Factors directing telomere dynamics in synaptic meiosis

2006 ◽  
Vol 34 (4) ◽  
pp. 550-553 ◽  
Author(s):  
H. Scherthan
Keyword(s):  
Nuclear Envelope ◽  
Budding Yeast ◽  
S Phase ◽  
Homologous Chromosomes ◽  
Prophase I ◽  
Yeast Meiosis ◽  
Bouquet Stage ◽  
Different Levels ◽  
Telomere Dynamics ◽  
Meiosis I

Meiosis creates haploid cells from diploid progenitors. Homologous chromosomes are moved, paired and segregated from each other in a specialized meiosis I division. A second division that lacks a preceding S-phase produces haploid cells. In prophase I, chromosomes attach with their telomeres to the nuclear envelope and undergo oscillating movements that become restricted to a limited nuclear sector during the widely conserved bouquet stage. Recent observations in budding yeast meiosis suggest that telomere clustering depends on actin, whereas exit from the bouquet stage requires meiotic cohesin. Telomere clustering may also be modulated by progression in recombination. These observations suggest that the unique meiotic nuclear topology and telomere dynamics are regulated at different levels.

scholarly journals FBXO47 regulates telomere-inner nuclear envelope integration by stabilizing TRF2 during meiosis

2019 ◽  
Author(s):  
Rong Hua ◽  
Huafang Wei ◽  
Chao Liu ◽  
Yue Zhang ◽  
Siyu Liu ◽  
...  
Keyword(s):  
Nuclear Envelope ◽  
Synaptonemal Complex ◽  
Meiotic Prophase ◽  
Homologous Chromosomes ◽  
Prophase I ◽  
Shelterin Complex ◽  
Meiotic Prophase I ◽  
F Box Protein ◽  
Bouquet Stage

Abstract During meiosis, telomere attachment to the inner nuclear envelope is required for proper pairing of homologous chromosomes and recombination. Here, we identified F-box protein 47 (FBXO47) as a regulator of the telomeric shelterin complex that is specifically expressed during meiotic prophase I. Knockout of Fbxo47 in mice leads to infertility in males. We found that the Fbxo47 deficient spermatocytes are unable to form a complete synaptonemal complex. FBXO47 interacts with TRF1/2, and the disruption of Fbxo47 destabilizes TRF2, leading to unstable telomere attachment and slow traversing through the bouquet stage. Our findings uncover a novel mechanism of FBXO47 in telomeric shelterin subunit stabilization during meiosis.

scholarly journals Meiosis I chromosome segregation is established through regulation of microtubule–kinetochore interactions

eLife ◽  
2012 ◽  
Vol 1 ◽  
Author(s):  
Matthew P Miller ◽  
Elçin Ünal ◽  
Gloria A Brar ◽  
Angelika Amon
Keyword(s):  
Chromosome Segregation ◽  
S Phase ◽  
Segregation Pattern ◽  
Homologous Chromosomes ◽  
Segregation Behavior ◽  
Prophase I ◽  
Kinetochore Assembly ◽  
Sister Chromatids ◽  
Unusual Chromosome ◽  
Meiosis I

During meiosis, a single round of DNA replication is followed by two consecutive rounds of nuclear divisions called meiosis I and meiosis II. In meiosis I, homologous chromosomes segregate, while sister chromatids remain together. Determining how this unusual chromosome segregation behavior is established is central to understanding germ cell development. Here we show that preventing microtubule–kinetochore interactions during premeiotic S phase and prophase I is essential for establishing the meiosis I chromosome segregation pattern. Premature interactions of kinetochores with microtubules transform meiosis I into a mitosis-like division by disrupting two key meiosis I events: coorientation of sister kinetochores and protection of centromeric cohesin removal from chromosomes. Furthermore we find that restricting outer kinetochore assembly contributes to preventing premature engagement of microtubules with kinetochores. We propose that inhibition of microtubule–kinetochore interactions during premeiotic S phase and prophase I is central to establishing the unique meiosis I chromosome segregation pattern.

