Coordinating the segregation of sister chromatids during the first meiotic division: evidence for sexual dimorphism

2001 ◽  
Vol 114 (13) ◽  
pp. 2417-2426 ◽  
Author(s):  
Craig A. Hodges ◽  
Renée LeMaire-Adkins ◽  
Patricia A. Hunt
Keyword(s):  
Sexual Dimorphism ◽  
Synaptonemal Complex ◽  
X Chromosome ◽  
Meiotic Division ◽  
Meiotic Chromosome ◽  
Female Meiosis ◽  
Homologous Chromosomes ◽  
Sister Chromatids ◽  
Chromatid Segregation ◽  
Protein Components

Errors during the first meiotic division are common in our species, but virtually all occur during female meiosis. The reason why oogenesis is more error prone than spermatogenesis remains unknown. Normal segregation of homologous chromosomes at the first meiotic division (MI) requires coordinated behavior of the sister chromatids of each homolog. Failure of sister kinetochores to act cooperatively at MI, or precocious sister chromatid segregation (PSCS), has been postulated to be a major contributor to human nondisjunction. To investigate the factors that influence PSCS we utilized the XO mouse, since the chromatids of the single X chromosome frequently segregate at MI, and the propensity for PSCS is influenced by genetic background. Our studies demonstrate that the strain-specific differences in PSCS are due to the actions of an autosomal trans-acting factor or factors. Since components of the synaptonemal complex are thought to play a role in centromere cohesion and kinetochore orientation, we evaluated the behavior of the X chromosome at prophase to determine if this factor influenced the propensity of the chromosome for self-synapsis. We were unable to directly correlate synaptic differences with subsequent segregation behavior. However, unexpectedly, we uncovered a sexual dimorphism that may partially explain sex-specific differences in the fidelity of meiotic chromosome segregation. Specifically, in the male remnants of the synaptonemal complex remain associated with the centromeres until anaphase of the second meiotic division (MII), whereas in the female, all traces of synaptonemal complex (SC) protein components are lost from the chromosomes before the onset of the first meiotic division. This finding suggests a sex-specific difference in the components used to correctly segregate chromosomes during meiosis, and may provide a reason for the high error frequency during female meiosis.

scholarly journals Synaptonemal complex proteins direct and constrain the localization of crossover-promoting proteins during Caenorhabditis elegans meiosis

2019 ◽  
Author(s):  
Cori K. Cahoon ◽  
Jacquellyn M. Helm ◽  
Diana E. Libuda
Keyword(s):  
Caenorhabditis Elegans ◽  
Synaptonemal Complex ◽  
Meiotic Chromosome ◽  
Variable Number ◽  
Specific Structure ◽  
Dna Breaks ◽  
Late Prophase ◽  
Homologous Chromosomes ◽  
Sister Chromatids ◽  
Double Strand Dna Breaks

AbstractCrossovers (COs) between homologous chromosomes are critical for meiotic chromosome segregation and form in the context of the synaptonemal complex (SC), a meiosis-specific structure that assembles between aligned homologs. During Caenorhabditis elegans meiosis, central region components of the SC (SYP proteins) are essential to repair double-strand DNA breaks (DSBs) as COs, but the roles of these SYP proteins in promoting CO formation are poorly understood. Here, we investigate the relationships between the SYP proteins and conserved CO-promoting factors by examining the immunolocalization of these factors in meiotic mutants where SYP proteins are absent, reduced, or mis-localized. Although COs do not form in syp null mutants, CO-promoting proteins COSA-1, MSH-5, and ZHP-3 nevertheless become co-localized at a variable number of DSB-dependent sites during late prophase, reflecting an inherent affinity of these factors for DSB repair sites. In contrast, in mutants where SYP proteins are present but form aggregates or display abnormal synapsis, CO-promoting proteins consistently track with SYP-1 localization. Moreover, CO-promoting proteins usually localize to a single site per SYP-1 structure, even in SYP aggregates or in mutants where SC forms between sister-chromatids, suggesting that CO regulation occurs within these structures. Further, we find that sister chromatids in the meiotic cohesin mutant rec-8 require both CO-promoting proteins and the SC to remain connected. Taken together, our findings support a model in which SYP proteins promote CO formation by directing and constraining the localization of CO-promoting factors to ensure that CO maturation occurs only between properly aligned homologous chromosomes.Article SummaryErrors during meiosis are the leading cause of birth defects and miscarriages in humans. Thus, the coordinated control of meiosis events is critical for the faithful inheritance of the genome each generation. The synaptonemal complex (SC) is a meiosis-specific structure that assembles between homologs chromosomes and is critical for the establishment and regulation of crossovers, which ensure the accurate segregation of the homologous chromosomes at meiosis I. Here we show that the SC proteins function to regulate crossovers by directing and constraining the localization of proteins involved in promoting the formation of crossovers.

