Ancestral and divergent roles of the Marchantia polymorpha ATAXIA TELANGIECTASIA AND RAD3-RELATED kinase in maintaining genome integrity and clonal fitness.

The eukaryotic ATAXIA TELANGIECTASIA AND RAD3-RELATED (ATR) kinase is essential for ensuring genomic integrity under conditions that cause replication defects. It triggers a transient cell cycle arrest and DNA repair by activating the DNA damage response pathway. While ATR kinases appear to be functionally conserved, species-specific phenotypes can be observed across the plant kingdom. To investigate the ancestral roles of the plant ATR, we identified its homolog in the model liverwort Marchantia polymorpha, which we named MpATR. Similar to other plant species, MpATR preserves meristematic cells during replication stress, whereas it mediates the response to double-strand breaks redundantly with ATAXIA-TELANGIECTASIA MUTATED (MpATM). However, unlike its counterpart in vascular plants, MpATR activity in liverwort is also essential for repressing the proliferation of differentiated cells. Furthermore, M. polymorpha does not rely on MpATR-controlled stem cell death to eliminate malignant cells. Moreover, even under control growth conditions, Mpatr mutants exhibit increasingly severe growth defects across successive vegetative clonal generations, which are aggravated in the Mpatm/atr double mutant, underscoring the critical role of MpATR in sustaining normal growth over successive generations. Overall, our study sheds light on the differential ATR dependency in liverwort versus vascular plants, emphasizing its evolutionary adaptation across plant species.