Herbivorous insects use diverse feeding strategies to obtain nutrients from their host plants. Rather than acting as passive victims in these interactions, plants respond to herbivory with the production of toxins and defensive proteins that target physiological processes in the insect. Herbivore-challenged plants also emit volatiles that attract insect predators and bolster resistance to future threats. This highly dynamic form of immunity is initiated by the recognition of insect oral secretions and signals from injured plant cells. These initial cues are transmitted within the plant by signal transduction pathways that include calcium ion fluxes, phosphorylation cascades, and, in particular, the jasmonate pathway, which plays a central and conserved role in promoting resistance to a broad spectrum of insects. A detailed understanding of plant immunity to arthropod herbivores will provide new insights into basic mechanisms of chemical communication and plant-animal coevolution and may also facilitate new approaches to crop protection and improvement.

Rapid, long-distance signaling in plants: A plant injured on one leaf by a nibbling insect can alert its other leaves to begin anticipatory defense responses. Working in the model plant Arabidopsis , Toyota et al. show that this systemic signal begins with the release of glutamate, which is perceived by glutamate receptor–like ion channels (see the Perspective by Muday and Brown-Harding). The ion channels then set off a cascade of changes in calcium ion concentration that propagate through the phloem vasculature and through intercellular channels called plasmodesmata. This glutamate-based long-distance signaling is rapid: Within minutes, an undamaged leaf can respond to the fate of a distant leaf. Science , this issue p. 1112 ; see also p. 1068

Jasmonate (JA) is a lipid-derived hormone that regulates diverse aspects of plant immunity and development. An amino acid-conjugated form of JA, jasmonoyl–isoleucine (JA–Ile), stimulates binding of the F-box protein coronatine-insensitive 1 (COI1) to, and subsequent ubiquitin-dependent degradation of, jasmonate ZIM domain (JAZ) proteins that repress transcription of JA-responsive genes. The virulence factor coronatine (COR), which is produced by plant pathogenic strains of Pseudomonas syringae , suppresses host defense responses by activating JA signaling in a COI1-dependent manner. Although previous data indicate that COR acts as a molecular mimic of JA–Ile, the mechanism by which JA–Ile and COR are perceived by plant cells remains unknown. Here, we show that interaction of tomato COI1 with divergent members of the JAZ family is highly specific for JA–Ile and structurally related JA conjugates and that COR is ≈1,000-fold more active than JA–Ile in promoting this interaction in vitro . JA–Ile competes for binding of COR to COI1–JAZ complexes, demonstrating that COR and JA–Ile are recognized by the same receptor. Binding of COR to the COI1–JAZ complex requires COI1 and is severely impaired by a point mutation in the putative ligand-binding pocket of COI1. Finally, we show that the C-terminal region of JAZ3 containing the highly conserved Jas motif is necessary and sufficient for hormone-induced COI1–JAZ interaction. These findings demonstrate that COI1 is a critical component of the JA receptor and that COR exerts its virulence effects by functioning as a potent agonist of this receptor system.

The plant hormone jasmonate coordinates immune and growth responses to increase plant survival in unpredictable environments. The core jasmonate signaling pathway comprises several functional modules, including a repertoire of COI1–JAZ (CORONATINE INSENSITIVE1–JASMONATE-ZIM DOMAIN) coreceptors that couple jasmonoyl-l-isoleucine perception to the degradation of JAZ repressors, JAZ-interacting transcription factors that execute physiological responses, and multiple negative feedback loops to ensure timely termination of these responses. Here, we review the jasmonate signaling pathway with an emphasis on understanding how transcriptional responses are specific, tunable, and evolvable. We explore emerging evidence that JAZ proteins integrate multiple informational cues and mediate crosstalk by propagating changes in protein–protein interaction networks. We also discuss recent insights into the evolution of jasmonate signaling and highlight how plant-associated organisms manipulate the pathway to subvert host immunity. Finally, we consider how this mechanistic foundation can accelerate the rational design of jasmonate signaling for improving crop resilience and harnessing the wellspring of specialized plant metabolites.

Jasmonic acid (JA) is a fatty acid–derived signaling molecule that regulates a broad range of plant defense responses against herbivores and some microbial pathogens. Molecular genetic studies in Arabidopsis have established that JA also performs a critical role in anther and pollen development but is not essential for other developmental aspects of the plant's life cycle. Here, we describe the phenotypic and molecular characterization of a sterile mutant of tomato (jasmonic acid–insensitive1 [jai1]) that is defective in JA signaling. Although the mutant exhibited reduced pollen viability, sterility was caused by a defect in the maternal control of seed maturation, which was associated with the loss of accumulation of JA-regulated proteinase inhibitor proteins in reproductive tissues. jai1 plants exhibited several defense-related phenotypes, including the inability to express JA-responsive genes, severely compromised resistance to two-spotted spider mites, and abnormal development of glandular trichomes. We demonstrate that these defects are caused by the loss of function of the tomato homolog of CORONATINE-INSENSITIVE1 (COI1), an F-box protein that is required for JA-signaled processes in Arabidopsis. These findings indicate that the JA/COI1 signaling pathway regulates distinct developmental processes in different plants and suggest a role for JA in the promotion of glandular trichome–based defenses.

Jasmonate (JA) and its amino acid conjugate, jasmonoyl-isoleucine (JA-Ile), play important roles in regulating plant defense responses to insect herbivores. Recent studies indicate that JA-Ile promotes the degradation of JASMONATE ZIM-domain (JAZ) transcriptional repressors through the activity of the E₃ ubiquitin-ligase SCF^COI1. Here, we investigated the regulation and function of JAZ genes during the interaction of Arabidopsis (Arabidopsis thaliana) with the generalist herbivore Spodoptera exigua. Most members of the JAZ gene family were highly expressed in response to S. exigua feeding and mechanical wounding. JAZ transcript levels increased within 5 min of mechanical tissue damage, coincident with a large (approximately 25-fold) rise in JA and JA-Ile levels. Wound-induced expression of JAZ and other CORONATINE-INSENSITIVE1 (COI1)-dependent genes was not impaired in the jar1-1 mutant that is partially deficient in the conversion of JA to JA-Ile. Experiments performed with the protein synthesis inhibitor cycloheximide provided evidence that JAZs, MYC2, and genes encoding several JA biosynthetic enzymes are primary response genes whose expression is derepressed upon COI1-dependent turnover of a labile repressor protein(s). We also show that overexpression of a modified form of JAZ1 (JAZ1Δ3A) that is stable in the presence of JA compromises host resistance to feeding by S. exigua larvae. These findings establish a role for JAZ proteins in the regulation of plant anti-insect defense, and support the hypothesis that JA-Ile and perhaps other JA derivatives activate COI1-dependent wound responses in Arabidopsis. Our results also indicate that the timing of JA-induced transcription in response to wounding is more rapid than previously realized.