scholarly journals Three-dimensional Ultrastructure of Saccharomyces cerevisiae Meiotic Spindles

2005 ◽  
Vol 16 (3) ◽  
pp. 1178-1188 ◽  
Author(s):  
Mark Winey ◽  
Garry P. Morgan ◽  
Paul D. Straight ◽  
Thomas H. Giddings ◽  
David N. Mastronarde
Keyword(s):  
Saccharomyces Cerevisiae ◽  
Meiotic Chromosome ◽  
Three Dimensional ◽  
Structural Basis ◽  
Mitotic Spindles ◽  
Yeast Saccharomyces Cerevisiae ◽  
Homologous Chromosomes ◽  
Sister Chromatids ◽  
Single Nucleus ◽  
Meiotic Spindles

Meiotic chromosome segregation leads to the production of haploid germ cells. During meiosis I (MI), the paired homologous chromosomes are separated. Meiosis II (MII) segregation leads to the separation of paired sister chromatids. In the budding yeast Saccharomyces cerevisiae, both of these divisions take place in a single nucleus, giving rise to the four-spored ascus. We have modeled the microtubules in 20 MI and 15 MII spindles by using reconstruction from electron micrographs of serially sectioned meiotic cells. Meiotic spindles contain more microtubules than their mitotic counterparts, with the highest number in MI spindles. It is possible to differentiate between MI versus MII spindles based on microtubule numbers and organization. Similar to mitotic spindles, kinetochores in either MI or MII are attached by a single microtubule. The models indicate that the kinetochores of paired homologous chromosomes in MI or sister chromatids in MII are separated at metaphase, similar to mitotic cells. Examination of both MI and MII spindles reveals that anaphase A likely occurs in addition to anaphase B and that these movements are concurrent. This analysis offers a structural basis for considering meiotic segregation in yeast and for the analysis of mutants defective in this process.

scholarly journals Transvection regulates the sex-biased expression of a fly X-linked gene

Science ◽  
2021 ◽  
Vol 371 (6527) ◽  
pp. 396-400 ◽  
Author(s):  
Charalampos Chrysovalantis Galouzis ◽  
Benjamin Prud’homme
Keyword(s):  
Gene Expression ◽  
Sexual Dimorphism ◽  
Sex Determination ◽  
Expression Pattern ◽  
X Chromosome ◽  
Expression Patterns ◽  
Gene Expression Patterns ◽  
Regulatory Interaction ◽  
Linked Gene ◽  
Homologous Chromosomes

Sexual dimorphism in animals results from sex-biased gene expression patterns. These patterns are controlled by genetic sex determination hierarchies that establish the sex of an individual. Here we show that the male-biased wing expression pattern of the Drosophila biarmipes gene yellow, located on the X chromosome, is independent of the fly sex determination hierarchy. Instead, we find that a regulatory interaction between yellow alleles on homologous chromosomes (a process known as transvection) silences the activity of a yellow enhancer functioning in the wing. Therefore, this enhancer can be active in males (XY) but not in females (XX). This transvection-dependent enhancer silencing requires the yellow intron and the chromatin architecture protein Mod(mdg4). Our results suggest that transvection can contribute more generally to the sex-biased expression of X-linked genes.

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.

scholarly journals Shugoshin protects centromere pairing and promotes segregation of non-exchange partner chromosomes in meiosis

2018 ◽  
Author(s):  
Luciana Previato de Almeida ◽  
Jared M. Evatt ◽  
Hoa H. Chuong ◽  
Emily L. Kurdzo ◽  
Craig A. Eyster ◽  
...  
Keyword(s):  
Synaptonemal Complex ◽  
Chromosome Segregation ◽  
Meiotic Prophase ◽  
Single Unit ◽  
Meiotic Chromosome ◽  
Model Systems ◽  
Meiotic Spindle ◽  
Homologous Chromosomes ◽  
Meiosis I

