SummaryUpon herbivore attack, plants activate an indirect defense, that is, the release of a complex mixture of volatiles that attract natural enemies of the herbivore. When plants are simultaneously exposed to two herbivore species belonging to different feeding guilds, one herbivore may interfere with the indirect plant defense induced by the other herbivore. However, little is understood about the mechanisms underlying such interference.Here, we address the effect of herbivory by the phloem-feeding whitefly Bemisia tabaci on the induced indirect defense of Arabidopsis thaliana plants to Plutella xylostella caterpillars, that is, the attraction of the parasitoid wasp Diadegma semiclausum.Assays with various Arabidopsis mutants reveal that B. tabaci infestation interferes with indirect plant defense induced by P. xylostella, and that intact jasmonic acid and ethylene signaling are required for such interference caused by B. tabaci. Chemical analysis of plant volatiles showed that the composition of the blend emitted in response to the caterpillars was significantly altered by co-infestation with whiteflies. Moreover, whitefly infestation also had a considerable effect on the transcriptomic response of the plant to the caterpillars.Understanding the mechanisms underlying a plant's responses to multiple attackers will be important for the development of crop protection strategies in a multi-attacker context.

To study whether natural variation in Arabidopsis thaliana could be used to dissect the genetic basis of responses to herbivory in terms of induced volatile emissions, nine accessions were characterized upon herbivory by biting-chewing Pieris rapae caterpillars or after treatment with the phytohormone jasmonic acid (JA). Analysis of 73 compounds in the headspace showed quantitative differences in the emission rates of several individual compounds among the accessions. Moreover, variation in the emission of volatile compounds after JA treatment was reflected in the behaviour of the parasitoid Diadegma semiclausum when they were offered the headspace volatiles of several combinations of accessions in two-choice experiments. Accessions also differ in transcript levels of genes that are associated with the emission of plant volatiles. The genes BSMT1 and Cyp72A13 could be connected to the emission of methyl salicylate and (E,E)-4,8,12-trimethyltrideca-1,3,7,11-tetraene (TMTT), respectively. Overall, Arabidopsis showed interesting phenotypic variations with respect to the volatile blend emitted in response to herbivory that can be exploited to identify genes and alleles that underlie this important plant trait.

SummaryHerbivorous insects are widespread and often serious constraints to crop production. The use of insect-resistant crops is a very effective way to control insect pests in agriculture, and the development of such crops can be greatly enhanced by knowledge on plant resistance mechanisms and the genes involved. Plants have evolved diverse ways to cope with insect attack that has resulted in natural variation for resistance towards herbivorous insects. Studying the molecular genetics and transcriptional background of this variation has facilitated the identification of resistance genes and processes that lead to resistance against insects. With the development of new technologies, molecular studies are not restricted to model plants anymore. This review addresses the need to exploit natural variation in resistance towards insects to increase our knowledge on resistance mechanisms and the genes involved. We will discuss how this knowledge can be exploited in breeding programmes to provide sustainable crop protection against insect pests. Additionally, we discuss the current status of genetic research on insect-resistance genes. We conclude that insect-resistance mechanisms are still unclear at the molecular level and that exploiting natural variation with novel technologies will contribute greatly to the development of insect-resistant crop varieties.

The indirect defense mechanisms of plants comprise the production of herbivore-induced plant volatiles that can attract natural enemies of plant attackers. One of the often emitted compounds after herbivory is methyl salicylate (MeSA). Here, we studied the importance of this caterpillar-induced compound in the attraction of the parasitoid wasp Diadegma semiclausum by using a mutant Arabidopsis line. Pieris rapae infested AtBSMT1-KO mutant Arabidopsis plants, compromised in the biosynthesis of MeSA, were more attractive to parasitoids than infested wild-type plants. This suggests that the presence of MeSA has negative effects on parasitoid host-finding behavior when exposed to wild-type production of herbivore-induced Arabidopsis volatiles. Furthermore, in line with this, we recorded a positive correlation between MeSA dose and repellence of D. semiclausum when supplementing the headspace of caterpillar-infested AtBSMT1-KO plants with synthetic MeSA.Electronic supplementary materialThe online version of this article (doi:10.1007/s10886-010-9787-1) contains supplementary material, which is available to authorized users.

Communities are riddled with indirect species interactions and these interactions can be modified by organisms that are parasitic or symbiotic with one of the indirectly interacting species. By inducing plant responses, herbivores are well known to alter the plant quality for subsequent feeders. The reduced performance of herbivores on induced plants cascades into effects on the performance of higher trophic level organisms such as parasitoids that develop inside herbivores. Parasitoids themselves may also, indirectly, interact with the host plant by affecting the behaviour and physiology of their herbivorous host. Here, we show that, through their herbivorous host, larvae of two parasitoid species differentially affect plant phenotypes leading to asymmetric interactions among parasitoid larvae developing in different hosts that feed on the same plant. Our results show that temporally separated parasitoid larvae are involved in indirect plant-mediated interactions by a network of trophic and non-trophic relationships.