Abstract
Cohesin subunit SMC1β is specific and essential for meiosis. Previous studies showed functions of SMC1β 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 SMC1β in SCC and synapsis and processes related to these two processes. Here we show that SMC1β 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 SMC1α. Besides supporting synapsis of autosomes, SMC1β is also required for synapsis and silencing of sex chromosomes. In absence of SMC1β, the silencing factor γH2AX 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. SMC1β 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 Smc1β−/− spermatocytes, but their repair is delayed on asynapsed chromosomes. SMC1α alone cannot support non-homologous associations. Together with previous knowledge, three main functions of SMC1β have emerged, which have multiple consequences for spermatocyte biology: generation of the loop-axis architecture of SCs, homologous and non-homologous synapsis, and SCC starting in early prophase I.
Highlights
Meiosis requires unique chromosome structures and dynamics, which are most prominent in the first of the two meiotic divisions
The current study aimed at elucidating in detail the role of SMC1b in sister chromatid cohesion (SCC) and synapsis, and a number of meiotic processes and features were analyzed, all of which relate to these two processes
We showed that loss of SMC1b causes partial asynapsis of many autosomes and total asynapsis of a few [36,57]
Summary
Meiosis requires unique chromosome structures and dynamics, which are most prominent in the first of the two meiotic divisions Two pairs of sister chromatids are formed from the two homologous chromosomes. In early meiotic prophase I the two pairs of sister chromatids form axial elements (AEs) through association with proteins like SYCP2 and SYCP3. The AEs start to pair and synapse, and full synapsis is reached in pachynema. The synaptonemal complex (SC) is generated, which in addition to AEs includes transverse elements made of SYCP1, SYCE1 and other proteins. SYCP1 serves as a marker for synapsis. Other proteins such as HORMAD1 are displaced from chromosomes upon synapsis and their association with chromosomes indicates asynapsed chromosomes or chromosomal regions [10,11]. We use the terms ‘‘asynapsed’’ for never synapsed, and the term ‘‘desynapsed’’ for lost synapsis
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