ABSTRACTFaithful chromosome segregation during meiosis I depends upon the formation of connections between homologous chromosomes. Crossovers between homologs connect the partners allowing them to attach to the meiotic spindle as a unit, such that they migrate away from one another at anaphase I. Homologous partners also become connected by pairing of their centromeres in meiotic prophase. This centromere pairing can promote proper segregation at anaphase I of partners that have failed to become joined by a crossover. Centromere pairing is mediated by synaptonemal complex (SC) proteins that persist at the centromere when the SC disassembles. Here, using mouse spermatocyte and yeast model systems, we tested the role of shugoshin in promoting meiotic centromere pairing by protecting centromeric synaptonemal components from disassembly. The results show that shugoshin protects centromeric SC in meiotic prophase and, in anaphase, promotes the proper segregation of partner chromosomes that are not linked by a crossover.SIGNIFICANCEMeiotic crossovers form a connection between homologous chromosomes that allows them to attach to the spindle as a single unit in meiosis I. In humans, failures in this process are a leading cause of aneuploidy. A recently described process, called centromere pairing, can also help connect meiotic chromosome partners in meiosis. Homologous chromosomes become tightly joined by a structure called the synaptonemal complex (SC) in meiotic prophase. After the SC disassembles, persisting SC proteins at the centromeres mediate their pairing. Here, studies in mouse spermatocytes and yeast are used to show that the shugoshin protein helps SC components persist at centromeres and helps centromere pairing promote the proper segregation of yeast chromosomes that fail to become tethered by crossovers.

scholarly journals Synaptonemal complex components are required for meiotic checkpoint function in C. elegans

2016 ◽  
Author(s):  
Tisha Bohr ◽  
Guinevere Ashley ◽  
Evan Eggleston ◽  
Kyra Firestone ◽  
Needhi Bhalla
Keyword(s):  
Synaptonemal Complex ◽  
Chromosome Segregation ◽  
Meiotic Chromosome ◽  
Checkpoint Response ◽  
Homologous Chromosomes ◽  
C Elegans ◽  
Homolog Pairing ◽  
The Stability ◽  
Complex Components

AbstractSynapsis involves the assembly of a proteinaceous structure, the synaptonemal complex (SC), between paired homologous chromosomes and is essential for proper meiotic chromosome segregation. In C. elegans, the synapsis checkpoint selectively removes nuclei with unsynapsed chromosomes by inducing apoptosis. This checkpoint depends on Pairing Centers (PCs), cis-acting sites that promote pairing and synapsis. We have hypothesized that the stability of homolog pairing at PCs is monitored by this checkpoint. Here, we report that SC components SYP-3, HTP-3, HIM-3 and HTP-1 are required for a functional synapsis checkpoint. Mutation of these components does not abolish PC function, demonstrating they are bonafide checkpoint components. Further, we identify mutant backgrounds in which the instability of homolog pairing at PCs does not correlate with the synapsis checkpoint response. Altogether, these data suggest that, in addition to homolog pairing, SC assembly may be monitored by the synapsis checkpoint.

scholarly journals SCF-Fbxo42 promotes synaptonemal complex assembly by downregulating PP2A-B56

2020 ◽  
Vol 220 (2) ◽  
Author(s):  
Pedro Barbosa ◽  
Liudmila Zhaunova ◽  
Simona Debilio ◽  
Verdiana Steccanella ◽  
Van Kelly ◽  
...  
Keyword(s):  
Genetic Diversity ◽  
Synaptonemal Complex ◽  
Ubiquitin Ligase ◽  
Posttranslational Modifications ◽  
Meiotic Prophase ◽  
Female Meiosis ◽  
Complex Assembly ◽  
Homologous Chromosomes ◽  
Ubiquitin Ligase Complex ◽  
Segregation Of Chromosomes

Meiosis creates genetic diversity by recombination and segregation of chromosomes. The synaptonemal complex assembles during meiotic prophase I and assists faithful exchanges between homologous chromosomes, but how its assembly/disassembly is regulated remains to be understood. Here, we report how two major posttranslational modifications, phosphorylation and ubiquitination, cooperate to promote synaptonemal complex assembly. We found that the ubiquitin ligase complex SCF is important for assembly and maintenance of the synaptonemal complex in Drosophila female meiosis. This function of SCF is mediated by two substrate-recognizing F-box proteins, Slmb/βTrcp and Fbxo42. SCF-Fbxo42 down-regulates the phosphatase subunit PP2A-B56, which is important for synaptonemal complex assembly and maintenance.

