SpRap1 and spRif1, recruited to telomeres by Taz1, are essential for telomere function in fission yeast

Abstract

Telomeres are essential for genome integrity. scRap1 (S. cerevisiae Rap1) directly binds to telomeric DNA [1–3] and regulates telomere length and telomere position effect (TPE) [4–6] by recruiting two different groups of proteins to its RCT (Rap1 C-terminal) domain [7]. The first group, Rif1 and Rif2, regulates telomere length [8, 9]. The second group, Sir3 and Sir4 [10], is involved in heterochromatin formation [11–13]. On the other hand, human TRF1 and TRF2, as well as their fission yeast homolog, Taz1, directly bind to telomeric DNA [14–16] and negatively regulate telomere length [16–20]. Taz1 also plays important roles in TPE and meiosis [16, 20, 21]. Human Rap1, the ortholog of scRap1, negatively regulates telomere length and appears to be recruited to telomeres by interacting with TRF2 [7]. Here, we describe two novel fission yeast proteins, spRap1 (S. pombe Rap1) and spRif1 (S. pombe Rif1), which are orthologous to scRap1 and scRif1, respectively. spRap1 and spRif1 are independently recruited to telomeres by interacting with Taz1. The rap1 mutant is severely defective in telomere length control, TPE, and telomere clustering toward the spindle pole body (SPB) at the premeiotic horsetail stage, indicating that spRap1 has critical roles in these telomere functions. The rif1 mutant also shows some defects in telomere length control and meiosis. Our results indicate that Taz1 provides binding sites for telomere regulators, spRap1 and spRif1, which perform the essential telomere functions. This study establishes the similarity of telomere organization in fission yeast and humans.