Ligand-receptor co-evolution shaped the jasmonate pathway in land plants

Jasmonoyl-isoleucine regulates defence, growth and developmental responses in eudicots. Bryophyte genomes have conserved sequences for all JA-Ile signalling pathway components, but in contrast to higher plants, the bioactive hormone has not been identified. We show that the JA-Ile receptor COI1 is functionally conserved in the bryophyte Marchantia polymorpha, but responds to a different ligand. Although Marchantia plants neither synthesize nor respond to JA-Ile, loss-of-function Mpcoi1 mutants have phenotypic defects reminiscent of COI1-dependent functions in Arabidopsis. AtCOI1 functionally complements Mpcoi1 mutation and confers JA-Ile responsiveness on M. polymorpha, as does a single amino acid substitution in MpCOI1 that switches ligand specificity. Mass spectrometry quantification of cyclopentenone derivatives, bioactivity analysis and COI1-ligand interaction assays pinpointed two isomers of the JA-Ile precursor dinor-OPDA (dinor-cis-OPDA and dinor-iso-OPDA) as the natural MpCOI1 ligands. Our results identify the ancestral jasmonate, confirm the functional conservation of its signalling pathway, and show that JA-Ile and COI1 emergence in higher plants from their ancestral counterparts required co-evolution of hormone biosynthetic complexity and receptor specificity. Six experimantal condition: 1_3 REPLICATES: Tak-2 treated 2 hours with OPDA 25µM (Experiment) vs Tak-2 mock (Control); 2_2 REPLICATES: Mutant Mpcoi1-2 treated 2 hours with OPDA 25µM (Experiment) vs mutant Mpcoi1-2 mock (Control); 3_3 REPLICATES: Mutant Mpcoi1-1 (Experiment) vs Tak-2 (Control) treated both 2 hours with OPDA 25µM; 4_3 REPLICATES: Mutant Mpcoi1-2 (Experiment) vs Tak-1 (Control) both treated 2 hours with OPDA 25µM; 5_3 REPLICATES: Tak-1 mechanical wounded (Experiment) vs Tak-1 Mock (Control); 6_3 REPLICATES: complemented line proMpEF:AtCOI1/Mpcoi1-1 treated 2 hours with 0.5 µMCOR (Experiment) vs Mutant Mpcoi1-1 (Control).