Two telomeric ends of acrocentric chromosome play distinct roles in homologous chromosome synapsis in the fetal mouse oocyte.

In mammalian oocytes, proper chromosome segregation at the first meiotic division is dictated by the presence and site of homologous chromosome recombination, which takes place in fetal life. Our current understanding of how homologous chromosomes find each other and initiate synapsis, which is prerequisite for homologous recombination, is limited. It is known that chromosome telomeres are anchored into the nuclear envelope (NE) at the early meiotic prophase I (MPI) and move along NE to facilitate homologous chromosome search and pairing. However, the mouse (Mus musculus) carries all acrocentric chromosomes with one telomeric end close to the centromere (subcentromeric telomere; C-telomere) and the other far away from the centromere (distal telomere; D-telomere), and how C- and D-telomeres participate in chromosome pairing and synapsis during the MPI progression is not well understood. Here, we found in the mouse oocyte that C- and D-telomeres transiently clustered in one area, but D-telomeres soon separated together from C-telomeres and then dispersed to preferentially initiate synapsis, while C-telomeres remained in clusters and synapsed at the last. In the Spo11 null oocyte, which is deficient in SPO11-dependent DSBs formation and homologous synapsis, the pattern of C- and D-telomere clustering and resolution was not affected, but synapsis was more frequently initiated at C-telomeres. These results suggest that SPO11 suppresses the early synapsis between C-telomeres in clusters.