scholarly journals The synaptonemal complex has liquid crystalline properties and spatially regulates meiotic recombination factors

eLife ◽  
2017 ◽  
Vol 6 ◽  
Author(s):  
Ofer Rog ◽  
Simone Köhler ◽  
Abby F Dernburg
Keyword(s):  
Signal Transduction ◽  
Synaptonemal Complex ◽  
Meiotic Recombination ◽  
Liquid Crystalline ◽  
Hydrophobic Interactions ◽  
Rapid Evolution ◽  
Three Dimensional ◽  
Homologous Chromosomes ◽  
Meiotic Progression ◽  
Meiotic Chromosomes

The synaptonemal complex (SC) is a polymer that spans ~100 nm between paired homologous chromosomes during meiosis. Its striated, periodic appearance in electron micrographs led to the idea that transverse filaments within this structure ‘crosslink’ the axes of homologous chromosomes, stabilizing their pairing. SC proteins can also form polycomplexes, three-dimensional lattices that recapitulate the periodic structure of SCs but do not associate with chromosomes. Here we provide evidence that SCs and polycomplexes contain mobile subunits and that their assembly is promoted by weak hydrophobic interactions, indicative of a liquid crystalline phase. We further show that in the absence of recombination intermediates, polycomplexes recapitulate the dynamic localization of pro-crossover factors during meiotic progression, revealing how the SC might act as a conduit to regulate chromosome-wide crossover distribution. Properties unique to liquid crystals likely enable long-range signal transduction along meiotic chromosomes and underlie the rapid evolution of SC proteins.

scholarly journals Mammalian BLM helicase is critical for integrating multiple pathways of meiotic recombination

2010 ◽  
Vol 188 (6) ◽  
pp. 779-789 ◽  
Author(s):  
J. Kim Holloway ◽  
Meisha A. Morelli ◽  
Peter L. Borst ◽  
Paula E. Cohen
Keyword(s):  
Meiotic Recombination ◽  
Genome Stability ◽  
Autosomal Recessive Disorder ◽  
Dna Structures ◽  
Homologous Chromosomes ◽  
Recq Helicases ◽  
Meiotic Progression ◽  
Meiotic Chromosomes ◽  
Conditional Mutant ◽  
Blm Helicase

Bloom’s syndrome (BS) is an autosomal recessive disorder characterized by growth retardation, cancer predisposition, and sterility. BS mutated (Blm), the gene mutated in BS patients, is one of five mammalian RecQ helicases. Although BLM has been shown to promote genome stability by assisting in the repair of DNA structures that arise during homologous recombination in somatic cells, less is known about its role in meiotic recombination primarily because of the embryonic lethality associated with Blm deletion. However, the localization of BLM protein on meiotic chromosomes together with evidence from yeast and other organisms implicates a role for BLM helicase in meiotic recombination events, prompting us to explore the meiotic phenotype of mice bearing a conditional mutant allele of Blm. In this study, we show that BLM deficiency does not affect entry into prophase I but causes severe defects in meiotic progression. This is exemplified by improper pairing and synapsis of homologous chromosomes and altered processing of recombination intermediates, resulting in increased chiasmata. Our data provide the first analysis of BLM function in mammalian meiosis and strongly argue that BLM is involved in proper pairing, synapsis, and segregation of homologous chromosomes; however, it is dispensable for the accumulation of recombination intermediates.

scholarly journals A compartmentalized signaling network mediates crossover control in meiosis

eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Liangyu Zhang ◽  
Simone Köhler ◽  
Regina Rillo-Bohn ◽  
Abby F Dernburg
Keyword(s):  
Caenorhabditis Elegans ◽  
Symmetry Breaking ◽  
Synaptonemal Complex ◽  
Chromosome Segregation ◽  
Molecular Basis ◽  
Liquid Crystalline ◽  
Ring Finger ◽  
Homologous Chromosomes ◽  
Crossover Interference ◽  
Ring Finger Proteins

