microRNA-mediated control of cell fate specification and patterning in Marchantia polymorpha

MicroRNAs (miRNAs) are small non-coding RNA molecules essential for growth and development in eukaryotes. In plants, the master gene DICER-LIKE 1 (DCL1) catalyzes the biogenesis of miRNAs by processing double-stranded precursors that give rise to mature miRNAs. We sought to understand the function and evolution of microRNAs using Marchantia polymorpha, a model bryophyte that allows comparative approaches to infer characteristics of the ancestral land plant. We functionally characterized loss-of-function mutants of MpDCL1 a generated by means of CRISPR-Cas9-mediated genomic edition and the miR166/CLASS III HD-ZIP regulatory circuit in Marchantia polymorpha. We report that MpDCL1a is required for the biogenesis of miRNAs and uncovered a central role for miR166/Homeodomain Zipper Class III-regulated auxin synthesis in the specification of cell identity, patterning, meristem function, laminar expansion, and the development of the body in the last common ancestor of the bryophytes and vascular plants. Our findings indicate that DCL1, Class III HD-ZIP, miR166, and auxin functioned in the development of the body of the last common ancestor of extant land plants and provide a novel working framework to interrogate the basic principles of cell specification and patterning in plants.