Spodoptera littoralis. The effect of 2,3-BD on the attraction of the parasitoid Cotesia marginiventris was more variable: 2,3-BD application to the headspace of the plants had no effect on the parasitoids, but application to the soil increased parasitoid attraction. Furthermore, inoculation of seeds with E.?aerogenes decreased plant attractiveness, whereas inoculation of soil with a total extract of soil microbes increased parasitoid attraction, suggesting that the effect of 2,3-BD on the parasitoid is indirect and depends on the composition of the microbial community.

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The prospect of applying chemical elicitors and plant strengtheners to enhance the biological control of crop pests

2014, Sobhy, Islam S., Erb, Matthias, Lou, Yonggen, Turlings, Ted

An imminent food crisis reinforces the need for novel strategies to increase crop yields worldwide. Effective control of pest insects should be part of such strategies, preferentially with reduced negative impact on the environment and optimal protection and utilization of existing biodiversity. Enhancing the presence and efficacy of native biological control agents could be one such strategy. Plant strengthener is a generic term for several commercially available compounds or mixtures of compounds that can be applied to cultivated plants in order to 'boost their vigour, resilience and performance'. Studies into the consequences of boosting plant resistance against pests and diseases on plant volatiles have found a surprising and dramatic increase in the plants' attractiveness to parasitic wasps. Here, we summarize the results from these studies and present new results from assays that illustrate the great potential of two commercially available resistance elicitors. We argue that plant strengtheners may currently be the best option to enhance the attractiveness of cultivated plants to biological control agents. Other options, such as the genetic manipulation of the release of specific volatiles may offer future solutions, but in most systems, we still miss fundamental knowledge on which key attractants should be targeted for this approach.

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Volatiles produced by soil-borne endophytic bacteria increase plant pathogen resistance and affect tritrophic interactions

2013, D'Alessandro, Marco, Erb, Matthias, Ton, Jurriaan, Brandenburg, Anna, Karlen, Danielle, Zopfi, Jakob, Turlings, Ted

Volatile organic compounds (VOCs) released by soil microorganisms influence plant growth and pathogen resistance. Yet, very little is known about their influence on herbivores and higher trophic levels. We studied the origin and role of a major bacterial VOC, 2,3-butanediol (2,3-BD), on plant growth, pathogen and herbivore resistance, and the attraction of natural enemies in maize. One of the major contributors to 2,3-BD in the headspace of soil-grown maize seedlings was identified as Enterobacter aerogenes, an endophytic bacterium that colonizes the plants. The production of 2,3-BD by E.?aerogenes rendered maize plants more resistant against the Northern corn leaf blight fungus Setosphaeria turcica. On the contrary, E.?aerogenes-inoculated plants were less resistant against the caterpillar Spodoptera littoralis. The effect of 2,3-BD on the attraction of the parasitoid Cotesia marginiventris was more variable: 2,3-BD application to the headspace of the plants had no effect on the parasitoids, but application to the soil increased parasitoid attraction. Furthermore, inoculation of seeds with E.?aerogenes decreased plant attractiveness, whereas inoculation of soil with a total extract of soil microbes increased parasitoid attraction, suggesting that the effect of 2,3-BD on the parasitoid is indirect and depends on the composition of the microbial community.

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Plant strengtheners enhance parasitoid attraction to herbivore-damaged cotton via qualitative and quantitative changes in induced volatiles

2014, Sobhy, Islam S., Erb, Matthias, Turlings, Ted

Background Herbivore-damaged plants release a blend of volatile organic compounds (VOCs) that differs from undamaged plants. These induced changes are known to attract the natural enemies of the herbivores and therefore are expected to be important determinants of the effectiveness of biological control in agriculture. One way of boosting this phenomenon is the application of plant strengtheners, which has been shown to enhance parasitoid attraction in maize. It is unclear if this is also the case for other important crops. Results We applied the plant strengtheners BTH (benzo (1,2,3) thiadiazole-7-carbothioic acid S-methyl ester) or laminarin to cotton plants and studied the effects on volatile releases and the attraction of three hymenopteran parasitoids, Cotesia marginiventris, Campoletis sonorensis and Microplitis rufiventris. After treated and untreated plants were induced by real or simulated caterpillar feeding, we found that BTH treatment increased the attraction of the parasitoids, whereas laminarin had no significant effect. BTH treatment selectively increased the release of two homoterpenes and reduced the emission of indole, the latter of which has been shown to interfere with parasitoid attraction in earlier studies. Canonical variate analyses of the data show that the parasitoid responses were dependent on the quality rather than the quantity of volatile emission in this tritrophic interaction. Conclusion Overall, these results strengthen the emerging paradigm that induction of plant defences with chemical elicitors such as BTH could provide a sustainable and environment-friendly strategy for biological control of pests by enhancing the attractiveness of cultivated plants to natural enemies of insect herbivores.

