A simple cell-cycle control system in <i>Marchantia polymorpha</i> provides a framework for understanding plant cell proliferation

Eukaryotic cell division is controlled by cyclins and cyclin-dependent kinases (CDKs). The high number of cyclin-CDK pairs in flowering plants hinders functional analysis due to redundancy, and how this system might have worked in early land plant ancestors remains unresolved. Our phylogenetic analysis showed that non-seed plants have 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, nonredundant set of core cell cycle genes. Single-cell RNA-seq and live imaging of fluorescent reporters revealed phase-specific expression of cell cycle genes during cell division, characterized by 1 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, consistent with their roles in the G1, S, and G2/M transitions. Our findings reveal conserved features of cell cycle control across eukaryotes and the ancestral state of land plants. Marchantia thus provides a powerful framework for understanding multicellular proliferation and its evolution, with the potential for engineering plant growth and development.