Some Things Never Change: Conserved MYC-Family bHLH Transcription Factors Mediate Dinor-OPDA Signaling in Liverworts

The lipidic phytohormone jasmonylisoleucine (JA-Ile) is a key mediator of stress-versus-growth signaling in vascular plants. Upon its accumulation, JA-Ile is detected by the F box receptor protein COI1 (CORONATINE INSENSITIVE1), which in turn leads to the ubiquitination and proteasomal degradation of JAZ (JASMONATE ZIM-DOMAIN) repressor proteins that would otherwise bind to and inhibit MYC-family basic helix-loophelix (bHLH) transcription factors. This hormone-triggered derepression of the jasmonate (JA) pathway allows for the induction of JA-related gene expression, physiological adjustments, and the accumulation of specializedmetabolites like glucosinolates and terpenoids (Wasternack and Hause, 2013). Studies exploring the evolutionary history and functional significance of JA signaling in early divergent land plants (bryophytes) have recently uncovered a conserved COI1-JAZ module centered on the perception of the modified JA and 12-oxo-phytodienoic acid (OPDA) precursor dinor-OPDA (dn-OPDA) rather than JA-Ile (Monte et al., 2018, 2019). In this issue, Peñuelas et al. (2019) build on this knowledge and determine the degree to which JA/dn-OPDA signaling in bryophytes relies on the conserved action of MYC-family bHLH transcription factors. Phylogenetic analyses identifiedMYChomologs with appropriate domain architecture in certain charophytic (freshwater) algal lineages and across land plants, indicating that MYC transcription factors predate the colonization of land. In the model liverwort Marchantia polymorpha, two ubiquitously expressedMpMYC homologs were discovered onmale (MpMYCY) or female (MpMYCX) sex chromosomes. Both MpMYC homologs interact strongly with the MpJAZ repressor through conserved interaction domains, similar to angiosperm MYC and JAZ homologs. Moreover,M.polymorphaMpMYChomologs interact with Arabidopsis (Arabidopsis thaliana) AtJAZ proteins, suggesting a strong evolutionary pressure to maintain MYC-JAZ interactions throughout the evolution of plants. Phenotypic analysis of overexpression and knockout lines revealed a functionally conserved role for MpMYC transcription factors inmediating dn-OPDAsignaling in M.polymorpha. Comparedwithwild-type liverworts,Mpmyc knockoutswere insensitive to the growth-suppressing effects of exogenous OPDA, whereas MpMYC overexpressors displayed heightened sensitivity (see figure). Microarray-based transcriptomic profiling of wild-type versusMpmyc liverworts that werewounded or treated with exogenous OPDA further defined a set of MYC-dependent genes whose promoters were enriched for conserved G-box motifs associated with MYC binding. This set of MpMYCdependent loci included terpenoid biosynthesis genes, whose relevance to OPDA-mediated anti-herbivory responses was supported by an enhanced susceptibility to generalist insect larvae in Mpmyc mutants that could not accumulate sesquiterpene terpenoids (Peñuelas et al., 2019). Reciprocal cross-speciescomplementation assays failed to rescue the JA/OPDA insensitivity phenotypes of Arabidopsis or M. polymorpha myc mutants, suggesting partial divergence between MYC signaling mechanisms in distantly related plant lineages. Upon further analysis, the authors discovered that MYC homologs could not interact with MED25 mediator subunits across species, rendering each homolog inactive when expressed out of context (Peñuelas et al., 2019). Suchcoevolutionary constraints may be indicative of parallel evolutionary pressures required to finetune stress-versus-growth responses as plants diversified on land. In any case, the Functional Conservation of MYC-regulated dn-OPDA Signaling in Liverworts.