scholarly journals Meiotic recombination modulates the structure and dynamics of the synaptonemal complex during C. elegans meiosis

2017 ◽  
Author(s):  
Divya Pattabiraman ◽  
Baptiste Roelens ◽  
Alexander Woglar ◽  
Anne M. Villeneuve
Keyword(s):  
Synaptonemal Complex ◽  
Central Region ◽  
Meiotic Recombination ◽  
Meiotic Prophase ◽  
Dynamic Properties ◽  
Stable State ◽  
Dynamic State ◽  
Homologous Chromosomes ◽  
C Elegans ◽  
A Site

AbstractDuring meiotic prophase, a structure called the synaptonemal complex (SC) assembles at the interface between aligned pairs of homologous chromosomes, and crossover recombination events occur between their DNA molecules. Here we investigate the inter-relationships between these two hallmark features of the meiotic program in the nematode C. elegans, revealing dynamic properties of the SC that are modulated by recombination. We demonstrate that the SC incorporates new subunits and switches from a more highly dynamic/labile state to a more stable state as germ cells progress through the pachytene stage of meiotic prophase. We further show that the more dynamic state of the SC is prolonged in mutants where meiotic recombination is impaired. Moreover, in meiotic mutants where recombination intermediates are present in limiting numbers, SC central region subunits become preferentially stabilized on the subset of chromosome pairs that harbor a site where pro-crossover factors COSA-1 and MutSγ are concentrated. Polo-like kinase PLK-2 becomes preferentially localized to the SCs of chromosome pairs harboring recombination sites prior to the enrichment of SC central region proteins on such chromosomes, and PLK-2 is required for this enrichment to occur. Further, late pachytene nuclei in a plk-2 mutant exhibit the more highly dynamic SC state. Together our data demonstrate that crossover recombination events elicit chromosome-autonomous stabilizing effects on the SC and implicate PLK-2 in this process. We discuss how this recombination-triggered modulation of SC state might contribute to regulatory mechanisms that operate during meiosis to ensure the formation of crossovers while at the same time limiting their numbers.

scholarly journals Polo-like kinase-dependent phosphorylation of the synaptonemal complex protein SYP-4 regulates double-strand break formation through a negative feedback loop.

eLife ◽  
2017 ◽  
Vol 6 ◽  
Author(s):  
Saravanapriah Nadarajan ◽  
Talley J Lambert ◽  
Elisabeth Altendorfer ◽  
Jinmin Gao ◽  
Michael D Blower ◽  
...  
Keyword(s):  
Synaptonemal Complex ◽  
Central Region ◽  
Feedback Loop ◽  
Strand Break ◽  
Dynamic State ◽  
Strand Breaks ◽  
Homologous Chromosomes ◽  
C Elegans ◽  
Complex Protein ◽  
Synaptonemal Complex Protein

The synaptonemal complex (SC) is an ultrastructurally conserved proteinaceous structure that holds homologous chromosomes together and is required for the stabilization of pairing interactions and the completion of crossover (CO) formation between homologs during meiosis I. Here, we identify a novel role for a central region component of the SC, SYP-4, in negatively regulating formation of recombination-initiating double-strand breaks (DSBs) via a feedback loop triggered by crossover designation in C. elegans. We found that SYP-4 is phosphorylated dependent on Polo-like kinases PLK-1/2. SYP-4 phosphorylation depends on DSB formation and crossover designation, is required for stabilizing the SC in pachytene by switching the central region of the SC from a more dynamic to a less dynamic state, and negatively regulates DSB formation. We propose a model in which Polo-like kinases recognize crossover designation and phosphorylate SYP-4 thereby stabilizing the SC and making chromosomes less permissive for further DSB formation.

scholarly journals Crossover patterning through kinase-regulated condensation and coarsening of recombination nodules

2021 ◽  
Author(s):  
Liangyu Zhang ◽  
Weston Stauffer ◽  
David Zwicker ◽  
Abby F. Dernburg
Keyword(s):  
Synaptonemal Complex ◽  
Meiotic Recombination ◽  
Ring Domain ◽  
Homologous Chromosomes ◽  
Crossover Interference ◽  
C Elegans ◽  
Recombination Nodules

