Emerging complexity: jasmonate-induced volatiles affect parasitoid choice

Plant responses to specific environmental stimuli at the molecular and genetic levels have been widely reported in recent decades, mainly as a consequence of the availability of new laboratory techniques. However, understanding the complex implications of these observations at the ecosystem level remains one of the greatest challenges facing plant science today. Recently, new experimental strategies have been designed to address complex interactions. For example, combinations of different insects have been used to study insect–plant interactions (Dicke et al., 2009) as well as parallel analysis of the responses to different types of pathogen which reflect more closely the conditions encountered in natural ecosystems (Pieterse et al., 2009). In this issue, the two papers by Bruinsma and colleagues also address such complex issues; the detailed analysis of plant responses to different herbivores and JA application are documented, and the responses of parasitic wasps that attack the herbivores are recorded. The authors’ experimental design and interpretation of the results highlight the importance of understanding the complexity of plant responses in the context of a whole ecosystem. In the last two decades, interest in plant–insect interactions using ecological, chemical, and molecular approaches has increased dramatically. Direct defence reactions of plants, such as the production of toxins or deterrent proteins like proteinase inhibitors, as well as indirect defence reactions, have been identified showing that the effectiveness of the natural enemies of attackers can be altered. In the latter case, the induced release of volatiles is a common phenomenon leading to the attraction of carnivores. Plants attacked by herbivores respond with the establishment of a chemical phenotype, releasing volatiles into the atmosphere that include terpenoids, phenylpropanoids or fatty acid-derived green leaf volatiles. The detailed composition of the volatile blend is insect-specific and depends on the type of attacker (e.g. chewing or sucking insects) and on their oral secretions released at the wound site of the plant. Moreover, the plant responses are different depending on whether the organs under attack are above or below ground. One basic question when analysing plant responses is what underlying mechanism leads to the expression of genes encoding the enzymes in volatile biosynthesis and the formation of deterrent proteins. A well-known signalling compound active in plant responses to wounding by herbivores, such as caterpillars, is jasmonic acid (JA) (Kessler and Baldwin, 2002). JA is known to regulate many plant responses to biotic and abiotic stresses and is active in the regulation of plant development (Wasternack, 2007). The challenge of present day studies is in understanding a plant’s responses to multiple attackers, for example, by analysing the responses in terms of volatile production and/or the attraction of parasitoids in a doubleattacker (e.g. aboveand below ground) context (Dicke et al., 2009; Poelman et al., 2008). The papers by Bruinsma et al. (2009a, b), founded on the long-term experience of the senior author’s laboratory in the analysis of tritrophic interactions, demonstrate a role for herbivore-induced plant volatiles in the attraction of the natural enemies of those herbivores. As a model plant, Brussels sprout, Brassica oleracea L. var. gemmifera, was used. Caterpillar-infested Brussels sprout plants attracted parasitoids such as Diadegma semiclausum and several Cotesia spp. within one hour of infestation. The experimental design was established with three species of parasitoids, Cotesia rubecula, C. glomerata, and D. semiclausum, which differ in their host range and specificity. Hosts of these parasitoids are Pieris sp. (cabbage white butterfly) or Plutella xylostella (diamondback moth) caterpillars, respectively. The aim of the work was to determine the preference of parasitoids for volatiles from JA-treated, herbivoreinfested or control plants in terms of time, dose effects, volatile blend, and levels of JA and its precursor 12oxophytodienoic acid (OPDA). Interestingly, in a comparison with untreated plants, the three parasitoids preferred plants emitting volatiles induced by JA-treatment, but, in the case of specific choice experiments between the JAtreated plants and herbivore-infested plants, they preferred the latter. This preference was timeand dose-dependent (Bruinsma et al., 2009b). As expected, herbivore attack led to an increase in JA levels. However, this increase was not accompanied by a concomitant increase in OPDA levels after Plutella xylostella attack, whereas attack by Pieris rapae (small cabbage white) increased the levels of both compounds. This is intriguing and of specific importance for the composition of the volatile blend. There are an