The Drosophila meiotic kleisin C(2)M functions before the meiotic divisions

Abstract

Stepwise and regionally controlled resolution of sister chromatid cohesion is thought to be crucial for faithful chromosome segregation during meiotic divisions. In yeast, the meiosis-specific alpha-kleisin subunit of the cohesin complex, Rec8, is protected from cleavage by separase but only during meiosis I and specifically within the pericentromeric region. While the Drosophila genome does not contain an obvious Rec8 orthologue, as other animal and plant genomes, it includes c(2)M, which encodes a distant alpha-kleisin family member involved in female meiosis. C(2)M associates in vivo with the Smc3 cohesin subunit, as previously shown for yeast Rec8. In contrast to Rec8, however, C(2)M accumulates predominantly after the pre-meiotic S-phase. Moreover, after association with the synaptonemal complex, it disappears again and cannot be detected on meiotic chromosomes by metaphase I. C(2)M cleavage fragments are not observed during completion of the meiotic divisions, and mutations within putative separase cleavage sites do not interfere with meiotic chromosome segregation. Therefore, C(2)M appears to function within the synaptonemal complex during prophase I but possibly not thereafter. This suggests that C(2)M may not confer sister chromatid cohesion needed for meiosis I and II chromosome segregation.

The Formation of the Central Element of the Synaptonemal Complex May Occur by Multiple Mechanisms: The Roles of the N- and C-Terminal Domains of the Drosophila C(3)G Protein in Mediating Synapsis and Recombination

“…If this is the case, C(3)G Cdel expression would be expected to have no effect on the assembly of LEs and on the localization of LE proteins. To investigate whether C(3)G Cdel disrupted the assembly of LEs along homologous chromosomes, we determined the localization of the LE protein C(2)M (Manheim and McKim 2003) using a P{gc(2)M-myc} transgene (Heidmann et al 2004). The localization of C(2)M-myc was unaffected by the expression of C(3)G Cdel (Figure 3, B-D).…”

Meiosis-specific cohesin mediates homolog recognition in mouse spermatocytes

“…Therefore, we assume that RAD21L plays only a minor role in canonical sister chromatid cohesion but a major role in homolog pairing and synapsis. In this regard, RAD21L might be functionally homologous to Drosophila meiotic a-kleisin C(2)M, which also localizes on chromatin after meiotic DNA replication and is required for events associated with meiotic exchange but not for sister chromatid cohesion (Heidmann et al 2004;Tanneti et al 2011). Divergence of the meiotic a-kleisin subunit is also observed in C. elegans, in which three different types of a-kleisin, REC-8, COH-3, and COH4, act redundantly to promote AE and SC formation, although each may have additional specialized functions as well (Severson et al 2009).…”

Functional links between Drosophila Nipped-B and cohesin in somatic and meiotic cells

“…Cohesin colocalizes with SC proteins and is involved in homolog pairing, SC formation, and SC structure in diverse organisms (Bannister et al 2004;Chan et al 2003;Eijpe et al 2000;Khetani and Bickel 2007;Klein et al 1999;Pasierbek et al 2001Pasierbek et al , 2003Revenkova et al 2004;Xu et al 2005). The C(2)M protein, which contains kleisin motifs similar to those in Rad21 and which interacts with Smc3, is needed for SC formation and the coalescence of Smc1 and Smc3 into chromosome cores (Heidmann et al 2004;Khetani and Bickel 2007;Manheim and McKim 2003). C(2)M, however, is not required for binding of the Smc1 and Smc3 cohesin subunits to either centromeres or chromosome arms (Khetani and Bickel 2007).…”