scholarly journals Spo13 prevents premature cohesin cleavage during meiosis

2019 ◽  
Vol 4 ◽  
pp. 29 ◽  
Author(s):  
Stefan Galander ◽  
Rachael E. Barton ◽  
David A. Kelly ◽  
Adèle L. Marston
Keyword(s):  
Regulatory Subunit ◽  
Homologous Chromosomes ◽  
Sister Chromatids ◽  
Functional Homolog ◽  
Sister Kinetochore ◽  
Phosphatase 2A ◽  
Cohesin Subunit ◽  
Yeast Meiosis ◽  
Mitosis And Meiosis ◽  
Meiosis I

Background: Meiosis produces gametes through two successive nuclear divisions, meiosis I and meiosis II. In contrast to mitosis and meiosis II, where sister chromatids are segregated, during meiosis I, homologous chromosomes are segregated. This requires the monopolar attachment of sister kinetochores and the loss of cohesion from chromosome arms, but not centromeres, during meiosis I. The establishment of both sister kinetochore mono-orientation and cohesion protection rely on the budding yeast meiosis I-specific Spo13 protein, the functional homolog of fission yeast Moa1 and mouse MEIKIN. Methods: Here we investigate the effects of loss of SPO13 on cohesion during meiosis I using a live-cell imaging approach. Results: Unlike wild type, cells lacking SPO13 fail to maintain the meiosis-specific cohesin subunit, Rec8, at centromeres and segregate sister chromatids to opposite poles during anaphase I. We show that the cohesin-destabilizing factor, Wpl1, is not primarily responsible for the loss of cohesion during meiosis I. Instead, premature loss of centromeric cohesin during anaphase I in spo13Δ cells relies on separase-dependent cohesin cleavage. Further, cohesin loss in spo13Δ anaphase I cells is blocked by forcibly tethering the regulatory subunit of protein phosphatase 2A, Rts1, to Rec8. Conclusions: Our findings indicate that separase-dependent cleavage of phosphorylated Rec8 causes premature cohesin loss in spo13Δ cells.

Live observation of fission yeast meiosis in recombination-deficient mutants

2001 ◽  
Vol 114 (15) ◽  
pp. 2843-2853 ◽  
Author(s):  
Monika Molnar ◽  
Jürg Bähler ◽  
Jürg Kohli ◽  
Yasushi Hiraoka
Keyword(s):  
Fission Yeast ◽  
Chromosome Segregation ◽  
Meiotic Division ◽  
Chiasma Formation ◽  
Homologous Chromosomes ◽  
Yeast Meiosis ◽  
Mutant Cells ◽  
Random Level ◽  
Meiosis I ◽  
Chromosome Disjunction

Regular segregation of homologous chromosomes during meiotic divisions is essential for the generation of viable progeny. In recombination-proficient organisms, chromosome disjunction at meiosis I generally occurs by chiasma formation between the homologs (chiasmate meiosis). We have studied meiotic stages in living rec8 and rec7 mutant cells of fission yeast, with special attention to prophase and the first meiotic division. Both rec8 and rec7 are early recombination mutants, and in rec7 mutants, chromosome segregation at meiosis I occurs without any recombination (achiasmate meiosis). Both mutants showed distinct irregularities in nuclear prophase movements. Additionally, rec7 showed an extended first division of variable length and with single chromosomes changing back and forth between the cell poles. Two other early recombination deficient mutants (rec14 and rec15) showed very similar phenotypes to rec7 during the first meiotic division, and the fidelity of achiasmate chromosome segregation slightly exceeded the expected random level. We discuss possible regulatory mechanisms of fission yeast to deal with achiasmate chromosome segregation.

scholarly journals Chromosome–nuclear envelope tethering – a process that orchestrates homologue pairing during plant meiosis?

