Tracing the Evolutionary Origins of Jasmonate Signaling: Co-Evolution of Oxylipin Metabolism and Hormone Perception in the Green Lineage.

Abstract

Jasmonates constitute a central class of lipid-derived signaling molecules that regulate plant defense, development, and environmental adaptation. Although jasmonic acid (JA) and its bioactive conjugate jasmonoyl-L-isoleucine (JA-Ile) are well characterized in angiosperms, recent evolutionary, biochemical, and structural studies have revealed that jasmonate signaling predates the origin of land plants. Jasmonates occur in streptophyte algae but are absent from chlorophytes, indicating that jasmonate biosynthesis evolved in the last common ancestor of streptophytes. However, the molecular nature, perception mechanisms, and biological functions of jasmonates have undergone profound changes during plant evolution. During terrestrialization, the recruitment of a pre-existing transcriptional regulatory network by a newly evolved COI1 receptor module established the canonical COI1/JAZ signaling system. Early diverging land plants employed dn-OPDA, a JA precursor, as the ancestral ligand, which was progressively replaced by JA amino acid conjugates such as JA-Ile in vascular plants. Here, we synthesize current evidence supporting a stepwise evolutionary model progressively shaping the COI1/JAZ-dependent hormone pathway. We discuss how (bio)chemical diversification of oxylipins, co-evolution of receptors and ligands, and the emergence of JA-Ile in vascular plants enabled the expansion, specificity, and systemic integration of jasmonate signaling as a requirement for plant terrestrialization.