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3-D-Glucopyranosyl-6-methoxy-2-benzoxazolinone (MBOA-N-Glc) is an insect detoxification product of maize 1,4-benzoxazin-3-ones

2014, Maag, Daniel, Dalvit, Claudio, Thevenet, Damien, Köhler, Angela, Wouters, Felipe C., Vassão, Daniel G., Gershenzon, Jonathan, Wolfender, Jean-Luc, Turlings, Ted, Erb, Matthias, Glauser, Gaetan

In order to defend themselves against arthropod herbivores, maize plants produce 1,4-benzoxazin-3-ones (BXs), which are stored as weakly active glucosides in the vacuole. Upon tissue disruption, BXs come into contact with ?-glucosidases, resulting in the release of active aglycones and their breakdown products. While some aglycones can be reglucosylated by specialist herbivores, little is known about how they detoxify BX breakdown products. Here we report on the structure of an N-glucoside, 3-?-d-glucopyranosyl-6-methoxy-2-benzoxazolinone (MBOA-N-Glc), purified from Spodoptera frugiperda faeces. In vitro assays showed that MBOA-N-Glc is formed enzymatically in the insect gut using the BX breakdown product 6-methoxy-2-benzoxazolinone (MBOA) as precursor. While Spodoptera littoralis and S. frugiperda caterpillars readily glucosylated MBOA, larvae of the European corn borer Ostrinia nubilalis were hardly able to process the molecule. Accordingly, Spodoptera caterpillar growth was unaffected by the presence of MBOA, while O. nubilalis growth was reduced. We conclude that glucosylation of MBOA is an important detoxification mechanism that helps insects tolerate maize BXs.

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Induced carbon reallocation and compensatory growth as root herbivore tolerance mechanisms

2014, Robert, Christelle A. M., Ferrieri, Richard A., Schirmer, Stefanie, Babst, Benjamin A., Schueller, Michael J., Machado, Ricardo A. R., Arce, Carla C. M., Hibbard, Bruce E., Gershenzon, Jonathan, Turlings, Ted, Erb, Matthias

Upon attack by leaf herbivores, many plants reallocate photoassimilates below ground. However, little is known about how plants respond when the roots themselves come under attack. We investigated induced resource allocation in maize plants that are infested by the larvae Western corn rootworm Diabrotica virgifera virgifera. Using radioactive 11CO2, we demonstrate that root-attacked maize plants allocate more new 11C carbon from source leaves to stems, but not to roots. Reduced meristematic activity and reduced invertase activity in attacked maize root systems are identified as possible drivers of this shoot reallocation response. The increased allocation of photoassimilates to stems is shown to be associated with a marked thickening of these tissues and increased growth of stem-borne crown roots. A strong quantitative correlation between stem thickness and root regrowth across different watering levels suggests that retaining photoassimilates in the shoots may help root-attacked plants to compensate for the loss of belowground tissues. Taken together, our results indicate that induced tolerance may be an important strategy of plants to withstand belowground attack. Furthermore, root herbivore-induced carbon reallocation needs to be taken into account when studying plant-mediated interactions between herbivores.

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Role of two UDP-Glycosyltransferases from the L group of arabidopsis in resistance against pseudomonas syringae

2014, Boachon, Benoît, Gamir, Jordi, Pastor, Victoria, Erb, Matthias, Dean, John V., Flors, Victor, Mauch-Mani, Brigitte

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Within-plant distribution of 1,4-benzoxazin-3-ones contributes to herbivore niche differentiation in maize

2014, Köhler, Angela, Maag, Daniel, Veyrat, Nathalie, Glauser, Gaétan, Wolfender, Jean-Luc, Turlings, Ted, Erb, Matthias

Plant defenses vary in space and time, which may translate into specific herbivore foraging patterns and feeding niche differentiation. To date, little is known about the effect of secondary metabolite patterning on within-plant herbivore foraging. We investigated how variation in the major maize secondary metabolites, 1,4-benzoxazin-3-one derivatives (BXDs), affects the foraging behavior of two leaf-chewing herbivores. BXD levels varied substantially within plants: Older leaves had higher levels of constitutive BXDs while younger leaves were consistently more inducible. These differences were observed independently of plant age, even though the concentrations of most BXDs declined markedly in older plants. Larvae of the well-adapted maize pest Spodoptera frugiperda preferred and grew better on young inducible leaves irrespective of plant age, while larvae of the generalist Spodoptera littoralis preferred and tended to grow better on old leaves. In BXD-free mutants, the differences in herbivore weight gain between old and young leaves were absent for both species, and leaf preferences of S. frugiperda were attenuated. In contrast, S. littoralis foraging patterns were not affected. In summary, our study shows that plant secondary metabolites differentially affect performance and foraging of adapted and non-adapted herbivores and thereby likely contribute to feeding niche differentiation.

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Direct and indirect plant defenses are not suppressed by endosymbionts of a specialist root herbivore

2013, Robert, Christelle Aurélie Maud, Frank, Daniel L., Leach, Kristen A., Turlings, Ted, Hibbard, Bruce Elliott, Erb, Matthias