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  • Publication
    Accès libre
    The role of abscisic acid and water stress in root herbivore-induced leaf resistance
    (2011) ;
    Köllner, Tobias G.
    ;
    Degenhardt, Jörg
    ;
    ;
    Hibbard, Bruce E.
    ;

    Herbivore-induced systemic resistance occurs in many plants and is commonly assumed to be adaptive. The mechanisms triggered by leaf-herbivores that lead to systemic resistance are largely understood, but it remains unknown how and why root herbivory also increases resistance in leaves.
    To resolve this, we investigated the mechanism by which the root herbivore Diabrotica virgifera induces resistance against lepidopteran herbivores in the leaves of Zea mays.
    Diabrotica virgifera infested plants suffered less aboveground herbivory in the field and showed reduced growth of Spodoptera littoralis caterpillars in the laboratory. Root herbivory did not lead to a jasmonate-dependent response in the leaves, but specifically triggered water loss and abscisic acid (ABA) accumulation. The induction of ABA by itself was partly responsible for the induction of leaf defenses, but not for the resistance against S. littoralis. Root-herbivore induced hydraulic changes in the leaves, however, were crucial for the increase in insect resistance.
    We conclude that the induced leaf resistance after root feeding is the result of hydraulic changes, which reduce the quality of the leaves for chewing herbivores. This finding calls into question whether root-herbivore induced leaf-resistance is an evolved response.
  • Publication
    Accès libre
    Sequence of arrival determines plant-mediated interactions between herbivores
    (2011) ;
    Robert, Christelle Aurélie Maud
    ;
    Hibbard, Bruce E.
    ;

    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
    Accès libre
    Modification of plant resistance and metabolism by above- and belowground herbivores
    (2009) ;
    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
    Accès libre
    Signal signature of aboveground-induced resistance upon belowground herbivory in maize
    (2009) ; ;
    Karlen, Danielle
    ;
    de Lange, Elvira S.
    ;
    ;
    D’Alessandro, Marco
    ;
    ;
    Ton, Jurriaan
    Plants activate local and systemic defence mechanisms upon exposure to stress. This innate immune response is partially regulated by plant hormones, and involves the accumulation of defensive metabolites. Although local defence reactions to herbivores are well studied, less is known about the impact of root herbivory on shoot defence. Here, we examined the effects of belowground infestation by the western corn rootworm Diabrotica virgifera virgifera on aboveground resistance in maize. Belowground herbivory by D. v. virgifera induced aboveground resistance against the generalist herbivore Spodoptera littoralis, and the necrotrophic pathogen Setosphaeria turcica. Furthermore, D. v. virgifera increased shoot levels of 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one (DIMBOA), and primed the induction of chlorogenic acid upon subsequent infestation by S. littoralis. To gain insight into the signalling network behind this below- and aboveground defence interaction, we compiled a set of 32 defence-related genes, which can be used as transcriptional marker systems to detect activities of different hormone-response pathways. Belowground attack by D. v. virgifera triggered an ABA-inducible transcription pattern in the shoot. The quantification of defence hormones showed a local increase in the production of oxylipins after root and shoot infestation by D. v. virgifera and S. littoralis, respectively. On the other hand, ABA accumulated locally and systemically upon belowground attack by D. v. virgifera. Furthermore, D. v. virgifera reduced the aboveground water content, whereas the removal of similar quantities of root biomass had no effect. Our study shows that root herbivory by D. v. virgifera specifically alters the aboveground defence status of a maize, and suggests that ABA plays a role in the signalling network mediating this interaction.