Chromosome Organization in Early Meiotic Prophase

One of the most fascinating aspects of meiosis is the extensive reorganization of the genome at the prophase of the first meiotic division (prophase I). The first steps of this reorganization are observed with the establishment of an axis structure, that connects sister chromatids, from which emanate arrays of chromatin loops. This axis structure, called the axial element, consists of various proteins, such as cohesins, HORMA-domain proteins, and axial element proteins. In many organisms, axial elements are required to set the stage for efficient sister chromatid cohesion and meiotic recombination, necessary for the recognition of the homologous chromosomes. Here, we review the different actors involved in axial element formation in Saccharomyces cerevisiae and in mouse. We describe the current knowledge of their localization pattern during prophase I, their functional interdependence, their role in sister chromatid cohesion, loop axis formation, homolog pairing before meiotic recombination, and recombination. We also address further challenges that need to be resolved, to fully understand the interplay between the chromosome structure and the different molecular steps that take place in early prophase I, which lead to the successful outcome of meiosis I.

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SOLO: a meiotic protein required for centromere cohesion, coorientation, and SMC1 localization in Drosophila melanogaster

The Journal of Cell Biology ◽

10.1083/jcb.200904040 ◽

2010 ◽

Vol 188 (3) ◽

pp. 335-349 ◽

Cited By ~ 24

Author(s):

Rihui Yan ◽

Sharon E. Thomas ◽

Jui-He Tsai ◽

Yukihiro Yamada ◽

Bruce D. McKee

Keyword(s):

Drosophila Melanogaster ◽

Sister Chromatid ◽

Sister Chromatid Cohesion ◽

Early Prophase ◽

Wild Type ◽

Sister Chromatids ◽

Chromatid Cohesion ◽

Mutant Phenotypes ◽

Meiosis I ◽

Novel Protein

Sister chromatid cohesion is essential to maintain stable connections between homologues and sister chromatids during meiosis and to establish correct centromere orientation patterns on the meiosis I and II spindles. However, the meiotic cohesion apparatus in Drosophila melanogaster remains largely uncharacterized. We describe a novel protein, sisters on the loose (SOLO), which is essential for meiotic cohesion in Drosophila. In solo mutants, sister centromeres separate before prometaphase I, disrupting meiosis I centromere orientation and causing nondisjunction of both homologous and sister chromatids. Centromeric foci of the cohesin protein SMC1 are absent in solo mutants at all meiotic stages. SOLO and SMC1 colocalize to meiotic centromeres from early prophase I until anaphase II in wild-type males, but both proteins disappear prematurely at anaphase I in mutants for mei-S332, which encodes the Drosophila homologue of the cohesin protector protein shugoshin. The solo mutant phenotypes and the localization patterns of SOLO and SMC1 indicate that they function together to maintain sister chromatid cohesion in Drosophila meiosis.

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TOP-2 is differentially required for the proper maintenance of cohesin on meiotic chromosomes in C. elegans spermatogenesis and oogenesis

10.1101/2021.12.26.474225 ◽

2021 ◽

Author(s):

Aimee Jaramillo-Lambert ◽

Christine Kiely Rourke

Keyword(s):

Sister Chromatid ◽

Topoisomerase Ii ◽

Meiotic Chromosome ◽

Sister Chromatid Cohesion ◽

Chromosome Length ◽

Aurora B ◽

Loss Of Function ◽

Late Prophase ◽

Prophase I ◽

Chromatid Cohesion

During meiotic prophase I, accurate segregation of homologous chromosomes requires the establishment of a chromosomes with a meiosis-specific architecture. Sister chromatid cohesins and the enzyme Topoisomerase II are important components of meiotic chromosome axes, but the relationship of these proteins in the context of meiotic chromosome segregation is poorly defined. Here, we analyzed the role of Topoisomerase II (TOP-2) in the timely release of sister chromatid cohesins during spermatogenesis and oogenesis of Caenorhabditis elegans. We show that there is a different requirement for TOP-2 in meiosis of spermatogenesis and oogenesis. The loss-of-function mutation top-2(it7) results in premature REC-8 removal in spermatogenesis, but not oogenesis. This is due to a failure to maintain the HORMA-domain proteins HTP-1 and HTP-2 (HTP-1/2) on chromosome axes at diakinesis and mislocalization of the downstream components that control sister chromatid cohesion release including Aurora B kinase. In oogenesis, top-2(it7) causes a delay in the localization of Aurora B to oocyte chromosomes but can be rescued through premature activation of the maturation promoting factor via knock-down of the inhibitor kinase WEE-1.3. The delay in Aurora B localization is associated with an increase in the length of diakinesis chromosomes and wee-1.3 RNAi mediated rescue of Auorora B localization in top-2(it7) is associated with a decrease in chromosome length. Our results imply that the sex-specific effects of Topoisomerase II on sister chromatid cohesion release are due to differences in the temporal regulation of meiosis and chromosome structure in late prophase I in spermatogenesis and oogenesis.

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The Multiple Roles of Cohesin in Meiotic Chromosome Morphogenesis and Pairing

Molecular Biology of the Cell ◽

10.1091/mbc.e08-06-0637 ◽

2009 ◽

Vol 20 (3) ◽

pp. 1030-1047 ◽

Cited By ~ 61

Author(s):

Gloria A. Brar ◽

Andreas Hochwagen ◽

Ly-sha S. Ee ◽

Angelika Amon

Keyword(s):

Sister Chromatid ◽

Meiotic Prophase ◽

Meiotic Chromosome ◽

Sister Chromatid Cohesion ◽

Multiple Roles ◽

Axis Formation ◽

Chromatid Cohesion ◽

Cohesin Subunit ◽

Chromosome Axis ◽

Segregation Of Chromosomes

Sister chromatid cohesion, mediated by cohesin complexes, is laid down during DNA replication and is essential for the accurate segregation of chromosomes. Previous studies indicated that, in addition to their cohesion function, cohesins are essential for completion of recombination, pairing, meiotic chromosome axis formation, and assembly of the synaptonemal complex (SC). Using mutants in the cohesin subunit Rec8, in which phosphorylated residues were mutated to alanines, we show that cohesin phosphorylation is not only important for cohesin removal, but that cohesin's meiotic prophase functions are distinct from each other. We find pairing and SC formation to be dependent on Rec8, but independent of the presence of a sister chromatid and hence sister chromatid cohesion. We identified mutations in REC8 that differentially affect Rec8's cohesion, pairing, recombination, chromosome axis and SC assembly function. These findings define Rec8 as a key determinant of meiotic chromosome morphogenesis and a central player in multiple meiotic events.

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