2020 ◽  
Vol 133 (15) ◽  
pp. jcs243667
Author(s):  
Adél Sepsi ◽  
Trude Schwarzacher
Keyword(s):  
Nuclear Envelope ◽  
Chromosome Segregation ◽  
Higher Plants ◽  
Nuclear Periphery ◽  
Genetic Material ◽  
Strand Break ◽  
Genome Integrity ◽  
Homologous Chromosomes ◽  
Prophase I ◽  
Plant Meiosis

ABSTRACTDuring prophase I of meiosis, homologous chromosomes pair, synapse and exchange their genetic material through reciprocal homologous recombination, a phenomenon essential for faithful chromosome segregation. Partial sequence identity between non-homologous and heterologous chromosomes can also lead to recombination (ectopic recombination), a highly deleterious process that rapidly compromises genome integrity. To avoid ectopic exchange, homology recognition must be extended from the narrow position of a crossover-competent double-strand break to the entire chromosome. Here, we review advances on chromosome behaviour during meiotic prophase I in higher plants, by integrating centromere- and telomere dynamics driven by cytoskeletal motor proteins, into the processes of homologue pairing, synapsis and recombination. Centromere–centromere associations and the gathering of telomeres at the onset of meiosis at opposite nuclear poles create a spatially organised and restricted nuclear state in which homologous DNA interactions are favoured but ectopic interactions also occur. The release and dispersion of centromeres from the nuclear periphery increases the motility of chromosome arms, allowing meiosis-specific movements that disrupt ectopic interactions. Subsequent expansion of interstitial synapsis from numerous homologous interactions further corrects ectopic interactions. Movement and organisation of chromosomes, thus, evolved to facilitate the pairing process, and can be modulated by distinct stages of chromatin associations at the nuclear envelope and their collective release.

scholarly journals Meiotic S-Phase Damage Activates Recombination without Checkpoint Arrest

2005 ◽  
Vol 16 (4) ◽  
pp. 1651-1660 ◽  
Author(s):  
Daniel G. Pankratz ◽  
Susan L. Forsburg
Keyword(s):  
Dna Damage ◽  
Fission Yeast ◽  
Meiotic Division ◽  
S Phase ◽  
Wild Type ◽  
Dna Breaks ◽  
Replication Checkpoint ◽  
Checkpoint Response ◽  
Homologous Chromosomes ◽  
Yeast Meiosis

Checkpoints operate during meiosis to ensure the completion of DNA synthesis and programmed recombination before the initiation of meiotic divisions. Studies in the fission yeast Schizosaccharomyces pombe suggest that the meiotic response to DNA damage due to a failed replication checkpoint response differs substantially from the vegetative response, and may be influenced by the presence of homologous chromosomes. The checkpoint responses to DNA damage during fission yeast meiosis are not well characterized. Here we report that DNA damage induced during meiotic S-phase does not activate checkpoint arrest. We also find that in wild-type cells, markers for DNA breaks can persist at least to the first meiotic division. We also observe increased spontaneous S-phase damage in checkpoint mutants, which is repaired by recombination without activating checkpoint arrest. Our results suggest that fission yeast meiosis is exceptionally tolerant of DNA damage, and that some forms of spontaneous S-phase damage can be repaired by recombination without activating checkpoint arrest.

scholarly journals Speedy A–Cdk2 binding mediates initial telomere–nuclear envelope attachment during meiotic prophase I independent of Cdk2 activation

2016 ◽  
Vol 114 (3) ◽  
pp. 592-597 ◽  
Author(s):  
Zhaowei Tu ◽  
Mustafa Bilal Bayazit ◽  
Hongbin Liu ◽  
Jingjing Zhang ◽  
Kiran Busayavalasa ◽  
...  
Keyword(s):  
Nuclear Envelope ◽  
Germ Cells ◽  
Meiotic Prophase ◽  
Homologous Pairing ◽  
Male And Female ◽  
Homologous Chromosomes ◽  
Cyclin Dependent Kinases ◽  
Prophase I ◽  
Meiotic Prophase I ◽  
Localization Domain