During meiosis, each pair of homologous chromosomes typically undergoes at least one crossover (crossover assurance), but these exchanges are strictly limited in number and widely spaced along chromosomes (crossover interference). The molecular basis for this chromosome-wide regulation remains mysterious. A family of meiotic RING finger proteins has been implicated in crossover regulation across eukaryotes. Caenorhabditis elegans expresses four such proteins, of which one (ZHP-3) is known to be required for crossovers. Here we investigate the functions of ZHP-1, ZHP-2, and ZHP-4. We find that all four ZHP proteins, like their homologs in other species, localize to the synaptonemal complex, an unusual, liquid crystalline compartment that assembles between paired homologs. Together they promote accumulation of pro-crossover factors, including ZHP-3 and ZHP-4, at a single recombination intermediate, thereby patterning exchanges along paired chromosomes. These proteins also act at the top of a hierarchical, symmetry-breaking process that enables crossovers to direct accurate chromosome segregation.

scholarly journals ZYP1 is required for obligate cross-over formation and cross-over interference in Arabidopsis

2021 ◽  
Vol 118 (14) ◽  
pp. e2021671118
Author(s):  
Martin G. France ◽  
Janina Enderle ◽  
Sarah Röhrig ◽  
Holger Puchta ◽  
F. Chris H. Franklin ◽  
...  
Keyword(s):  
Genetic Analysis ◽  
Synaptonemal Complex ◽  
Class Ii ◽  
Class I ◽  
Crossing Over ◽  
Wild Type ◽  
Homologous Chromosomes ◽  
Virtual Absence ◽  
Meiotic Progression ◽  
Null Mutants

The synaptonemal complex is a tripartite proteinaceous ultrastructure that forms between homologous chromosomes during prophase I of meiosis in the majority of eukaryotes. It is characterized by the coordinated installation of transverse filament proteins between two lateral elements and is required for wild-type levels of crossing over and meiotic progression. We have generated null mutants of the duplicated Arabidopsis transverse filament genes zyp1a and zyp1b using a combination of T-DNA insertional mutants and targeted CRISPR/Cas mutagenesis. Cytological and genetic analysis of the zyp1 null mutants reveals loss of the obligate chiasma, an increase in recombination map length by 1.3- to 1.7-fold and a virtual absence of cross-over (CO) interference, determined by a significant increase in the number of double COs. At diplotene, the numbers of HEI10 foci, a marker for Class I interference-sensitive COs, are twofold greater in the zyp1 mutant compared to wild type. The increase in recombination in zyp1 does not appear to be due to the Class II interference-insensitive COs as chiasmata were reduced by ∼52% in msh5/zyp1 compared to msh5. These data suggest that ZYP1 limits the formation of closely spaced Class I COs in Arabidopsis. Our data indicate that installation of ZYP1 occurs at ASY1-labeled axial bridges and that loss of the protein disrupts progressive coalignment of the chromosome axes.

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.

Three-Dimensional reconstruction of the synaptonemal complex from high-pressure frozen maize meiocytes using IVEM Tomography

1994 ◽  
Vol 52 ◽  
pp. 14-15
Author(s):  
Jennifer C. Fung ◽  
David A. Agard ◽  
John W. Sedat
Keyword(s):  
Synaptonemal Complex ◽  
Three Dimensional ◽  
Central Element ◽  
Homologous Chromosomes ◽  
Macromolecular Assembly ◽  
Dimensional Reconstruction ◽  
Protein Components ◽  
Basic Features ◽  
General Architecture ◽  
Internal Architecture

The synaptonemal complex (SC) is a key macromolecular assembly formed during meiosis of most eukaryotes. It has a crucial role in maintaining synapsis between homologous chromosomes and in ensuring proper segregation of the homologs through the establishment of functional chiasmata. Recently, biochemical and genetic efforts have begun to identify some of the protein components of the SC. As these efforts progress, a more detailed analysis of SC structure will also be needed to incorporate these new components into the overall organization of the SC.Early efforts into the analysis of SC structure have established that its general architecture is conserved throughout many organisms. The basic features found in every SC are the two lateral elements and the central element, both which run longitudinally between the homologs during the pachytene stage of prophase I. Transverse elements which run perpendicular to the homolog axis through the central region are also often found. Although the general features of the SC are conserved, the internal architecture of these components can differ.