AbstractMeiotic recombination is highly regulated to ensure precise segregation of homologous chromosomes. Evidence from diverse organisms indicates that the synaptonemal complex (SC), which assembles between paired chromosomes, plays essential roles in crossover formation and patterning. Several additional “pro-crossover” proteins are also required for recombination intermediates to become crossovers. These typically form multiple foci or recombination nodules along SCs, and later accumulate at fewer, widely spaced sites. Here we report that in C. elegans CDK-2 is required to stabilize all crossover intermediates and stabilizes interactions among pro-crossover factors by phosphorylating MSH-5. Additionally, we show that the conserved RING domain proteins ZHP-3/4 diffuse along the SC and remain dynamic following their accumulation at recombination sites. Based on these and previous findings we propose a model in which recombination nodules arise through spatially restricted biomolecular condensation and then undergo a regulated coarsening process, resulting in crossover interference.

Rec8 cohesin-mediated loop-axis chromatin architecture is required for meiotic recombination

2021 ◽  
Author(s):  
Takeshi Sakuno ◽  
Sanki Tashiro ◽  
Hideki Tanizawa ◽  
Osamu Iwasaki ◽  
Da-Qiao Ding ◽  
...  
Keyword(s):  
Fission Yeast ◽  
Synaptonemal Complex ◽  
Meiotic Recombination ◽  
Meiotic Prophase ◽  
Essential Role ◽  
Homologous Chromosomes ◽  
Functional Correlation ◽  
Chromatin Architecture ◽  
Central Elements ◽  
Linear Elements

During meiotic prophase, cohesin-dependent axial structures are formed in the synaptonemal complex (SC). However, the functional correlation between these structures and cohesion remains elusive. Here, we examined the formation of the cohesin-dependent axial structure in fission yeast, which forms atypical SCs composed of linear elements (LinEs) resembling the lateral elements of SC but lacking the central elements. The results demonstrated that Rec8 cohesin is crucial for the formation of the loop-axis structure within the atypical SC. Furthermore, the Rec8-mediated loop-axis structure is formed in the absence of LinEs and provides a structural platform for aligning homologous chromosomes. We also identified a rec8 mutant that lost the ability to assemble the loop-axis structure without losing cohesion. Remarkably, this mutant showed defects in the LinE assembly, resulting in a significant reduction in meiotic recombination. Collectively, our results demonstrate an essential role for the Rec8-dependent loop-axis structure in LinE assembly, facilitating meiotic recombination.

scholarly journals Lateral Elements Inside Synaptonemal Complex-Like Polycomplexes in ndt80 Mutants of Yeast Bind DNA

Genetics ◽  
2003 ◽  
Vol 163 (2) ◽  
pp. 539-544 ◽  
Author(s):  
Hasanuzzaman Bhuiyan ◽  
Gunilla Dahlfors ◽  
Karin Schmekel
Keyword(s):  
In Situ Hybridization ◽  
Electron Microscope ◽  
Synaptonemal Complex ◽  
Immunoelectron Microscopy ◽  
Meiotic Prophase ◽  
Lateral Element ◽  
Homologous Chromosomes ◽  
Meiotic Prophase I ◽  
Dna Antibodies

Abstract The synaptonemal complex (SC) keeps the synapsed homologous chromosomes together during pachytene in meiotic prophase I. Structures that resemble stacks of SCs, polycomplexes, are sometimes found before or after pachytene. We have investigated ndt80 mutants of yeast, which arrest in pachytene. SCs appear normal in spread chromosome preparations, but are only occasionally found in intact nuclei examined in the electron microscope. Instead, large polycomplexes occur in almost every ndt80 mutant nucleus. Immunoelectron microscopy using DNA antibodies show strong preferential labeling to the lateral element parts of the polycomplexes. In situ hybridization using chromosome-specific probes confirms that the chromosomes in ndt80 mutants are paired and attached to the SCs. Our results suggest that polycomplexes can be involved in binding of chromosomes and possibly also in synapsis.

scholarly journals Synaptonemal Complex dimerization regulates chromosome alignment and crossover patterning in meiosis

2020 ◽  
Author(s):  
Spencer G. Gordon ◽  
Lisa E. Kursel ◽  
Kewei Xu ◽  
Ofer Rog
Keyword(s):  
Synaptonemal Complex ◽  
Sequence Homology ◽  
Genetic Information ◽  
Large Scale ◽  
Molecular Mechanisms ◽  
Homologous Chromosomes ◽  
C Elegans ◽  
Local Sequence ◽  
Chromosome Alignment ◽  
Dimerization Interface