Telomere attachment to the nuclear envelope (NE) is a prerequisite for chromosome movement during meiotic prophase I that is required for pairing of homologous chromosomes, synapsis, and homologous recombination. Here we show that Speedy A, a noncanonical activator of cyclin-dependent kinases (Cdks), is specifically localized to telomeres in prophase I male and female germ cells in mice, and plays an essential role in the telomere–NE attachment. Deletion of Spdya in mice disrupts telomere–NE attachment, and this impairs homologous pairing and synapsis and leads to zygotene arrest in male and female germ cells. In addition, we have identified a telomere localization domain on Speedy A covering the distal N terminus and the Cdk2-binding Ringo domain, and this domain is essential for the localization of Speedy A to telomeres. Furthermore, we found that the binding of Cdk2 to Speedy A is indispensable for Cdk2’s localization on telomeres, suggesting that Speedy A and Cdk2 might be the initial components that are recruited to the NE for forming the meiotic telomere complex. However, Speedy A-Cdk2–mediated telomere–NE attachment is independent of Cdk2 activation. Our results thus indicate that Speedy A and Cdk2 might mediate the initial telomere–NE attachment for the efficient assembly of the telomere complex that is essential for meiotic prophase I progression.

scholarly journals A ZIP1 Separation-of-Function Allele Reveals that Meiotic Centromere Pairing Drives Meiotic Segregation of Achiasmate Chromosomes in Budding Yeast

2018 ◽  
Author(s):  
Emily L. Kurdzo ◽  
Hoa H Chuong ◽  
Dean S. Dawson
Keyword(s):  
Chromosome Number ◽  
Single Unit ◽  
Genetic Recombination ◽  
Budding Yeast ◽  
Homologous Chromosomes ◽  
Normal Number ◽  
Relationship Of ◽  
Distinct Features ◽  
The Relationship ◽  
Meiosis I

ABSTRACTIn meiosis I, homologous chromosomes segregate away from each other - the first of two rounds of chromosome segregation that allow the formation of haploid gametes. In prophase I, homologous partners become joined along their length by the synaptonemal complex (SC) and crossovers form between the homologs to generate links called chiasmata. The chiasmata allow the homologs to act as a single unit, called a bivalent, as the chromosomes attach to the microtubules that will ultimately pull them away from each other at anaphase I. Recent studies, in several organisms, have shown that when the SC disassembles at the end of prophase, residual SC proteins remain at the homologous centromeres providing an additional link between the homologs. In budding yeast, this centromere pairing is correlated with improved segregation of the paired partners in anaphase. However, the causal relationship of prophase centromere pairing and subsequent disjunction in anaphase has been difficult to demonstrate as has been the relationship between SC assembly and the assembly of the centromere pairing apparatus. Here, a series of in-frame deletion mutants of the SC component Zip1 were used to address these questions. The identification of separation-of-function alleles that disrupt centromere pairing, but not SC assembly, have made it possible to demonstrate that centromere pairing and SC assembly have mechanistically distinct features and that prophase centromere pairing function of Zip1 drives disjunction of the paired partners in anaphase I.AUTHOR SUMMARYThe generation of gametes requires the completion of a specialized cell división called meiosis. This division is unique in that it produces cells (gametes) with half the normal number of chromosomes (such that when two gametes fuse the normal chromosome number is restored). Chromosome number is reduced in meiosis by following a single round of chromosome duplication with two rounds of segregation. In the first round, meiosis I, homologous chromosomes first pair with each other, then attach to cellular cables, called microtubules, that pull them to opposite sides of the cell. It has long been known that the homologous partners become linked to each other by genetic recombination in a way that helps them behave as a single unit when they attach to the microtubules that will ultimately pull them apart. Recently, it was shown, in budding yeast and other organisms, that homologous partners can also pair at their centromeres. Here we show that this centromere pairing also contributes to proper segregation of the partners away from each other at meiosis I, and demonstrate that one protein involved in this process is able to participate in multiple mechanisms that help homologous chromosomes to pair with each other before being segregated in meiosis I.

scholarly journals Meiosis-specific prophase-like pathway controls cleavage-independent release of cohesin by Wapl phosphorylation

2018 ◽  
Author(s):  
Kiran Challa ◽  
V Ghanim Fajish ◽  
Miki Shinohara ◽  
Franz Klein ◽  
Susan M. Gasser ◽  
...  
Keyword(s):  
Chromosome Segregation ◽  
Sister Chromatid ◽  
Meiotic Prophase ◽  
Budding Yeast ◽  
Cell Cycle Regulators ◽  
Late Prophase ◽  
Homologous Chromosomes ◽  
Prophase I ◽  
Meiotic Prophase I ◽  
Meiotic Chromosomes

