Modification of plant resistance and metabolism by above- and belowground herbivores

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 <i>vice versa</i>. This thesis investigates how shoots of maize plants respond to root attack by lavae of the beetle <i>Diabrotica virgifera</i> and <i>vice versa</i>, how roots react to shoot attack by <i>Spodoptera littoralis</i> 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 <i>D. virgifera</i> 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 <i>D. virgifera</i>. 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 <i>Setosphaeria turcica</i> and the herbivore <i>S. littoralis</i> in the laboratory, as well as against lepidopteran pests in the field, demonstrating that <i>D. virgifera</i> has an ecologically important impact on aboveground interactions. While the observed ABA response can explain the reduction of <i>S. turcica</i> growth in the leaves (chapter 2), <i>S. littoralis</i> was negatively affected by the reduction of leaf-water contents (chapter 3). Shoot herbivory by <i>S. littoralis</i> 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. <i>S. littoralis</i> had a strong impact on root protein biosynthesis, a novel finding that demands further attention. The strong effect of <i>S. littoralis</i> infestation on root physiology was reflected in a dramatically increased resistance of attacked maize plants against <i>D. virgifera</i>. 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.

Thèse de doctorat : Université de Neuchâtel, 2009 ; Th. 2084