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  • Publication
    Métadonnées seulement
    Volatiles produced by soil-borne endophytic bacteria increase plant pathogen resistance and affect tritrophic interactions
    (2013)
    D'Alessandro, Marco
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    Ton, Jurriaan
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    Brandenburg, Anna
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    Karlen, Danielle
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    ;
    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.
  • Publication
    Métadonnées seulement
    Plant elicitor peptides are conserved signals regulating direct and indirect antiherbivore defense
    (2013)
    Huffaker, Alisa
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    Pearce, Gregory
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    ; ; ;
    Sartor, Ryan
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    Shen, Zhouxin
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    Briggs, Steven P.
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    Vaughan, Martha M.
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    Alborn, Hans T.
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    Teal, Peter E. A.
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    Schmelz, Eric A.
    Insect-induced defenses occur in nearly all plants and are regulated by conserved signaling pathways. As the first described plant peptide signal, systemin regulates antiherbivore defenses in the Solanaceae, but in other plant families, peptides with analogous activity have remained elusive. In the current study, we demonstrate that a member of the maize (Zea mays) plant elicitor peptide (Pep) family, ZmPep3, regulates responses against herbivores. Consistent with being a signal, expression of the ZmPROPEP3 precursor gene is rapidly induced by Spodoptera exigua oral secretions. At concentrations starting at 5 pmol per leaf, ZmPep3 stimulates production of jasmonic acid, ethylene, and increased expression of genes encoding proteins associated with herbivory defense. These include proteinase inhibitors and biosynthetic enzymes for production of volatile terpenes and benzoxazinoids. In accordance with gene expression data, plants treated with ZmPep3 emit volatiles similar to those from plants subjected to herbivory. ZmPep3-treated plants also exhibit induced accumulation of the benzoxazinoid phytoalexin 2-hydroxy-4,7-dimethoxy-1,4-benzoxazin-3-one glucoside. Direct and indirect defenses induced by ZmPep3 contribute to resistance against S. exigua through significant reduction of larval growth and attraction of Cotesia marginiventris parasitoids. ZmPep3 activity is specific to Poaceous species; however, peptides derived from PROPEP orthologs identified in Solanaceous and Fabaceous plants also induce herbivory-associated volatiles in their respective species. These studies demonstrate that Peps are conserved signals across diverse plant families regulating antiherbivore defenses and are likely to be the missing functional homologs of systemin outside of the Solanaceae.
  • Publication
    Métadonnées seulement
    Volatiles produced by soil-borne endophytic bacteria increase plant pathogen resistance and affect tritrophic interactions
    (2014)
    D'Alessandro, Marco
    ;
    ;
    Ton, Jurriaan
    ;
    Brandenburg, Anna
    ;
    Karlen, Danielle
    ;
    ;
    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.
  • Publication
    Métadonnées seulement
    A specialist root herbivore exploits defensive metabolites to locate nutritious tissues
    (2012)
    Robert, Christelle Aurélie Maud
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    ; ;
    Marti, Guillaume
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    Doyen, G. R.
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    Gaillard, Mickaël David Philippe
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    Köllner, Tobias G.
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    Giron, David
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    Body, Mélanie
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    Babst, Benjamin A.
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    Ferrieri, Richard A.
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    The most valuable organs of plants are often particularly rich in essential elements, but also very well defended. This creates a dilemma for herbivores that need to maximise energy intake while minimising intoxication. We investigated how the specialist root herbivore Diabrotica virgifera solves this conundrum when feeding on wild and cultivated maize plants. We found that crown roots of maize seedlings were vital for plant development and, in accordance, were rich in nutritious primary metabolites and contained higher amounts of the insecticidal 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one (DIMBOA) and the phenolic compound chlorogenic acid. The generalist herbivores Diabrotica balteata and Spodoptera littoralis were deterred from feeding on crown roots, whereas the specialist D. virgifera preferred and grew best on these tissues. Using a 1,4-benzoxazin-3-one-deficient maize mutant, we found that D. virgifera is resistant to DIMBOA and other 1,4-benzoxazin-3-ones and that it even hijacks these compounds to optimally forage for nutritious roots.
