Replicated repurposing of an ancestral transcriptional complex in land plants

In flowering plants, transcriptional complexes with a common composition have been found to regulate multiple pathways in the epidermal cell layer, including the production of flavonoid pigments and the differentiation of trichomes and root hairs. These complexes are composed of transcription factors from the MYB and bHLH families along with a WDR scaffold protein (MBW complexes). The MYB member has been found to be the most pathway-specific component of the complex, and modifications to these MYB genes are overrepresented in studies investigating the genetic basis of differences in pigmentation phenotypes. Here, we investigated the origin of this complex and its independent functional diversification in the liverwort lineage. We found evidence that homologous transcriptional complexes form in Marchantia polymorpha, indicating that they are ancestral to land plants. The single orthologous bHLH gene, MpbHLH12, regulates both pathways controlled by the two orthologous MYB genes, MpMYB14 and MpMYB02. Moreover, MpbHLH12 interacts with two of the TTG1-like WDR proteins in M. polymorpha, although their functional role has yet to be determined. We propose that two transcriptional complexes with alternative MYB paralogs in M. polymorpha represent an ancestral function, regulation of the flavonoid pathway, and a derived function, maturation of liverwort-specific oil bodies. Notably, we find independently in the liverworts, as has been observed in angiosperms, that functional diversification is associated with duplication of the MYB member and co-option of its interaction partners.