scholarly journals Divergent kleisin subunits of cohesin specify mechanisms to tether and release meiotic chromosomes

eLife ◽  
2014 ◽  
Vol 3 ◽  
Author(s):  
Aaron F Severson ◽  
Barbara J Meyer
Keyword(s):  
Synaptonemal Complex ◽  
Sister Chromatid ◽  
New Model ◽  
C Elegans ◽  
Meiotic Chromosomes ◽  
Crossover Site ◽  
Independent Functions ◽  
Chromatid Cohesion ◽  
Independent Mechanism ◽  
Chromosomal Territories

We show that multiple, functionally specialized cohesin complexes mediate the establishment and two-step release of sister chromatid cohesion that underlies the production of haploid gametes. In C. elegans, the kleisin subunits REC-8 and COH-3/4 differ between meiotic cohesins and endow them with distinctive properties that specify how cohesins load onto chromosomes and then trigger and release cohesion. Unlike REC-8 cohesin, COH-3/4 cohesin becomes cohesive through a replication-independent mechanism initiated by the DNA double-stranded breaks that induce crossover recombination. Thus, break-induced cohesion also tethers replicated meiotic chromosomes. Later, recombination stimulates separase-independent removal of REC-8 and COH-3/4 cohesins from reciprocal chromosomal territories flanking the crossover site. This region-specific removal likely underlies the two-step separation of homologs and sisters. Unexpectedly, COH-3/4 performs cohesion-independent functions in synaptonemal complex assembly. This new model for cohesin function diverges from that established in yeast but likely applies directly to plants and mammals, which utilize similar meiotic kleisins.

scholarly journals Shugoshin is essential for meiotic prophase checkpoints in C. elegans

2018 ◽  
Author(s):  
Tisha Bohr ◽  
Christian R. Nelson ◽  
Stefani Giacopazzi ◽  
Piero Lamelza ◽  
Needhi Bhalla
Keyword(s):  
Sister Chromatid ◽  
Meiotic Prophase ◽  
Meiotic Chromosome ◽  
Sister Chromatid Cohesion ◽  
Chromosomal Protein ◽  
Loss Of Function ◽  
Chromosome Architecture ◽  
C Elegans ◽  
Meiotic Chromosomes ◽  
Chromatid Cohesion

AbstractThe conserved factor Shugoshin is dispensable in C. elegans for the two-step loss of sister chromatid cohesion that directs the proper segregation of meiotic chromosomes. We show that the C. elegans ortholog of Shugoshin, SGO-1, is required for checkpoint activity in meiotic prophase. This role in checkpoint function is similar to that of the meiotic chromosomal protein, HTP-3. Null sgo-1 mutants exhibit additional phenotypes similar to that of a partial loss of function allele of HTP-3: premature synaptonemal complex disassembly, the activation of alternate DNA repair pathways and an inability to recruit a conserved effector of the DNA damage pathway, HUS-1. SGO-1 localizes to pre-meiotic nuclei, when HTP-3 is present but not yet loaded onto chromosome axes, suggesting an early role in regulating meiotic chromosome metabolism. We propose that SGO-1 acts during pre-meiotic replication to ensure fully functional meiotic chromosome architecture, rendering these chromosomes competent for checkpoint activity and normal progression of meiotic recombination. Given that most research on Shugoshin has been focused on its regulation of sister chromatid cohesion in meiosis, this novel role may be conserved but previously uncharacterized in other organisms. Further, our findings expand the repertoire of Shugoshin’s functions beyond coordinating regulatory activities at the centromere.

scholarly journals Phosphorylation of the synaptonemal complex protein SYP-1 promotes meiotic chromosome segregation

2017 ◽  
Author(s):  
Aya Sato-Carlton ◽  
Chihiro Nakamura-Tabuchi ◽  
Stephane Kazuki Chartrand ◽  
Tomoki Uchino ◽  
Peter Mark Carlton
Keyword(s):  
Synaptonemal Complex ◽  
Meiotic Chromosome ◽  
C Elegans ◽  
Chromosome Domains ◽  
Chromatid Cohesion ◽  
Complex Protein ◽  
Chromosomal Passenger ◽  
Synaptonemal Complex Protein ◽  
A Site ◽  
Meiosis I

AbstractChromosomes that have undergone crossing-over in meiotic prophase must maintain sister chromatid cohesion somewhere along their length between the first and second meiotic divisions. While many eukaryotes use the centromere as a site to maintain cohesion, the holocentric organism C. elegans instead creates two chromosome domains of unequal length termed the short arm and long arm, which become the first and second site of cohesion loss at meiosis I and II. The mechanisms that confer distinct functions to the short and long arm domains remain poorly understood. Here, we show that phosphorylation of the synaptonemal complex protein SYP-1 is required to create these domains. Once crossovers are made, phosphorylated SYP-1 and PLK-2 become cooperatively confined to short arms and guide phosphorylated histone H3 and the chromosomal passenger complex to the site of meiosis I cohesion loss. Our results show that PLK-2 and phosphorylated SYP-1 ensure creation of the short arm subdomain, promoting disjunction of chromosomes in meiosis I.

