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Journal of Cell Science Aug 2020During prophase I of meiosis, homologous chromosomes pair, synapse and exchange their genetic material through reciprocal homologous recombination, a phenomenon... (Review)
Review
During 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.
Topics: Centromere; Chromosome Pairing; Chromosome Segregation; Meiosis; Nuclear Envelope; Telomere
PubMed: 32788229
DOI: 10.1242/jcs.243667 -
Cell Research May 2017Targeted proteolysis plays an important role in the execution and regulation of many cellular events. Two recent papers in Science identify novel roles for...
Targeted proteolysis plays an important role in the execution and regulation of many cellular events. Two recent papers in Science identify novel roles for proteasome-mediated proteolysis in homologous chromosome pairing, recombination, and segregation during meiosis.
Topics: Chromosome Pairing; Chromosomes; Meiosis; Proteasome Endopeptidase Complex; Recombination, Genetic
PubMed: 28266542
DOI: 10.1038/cr.2017.28 -
Cell Cycle (Georgetown, Tex.) Oct 2016
Topics: Cell Cycle Proteins; Chromosomal Proteins, Non-Histone; Chromosome Pairing; Chromosomes; Meiosis; Synaptonemal Complex
PubMed: 27359070
DOI: 10.1080/15384101.2016.1204853 -
Nucleus (Austin, Tex.) Nov 2017Meiosis is a specialized cellular division occurring in organisms capable of sexual reproduction that leads to the formation of gametes containing half of the original... (Review)
Review
Meiosis is a specialized cellular division occurring in organisms capable of sexual reproduction that leads to the formation of gametes containing half of the original chromosome number. During the earliest stage of meiosis, prophase I, pairing of homologous chromosomes is achieved in preparation for their proper distribution in the coming divisions. An important question is how do homologous chromosomes find each other and establish pairing interactions. Early studies demonstrated that chromosomes are dynamic in nature and move during this early stage of meiosis. More recently, there have been several studies across different models showing the conserved nature and importance of this chromosome movement, as well as the key components involved in chromosome movement. This review will cover these major findings and also introduce unexamined areas of regulation in meiotic prophase I chromosome movement.
Topics: Animals; Chromosome Pairing; Chromosomes; Cytoskeleton; Humans; Meiosis; Movement; Telomere
PubMed: 28892406
DOI: 10.1080/19491034.2017.1358329 -
Chromosoma Mar 2014Rapid chromosome movement during prophase of the first meiotic division has been observed in many organisms. It is generally concomitant with formation of the "meiotic... (Review)
Review
Rapid chromosome movement during prophase of the first meiotic division has been observed in many organisms. It is generally concomitant with formation of the "meiotic chromosome bouquet," a special chromosome configuration in which one or both chromosome ends attach to the nuclear envelope and become concentrated within a limited area. The precise function of the chromosomal bouquet is still not fully understood. Chromosome mobility is implicated in homologous chromosome pairing, synaptonemal complex formation, recombination, and resolution of chromosome entanglements. The basic mechanistic module through which forces are exerted on chromosomes is widely conserved; however, phenotypic differences have been reported among various model organisms once movement is abrogated. Movements are transmitted to the chromosome ends by the nuclear membrane-bridging SUN/KASH complex and are dependent on cytoskeletal filaments and motor proteins located in the cytoplasm. Here we review the recent findings on chromosome mobility during meiosis in an animal model system: the Caenorhabditis elegans nematode.
Topics: Animals; Caenorhabditis elegans; Chromosome Pairing; Chromosomes; Meiotic Prophase I; Movement; Pachytene Stage
PubMed: 24036686
DOI: 10.1007/s00412-013-0436-7 -
Journal of Genetics and Genomics = Yi... Mar 2014Meiosis is a key event in gametogenesis that generates new combinations of genetic information and is required to reduce the chromosome content of the gametes. Meiotic... (Review)
Review
Meiosis is a key event in gametogenesis that generates new combinations of genetic information and is required to reduce the chromosome content of the gametes. Meiotic chromosomes undergo a number of specialised events during prophase to allow meiotic recombination, homologous chromosome synapsis and reductional chromosome segregation to occur. In mammalian cells, DNA physically associates with histones to form chromatin, which can be modified by methylation, phosphorylation, ubiquitination and acetylation to help regulate higher order chromatin structure, gene expression, and chromosome organisation. Recent studies have identified some of the enzymes responsible for generating chromatin modifications in meiotic mammalian cells, and shown that these chromatin modifying enzymes are required for key meiosis-specific events that occur during meiotic prophase. This review will discuss the role of chromatin modifications in meiotic recombination, homologous chromosome synapsis and regulation of meiotic gene expression in mammals.
Topics: Acetylation; Animals; Centromere; Chromatin; DNA; Gene Expression; Histones; Methylation; Methyltransferases; Mice; Phosphorylation; Polycomb-Group Proteins; Prophase; Ubiquitination
PubMed: 24656230
DOI: 10.1016/j.jgg.2014.01.003 -
Molecular Cell Sep 2020A long-standing conundrum is how mitotic chromosomes can compact, as required for clean separation to daughter cells, while maintaining close parallel alignment of...