  • Publication
    Métadonnées seulement
    The underestimated role of roots in defense against leaf attackers
    (2009) ;
    Lenk, C.
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    Degenhardt, Jörg
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    Plants have evolved intricate strategies to withstand attacks by herbivores and pathogens. Although it is known that plants change their primary and secondary metabolism in leaves to resist and tolerate aboveground attack, there is little awareness of the role of roots in these processes. This is surprising given that plant roots are responsible for the synthesis of plant toxins, play an active role in environmental sensing and defense signaling, and serve as dynamic storage organs to allow regrowth. Hence, studying roots is essential for a solid understanding of resistance and tolerance to leaf-feeding insects and pathogens. Here, we highlight this function of roots in plant resistance to aboveground attackers, with a special focus on systemic signaling and insect herbivores.
  • Publication
    Accès libre
    Modification of plant resistance and metabolism by above- and belowground herbivores
    ;
    Turlings, Théodor
    Plants are often attacked by above- and belowground herbivores. As a result, they have evolved defense mechanisms to protect both their roots and shoot. However, physiological processes in roots and shoots are tightly connected, and attack of one of these plant parts can dramatically alter primary and secondary metabolism of the other (chapter 1). It is therefore important to understand how the plant reacts aboveground upon belowground insect attack and vice versa. This thesis investigates how shoots of maize plants respond to root attack by lavae of the beetle Diabrotica virgifera and vice versa, how roots react to shoot attack by Spodoptera littoralis caterpillars. This is one of the first studies highlighting the physiology and potential evolutionary significance of plant-mediated above-belowground interactions. The results obtained show that root infestation by D. virgifera broadly increases defenses in maize leaves, mostly after prolonged infestation (chapters 2-4). Many of these processes were found to be inducible by absisic acid (ABA), a well-known stress-hormone that increased in concentration aboveground after prolonged belowground attack by D. virgifera. The increase of ABA coincided with a decrease of leaf-water content, and our experiments suggest that the observed ABA-dependent defense reaction is the consequence of a physiological stress induced by the root herbivore. The changes in shoot physiology boosted the plant’s resistance against the necrotrophic pathogen Setosphaeria turcica and the herbivore S. littoralis in the laboratory, as well as against lepidopteran pests in the field, demonstrating that D. virgifera has an ecologically important impact on aboveground interactions. While the observed ABA response can explain the reduction of S. turcica growth in the leaves (chapter 2), S. littoralis was negatively affected by the reduction of leaf-water contents (chapter 3). Shoot herbivory by S. littoralis profoundly altered root gene expression, even early after infestation (chapter 4). The reaction in the roots was entirely different from the changes in shoot transcriptional profiles, suggesting that the root-shoot signal(s) are dissimilar to the known systemic shoot defense signals. S. littoralis had a strong impact on root protein biosynthesis, a novel finding that demands further attention. The strong effect of S. littoralis infestation on root physiology was reflected in a dramatically increased resistance of attacked maize plants against D. virgifera. In conclusion, both root- and shoot herbivores change the physiology of plants not only locally, but also in the unattacked parts. These changes increase the resistance of the plant against herbivores and pathogens. Root-herbivore induced shoot resistance seems to be caused by physiological constraints rather than plant adaptive behaviour, while shoot-herbivore induced root resistance is likely to be the result of the plant’s integrated, systemic defensive system.
  • Publication
    Métadonnées seulement
    Within-plant distribution of 1,4-benzoxazin-3-ones contributes to herbivore niche differentiation in maize
    (2014)
    Köhler, Angela
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    ; ;
    Glauser, Gaétan
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    Wolfender, Jean-Luc
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    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.
