Monte, I. | bioRxiv Science

bioRxiv2023

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.

plant biology↗

bioRxiv2021

Chemical screen identifies a small molecule antagonizing JA-Ile perception and auxin responses.

The phytohormone JA-Ile regulates many stress responses and developmental processes in plants. A co-receptor complex formed by the F-box protein COI1 (Coronatine Insensitive 1) and a JAZ (Jasmonate ZIM-domain) repressor perceives the hormone. JA-Ile antagonists are invaluable tools for exploring the role of JA-Ile in specific tissues and developmental stages, and for identifying regulatory processes of the signalling pathway. Using two complementary chemical screens, we identified three compounds that exhibit a robust inhibitory effect on both the hormone-mediated COI-JAZ interaction and degradation of JAZ1 and JAZ9 in vivo. One molecule, J4, also restrains specific JA-induced physiological responses in different angiosperm plants, including JA-mediated gene expression, growth inhibition, chlorophyll degradation and anthocyanin accumulation. Interaction experiments with purified proteins indicate that J4 directly interferes with the formation of the Arabidopsis (Arabidopsis thaliana) COI1-JAZ complex otherwise induced by JA. The antagonistic effect of J4 on COI1- JAZ also occurs in the liverwort Marchantia polymorpha, suggesting the mode of action is conserved in land plants. Besides JA signalling, J4 works as an antagonist of the closely-related auxin signalling pathway, preventing TIR1/Aux-IAA interaction and auxin responses in planta, including hormone-mediated degradation of an auxin repressor, gene expression and gravitropic response. However, J4 does not affect other hormonal pathways. Altogether, our results show that this dual antagonist competes with JA-Ile and auxin, preventing the formation of phylogenetically related receptor complexes. J4 may be a useful tool to dissect both the JA-Ile and auxin pathways in particular tissues and developmental stages since it reversibly inhibits these pathways. One sentence summaryA chemical screen identified a molecule that antagonizes jasmonate perception by directly interfering with receptor complex formation in phylogenetically distant vascular and non-vascular plants.

plant biology↗