Meristem dormancy in a dichotomous branching system is regulated by a liverwort-specific miRNA and a clade III SPL gene in Marchantia polymorpha

The shape of modular organisms depends on branching architecture, which in plants is determined by the fates of generative centres called meristems. The branches of the liverwort Marchantia polymorpha are derived from two adjacent meristems that develop at thallus apices. These meristems may be active and develop branches or may be dormant and do not form branches. The relative number and position of active and dormant meristems defines overall shape and form of the thallus. We show that the clade III SQUAMOSA PROMOTER BINDING PROTEIN LIKE (SPL) transcription factor, MpSPL1, is required for meristem dormancy. The activity of MpSPL1 is regulated by the liverwort-specific Mpo-MR13 miRNA which in turn is regulated by PIF-mediated phytochrome signaling. An unrelated miRNA, MIR156, represses a different SPL gene (belonging to clade IV) that inhibits branching during the shade avoidance response in Arabidopsis thaliana. This suggests that a conserved mechanism of phytochrome signaling modulates branching architecture in liverworts and angiosperms and therefore likely operated in the last common ancestor. However, PIF-mediated phytochrome signaling represses the expression of different miRNA genes with different SPL targets during dichotomous, apical branching in liverworts and during lateral, subapical branching in angiosperms. We speculate that the mechanism that acts downstream of light and regulates meristem dormancy evolved independently in liverworts and angiosperms.