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  • Publication
    Métadonnées seulement
    Direct and indirect plant defenses are not suppressed by endosymbionts of a specialist root herbivore
    (2013)
    Robert, Christelle Aurélie Maud
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    Frank, Daniel L.
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    Leach, Kristen A.
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    Hibbard, Bruce Elliott
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  • Publication
    Métadonnées seulement
    Metabolomics reveals herbivore-induced metabolites of resistance and susceptibility in maize leaves and roots
    (2013)
    Marti, Guillaume
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    Boccard, J.
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    Doyen, G. R.
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    Robert, Christelle Aurélie Maud
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    Rudaz, S.
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    Wolfender, Jean-Luc
    Plants respond to herbivory by reprogramming their metabolism. Most research in this context has focused on locally induced compounds that function as toxins or feeding deterrents. We developed an ultra-high-pressure liquid chromatography time-of-flight mass spectrometry (UHPLC-TOF-MS)-based metabolomics approach to evaluate local and systemic herbivore-induced changes in maize leaves, sap, roots and root exudates without any prior assumptions about their function. Thirty-two differentially regulated compounds were identified from Spodoptera littoralis-infested maize seedlings and isolated for structure assignment by microflow nuclear magnetic resonance (CapNMR). Nine compounds were quantified by a high throughput direct nano-infusion tandem mass spectrometry/mass spectrometry (MS/MS) method. Leaf infestation led to a marked local increase of 1,3-benzoxazin-4-ones, phospholipids, N-hydroxycinnamoyltyramines, azealic acid and tryptophan. Only few changes were found in the root metabolome, but 1,3-benzoxazin-4-ones increased in the vascular sap and root exudates. The role of N-hydroxycinnamoyltyramines in plantherbivore interactions is unknown, and we therefore tested the effect of the dominating p-coumaroyltyramine on S. littoralis. Unexpectedly, p-coumaroyltyramine was metabolized by the larvae and increased larval growth, possibly by providing additional nitrogen to the insect. Taken together, this study illustrates that herbivore attack leads to the induction of metabolites that can have contrasting effects on herbivore resistance in the leaves and roots.
  • 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
    The maize lipoxygenase, ZmLOX10, mediates green leaf volatile, jasmonate and herbivore-induced plant volatile production for defense against insect attack
    (2013)
    Christensen, S. A.
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    Nemchenko, A.
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    Borrego, E.
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    Murray, I.
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    Sobhy, I. S.
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    Bosak, L.
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    DeBlasio, S.
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    Robert, Christelle Aurélie Maud
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    Vaughn, K. A.
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    Herrfurth, C.
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    Tumlinson, James
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    Feussner, I.
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    Jackson, D.
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    Engelberth, J.
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    Nansen, C.
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    Meeley, R.
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    Kolomiets, M. V.
    Fatty acid derivatives are of central importance for plant immunity against insect herbivores; however, major regulatory genes and the signals that modulate these defense metabolites are vastly understudied, especially in important agro-economic monocot species. Here we show that products and signals derived from a single Zea mays (maize) lipoxygenase (LOX), ZmLOX10, are critical for both direct and indirect defenses to herbivory. We provide genetic evidence that two 13-LOXs, ZmLOX10 and ZmLOX8, specialize in providing substrate for the green leaf volatile (GLV) and jasmonate (JA) biosynthesis pathways, respectively. Supporting the specialization of these LOX isoforms, LOX8 and LOX10 are localized to two distinct cellular compartments, indicating that the JA and GLV biosynthesis pathways are physically separated in maize. Reduced expression of JA biosynthesis genes and diminished levels of JA in lox10 mutants indicate that LOX10-derived signaling is required for LOX8-mediated JA. The possible role of GLVs in JA signaling is supported by their ability to partially restore wound-induced JA levels in lox10 mutants. The impaired ability of lox10 mutants to produce GLVs and JA led to dramatic reductions in herbivore-induced plant volatiles (HIPVs) and attractiveness to parasitoid wasps. Because LOX10 is under circadian rhythm regulation, this study provides a mechanistic link to the diurnal regulation of GLVs and HIPVs. GLV-, JA- and HIPV-deficient lox10 mutants display compromised resistance to insect feeding, both under laboratory and field conditions, which is strong evidence that LOX10-dependent metabolites confer immunity against insect attack. Hence, this comprehensive gene to agro-ecosystem study reveals the broad implications of a single LOX isoform in herbivore defense.
  • Publication
    Métadonnées seulement
    A specialist root herbivore reduces plant resistance and uses an induced plant volatile to aggregate in a density-dependent manner
    (2012)
    Robert, Christelle Aurélie Maud
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    Hibbard, Bruce Elliott
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    French, B. W.
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    1. Leaf-herbivore attack often triggers induced resistance in plants. However, certain specialist herbivores can also take advantage of the induced metabolic changes. In some cases, they even manipulate plant resistance, leading to a phenomenon called induced susceptibility. Compared to above-ground plant-insect interactions, little is known about the prevalence and consequences of induced responses below-ground. 2. A recent study suggested that feeding by the specialist root herbivore Diabrotica virgifera virgifera makes maize roots more susceptible to conspecifics. To better understand this phenomenon, we conducted a series of experiments to study the behavioural responses and elucidate the underlying biochemical mechanisms. 3. We found that D. virgifera benefitted from feeding on a root system in groups of intermediate size (39 larvae/plant in the laboratory), whereas its performance was reduced in large groups (12 larvae/plant). Interestingly, the herbivore was able to select host plants with a suitable density of conspecifics by using the induced plant volatile (E)-beta-caryophyllene in a dose-dependent manner. Using a split root experiment, we show that the plant-induced susceptibility is systemic and, therefore, plant mediated. Chemical analyses on plant resource reallocation and defences upon herbivory showed that the systemic induced-susceptibility is likely to stem from a combination of (i) increased free amino acid concentrations and (ii) relaxation of defence inducibility. 4. These findings show that herbivores can use induced plant volatiles in a density-dependent manner to aggregate on a host plant and change its metabolism to their own benefit. Our study furthermore helps to explain the remarkable ecological success of D. virgifera in maize fields around the world.