scholarly journals Meiotic cohesin REC8 marks the axial elements of rat synaptonemal complexes before cohesins SMC1β and SMC3

2003 ◽  
Vol 160 (5) ◽  
pp. 657-670 ◽  
Author(s):  
Maureen Eijpe ◽  
Hildo Offenberg ◽  
Rolf Jessberger ◽  
Ekaterina Revenkova ◽  
Christa Heyting
Keyword(s):  
Synaptonemal Complex ◽  
Sister Chromatid ◽  
Meiotic Prophase ◽  
S Phase ◽  
Synaptonemal Complexes ◽  
Sister Chromatids ◽  
Chromatid Cohesion ◽  
Axial Element ◽  
Striking Contrast ◽  
Metaphase I

In meiotic prophase, the sister chromatids of each chromosome develop a common axial element (AE) that is integrated into the synaptonemal complex (SC). We analyzed the incorporation of sister chromatid cohesion proteins (cohesins) and other AE components into AEs. Meiotic cohesin REC8 appeared shortly before premeiotic S phase in the nucleus and formed AE-like structures (REC8-AEs) from premeiotic S phase on. Subsequently, meiotic cohesin SMC1β, cohesin SMC3, and AE proteins SCP2 and SCP3 formed dots along REC8-AEs, which extended and fused until they lined REC8-AEs along their length. In metaphase I, SMC1β, SMC3, SCP2, and SCP3 disappeared from the chromosome arms and accumulated around the centromeres, where they stayed until anaphase II. In striking contrast, REC8 persisted along the chromosome arms until anaphase I and near the centromeres until anaphase II. We propose that REC8 provides a basis for AE formation and that the first steps in AE assembly do not require SMC1β, SMC3, SCP2, and SCP3. Furthermore, SMC1β, SMC3, SCP2, and SCP3 cannot provide arm cohesion during metaphase I. We propose that REC8 then provides cohesion. RAD51 and/or DMC1 coimmunoprecipitates with REC8, suggesting that REC8 may also provide a basis for assembly of recombination complexes.

scholarly journals Quantitative Cytogenetics Reveals Molecular Stoichiometry and Longitudinal Organization of Meiotic Chromosome Axes and Loops

2019 ◽  
Author(s):  
Alexander Woglar ◽  
Kei Yamaya ◽  
Baptiste Roelens ◽  
Alistair Boettiger ◽  
Simone Köhler ◽  
...  
Keyword(s):  
Sister Chromatid ◽  
De Novo ◽  
Meiotic Chromosome ◽  
S Phase ◽  
C Elegans ◽  
Sister Chromatids ◽  
Chromatid Cohesion ◽  
Molecular Bases ◽  
Chromosome Axis ◽  
Specialized Organization

ABSTRACTDuring meiosis, chromosomes adopt a specialized organization involving assembly of a cohesin-based axis along their lengths, with DNA loops emanating from this axis. We applied novel, quantitative and widely applicable cytogenetic strategies to elucidate the molecular bases of this organization using C. elegans. Analyses of WT chromosomes and de novo circular mini-chromosomes revealed that meiosis-specific HORMA-domain proteins assemble into cohorts in defined numbers and co-organize the axis together with two functionally-distinct cohesin complexes (REC-8 and COH-3/4) in defined stoichiometry. We further found that REC-8 cohesins, which load during S phase and mediate sister chromatid cohesion, usually occur as individual complexes, supporting a model wherein sister cohesion is mediated locally by a single cohesin ring. REC-8 complexes are interspersed in an alternating pattern with cohorts of axis-organizing COH-3/4 complexes (averaging three per cohort), which are insufficient to confer cohesion but can bind to individual chromatids, suggesting a mechanism to enable formation of asymmetric sister chromatid loops. Indeed, immuno-FISH assays demonstrate frequent asymmetry in genomic content between the loops formed on sister chromatids. We discuss how features of chromosome axis/loop architecture inferred from our data can help to explain enigmatic, yet essential, aspects of the meiotic program.

scholarly journals Revised and Improved Procedure for Immunolocalization of Male Meiotic Chromosomal Proteins and Spindle in Plants without the Use of Enzymes

Plants ◽  
2018 ◽  
Vol 7 (4) ◽  
pp. 93
Author(s):  
Kuntal De ◽  
Li Yuan ◽  
Christopher Makaroff
Keyword(s):  
Arabidopsis Thaliana ◽  
Chromosome Segregation ◽  
Sister Chromatid ◽  
Model Organism ◽  
Meiotic Spindle ◽  
Chromosomal Proteins ◽  
Meiotic Chromosomes ◽  
Wide Range ◽  
Chromatid Cohesion ◽  
Spindle Structure

