Dcr1 senses R-loops for RNAPII termination at sites of replication stress and repair pathway choice

Stalled RNA polymerase II (RNAPII) threatens genome integrity, yet how cells resolve transcription blocks at difficult-to-terminate sites is unclear. Leveraging the compact genome of fission yeast and termination defects associated with the non-canonical function of Dcr1, we unravel the recognition and release mechanisms of stalled RNAPII. Through dual recognition, Dcr1 senses the difficult-to-terminate context-stalled RNAPII and accumulated R-loops-and recruits the termination factor Dhp1 to ensure efficient RNAPII release. Failure of this mechanism causes termination defects that impede replication forks, necessitating DNA polymerase delta (DNAPδ)-mediated replication fork restart at stalled sites. Moreover, Dcr1 promotes genome stability by repurposing its hybrid-recognition ability to engage Rad51, thereby biasing DNA repair toward high-fidelity homologous recombination. Our work defines a key chromatin context and mechanisms governing RNAPII termination, establishing Dcr1 as a molecular hub that directly couples the fidelity of transcription termination to the stability of the genome during replication and repair.