Meiotic Cohesin SMC1b Provides Prophase I Centromeric Cohesion and Is Required for Multiple Synapsis-Associated Functions

Cohesin subunit SMC1b is specific and essential for meiosis. Previous studies showed functions of SMC1b in determining the axis-loop structure of synaptonemal complexes (SCs), in providing sister chromatid cohesion (SCC) in metaphase I and thereafter, in protecting telomere structure, and in synapsis. However, several central questions remained unanswered and concern roles of SMC1b in SCC and synapsis and processes related to these two processes. Here we show that SMC1b substantially supports prophase I SCC at centromeres but not along chromosome arms. Arm cohesion and some of centromeric cohesion in prophase I are provided by non-phosphorylated SMC1a. Besides supporting synapsis of autosomes, SMC1b is also required for synapsis and silencing of sex chromosomes. In absence of SMC1b, the silencing factor cH2AX remains associated with asynapsed autosomes and fails to localize to sex chromosomes. Microarray expression studies revealed up-regulated sex chromosome genes and many down-regulated autosomal genes. SMC1b is further required for non-homologous chromosome associations observed in absence of SPO11 and thus of programmed double-strand breaks. These breaks are properly generated in Smc1b2/2 spermatocytes, but their repair is delayed on asynapsed chromosomes. SMC1a alone cannot support non-homologous associations. Together with previous knowledge, three main functions of SMC1b have emerged, which have multiple consequences for spermatocyte biology: generation of the loop