Comparisons of LIPOXYGENASE3- and JASMONATE-RESISTANT4/6-Silenced Plants Reveal That Jasmonic Acid and Jasmonic Acid-Amino Acid Conjugates Play Different Roles in Herbivore Resistance of Nicotiana attenuata    

Abstract

Whereas jasmonic acid (JA) and its amino acid conjugates, particularly JA-isoleucine (Ile), are known to play important roles in plant-herbivore interactions, whether other compounds also function as signals independently of JA-Ile and whether conjugates elicit systemic responses are unknown. To answer these questions, we simultaneously silenced JASMONATE-RESISTANT4 (JAR4) and JAR6, two functionally redundant enzymes in Nicotiana attenuata that conjugate JA to amino acids to produce plants (irjar4/6) with low levels of JA-Ile, JA-leucine (Leu), and JA-valine (Val; ,16% of wild type). As expected, irjar4/6 plants are more vulnerable to herbivore attack, but only JA-Ile-not JA-Leu or JA-Val-applications restored the resistance of irjar4/6 plants, suggesting that JA-Leu and JA-Val do not mediate herbivore defense responses. Interestingly, the direct defense traits of irjar4/6 plants are significantly higher than those in LIPOXYGENASE3 (LOX3)-silenced (aslox3) plants, which are impaired in JA biosynthesis, and JA-Ile treatment could not fully restore the resistance of aslox3 plants. We thus conclude that JA, its precursors, or other metabolites complement the function of JA-Ile by eliciting a panoply of induced defenses. Similarly, transcriptional profiling of wild-type, irjar4/6, and aslox3 plants with microarrays demonstrated that JA-Ile and JA play overlapping yet distinct roles in herbivore defense. Analysis of transcripts in distal tissues demonstrated that JAR activity is essential in eliciting systemic responses. However, attempts to recover JA-13 C 6 -Ile in systemic leaves and roots after feeding wounded leaves with 13 C 6 -Ile were unsuccessful, suggesting that JA-Ile is not a long-distance signal, but is rather synthesized after the arrival of an unknown mobile signal to systemic tissues.

Role of NINJA in root jasmonate signaling

“…A similar intermediate phenotype was observed in Nicotiana attenuata lines silenced in JAR1 homologs (24), and it correlates with our observation that wound-induced JAZ10 transcription was decreased but still present in aerial tissues of jar1-1 and jar1-13 (Fig. 2B).…”

COI1 is a critical component of a receptor for jasmonate and the bacterial virulence factor coronatine

“…It is noteworthy that JA-Val, whose synthesis is catalyzed by JAR1-like enzymes (14,32), was as active as JA-Ile in stimulating COI1 binding to JAZ3. This finding indicates that JA-Val may function as an endogenous signal for COI1-dependent responses, particularly in tissues that contain high JA-Val levels.…”

Plant Interactions with Arthropod Herbivores: State of the Field

“…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.…”