Meiotic cohesins modulate chromosome compaction during meiotic prophase in fission yeast

Abstract

The meiotic cohesin Rec8 is required for the stepwise segregation of chromosomes during the two rounds of meiotic division. By directly measuring chromosome compaction in living cells of the fission yeast Schizosaccharomyces pombe, we found an additional role for the meiotic cohesin in the compaction of chromosomes during meiotic prophase. In the absence of Rec8, chromosomes were decompacted relative to those of wild-type cells. Conversely, loss of the cohesin-associated protein Pds5 resulted in hypercompaction. Although this hypercompaction requires Rec8, binding of Rec8 to chromatin was reduced in the absence of Pds5, indicating that Pds5 promotes chromosome association of Rec8. To explain these observations, we propose that meiotic prophase chromosomes are organized as chromatin loops emanating from a Rec8-containing axis: the absence of Rec8 disrupts the axis, resulting in disorganized chromosomes, whereas reduced Rec8 loading results in a longitudinally compacted axis with fewer attachment points and longer chromatin loops.

Cell cycle control of spindle elongation

“…38,39 For mitotic chromosomes this number is estimated to be 3,000-2,00,000 in vertebrates [39][40][41] but only 140 in S. cerevisiae 32 and 700 in S. pombe. 42 Thus, the degree of chromosome compaction in mitosis compared to interphase rises dramatically in higher eukaryotes. Although it is generally believed that maximal chromosome condensation is achieved in metaphase when chromosomes line up on the metaphase plate, this view has been challenged recently.…”

Untimely expression of gametogenic genes in vegetative cells causes uniparental disomy

“…In vegetative cells, mitotic cohesin containing Rad21 and Psc3 is preferentially enriched across heterochromatin domains including at centromeres, and shows distinct peaks at specific sites on chromosomal arms 5,6,9,21 . As cells enter meiosis, Rec8-Rec11 replaces Rad21-Psc3 on arms, while Rec8 partners with Psc3 at centromeres 22,23 . Interestingly, we found that Rec8 and its interaction partner Rec11 were loaded onto chromosomal arms in mmi1 ∆ cells, at sites normally occupied by mitotic cohesin (Extended Data Fig.…”

Excluded volume effect enhances the homology pairing of model chromosomes

“…The distributions of the nucleosomes and the binding sites of DNA-associated proteins differ substantially among the 1st, 2nd, and 3rd chromosomes in S. pombe [14,15], since they are highly dependent on DNA sequences that show vast variation among the three chromosomes. In general, the distributions of the nucleosomes and DNA-associated protein-binding sites determine the higherorder physical structure of chromatin [14][15][16].…”

“…In general, the distributions of the nucleosomes and DNA-associated protein-binding sites determine the higherorder physical structure of chromatin [14][15][16]. This fact suggests that homologous chromosomes are structurally similar, whereas the structures of non-homologous chromosomes differ greatly.…”

“…Although S. pombe cells are usually haploid, they often become diploid through zygote formation and exhibit genetic recombination during meiotic prophase, as illustrated in Fig. 1(a, b) [11][12][13][14]. Thus, this organism has been considered as an ideal model for experimental studies of chromosomal dynamics during meiosis.…”