Jasmonate-Related MYC Transcription Factors Are Functionally Conserved in Marchantia polymorpha

Abstract

The lipid-derived phytohormone jasmonoyl-isoleucine regulates plant immunity, growth and development in vascular plants by activating genome-wide transcriptional reprogramming. In Arabidopsis (Arabidopsis thaliana), this process is largely orchestrated by the master regulator MYC2 and related transcription factors (TFs). However, the TFs activating this pathway in basal plant lineages are currently unknown. We report the functional conservation of MYC-related TFs between the eudicot Arabidopsis and the liverwort Marchantia polymorpha, a plant belonging to an early diverging lineage of land plants. Phylogenetic analysis suggests that MYC function first appeared in charophycean algae and therefore predates the evolutionary appearance of any other jasmonate pathway component. M. polymorpha possesses two functionally interchangeable MYC genes, one in females and one in males. Similar to AtMYC2, MpMYCs showed nuclear localization, interaction with JASMONATE-ZIM-DOMAIN PROTEIN repressors, and regulation by light. Phenotypic and molecular characterization of loss-and gain-of-function mutants demonstrated that MpMYCs are necessary and sufficient for activating the jasmonate pathway in M. polymorpha, but unlike their Arabidopsis orthologs, do not regulate fertility. Therefore, despite 450 million years of independent evolution, MYCs are functionally conserved between bryophytes and eudicots. Genetic conservation in an early diverging lineage suggests that MYC function existed in the common ancestor of land plants and evolved from a preexisting MYC function in charophycean algae.

A Phytochrome B-Independent Pathway Restricts Growth at High Levels of Jasmonate Defense

“…MYCs as conserved regulators of JA-induced shoot growth inhibition (Zhang and Turner, 2008;Major et al, 2017;Guo et al, 2018b;Peñuelas et al, 2019). MYCs can influence leaf development by interfering with the activity of PHYTOCHROME-INTERACTING FACTORS (e.g., PIF4) and by promoting the activity of ELONGATED HYPOCOTYL 5 (HY5), a central regulator of photomorphogenesis (Zhang et al, 2018;Ortigosa et al, 2019).…”

Oil body formation inMarchantia polymorphais controlled by MpC1HDZ and serves as a defense against arthropod herbivores

“…That Mp C1HDZ expression is not altered in Mp MYB02 gain-of-function alleles [35] suggests that Mp MYB02 is downstream MpC1HDZ activity, however, it is unknown whether MpMYB02 is also specifically expressed in oil body cells or participates in oil body cell differentiation and terpenoid biosynthesis. In contrast, we did not find any relationship of Mp C1HDZ with Mp MYCX/Y , which is associated with the defense-related induction of sesquiterpenoid biosynthesis in response to herbivory [67], or with ABA signaling, which is associated with bis(bibenzyl) increase under UV-C light stress [38].…”

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

“…Microarray-based transcriptomic profiling of wild-type versus Mpmyc liverworts that were wounded 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 (Peñ uelas et al, 2019).Reciprocal cross-species complementation 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 (Peñ uelas et al, 2019).…”

“…Microarray-based transcriptomic profiling of wild-type versus Mpmyc liverworts that were wounded 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 (Peñ uelas et al, 2019).…”

“…Reciprocal cross-species complementation 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 (Peñ uelas et al, 2019). Such coevolutionary constraints may be indicative of parallel evolutionary pressures required to finetune stress-versus-growth responses as plants diversified on land.…”