Not only do telomeres protect chromosome ends from DNA damage responses, but also they promote meiotic centromere maintenance and nuclear envelope breakdown. Here we focus on when and how telomeres become important for centromeres. In meiotic prophase, telomeres cluster at the nuclear envelope to form the meiotic bouquet. We found that the fission yeast bouquet is crucial for centromere integrity. Surprisingly, centromere maintenance becomes precarious upon meiotic entry; kinetochore components, including the centromeric CenpA histone variant, dissociate from 2-4% of meiotic centromeres. However, localization of centromeres to the telomere-adjacent microdomain promotes centromere reassembly. In bouquet-deficient cells, loss of this microdomain leads to kinetochore loss and chromosome missegregation [Klutstein et al Nat Cell Biol 2015].
Why do centromeres tend to fall apart during meiosis, and how do telomeres promote their reassembly? We find that the loss of Rec12Spo11 (which creates meiotic DNA double strand breaks) rescues the kinetochore defects in bouquet mutants in a manner independent of its catalytic activity; conversely, overexpression of Rec12 exacerbates the defects. The Rec8 meiotic cohesin also dismantles centromeres. Moreover, mitotically expressed Rec12 or Rec8 causes kinetochore loss in proliferating cells, both fission yeast and human cells. Hence, since
Spo11 and Rec8 are inappropriately expressed in many cancers, this deleterious activity of Spo11/Rec8 in compromising centromere function may play a role in carcinogenesis. The reassembly promoted by telomeres depends on a pathway from telomeric heterochromatin to Aurora B kinase and centromere factors.