Jasmonate signaling: a conserved mechanism of hormone sensing

Abstract

The lipid-derived hormone jasmonate (JA) regulates diverse aspects of plant immunity and development. Among the central components of the JA signaling cascade are the E3 ubiquitin ligase SCFCOI1 and Jasmonate ZIM-domain (JAZ) proteins that repress transcription of JA-responsive genes. Recent studies provide evidence that amino acid-conjugated forms of JA initiate signal transduction upon formation of a coronatine-insensitive1 (COI1)-JA-JAZ ternary complex in which JAZs are ubiquitinated and subsequently degraded. Coronatine, a virulence factor produced by the plant pathogen Pseudomonas syringae, is a potent agonist of this hormone receptor system. Coronatine-induced targeting of JAZs to COI1 obstructs host immune responses to P. syrinage, providing a striking example of how pathogens exploit hormone signaling pathways in the host to promote disease. These findings, together with homology between COI1 and the auxin receptor, TIR1, extend the paradigm of F-box proteins as intracellular sensors of small molecules, and suggest a common evolutionary origin of the auxin and JA response pathways.

Figure 1. Model of JA signal transduction

In plant cells containing low JA levels, JA-responsive genes are repressed (OFF) by JAZ proteins (denoted with their ZIM and Jas motifs) that restrain the activity of transcription factors (TF; e.g., MYC2) involved in the expression of early response genes. The transition from the repressed to the active (ON) state of gene expression is initiated by developmental or environmental cues (e.g., biotic stress) that increase the accumulation of bioactive JAs (orange oval; see Box 1). COI1 is an F-box protein that determines the substrate specificity of the SCF-type E₃ ubiquitin ligase, SCF^COI1 (blue oval). Bioactive JAs, such as JA-Ile, are proposed to bind to the LRR domain of COI1. Interaction of JAZs with ligand-bound COI1 leads to the formation of a COI1-ligand-JAZ ternary complex in which JAZs are polyubiquitinated (filled black circles) and subsequently degraded by the 26S proteasome (26S). Signaling is attenuated by metabolism of bioactive JAs to inactive forms of the hormone (orange hexagon), as well as by JA-induced de novo JAZ synthesis. Some plant pathogenic strains of Pseudomonas syringae produce a virulence factor called coronatine (purple oval) that is structurally similar to JA-Ile (Box 1). High-affinity binding of coronatine to COI1-JAZ complexes promotes proteolytic destruction of JAZs. Direct binding of JA-Ile or COR to COI1 in the absence of JAZ has not yet been demonstrated, and thus it is possible that COI1 and JAZ function as coreceptors. The model predicts that coi1 mutants fail to respond to JA and coronatine because JAZ proteins are not degraded in the presence of these signals.

Figure 2. The JAZ protein family in Arabidopsis

The phylogeny includes JAZ and PEAPOD (PPD) proteins, which are members of the larger family of TIFY proteins that is defined by the TIF[F/Y]XG motif in the ZIM domain (red bar). JAZs are distinguished from other TIFY proteins by the presence of the C-terminally located Jas motif, SLX₂FX₂KRX₂RX₅PY (dark blue bar). PPD proteins contain a modified Jas motif (light blue bar) that lacks several invariant residues of the motif (Fig. S1, Supplemental material). The relative size of each protein and the position of the conserved motifs are drawn to scale.

Figure 3. Homology model of COI1

The x-ray crystal structure of TIR1 (a) [50**] was used as a template to construct a homology model of COI1 (b) with the program SWISS-MODEL. Images were rendered using PyMol software. The positions of the IP₆ co-factor and auxin in the TIR structure are indicated.

Figure 3. Homology model of COI1

The x-ray crystal structure of TIR1 (a) [50**] was used as a template to construct a homology model of COI1 (b) with the program SWISS-MODEL. Images were rendered using PyMol software. The positions of the IP₆ co-factor and auxin in the TIR structure are indicated.