Three-Dimensional reconstruction of the synaptonemal complex from pachytene maize meiocytes using Electron Microscopy tomography

1993 ◽  
Vol 51 ◽  
pp. 182-183
Author(s):  
Jennifer C. Fung ◽  
Bethe A. Scalettar ◽  
David A. Agard ◽  
John W. Sedat
Keyword(s):  
Electron Microscopy ◽  
Synaptonemal Complex ◽  
Chromosome Segregation ◽  
Three Dimensional ◽  
Central Element ◽  
Amorphous Structure ◽  
Two Dimensional ◽  
Homologous Chromosomes ◽  
Exact Function ◽  
Dimensional Reconstruction

The synaptonemal complex (SC) is a structure involved in the synapsis of homologous chromosomes during the prophase I stage of meiosis. Although the exact function of the complex is unknown, it has been suggested that one possible role might be to promote recombination by ensuring close synapsis of the homologous chromosomes. In addition, it is thought that the SC may also be required to convert the resulting recombination events into functional chiasmata to provide for proper chromosome segregation at the end of the first stage of meiosis.The SC structure itself is highly conserved across a variety of species. The organization of the SC is tripartite consisting of lateral, central and transverse elements. Two-dimensional cytological observations have been made to characterize the general features of these SC components. The lateral elements are 300 - 500 Å wide proteinaceous structures which flank the synapsed regions of the chromosome bivalent. Between the two lateral elements is a central region containing the central element commonly characterized as a less dense amorphous structure.

scholarly journals The Yeast Motor Protein, Kar3p, Is Essential for Meiosis I

1997 ◽  
Vol 139 (2) ◽  
pp. 459-467 ◽  
Author(s):  
Carol A. Bascom-Slack ◽  
Dean S. Dawson
Keyword(s):  
Synaptonemal Complex ◽  
Meiotic Recombination ◽  
Molecular Motor ◽  
Motor Protein ◽  
Double Strand Breaks ◽  
Wild Type ◽  
Strand Breaks ◽  
Homologous Chromosomes ◽  
Low Levels ◽  
Meiosis I

The recognition and alignment of homologous chromosomes early in meiosis is essential for their subsequent segregation at anaphase I; however, the mechanism by which this occurs is unknown. We demonstrate here that, in the absence of the molecular motor, Kar3p, meiotic cells are blocked with prophase monopolar microtubule arrays and incomplete synaptonemal complex (SC) formation. kar3 mutants exhibit very low levels of heteroallelic recombination. kar3 mutants do produce double-strand breaks that act as initiation sites for meiotic recombination in yeast, but at levels severalfold reduced from wild-type. These data are consistent with a meiotic role for Kar3p in the events that culminate in synapsis of homologues.

scholarly journals Getting there: understanding the chromosomal recruitment of the AAA+ ATPase Pch2/TRIP13 during meiosis

2021 ◽  
Author(s):  
Richard Cardoso da Silva ◽  
Gerben Vader
Keyword(s):  
Rna Polymerase Ii ◽  
Meiotic Recombination ◽  
Origin Recognition Complex ◽  
Comprehensive Overview ◽  
Homologous Chromosomes ◽  
Functional Roles ◽  
Aaa Atpase ◽  
Meiotic Chromosomes ◽  
Chromosomal Association ◽  
Dna Break

AbstractThe generally conserved AAA+ ATPase Pch2/TRIP13 is involved in diverse aspects of meiosis, such as prophase checkpoint function, DNA break regulation, and meiotic recombination. The controlled recruitment of Pch2 to meiotic chromosomes allows it to use its ATPase activity to influence HORMA protein-dependent signaling. Because of the connection between Pch2 chromosomal recruitment and its functional roles in meiosis, it is important to reveal the molecular details that govern Pch2 localization. Here, we review the current understanding of the different factors that control the recruitment of Pch2 to meiotic chromosomes, with a focus on research performed in budding yeast. During meiosis in this organism, Pch2 is enriched within the nucleolus, where it likely associates with the specialized chromatin of the ribosomal (r)DNA. Pch2 is also found on non-rDNA euchromatin, where its recruitment is contingent on Zip1, a component of the synaptonemal complex (SC) that assembles between homologous chromosomes. We discuss recent findings connecting the recruitment of Pch2 with its association with the Origin Recognition Complex (ORC) and reliance on RNA Polymerase II-dependent transcription. In total, we provide a comprehensive overview of the pathways that control the chromosomal association of an important meiotic regulator.

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