Meiotic Chromosome Dynamics Dependent Upon the rec8+, rec10+ and rec11+ Genes of the Fission Yeast Schizosaccharomyces pombe

Abstract During meiosis homologous chromosomes replicate once, pair, experience recombination, and undergo two rounds of segregation to produce haploid meiotic products. The rec8+, rec10+, and rec11+ genes of the fission yeast Schizosaccharomyces pombe exhibit similar specificities for meiotic recombination and rec8+ is required for sister chromatid cohesion and homolog pairing. We applied cytological and genetic approaches to identify potential genetic interactions and to gauge the fidelity of meiotic chromosome segregation in the mutants. The rec8+ gene was epistatic to rec10+ and to rec11+, but there was no clear epistatic relationship between rec10+ and rec11+. Reciprocal (crossover) recombination in the central regions of all three chromosomes was compromised in the rec mutants, but recombination near the telomeres was nearly normal. Each of the mutants also exhibited a high rate of aberrant segregation for all three chromosomes. The rec8 mutations affected mainly meiosis I segregation. Remarkably, the rec10 and rec11 mutations, which compromised recombination during meiosis I, affected mainly meiosis II segregation. We propose that these genes encode regulators or components of a “meiotic chromatid cohesion” pathway involved in establishing, maintaining, and appropriately releasing meiotic interactions between chromosomes. A model of synergistic interactions between sister chromatid cohesion and crossover position suggests how crossovers and cohesion help ensure the proper segregation of chromosomes in each of the meiotic divisions.

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Double or nothing: a Drosophila mutation affecting meiotic chromosome segregation in both females and males.

Genetics ◽

10.1093/genetics/136.3.953 ◽

1994 ◽

Vol 136 (3) ◽

pp. 953-964 ◽

Cited By ~ 2

Author(s):

D P Moore ◽

W Y Miyazaki ◽

J E Tomkiel ◽

T L Orr-Weaver

Keyword(s):

Cell Death ◽

Chromosome Segregation ◽

Sister Chromatid ◽

Meiotic Chromosome ◽

Sister Chromatid Cohesion ◽

Aberrant Chromosome ◽

Chromatid Cohesion ◽

Meiotic Nondisjunction ◽

Lethal Allele ◽

Meiosis I

Abstract We describe a Drosophila mutation, Double or nothing (Dub), that causes meiotic nondisjunction in a conditional, dominant manner. Previously isolated mutations in Drosophila specifically affect meiosis either in females or males, with the exception of the mei-S332 and ord genes which are required for proper sister-chromatid cohesion. Dub is unusual in that it causes aberrant chromosome segregation almost exclusively in meiosis I in both sexes. In Dub mutant females both nonexchange and exchange chromosomes undergo nondisjunction, but the effect of Dub on nonexchange chromosomes is more pronounced. Dub reduces recombination levels slightly. Multiple nondisjoined chromosomes frequently cosegregate to the same pole. Dub results in nondisjunction of all chromosomes in meiosis I of males, although the levels are lower than in females. When homozygous, Dub is a conditional lethal allele and exhibits phenotypes consistent with cell death.

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Rec8p, a Meiotic Recombination and Sister Chromatid Cohesion Phosphoprotein of the Rad21p Family Conserved from Fission Yeast to Humans

Molecular and Cellular Biology ◽

10.1128/mcb.19.5.3515 ◽

1999 ◽

Vol 19 (5) ◽

pp. 3515-3528 ◽

Cited By ~ 144

Author(s):

Sandro Parisi ◽

Michael J. McKay ◽

Monika Molnar ◽

M. Anne Thompson ◽

Peter J. van der Spek ◽

...

Keyword(s):

Fission Yeast ◽

Sister Chromatid ◽

Germ Line ◽

Sequence Similarity ◽

Sister Chromatid Cohesion ◽

Specific Expression ◽

Chromatid Cohesion ◽

Prophase Nucleus ◽

Chromosome Iii ◽

Meiosis I

ABSTRACT Our work and that of others defined mitosis-specific (Rad21 subfamily) and meiosis-specific (Rec8 subfamily) proteins involved in sister chromatid cohesion in several eukaryotes, including humans. Mutation of the fission yeast Schizosaccharomyces pombe rec8 gene was previously shown to confer a number of meiotic phenotypes, including strong reduction of recombination frequencies in the central region of chromosome III, absence of linear element polymerization, reduced pairing of homologous chromosomes, reduced sister chromatid cohesion, aberrant chromosome segregation, defects in spore formation, and reduced spore viability. Here we extend the description of recombination reduction to the central regions of chromosomes I and II. We show at the protein level that expression ofrec8 is meiosis specific and that Rec8p localizes to approximately 100 foci per prophase nucleus. Rec8p was present in an unphosphorylated form early in meiotic prophase but was phosphorylated prior to meiosis I, as demonstrated by analysis of the mei4mutant blocked before meiosis I. Evidence for the persistence of Rec8p beyond meiosis I was obtained by analysis of the mutantmes1 blocked before meiosis II. A human gene, which we designate hrec8, showed significant primary sequence similarity to rec8 and was mapped to chromosome 14. High mRNA expression of mouse and human rec8 genes was found only in germ line cells, specifically in testes and, interestingly, in spermatids. hrec8 was also expressed at a low level in the thymus. Sequence similarity and testis-specific expression indicate evolutionarily conserved functions of Rec8p in meiosis. Possible roles of Rec8p in the integration of different meiotic events are discussed.

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Cis-acting determinants affecting centromere function, sister-chromatid cohesion and reciprocal recombination during meiosis in Saccharomyces cerevisiae.