  • Publication
    Métadonnées seulement
    Genetically engineered maize plants reveal distinct costs and benefits of constitutive volatile emissions in the field
    (2013)
    Robert, Christelle Aurélie Maud
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    ; ;
    Hibbard, Bruce Elliott
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    Gaillard, Mickaël David Philippe
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    Bilat, Julia
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    Degenhardt, Jörg
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    Cambet-Petit-Jean, Xavier
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    Genetic manipulation of plant volatile emissions is a promising tool to enhance plant defences against herbivores. However, the potential costs associated with the manipulation of specific volatile synthase genes are unknown. Therefore, we investigated the physiological and ecological effects of transforming a maize line with a terpene synthase gene in field and laboratory assays, both above- and below ground. The transformation, which resulted in the constitutive emission of (E)--caryophyllene and -humulene, was found to compromise seed germination, plant growth and yield. These physiological costs provide a possible explanation for the inducibility of an (E)--caryophyllene-synthase gene in wild and cultivated maize. The overexpression of the terpene synthase gene did not impair plant resistance nor volatile emission. However, constitutive terpenoid emission increased plant apparency to herbivores, including adults and larvae of the above ground pest Spodoptera frugiperda, resulting in an increase in leaf damage. Although terpenoid overproducing lines were also attractive to the specialist root herbivore Diabrotica virgifera virgifera below ground, they did not suffer more root damage in the field, possibly because of the enhanced attraction of entomopathogenic nematodes. Furthermore, fewer adults of the root herbivore Diabrotica undecimpunctata howardii were found to emerge near plants that emitted (E)--caryophyllene and -humulene. Yet, overall, under the given field conditions, the costs of constitutive volatile production overshadowed its benefits. This study highlights the need for a thorough assessment of the physiological and ecological consequences of genetically engineering plant signals in the field to determine the potential of this approach for sustainable pest management strategies.
  • Publication
    Métadonnées seulement
    Sequence of arrival determines plant-mediated interactions between herbivores
    (2011) ;
    Robert, Christelle Aurélie Maud
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    Hibbard, Bruce Elliott
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    P>1. Induced changes in plant quality can mediate indirect interactions between herbivores. Although the sequence of attack by different herbivores has been shown to influence plant responses, little is known about how this affects the herbivores themselves. 2. We therefore investigated how induction by the leaf herbivore Spodoptera frugiperda influences resistance of teosinte (Zea mays mexicana) and cultivated maize (Zea mays mays) against root-feeding larvae of Diabrotica virgifera virgifera. The importance of the sequence of arrival was tested in the field and laboratory. 3. Spodoptera frugiperda infestation had a significant negative effect on colonization by D. virgifera larvae in the field and weight gain in the laboratory, but only when S. frugiperda arrived on the plant before the root herbivore. When S. frugiperda arrived after the root herbivore had established, no negative effects on larval performance were detected. Yet, adult emergence of D. virgifera was reduced even when the root feeder had established first, indicating that the negative effects were not entirely absent in this treatment. 4. The defoliation of the plants was not a decisive factor for the negative effects on root herbivore development, as both minor and major leaf damage resulted in an increase in root resistance and the extent of biomass removal was not correlated with root-herbivore growth. We propose that leaf-herbivore-induced increases in feeding-deterrent and/or toxic secondary metabolites may account for the sequence-specific reduction in root-herbivore performance. 5. Synthesis. Our results demonstrate that the sequence of arrival can be an important determinant of plant-mediated interactions between insect herbivores in both wild and cultivated plants. Arriving early on a plant may be an important strategy of insects to avoid competition with other herbivores. To fully understand plant-mediated interactions between insect herbivores, the sequence of arrival should be taken into account.
  • Publication
    Métadonnées seulement
    Induced carbon reallocation and compensatory growth as root herbivore tolerance mechanisms
    (2014)
    Robert, Christelle A. M.
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    Ferrieri, Richard A.
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    Schirmer, Stefanie
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    Babst, Benjamin A.
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    Schueller, Michael J.
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    Machado, Ricardo A. R.
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    Arce, Carla C. M.
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    Hibbard, Bruce E.
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    Gershenzon, Jonathan
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    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.