A long-standing conundrum is how mitotic chromosomes can compact, as required for clean separation to daughter cells, while maintaining close parallel alignment of sister chromatids. Pursuit of this question, by high resolution 3D fluorescence imaging of living and fixed mammalian cells, has led to three discoveries. First, we show that the structural axes of separated sister chromatids are linked by evenly spaced "mini-axis" bridges. Second, when chromosomes first emerge as discrete units, at prophase, they are organized as co-oriented sister linear loop arrays emanating from a conjoined axis. We show that this same basic organization persists throughout mitosis, without helical coiling. Third, from prophase onward, chromosomes are deformed into sequential arrays of half-helical segments of alternating handedness (perversions), accompanied by correlated kinks. These arrays fluctuate dynamically over <15 s timescales. Together these discoveries redefine the foundation for thinking about the evolution of mitotic chromosomes as they prepare for anaphase segregation.
Topics: Adenosine Triphosphatases; Anaphase; Animals; Cell Cycle Proteins; Chromatids; Chromosomal Proteins, Non-Histone; Chromosomes; DNA Topoisomerases, Type II; DNA-Binding Proteins; Imaging, Three-Dimensional; Mammals; Metaphase; Mitosis; Prophase
PubMed: 32768407
DOI: 10.1016/j.molcel.2020.07.002 -
Proceedings of the National Academy of... Aug 1996A physical connection between homologs is required for reductional segregation at the first division of meiosis. This connection is usually provided by one or a few... (Review)
Review
A physical connection between homologs is required for reductional segregation at the first division of meiosis. This connection is usually provided by one or a few well-spaced crossovers. A speculative overview of processes leading to formation of these crossovers is presented.
Topics: Animals; Biological Evolution; Cell Cycle; Chromosomes; Crossing Over, Genetic; Humans; Meiosis; Mitosis; Plants; Prophase; Recombination, Genetic; Saccharomyces cerevisiae; Synaptonemal Complex
PubMed: 8710842
DOI: 10.1073/pnas.93.16.8167 -
Proceedings of the National Academy of... Nov 2022In the early stages of meiosis, maternal and paternal chromosomes pair with their homologous partner and recombine to ensure exchange of genetic information and proper...
In the early stages of meiosis, maternal and paternal chromosomes pair with their homologous partner and recombine to ensure exchange of genetic information and proper segregation. These events can vary drastically between species and between males and females of the same species. In in contrast to females, males do not form synaptonemal complexes (SCs), do not recombine, and have no crossing over; yet, males are able to segregate their chromosomes properly. Here, we investigated the early steps of homolog pairing in males. We found that homolog centromeres are not paired in germline stem cells (GSCs) and become paired in the mitotic region before meiotic entry, similarly to females. Surprisingly, male germline cells express SC proteins, which localize to centromeres and promote pairing. We further found that the SUN/KASH (LINC) complex and microtubules are required for homolog pairing as in females. Chromosome movements in males, however, are much slower than in females and we demonstrate that this slow dynamic is compensated in males by having longer cell cycles. In agreement, slowing down cell cycles was sufficient to rescue pairing-defective mutants in female meiosis. Our results demonstrate that although meiosis differs significantly between males and females, sex-specific cell cycle kinetics integrate similar molecular mechanisms to achieve proper centromere pairing.
Topics: Animals; Male; Female; Chromosome Pairing; Drosophila; Synaptonemal Complex; Centromere; Meiosis; Chromosomes; Chromosome Segregation
PubMed: 36375065
DOI: 10.1073/pnas.2207660119 -
Journal of Molecular Cell Biology Dec 2021Meiosis produces the haploid gametes required by all sexually reproducing organisms, occurring in specific temperature ranges in different organisms. However, how...
Meiosis produces the haploid gametes required by all sexually reproducing organisms, occurring in specific temperature ranges in different organisms. However, how meiotic thermotolerance is regulated remains largely unknown. Using the model organism Caenorhabditis elegans, here, we identified the synaptonemal complex (SC) protein SYP-5 as a critical regulator of meiotic thermotolerance. syp-5-null mutants maintained a high percentage of viable progeny at 20°C but produced significantly fewer viable progeny at 25°C, a permissive temperature in wild-type worms. Cytological analysis of meiotic events in the mutants revealed that while SC assembly and disassembly, as well as DNA double-strand break repair kinetics, were not affected by the elevated temperature, crossover designation, and bivalent formation were significantly affected. More severe homolog segregation errors were also observed at elevated temperature. A temperature switching assay revealed that late meiotic prophase events were not temperature-sensitive and that meiotic defects during pachytene stage were responsible for the reduced viability of syp-5 mutants at the elevated temperature. Moreover, SC polycomplex formation and hexanediol sensitivity analysis suggested that SYP-5 was required for the normal properties of the SC, and charge-interacting elements in SC components were involved in regulating meiotic thermotolerance. Together, these findings provide a novel molecular mechanism for meiotic thermotolerance regulation.
Topics: Animals; Animals, Genetically Modified; Caenorhabditis elegans; Caenorhabditis elegans Proteins; Computational Biology; Meiosis; Synaptonemal Complex; Thermotolerance
PubMed: 34081106
DOI: 10.1093/jmcb/mjab035