Genetics ◽

10.1093/genetics/139.3.1159 ◽

1995 ◽

Vol 139 (3) ◽

pp. 1159-1173 ◽

Cited By ~ 2

Author(s):

D D Sears ◽

J H Hegemann ◽

J H Shero ◽

P Hieter

Keyword(s):

Gene Conversion ◽

Sister Chromatid ◽

Meiotic Chromosome ◽

Critical Role ◽

Sister Chromatid Cohesion ◽

Wild Type ◽

Artificial Chromosomes ◽

Centromere Function ◽

Chromatid Cohesion ◽

Meiosis I

Abstract We have employed a system that utilizes homologous pairs of human DNA-derived yeast artificial chromosomes (YACs) as marker chromosomes to assess the specific role(s) of conserved centromere DNA elements (CDEI, CDEII and CDEIII) in meiotic chromosome disjunction fidelity. Thirteen different centromere (CEN) mutations were tested for their effects on meiotic centromere function. YACs containing a wild-type CEN DNA sequence segregate with high fidelity in meiosis I (99% normal segregation) and in meiosis II (96% normal segregation). YACs containing a 31-bp deletion mutation in centromere DNA element II (CDEII delta 31) in either a heterocentric (mutant/wild type), homocentric (mutant/mutant) or monosomic (mutant/--) YAC pair configuration exhibited high levels (16-28%) of precocious sister-chromatid segregation (PSS) and increased levels (1-6%) of nondisjunction meiosis I (NDI). YACs containing this mutation also exhibit high levels (21%) of meiosis II nondisjunction. Interestingly, significant alterations in homolog recombination frequency were observed in the exceptional PSS class of tetrads, suggesting unusual interactions between prematurely separated sister chromatids and their homologous nonsister chromatids. We also have assessed the meiotic segregation effects of rare gene conversion events occurring at sites located immediately adjacent to or distantly from the centromere region. Proximal gene conversion events were associated with extremely high levels (60%) of meiosis I segregation errors (including both PSS and NDI), whereas distal events had no apparent effect. Taken together, our results indicate a critical role for CDEII in meiosis and underscore the importance of maintaining sister-chromatid cohesion for proper recombination in meiotic prophase and for proper disjunction in meiosis I.

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Faculty Opinions recommendation of Protein phosphatase 2A protects centromeric sister chromatid cohesion during meiosis I.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.1023795.367924 ◽

2006 ◽

Author(s):

Jonathan Millar

Keyword(s):

Sister Chromatid ◽

Protein Phosphatase ◽

Protein Phosphatase 2A ◽

Sister Chromatid Cohesion ◽

Chromatid Cohesion ◽

Phosphatase 2A ◽

Meiosis I

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Multiple Subunits of the Caenorhabditis elegans Anaphase-Promoting Complex Are Required for Chromosome Segregation During Meiosis I

Genetics ◽

10.1093/genetics/160.2.805 ◽

2002 ◽

Vol 160 (2) ◽

pp. 805-813 ◽

Cited By ~ 3

Author(s):

Edward S Davis ◽

Lucia Wille ◽

Barry A Chestnut ◽

Penny L Sadler ◽

Diane C Shakes ◽

...

Keyword(s):

Rna Interference ◽

Caenorhabditis Elegans ◽

Chromosome Segregation ◽

Sister Chromatid ◽

Sister Chromatid Cohesion ◽

Anaphase Promoting Complex ◽

Genetic Screens ◽

Chromatid Cohesion ◽

Interference Studies ◽

Meiosis I

Abstract Two genes, originally identified in genetic screens for Caenorhabditis elegans mutants that arrest in metaphase of meiosis I, prove to encode subunits of the anaphase-promoting complex or cyclosome (APC/C). RNA interference studies reveal that these and other APC/C subunits are essential for the segregation of chromosomal homologs during meiosis I. Further, chromosome segregation during meiosis I requires APC/C functions in addition to the release of sister chromatid cohesion.

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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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Fission yeast Pds5 is required for accurate chromosome segregation and for survival after DNA damage or metaphase arrest

Journal of Cell Science ◽

10.1242/jcs.115.3.587 ◽

2002 ◽

Vol 115 (3) ◽

pp. 587-598 ◽

Cited By ~ 3

Author(s):

Shao-Win Wang ◽

Rebecca L. Read ◽

Chris J. Norbury

Keyword(s):

Dna Damage ◽

Fission Yeast ◽

Sister Chromatid ◽

Budding Yeast ◽

Eukaryotic Cell ◽

Sister Chromatid Cohesion ◽

Chromosome Loss ◽

Dependent Manner ◽

Yeast Saccharomyces Cerevisiae ◽

Chromatid Cohesion

Sister chromatid cohesion, which is established during the S phase of the eukaryotic cell cycle and persists until the onset of anaphase, is essential for the maintenance of genomic integrity. Cohesion requires the multi-protein complex cohesin, as well as a number of accessory proteins including Pds5/BIMD/Spo76. In the budding yeast Saccharomyces cerevisiae Pds5 is an essential protein that localises to chromosomes in a cohesin-dependent manner. Here we describe the characterisation in the fission yeast Schizosaccharomyces pombe of pds5+, a novel,non-essential orthologue of S. cerevisiae PDS5. The S. pombePds5 protein was localised to punctate nuclear foci in a manner that was dependent on the Rad21 cohesin component. This, together with additional genetic evidence, points towards an involvement of S. pombe Pds5 in sister chromatid cohesion. S. pombe pds5 mutants were hypersensitive to DNA damage and to mitotic metaphase delay, but this sensitivity was apparently not due to precocious loss of sister chromatid cohesion. These cells also suffered increased spontaneous chromosome loss and meiotic defects and their viability was dependent on the spindle checkpoint protein Bub1. Thus, while S. pombe Pds5 has an important cohesin-related role, this differs significantly from that of the equivalent budding yeast protein.

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