Evolution of the jasmonate ligands and their biosynthetic pathways

Jasmonates are phytohormones that regulate multiple aspects of plant development and responses to stress, activating a conserved signaling pathway in land plants. The characterization of jasmonates biosynthetic and signaling pathways revealed that (+)-7-iso-JA-Ile (JA-Ile) is the ligand for the COI1/JAZ receptor in angiosperms, where jasmonates are synthesized through the OPR3-dependent or OPR3-independent pathways. More recently, studies on different model species identified dn-cis-OPDA, dn-iso-OPDA and {Delta}4-dn-iso-OPDA as the ligands of the COI1/JAZ receptor in the liverwort Marchantia polymorpha, and a receptor-independent role for several jasmonates in streptophytes. To understand the distribution of bioactive jasmonates in the green lineage and how their biosynthetic pathways evolved, we combined phylogenetic analyses and jasmonates metabolomics in representative species from different lineages. We found that both OPDA and dn-cis-OPDA are ubiquitous in land plants and present also in charophyte algae, underscoring their importance as ancestral signalling molecules. In contrast, JA-Ile biosynthesis emerged within lycophytes coincident with the evolutionary appearance of JAR1 function. We show that JA biosynthesis mediated by OPR1/OPR2 appeared in charophytes most likely as a degradation pathway of OPDA/dn-cis-OPDA before OPR3 emergence. Therefore, our results demonstrate that the OPR3-independent JA biosynthesis pathway is ancient and predates the evolutionary appearance of the OPR3-dependent pathway. Moreover, we identified a negative correlation between dn-iso-OPDA and JA-Ile in land plants which supports that dn-iso-OPDA is the relevant form of the hormone perceived by COI1/JAZ in bryophytes and lycophytes.