Plant interactions with arthropod herbivores: state of the field.

Interactions between plants and their arthropod herbivores dominate the terrestrial ecology of our planet. The survival of an estimated one million or more phytophagous insect species depends on plants as a source of food. Plant-eating arthropods employ sophisticated feeding strategies to obtain nutrients from all aboveground and belowground plant parts. Rather than being passive victims in these interactions, plants cope with herbivory through the production of myriad specialized metabolites and proteins that exert toxic, repellent, or antinutritive effects on their animal attackers (see Zhu-Salzman et al., 2008). The coevolutionary struggle between arthropod herbivores and plants to consume or not to be consumed, respectively, has shaped not only the extraordinary diversity of plant metabolism, but also the genetic diversity of plants. The central role of plant chemicals in mediating interactions with arthropod herbivores has attracted the attention of insect physiologists and population ecologists for more than 50 years (see Berenbaum and Zangerl, 2008). Widespread interest in this field among plant biologists, however, can be traced back to 1972, when Clarence ‘‘Bud’’ Ryan (Fig. 1) and colleagues at Washington State University reported that insect feeding on potato and tomato plants activates local and systemic expression of proteinase inhibitors that disrupt the activity of digestive proteases in the insect gut (Green and Ryan, 1972). This seminal discovery was instrumental in establishing the paradigm that plant defense responses to herbivore attack are rapid and highly dynamic. The general theme of induced resistance runs through much, if not most, plant-insect interaction research published in Plant Physiology. Remarkable progress in understanding plant relations with arthropod herbivores has been achieved in the recent past; these advances were the genesis of this Focus Issue. Plant-herbivore interaction research is arguably one of the most multidisciplinary endeavors in plant biology. Like all research concerned with inter-species relationships, numerous disciplines are required to accurately describe the range of chemical and ecological processes that influence the outcome of plantherbivore interactions. A defining aspect of the field has been its focus on animals as the ‘‘other organism.’’ The complexity of animal behavior, together with the technical difficulties associated with genetic manipulation of plant-eating animals, poses unique but not insurmountable challenges. As discussed in Updates by Zheng and Dicke (2008) and by Schwachtje and Baldwin (2008), an important research trend is the use of plant-insect systems to address questions of ecological relevance. The merging of molecular and ecological disciplines offers a powerful approach to understand gene function and evolution in an ecological context. Much of contemporary plant-herbivore interaction research is focused on understanding the molecular mechanisms and ecological consequences of induced plant responses to herbivory. In their Update, Mithöfer and Boland (2008) discuss the early signaling events at the plant-herbivore interface. Wu et al. (2008) show that there can be significant within-species differences in these early signaling responses. Frost et al. (2008) describe molecular and ecological aspects of defense ‘‘priming,’’ which has become an important area of research. In her Update, Walling (2008) describes various mechanisms by which insects evade host defense responses, thereby highlighting the co-evolutionary nature of plant-herbivore relations. It is now clear that the jasmonate (JA) family of lipidderived signals plays a prominent and conserved role in promoting plant resistance to herbivores. Browse and Howe (2008) discuss these roles, as well as recent progress in elucidating the mechanism of JA signaling. One notable recent discovery is that an amino acidconjugated form of JA, JA-Ile, is a bioactive signal for defense responses and a potential ligand for the JA receptor. An article by Wang et al. (2008) indicates that JA and JA-Ile serve distinct (but overlapping) roles in defense. Chung et al. (2008) show that the levels of both JA and JA-Ile increase within 5 min of mechanical tissue damage, and provide genetic evidence that the JAZ proteins, which negatively regulate JA responses, play a role in regulating host plant resistance to herbivory. An article by Arimura et al. (2008) shows that the temporal pattern of leaf damage plays a critical role in the emission of plant volatiles that attract natural enemies of the herbivore, and that JA is likely involved in the control of this response. Lin et al. (2008) in this issue show how genome duplication allowed neofunctionalization of a terpene synthase that contributes to herbivore-induced volatile release. In an article by Jassbi et al. (2008), direct antifeedant effects of diterpenoids are demonstrated through insect bioassays involving plants that are silenced in the expression of these compounds. Koornneef and Pieterse (2008) discuss recent progress in our understanding of how JA and other signaling pathways influence the outcome of plant-pest interactions. The phenomenon of signal cross talk in plant biology has gained increased attention as scientists seek to understand how plants respond to simultaneous attack by multiple herbivores and pathogens. A novel example www.plantphysiol.org/cgi/doi/10.1104/pp.104.900247