AbstractDuring sexual reproduction the parental homologous chromosomes find each other (pair) and align along their lengths by integrating local sequence homology with large-scale contiguity, thereby allowing for precise exchange of genetic information. The Synaptonemal Complex (SC) is a conserved zipper-like structure that assembles between the homologous chromosomes. This phase-separated interface brings chromosomes together and regulates exchanges between them. However, the molecular mechanisms by which the SC carries out these functions remain poorly understood. Here we isolated and characterized two mutations in the dimerization interface in the middle of the SC zipper in C. elegans. The mutations perturb both chromosome alignment and the regulation of genetic exchanges. Underlying the chromosome-scale phenotypes are distinct alterations to the way SC subunits interact with one another. We propose that the SC brings homologous chromosomes together through two biophysical activities: obligate dimerization that prevents assembly on unpaired chromosomes; and a tendency to phase-separate that extends pairing interactions along the entire length of the chromosomes.

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 Crossing over is coupled to late meiotic prophase bivalent differentiation through asymmetric disassembly of the SC

2005 ◽  
Vol 168 (5) ◽  
pp. 683-689 ◽  
Author(s):  
Kentaro Nabeshima ◽  
Anne M. Villeneuve ◽  
Monica P. Colaiácovo
Keyword(s):  
Caenorhabditis Elegans ◽  
Symmetry Breaking ◽  
Synaptonemal Complex ◽  
Central Region ◽  
Meiotic Prophase ◽  
Homologous Chromosome ◽  
Meiotic Chromosome ◽  
Crossing Over ◽  
Γ Irradiation ◽  
Irradiation Treatment

Homologous chromosome pairs (bivalents) undergo restructuring during meiotic prophase to convert a configuration that promotes crossover recombination into one that promotes bipolar spindle attachment and localized cohesion loss. We have imaged remodeling of meiotic chromosome structures after pachytene exit in Caenorhabditis elegans. Chromosome shortening during diplonema is accompanied by coiling of chromosome axes and highly asymmetric departure of synaptonemal complex (SC) central region proteins SYP-1 and SYP-2, which diminish over most of the length of each desynapsing bivalent while becoming concentrated on axis segments distal to the single emerging chiasma. This and other manifestations of asymmetry along chromosomes are lost in synapsis-proficient crossover-defective mutants, which often retain SYP-1,2 along the full lengths of coiled diplotene axes. Moreover, a γ-irradiation treatment that restores crossovers in the spo-11 mutant also restores asymmetry of SYP-1 localization. We propose that crossovers or crossover precursors serve as symmetry-breaking events that promote differentiation of subregions of the bivalent by triggering asymmetric disassembly of the SC.

The desynaptic mutant of maize as a combined defect of synaptonemal complex and chiasma maintenance

Genome ◽  
1991 ◽  
Vol 34 (6) ◽  
pp. 879-887 ◽  
Author(s):  
M. P. Maguire ◽  
A. M. Paredes ◽  
R. W. Riess
Keyword(s):  
Electron Microscopy ◽  
Synaptonemal Complex ◽  
Central Region ◽  
Meiotic Prophase ◽  
Heterochromatic Region ◽  
Crossing Over ◽  
Related Strain ◽  
Normal Cells ◽  
Normal Crossing ◽  
Mutant Cells

The phenotype of the desynaptic (dy) mutant of maize in microsporocytes at meiotic prophase was compared with normal microsporocytes of a closely related strain and with microsporocytes of a maize inbred line (KYS) assumed to be normal. Strikingly more univalents and open arms of bivalents were found in the mutant cells than in normal cells at diakinesis, and where there was heterozygosity for a distal knob (heterochromatic region), separation was usually equational, indicating the occurrence of normal crossing-over followed by failure of chiasma maintenance in the mutant. Differences found in the mutant by electron microscopy were a statistically significant wider dimension of the synaptonemal complex central region and also less twisting of synapsed configurations at pachytene. It is suggested that these are side-effect symptoms of a defect in the synaptonemal complex (or associated substance), which is expressed later as sporadic loss of chiasma maintenance.Key words: desynaptic, chiasma maintenance, synaptonemal complex.

