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

TLDR

Jasmonate signaling in plants relies on the F‑box protein COI1 binding jasmonoyl‑isoleucine to target JAZ repressors for degradation, and the bacterial toxin coronatine mimics this hormone to suppress immunity, but the exact perception mechanism was previously unknown. We show that COI1 specifically recognizes JA‑Ile and related conjugates, that coronatine is ~1,000‑fold more potent, competes for the same binding site, requires COI1 and a conserved Jas motif in JAZ3, thereby establishing COI1 as the essential JA receptor and coronatine as a potent agonist.

Abstract

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.