Evolutionary acquisition of an interaction between conserved proteins drives plant-specific cell cycle progression

The cell cycle is fundamental to eukaryotes and regulated in conserved and kingdom-specific manners. However, the molecular mechanisms underlying plant-specific cell-cycle control remain unclear. Here, we demonstrate that a plant-specific N-terminal extension of PAF1 facilitates the assembly of transcriptional machinery that regulates plant-specific cell-cycle progression. This exclusively-evolved extension mediates direct interaction between PAF1 and SKIP within plantae. The resulting PAF1c-SKIP complex binds to a plant-specific CDKB locus in a PAF1-dependent manner, activating its expression to drive cell-cycle progression from unicellular algae to angiosperms. The intrinsically disordered N-terminal extension of PAF1 undergoes phase separation. Both this extension and its phase separation capacity are critical for functional PAF1c-SKIP complex formation and cell-cycle progression. Our findings illustrate how evolutionary repurposing of ancient protein domains through evolutionary gain of an IDR-like N-terminal extension enables plants to develop a unique molecular mechanism for kingdom-specific cell cycle strategies. The cell cycle is regulated by conserved and kingdom-specific mechanisms. The authors demonstrate that a plant-specific N-terminal extension of the PAF1 protein facilitates formation of a complex between PAF1 and SKIP and promotes cell-cycle progression.