SUMO-Dependent Relocalization of Eroded Telomeres to Nuclear Pore Complexes Controls Telomere Recombination

In budding yeast, inactivation of telomerase and ensuing telomere erosion cause relocalization of telomeres to nuclear pore complexes (NPCs). However, neither the mechanism of such relocalization nor its significance are understood. We report that proteins bound to eroded telomeres are recognized by the SUMO (small ubiquitin-like modifier)-targeted ubiquitin ligase (STUbL) Slx5-Slx8 and become increasingly SUMOylated. Recruitment of Slx5-Slx8 to eroded telomeres facilitates telomere relocalization to NPCs and type II telomere recombination, a counterpart of mammalian alternative lengthening of telomeres (ALT). Moreover, artificial tethering of a telomere to a NPC promotes type II telomere recombination but cannot bypass the lack of Slx5-Slx8 in this process. Together, our results indicate that SUMOylation positively contributes to telomere relocalization to the NPC, where poly-SUMOylated proteins that accumulated over time have to be removed. We propose that STUbL-dependent relocalization of telomeres to NPCs constitutes a pathway in which excessively SUMOylated proteins are removed from “congested” intermediates to ensure unconventional recombination. [Display omitted] •SUMO modification accumulates at eroded telomeres after loss of telomerase•SUMOlyation promotes recruitment of Slx5-Slx8 STUbL to eroded telomeres•Rfa1 is SUMOylated during telomere erosion and physically interacts with Slx5•STUbL-dependent targeting of telomeres to NPCs promotes type II recombination Churikov et al. show that eroded telomeres become SUMOylated and recruit Slx5-Slx8 SUMO-targeted ubiquitin ligase. The Slx5-Slx8 complex is essential for telomere relocalization to nuclear pore complexes, a process that promotes the formation of telomerase-independent survivors via type II recombination.