Herbivore attack is known to increase the emission of volatiles, which attract predators to herbivore-damaged plants in the laboratory and agricultural systems. We quantified volatile emissions from Nicotiana attenuata plants growing in natural populations during attack by three species of leaf-feeding herbivores and mimicked the release of five commonly emitted volatiles individually. Three compounds ( cis-3 -hexen-1-ol, linalool, and cis -α-bergamotene) increased egg predation rates by a generalist predator; linalool and the complete blend decreased lepidopteran oviposition rates. As a consequence, a plant could reduce the number of herbivores by more than 90% by releasing volatiles. These results confirm that indirect defenses can operate in nature.

▪ Abstract Plants respond to herbivore attack with a bewildering array of responses, broadly categorized as direct and indirect defenses, and tolerance. Plant-herbivore interactions are played out on spatial scales that include the cellular responses, well-studied in plant-pathogen interactions, as well as responses that function at whole-plant and community levels. The plant's wound response plays a central role but is frequently altered by insect-specific elicitors, giving plants the potential to optimize their defenses. In this review, we emphasize studies that advance the molecular understanding of elicited direct and indirect defenses and include verifications with insect bioassays. Large-scale transcriptional changes accompany insect-induced resistance, which is organized into specific temporal and spatial patterns and points to the existence of herbivore-specific trans-activating elements orchestrating the responses. Such organizational elements could help elucidate the molecular control over the diversity of responses elicited by herbivore attack.

We transformed the native tobacco, Nicotiana attenuata , to silence its lipoxygenase, hydroperoxide lyase, and allene oxide synthase genes in order to inhibit oxylipin signaling, known to mediate the plant's direct and indirect defenses. When planted into native habitats, lipoxygenase-deficient plants were more vulnerable to N. attenuata 's adapted herbivores but also attracted novel herbivore species, which fed and reproduced successfully. In addition to highlighting the value of genetically silencing plants to study ecological interactions in nature, these results show that lipoxygenase-dependent signaling determines host selection for opportunistic herbivores and that induced defenses influence herbivore community composition.

A recent surge in attention devoted to the ecology of soil biota has prompted interest in quantifying similarities and differences between interactions occurring in above‐ and belowground communities. Furthermore, linkages that interconnect the dynamics of these two spatially distinct ecosystems are increasingly documented. We use a similar approach in the context of understanding plant defenses to herbivory, including how they are allocated between leaves and roots (constitutive defenses), and potential cross‐system linkages (induced defenses). To explore these issues we utilized three different empirical approaches. First, we manipulated foliar and root herbivory on tobacco (Nicotiana tabacum) and measured changes in the secondary chemistry of above‐ and belowground tissues. Second, we reviewed published studies that compared levels of secondary chemistry between leaves and roots to determine how plants distribute putative defense chemicals across the above‐ and belowground systems. Last, we used meta‐analysis to quantify the impact of induced responses across plant tissue types. In the tobacco system, leaf‐chewing insects strongly induced higher levels of secondary metabolites in leaves but had no impact on root chemistry. Nematode root herbivores, however, elicited changes in both leaves and roots. Virtually all secondary chemicals measured were elevated in nematode‐induced galls, whereas the impact of root herbivory on foliar chemistry was highly variable and depended on where chemicals were produced within the plant. Importantly, nematodes interfered with aboveground metabolites that have biosynthetic sites located in roots (e.g., nicotine) but had the opposite effect (i.e., nematodes elevated foliar expression) on chemicals produced in shoots (e.g., phenolics and terpenoids). Results from our literature review suggest that, overall, constitutive defense levels are extremely similar when comparing leaves with roots, although certain chemical classes (e.g., alkaloids, glucosinolates) are differentially allocated between above‐ and belowground parts. Based on a meta‐analysis of induced defense studies we conclude that: (1) foliar induction generates strong responses in leaves, but much weaker responses in roots, and (2) root induction elicits responses of equal magnitude in both leaves and roots. We discuss the importance of this asymmetry and the paradox of cross‐system induction in relation to optimal defense theory and interactions between above‐ and belowground herbivory.