Immunolocalization studies to visualize the distribution of proteins on meiotic chromosomes have become an integral part of studies on meiosis in the model organism Arabidopsis thaliana. These techniques have been used to visualize a wide range of meiotic proteins involved in different aspects of meiosis, including sister chromatid cohesion, recombination, synapsis, and chromosome segregation. However, the analysis of meiotic spindle structure by immunofluorescence is of outstanding importance in plant reproductive biology and is very challenging. In the following report, we describe the complete and easy protocol for the localization of proteins to the male meiotic spindle and male meiotic chromosomes. The protocol is fast, improved, and robust without the use of any harsh enzymes.

scholarly journals Caenorhabditis elegans EVL-14/PDS-5 and SCC-3 Are Essential for Sister Chromatid Cohesion in Meiosis and Mitosis

2003 ◽  
Vol 23 (21) ◽  
pp. 7698-7707 ◽  
Author(s):  
Fang Wang ◽  
John Yoder ◽  
Igor Antoshechkin ◽  
Min Han
Keyword(s):  
Caenorhabditis Elegans ◽  
Sister Chromatid ◽  
Positional Cloning ◽  
Germ Line ◽  
Sister Chromatid Cohesion ◽  
Late Prophase ◽  
C Elegans ◽  
Cell Divisions ◽  
Somatic Gonad ◽  
Chromatid Cohesion

ABSTRACT Sister chromatid cohesion is fundamental for the faithful transmission of chromosomes during both meiosis and mitosis. Proteins involved in this process are highly conserved from yeasts to humans. In screenings for sterile animals with abnormal vulval morphology, mutations in the Caenorhabditis elegans evl-14 and scc-3 genes were isolated. Defects in cell divisions were observed in germ line as well as in vulval and somatic gonad lineages. Through positional cloning of these genes, we have shown that EVL-14 and SCC-3 are likely the only C. elegans homologs of the yeast sister chromatid cohesion proteins Pds5 and Scc3, respectively. Both evl-14 and scc-3 mutants displayed defects in the meiotic germ line. In evl-14 mutants, synaptonemal complexes (SCs) were detectable but more than the usual six DAPI (4′,6′-diamidino-2-phenylindole)-positive structures were seen at diakinesis, suggesting that EVL-14/PDS-5 is important for the maintenance of sister chromatid cohesion in late prophase. In scc-3 mutant animals, normal SCs were not visible and ∼24 DAPI-positive structures were seen at diakinesis, indicating that SCC-3 is necessary for sister chromatid cohesion. Immunostaining revealed that localization of REC-8, a homolog of the yeast meiotic cohesin subunit Rec8, to the chromosomes depends on the presence of SCC-3 but not that of EVL-14/PDS-5. scc-3 RNA interference (RNAi)-treated embryos were 100% lethal and displayed defects in cell divisions. evl-14 RNAi caused a range of phenotypes. These results indicate that EVL-14/PDS-5 and SCC-3 have functions in both mitosis and meiosis.

scholarly journals Eco1-dependent cohesin acetylation anchors chromatin loops and cohesion to define functional meiotic chromosome domains

2021 ◽  
Author(s):  
Rachael E Barton ◽  
Lucia F Massari ◽  
Daniel Robertson ◽  
Adele L Marston
Keyword(s):  
Chromosome Segregation ◽  
Sister Chromatid ◽  
Meiotic Chromosome ◽  
Chromatin Loops ◽  
Meiotic Chromosomes ◽  
Sister Chromatids ◽  
Gamete Formation ◽  
Chromosome Domains ◽  
Chromatid Cohesion ◽  
Cohesin Subunit

Cohesin organizes the genome by forming intra-chromosomal loops and inter-sister chromatid linkages. During gamete formation by meiosis, chromosomes are reshaped to support crossover recombination and two consecutive rounds of chromosome segregation. Here we show that Eco1 acetyltransferase positions both chromatin loops and sister chromatid cohesion to organize meiotic chromosomes into functional domains in budding yeast. Eco1 acetylates the Smc3 cohesin subunit in meiotic S phase to establish chromatin boundaries, independently of DNA replication. Boundary formation by Eco1 is critical for prophase exit and for the maintenance of cohesion until meiosis II, but is independent of the ability of Eco1 to antagonize the cohesin-release factor, Wpl1. Conversely, prevention of cohesin release by Wpl1 is essential for centromeric cohesion, kinetochore monoorientation and co-segregation of sister chromatids in meiosis I. Our findings establish Eco1 as a key determinant of chromatin boundaries and cohesion positioning, revealing how local chromosome structuring directs genome transmission into gametes.

scholarly journals Handcuff for sisters: A new model for sister chromatid cohesion

Cell Cycle ◽  
2009 ◽  
Vol 8 (3) ◽  
pp. 399-402 ◽  
Author(s):  
Nenggang Zhang ◽  
Debananda Pati
Keyword(s):  
Sister Chromatid ◽  
Sister Chromatid Cohesion ◽  
New Model ◽  
Chromatid Cohesion
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