Hendrik Peter Bernelot Moens (1931–2008)

Genome ◽  
2008 ◽  
Vol 51 (12) ◽  
pp. 1063-1067 ◽  
Author(s):  
Edyta Marcon
Keyword(s):  
North Carolina ◽  
Synaptonemal Complex ◽  
Meiotic Prophase ◽  
Structural Characteristics ◽  
Specific Structure ◽  
Homologous Chromosomes ◽  
Time Points ◽  
Duke University ◽  
Protein Components ◽  
Functional Components

The synaptonemal complex (SC) is a proteinaceous structure that physically holds the two homologous chromosomes together during meiotic prophase. First observed in 1956 by Montrose J. Moses (Duke University, Durham, North Carolina) in meiotic prophase spermatocytes of crayfish, the SC was found in many other species. Initially, the research into the SC focused on its structural characteristics, but with the availability of antibodies, the focus shifted to the protein components of the complex, and later, attention was diverted to the proteins associated with this structure at different time points during meiotic prophase. Various possible roles of this meiotic-specific structure have been debated since the discovery of the SC structure but consensus has yet to be reached. Dr. Peter Moens has been an internationally recognized expert on the SC, being involved in all of the steps and characterizing many of the structural and functional components of the complex mainly in mice but also in other species.

scholarly journals Centromere repositioning causes inversion of meiosis and generates a reproductive barrier

2019 ◽  
Vol 116 (43) ◽  
pp. 21580-21591 ◽  
Author(s):  
Min Lu ◽  
Xiangwei He
Keyword(s):  
Meiotic Chromosome ◽  
Feedback Mechanism ◽  
Reproductive Barrier ◽  
Evolutionary Time ◽  
Homologous Chromosomes ◽  
Sister Chromatids ◽  
Inverted Order ◽  
Canonical Order ◽  
Evolutionary New Centromeres

The chromosomal position of each centromere is determined epigenetically and is highly stable, whereas incremental cases have supported the occurrence of centromere repositioning on an evolutionary time scale (evolutionary new centromeres, ENCs), which is thought to be important in speciation. The mechanisms underlying the high stability of centromeres and its functional significance largely remain an enigma. Here, in the fission yeast Schizosaccharomyces pombe, we identify a feedback mechanism: The kinetochore, whose assembly is guided by the centromere, in turn, enforces centromere stability. Upon going through meiosis, specific inner kinetochore mutations induce centromere repositioning—inactivation of the original centromere and formation of a new centromere elsewhere—in 1 of the 3 chromosomes at random. Repositioned centromeres reside asymmetrically in the pericentromeric regions and cells carrying them are competent in mitosis and homozygotic meiosis. However, when cells carrying a repositioned centromere are crossed with those carrying the original centromere, the progeny suffer severe lethality due to defects in meiotic chromosome segregation. Thus, repositioned centromeres constitute a reproductive barrier that could initiate genetic divergence between 2 populations with mismatched centromeres, documenting a functional role of ENCs in speciation. Surprisingly, homozygotic repositioned centromeres tend to undergo meiosis in an inverted order—that is, sister chromatids segregate first, and homologous chromosomes separate second—whereas the original centromeres on other chromosomes in the same cell undergo meiosis in the canonical order, revealing hidden flexibility in the perceived rigid process of meiosis.

The initiation of meiotic chromosome pairing: the cytological view

Genome ◽  
1990 ◽  
Vol 33 (6) ◽  
pp. 759-778 ◽  
Author(s):  
Josef Loidl
Keyword(s):  
Synaptonemal Complex ◽  
Chromosome Pairing ◽  
Meiotic Chromosome ◽  
Meiotic Pairing ◽  
Cytological Evidence ◽  
Homologous Chromosomes ◽  
Synaptonemal Complex Formation ◽  
Meiotic Synapsis ◽  
The One ◽  
First Contact

Opposing views are held with respect to the time when and the mechanisms whereby homologous chromosomes find each other for meiotic synapsis. On the one hand, some evidence has been presented for somatic homologous associations or some other kind of relationship between chromosomes in somatic cells as a preliminary to meiotic pairing. On the other hand, it is argued by many that homologous contacts are first established at meiotic prophase prior to, or in the course of, synaptonemal complex formation. The present paper reviews the controversial cytological evidence, hypotheses, and ideas on how the first contact between homologous chromosomes comes about.Key words: synapsis, meiosis, presynaptic alignment, homologous recognition, synaptonemal complex, chromosome pairing.

Sign in / Sign up

Export Citation Format

Share Document