Carlo Rinaldi, Federica Pagnotta, Renata Tisi, Maria Pia Longhese
In eukaryotes, DNA double-strand breaks (DSBs) activate Tel1/ATM- and Mec1/ATR-dependent checkpoint signaling and can be repaired by homologous recombination (HR), which requires DNA end resection, typically initiated by the MRX/MRN complex. In budding yeast, Sae2/CtIP promotes MRX-dependent end processing, limits Tel1-Rad53 signaling, and contributes to DSB end-tethering. Here, we identify a Tel1 FAT-domain variant, Tel1-400, that increases the DNA damage resistance of sae2Δ cells by suppressing their DSB end-tethering defect through Rad9 phosphorylation-dependent oligomerization. Tel1-400 accumulates more strongly at DSBs than wild-type Tel1 and enhances DNA-damage-induced Rad9 phosphorylation. An oligomerization-defective rad9 phosphosite mutant prevents Tel1-400 from improving DSB end-tethering in sae2Δ cells, whereas chemically induced Rad9 dimerization restores this ability. Rad9 also supports DSB end-tethering in Sae2-proficient cells, as the same rad9 phosphosite mutant increases end separation in an otherwise wild-type background. Functionally, Tel1-400 shifts repair in sae2Δ cells toward strand-invasion-dependent HR while reducing single-strand annealing, and this repair-pathway bias requires Rad9 oligomerization. Together, these findings identify a Tel1-Rad9 pathway in which increased Tel1 association at DNA breaks enhances Rad9 phosphorylation and self-assembly, thereby promoting DSB end-tethering and influencing recombination pathway choice.