scholarly journals akirin is required for diakinesis bivalent structure and synaptonemal complex disassembly at meiotic prophase I

2013 ◽  
Vol 24 (7) ◽  
pp. 1053-1067 ◽  
Author(s):  
Amy M. Clemons ◽  
Heather M. Brockway ◽  
Yizhi Yin ◽  
Bhavatharini Kasinathan ◽  
Yaron S. Butterfield ◽  
...  
Keyword(s):  
Synaptonemal Complex ◽  
Meiotic Prophase ◽  
Chromosome Condensation ◽  
Late Prophase ◽  
Homologous Chromosomes ◽  
Prophase I ◽  
Meiotic Prophase I ◽  
Evolutionarily Conserved ◽  
Key Events

During meiosis, evolutionarily conserved mechanisms regulate chromosome remodeling, leading to the formation of a tight bivalent structure. This bivalent, a linked pair of homologous chromosomes, is essential for proper chromosome segregation in meiosis. The formation of a tight bivalent involves chromosome condensation and restructuring around the crossover. The synaptonemal complex (SC), which mediates homologous chromosome association before crossover formation, disassembles concurrently with increased condensation during bivalent remodeling. Both chromosome condensation and SC disassembly are likely critical steps in acquiring functional bivalent structure. The mechanisms controlling SC disassembly, however, remain unclear. Here we identify akir-1 as a gene involved in key events of meiotic prophase I in Caenorhabditis elegans. AKIR-1 is a protein conserved among metazoans that lacks any previously known function in meiosis. We show that akir-1 mutants exhibit severe meiotic defects in late prophase I, including improper disassembly of the SC and aberrant chromosome condensation, independently of the condensin complexes. These late-prophase defects then lead to aberrant reconfiguring of the bivalent. The meiotic divisions are delayed in akir-1 mutants and are accompanied by lagging chromosomes. Our analysis therefore provides evidence for an important role of proper SC disassembly in configuring a functional bivalent structure.

scholarly journals A Cytoplasmic Dynein Heavy Chain Is Required for Oscillatory Nuclear Movement of Meiotic Prophase and Efficient Meiotic Recombination in Fission Yeast

1999 ◽  
Vol 145 (6) ◽  
pp. 1233-1250 ◽  
Author(s):  
Ayumu Yamamoto ◽  
Robert R. West ◽  
J. Richard McIntosh ◽  
Yasushi Hiraoka
Keyword(s):  
Fission Yeast ◽  
Heavy Chain ◽  
Meiotic Recombination ◽  
Meiotic Prophase ◽  
Fluorescent Protein ◽  
Cytoplasmic Dynein ◽  
Spindle Pole ◽  
Nuclear Movement ◽  
Homologous Chromosomes ◽  
Dynein Heavy Chain

Meiotic recombination requires pairing of homologous chromosomes, the mechanisms of which remain largely unknown. When pairing occurs during meiotic prophase in fission yeast, the nucleus oscillates between the cell poles driven by astral microtubules. During these oscillations, the telomeres are clustered at the spindle pole body (SPB), located at the leading edge of the moving nucleus and the rest of each chromosome dangles behind. Here, we show that the oscillatory nuclear movement of meiotic prophase is dependent on cytoplasmic dynein. We have cloned the gene encoding a cytoplasmic dynein heavy chain of fission yeast. Most of the cells disrupted for the gene show no gross defect during mitosis and complete meiosis to form four viable spores, but they lack the nuclear movements of meiotic prophase. Thus, the dynein heavy chain is required for these oscillatory movements. Consistent with its essential role in such nuclear movement, dynein heavy chain tagged with green fluorescent protein (GFP) is localized at astral microtubules and the SPB during the movements. In dynein-disrupted cells, meiotic recombination is significantly reduced, indicating that the dynein function is also required for efficient meiotic recombination. In accordance with the reduced recombination, which leads to reduced crossing over, chromosome missegregation is increased in the mutant. Moreover, both the formation of a single cluster of centromeres and the colocalization of homologous regions on a pair of homologous chromosomes are significantly inhibited in the mutant. These results strongly suggest that the dynein-driven nuclear movements of meiotic prophase are necessary for efficient pairing of homologous chromosomes in fission yeast, which in turn promotes efficient meiotic recombination.

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