Reduced Rif2 and no Mec1 targets short telomeres for elongation rather than double-strand break repair

S. cerevisiae telomerase binds and preferentially elongates short telomeres, events that require the checkpoint kinase Tel1. We show that the Mre11 complex bound preferentially to short telomeres, which can explain the preferential binding of Tel1 to these ends. Compared to wild type length telomeres, short telomeres generated by incomplete replication had low levels of the telomerase inhibitory protein Rif2. Moreover, in the absence of Rif2, Tel1 bound equally well to short and wild type length telomeres, arguing that low Rif2 content marks short telomeres for preferential elongation. Using congenic strains, a double strand break bound ≥140 times as much Mec1 in the first cell cycle after breakage as did a short telomere in the same time frame. Replication protein A binding was also much lower at short telomeres. The absence of Mec1 at short telomeres can explain why they do not trigger a checkpoint-mediated cell cycle arrest.