  • 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
    Herbivore-induced plant volatiles mediate host selection by a root herbivore
    (2012)
    Robert, Christelle Aurélie Maud
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    Duployer, M.
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    Doyen, G. R.
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    In response to herbivore attack, plants mobilize chemical defenses and release distinct bouquets of volatiles. Aboveground herbivores are known to use changes in leaf volatile patterns to make foraging decisions, but it remains unclear whether belowground herbivores also use volatiles to select suitable host plants. We therefore investigated how above- and belowground infestation affects the performance of the root feeder Diabrotica virgifera virgifera, and whether the larvae of this specialized beetle are able to use volatile cues to assess from a distance whether a potential host plant is already under herbivore attack. Diabrotica virgifera larvae showed stronger growth on roots previously attacked by conspecific larvae, but performed more poorly on roots of plants whose leaves had been attacked by larvae of the moth Spodoptera littoralis. Fittingly, D similar to virgifera larvae were attracted to plants that were infested with conspecifics, whereas they avoided plants that were attacked by S similar to littoralis. We identified (E)-beta-caryophyllene, which is induced by D similar to virgifera, and ethylene, which is suppressed by S similar to littoralis, as two signals used by D similar to virgifera larvae to locate plants that are most suitable for their development. Our study demonstrates that soil-dwelling insects can use herbivore-induced changes in root volatile emissions to identify suitable host plants.
  • Publication
    Métadonnées seulement
    Induction of root-resistance by leaf-herbivory follows a vertical gradient
    (2011) ;
    Robert, Christelle Aurélie Maud
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    Leaf-herbivory can lead to systemic changes in root metabolism and resistance. As yet, it is unknown if these changes affect the whole root system, or if they are more pronounced in the upper root parts, which are closer to the actual site of attack. As this spatial aspect may be an important determinant of the interactions that can be expected to occur within the rhizosphere, we investigated if leaf-herbivore induced root resistance differs between upper and lower roots of maize. We also tested if the density of leaf-herbivores correlates with intensity of the root response. The systemic increase in resistance was found to be more pronounced in the upper than the lower roots and was independent of leaf herbivore density. The results suggest that there is a vertical gradient in the strength of the root response following leaf-herbivory, and that soil organisms living closer to the surface may be more affected by leaf-attack than the ones living in deeper soil layers.
  • Publication
    Accès libre
    Synergies and trade-offs between insect and pathogen resistance in maize leaves and roots
    (2011) ;
    Balmer, Yves
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    de Lange, Elvira S.
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    von Merey, Georg
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    Robert, Christelle Aurélie Maud
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    Sobhy, Islam
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    Determining links between plant defence strategies is important to understand plant evolution and to optimize crop breeding strategies. Although several examples of synergies and trade-offs between defence traits are known for plants that are under attack by multiple organisms, few studies have attempted to measure correlations of defensive strategies using specific single attackers. Such links are hard to detect in natural populations because they are inherently confounded by the evolutionary history of different ecotypes. We therefore used a range of 20 maize inbred lines with considerable differences in resistance traits to determine if correlations exist between leaf and root resistance against pathogens and insects. Aboveground resistance against insects was positively correlated with the plant's capacity to produce volatiles in response to insect attack. Resistance to herbivores and resistance to a pathogen, on the other hand, were negatively correlated. Our results also give first insights into the intraspecific variability of root volatiles release in maize and its positive correlation with leaf volatile production. We show that the breeding history of the different genotypes (dent versus flint) has influenced several defensive parameters. Taken together, our study demonstrates the importance of genetically determined synergies and trade-offs for plant resistance against insects and pathogens.
  • Publication
    Accès libre
    Systemic root signalling in a belowground, volatile-mediated tritrophic interaction
    (2011) ; ;
    Robert, Christelle Aurélie Maud
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    Plants attacked by leaf herbivores release volatile organic compounds (VOCs) both locally from the wounded site and systemically from non-attacked tissues. These volatiles serve as attractants for predators and parasitoids. This phenomenon is well described for plant leaves, but systemic induction of VOCs in the roots has remained unstudied. We assessed the spatial and temporal activation of the synthesis and release of (E)-β-caryophyllene (EβC) in maize roots upon feeding by larvae of Diabrotica virgifera virgifera, as well as the importance of systemically produced EβC for the attraction of the entomopathogenic nematode Heterorhabditis megidis. The production of EβC was found to be significantly stronger at the site of attack than in non-attacked tissues. A weak, but significant, increase in transcriptional activity of the EβC synthase gene tps23 and a corresponding increase in EβC content were observed in the roots above the feeding site and in adjacent roots, demonstrating for the first time that herbivory triggers systemic production of a volatile within root systems. In belowground olfactometers, the nematodes were significantly more attracted towards local feeding sites than systemically induced roots. The possible advantages and disadvantages of systemic volatile signalling in roots are discussed.