Meiotic cohesin-based chromosome structure is essential for homologous chromosome pairing in Schizosaccharomyces pombe

Abstract

Chromosome structure is dramatically altered upon entering meiosis to establish chromosomal architectures necessary for the successful progression of meiosis-specific events. An early meiotic event involves the replacement of the non-SMC mitotic cohesins with their meiotic equivalents in most part of the chromosome, forming an axis on meiotic chromosomes. We previously demonstrated that the meiotic cohesin complex is required for chromosome compaction during meiotic prophase in the fission yeast Schizosaccharomyces pombe. These studies revealed that chromosomes are elongated in the absence of the meiotic cohesin subunit Rec8 and shortened in the absence of the cohesin-associated protein Pds5. In this study, using super-resolution structured illumination microscopy, we found that Rec8 forms a linear axis on chromosomes, which is required for the organized axial structure of chromatin during meiotic prophase. In the absence of Pds5, the Rec8 axis is shortened whereas chromosomes are widened. In rec8 or pds5 mutants, the frequency of homologous chromosome pairing is reduced. Thus, Rec8 and Pds5 play an essential role in building a platform to support the chromosome architecture necessary for the spatial alignment of homologous chromosomes.

PDS5 proteins regulate the length of axial elements and telomere integrity during male mouse meiosis

“…Spermatocytes lacking both PDS5 proteins are able to fulfill complete synapsis, but display severely shortened AEs/LEs in prophase I. A similar shortening of chromosome axes in the absence of PDS5 has been described in other organisms (van Heemst et al, 1999;Wang et al, 2003;Jin et al, 2009;Ding et al, 2016). The extent of SC shortening in Pds5AB deficient mouse spermatocytes is comparable, or even greater, to that found in spermatocytes from cohesin knock out mouse models (Biswas et al, 2016;Ward et al, 2016).…”

“…The single orthologs of PDS5 in Sordaria macrospora (Spo76p) and budding yeast are located at AEs/LEs during prophase I stages (van Heemst et al, 1999;Zhang et al, 2005;Jin et al, 2009). Analyses of meiosis in Pds5 mutants in Sordaria, budding and fission yeasts, and the worm Caenorhabditis elegans indicate that this protein is involved in cohesion, formation of AEs/LEs, condensation, homolog pairing and repair of DSBs (van Heemst et al, 1999;Wang et al, 2003;Zhang et al, 2005;Ding et al, 2006;Jin et al, 2009;Ding et al, 2016). In mammaliam meiosis, like in mitosis, both PDS5A and PDS5B are present.…”

Meiotic cohesin subunits RAD21L and REC8 are positioned at distinct regions between lateral elements and transverse filaments in the synaptonemal complex of mouse spermatocytes

“…5). A recent work using 3D-SIM in fission yeast meiosis also suggests that Rec8, the only meiotic α-kleisin in this species, plays an essential role in building a platform to support the chromosome architecture necessary for the spatial alignment of homologs [52]. Therefore, it seems that the role of meiosis-specific cohesin subunits in establishing the linkage between homologs is conserved among eukaryotes.…”

Super-Resolution Microscopy in Studying the Structure and Function of the Cell Nucleus

“…The spatial organization of a meiotic chromosome was studied using various SRM methods [78]. In yeast cells, 3D-SIM demonstrated the formation of a chromosome axis from meiotic cohesin, as well as impairment in the chromosome structure in the absence of cohesin [79, 80]. …”