A simple cell-cycle control system in Marchantia provides a framework for understanding plant cell proliferation

Cell division in eukaryotes is controlled by cyclins and cyclin-dependent kinases (CDKs). Our knowledge on how the cell cycle control system works in plants is limited to a few model species. The high number of cyclin-CDK pairs in flowering plants and other species hinders functional analysis due to redundancy. The question of how this system might have worked in early land plant ancestors is unresolved. Through a comprehensive phylogenetic analysis, we show that non-seed plants display a simple system of cell cycle genes, suggesting that the complexity in seed plants is a derived feature. To explore simpler systems, we studied the liverwort Marchantia polymorpha, which possesses a reduced, non-redundant set of core cell-cycle genes. Using single-cell RNA-seq and live imaging of fluorescent reporters, we found a striking pattern of phase-specific expression of cell cycle genes during cell division. This system is characterized by one predominant cyclin per phase in the vegetative gametophyte, with limited overlap at transitions. Live imaging of tagged cyclins indicated that protein turnover and localization contribute to phase specificity. Functional studies revealed that MpCYCD;1 is sufficient to promote cell cycle re-entry, while overexpression of MpCYCA and MpCYCB;1 causes growth arrest, aligning with their roles in G1, S, and G2/M transitions. Our findings reveal conserved features about cell cycle control across eukaryotes and the ancestral state in land plants. Marchantia possesses a reduced system and provides a powerful framework for understanding multicellular proliferation and its evolution, with potential for engineering plant growth and development.