AbstractSister chromatid cohesion on chromosome arms is essential for the segregation of homologous chromosomes during meiosis I while it is dispensable for sister chromatid separation during mitosis. It was assumed that, unlike the situation in mitosis, chromosome arms retain cohesion prior to onset of anaphase-I. Paradoxically, reduced immunostaining signals of meiosis-specific cohesin, including the kleisin Rec8, from the chromosomes were observed during late prophase-I of budding yeast. This decrease is seen in the absence of Rec8 cleavage and depends on condensin-mediated recruitment of Polo-like kinase (PLK/Cdc5). In this study, we confirmed that this release indeed accompanies the dissociation of acetylated Smc3 as well as Rec8 from meiotic chromosomes during late prophase-I. This release requires, in addition to PLK, the cohesin regulator, Wapl (Rad61/Wpl1 in yeast), and Dbf4-dependent Cdc7 kinase (DDK). Meiosis-specific phosphorylation of Rad61/Wpl1 and Rec8 by PLK and DDK collaboratively promote this release. This process is similar to the vertebrate “prophase” pathway for cohesin release during G2 phase and pro-metaphase. In yeast, meiotic cohesin release coincides with PLK-dependent compaction of chromosomes in late meiotic prophase-I. We suggest that yeast uses this highly regulated cleavage-independent pathway to remove cohesin during late prophase-I to facilitate morphogenesis of condensed metaphase-I chromosomes.Author SummaryIn meiosis the life and health of future generations is decided upon. Any failure in chromosome segregation has a detrimental impact. Therefore, it is currently believed that the physical connections between homologous chromosomes are maintained by meiotic cohesin with exceptional stability. Indeed, it was shown that cohesive cohesin does not show an appreciable turnover during long periods in oocyte development. In this context, it was long assumed but not properly investigated, that the prophase pathway for cohesin release would be specific to mitotic cells and will be safely suppressed during meiosis so as not to endanger the valuable chromosome connections. However, a previous study on budding yeast meiosis suggests the presence of cleavage-independent pathway of cohesin release during late prophase-I. In the work presented here we confirmed that the prophase pathway is not suppressed during meiosis, at least in budding yeast and showed that this cleavage-independent release is regulated by meiosis-specific phosphorylation of two cohesin subunits, Rec8 and Rad61(Wapl) by two cell-cycle regulators, PLK and DDK. Our results suggest that late meiotic prophase-I actively controls cohesin dynamics on meiotic chromosomes for chromosome segregation.

scholarly journals Cdc7-Dbf4 Regulates NDT80 Transcription as Well as Reductional Segregation during Budding Yeast Meiosis

2008 ◽  
Vol 19 (11) ◽  
pp. 4956-4967 ◽  
Author(s):  
Hsiao-Chi Lo ◽  
Lihong Wan ◽  
Adam Rosebrock ◽  
Bruce Futcher ◽  
Nancy M. Hollingsworth
Keyword(s):  
Dna Replication ◽  
Protein Kinase ◽  
Dna Synthesis ◽  
Budding Yeast ◽  
Genetic Approach ◽  
Chemical Genetic ◽  
Meiotic Progression ◽  
Cdc7 Kinase ◽  
Yeast Meiosis ◽  
Meiosis I

In budding yeast, as in other eukaryotes, the Cdc7 protein kinase is important for initiation of DNA synthesis in vegetative cells. In addition, Cdc7 has crucial meiotic functions: it facilitates premeiotic DNA replication, and it is essential for the initiation of recombination. This work uses a chemical genetic approach to demonstrate that Cdc7 kinase has additional roles in meiosis. First, Cdc7 allows expression of NDT80, a meiosis-specific transcriptional activator required for the induction of genes involved in exit from pachytene, meiotic progression, and spore formation. Second, Cdc7 is necessary for recruitment of monopolin to sister kinetochores, and it is necessary for the reductional segregation occurring at meiosis I. The use of the same kinase to regulate several distinct meiosis-specific processes may be important for the coordination of these processes during meiosis.

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