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Genetics Oct 2023Meiosis is a specialized cell division program that is essential for sexual reproduction. The two meiotic divisions reduce chromosome number by half, typically...
Meiosis is a specialized cell division program that is essential for sexual reproduction. The two meiotic divisions reduce chromosome number by half, typically generating haploid genomes that are packaged into gametes. To achieve this ploidy reduction, meiosis relies on highly unusual chromosomal processes including the pairing of homologous chromosomes, assembly of the synaptonemal complex, programmed formation of DNA breaks followed by their processing into crossovers, and the segregation of homologous chromosomes during the first meiotic division. These processes are embedded in a carefully orchestrated cell differentiation program with multiple interdependencies between DNA metabolism, chromosome morphogenesis, and waves of gene expression that together ensure the correct number of chromosomes is delivered to the next generation. Studies in the budding yeast Saccharomyces cerevisiae have established essentially all fundamental paradigms of meiosis-specific chromosome metabolism and have uncovered components and molecular mechanisms that underlie these conserved processes. Here, we provide an overview of all stages of meiosis in this key model system and highlight how basic mechanisms of genome stability, chromosome architecture, and cell cycle control have been adapted to achieve the unique outcome of meiosis.
Topics: Recombination, Genetic; Saccharomycetales; Meiosis; Saccharomyces cerevisiae; Synaptonemal Complex
PubMed: 37616582
DOI: 10.1093/genetics/iyad125 -
Molecular Aspects of Medicine Jun 2024Meiosis is a critical step for spermatogenesis and oogenesis. Meiosis commences with pre-meiotic S phase that is subsequently followed by meiotic prophase. The meiotic... (Review)
Review
Meiosis is a critical step for spermatogenesis and oogenesis. Meiosis commences with pre-meiotic S phase that is subsequently followed by meiotic prophase. The meiotic prophase is characterized by the meiosis-specific chromosomal events such as chromosome recombination and homolog synapsis. Meiosis initiator (MEIOSIN) and stimulated by retinoic acid gene 8 (STRA8) initiate meiosis by activating the meiotic genes by installing the meiotic prophase program at pre-meiotic S phase. This review highlights the mechanisms of meiotic initiation and meiotic prophase progression from the point of the gene expression program and its relevance to infertility. Furthermore, upstream pathways that regulate meiotic initiation will be discussed in the context of spermatogenic development, indicating the sexual differences in the mode of meiotic entry.
Topics: Spermatogenesis; Humans; Meiosis; Animals; Male; Meiotic Prophase I; Prophase
PubMed: 38797021
DOI: 10.1016/j.mam.2024.101282 -
Biology of Reproduction Nov 2019Oocyte meiotic maturation is a vital and final process in oogenesis. Unlike somatic cells, the oocyte needs to undergo two continuous meiotic divisions (meiosis I and... (Review)
Review
Oocyte meiotic maturation is a vital and final process in oogenesis. Unlike somatic cells, the oocyte needs to undergo two continuous meiotic divisions (meiosis I and meiosis II) to become a haploid gamete. Notably, oocyte meiotic progression includes two rounds of unique meiotic arrest and resumption. The first arrest occurs at the G2 (germinal vesicle) stage and meiosis resumption is stimulated by a gonadotropin surge; the second arrest takes place at the metaphase II stage, the stage from which it is released when fertilization takes place. The maturation-promoting factor, which consists of cyclin B1 (CCNB1) and cyclin-dependent kinase 1 (CDK1), is responsible for regulating meiotic resumption and progression, while CDK1 is the unique CDK that acts as the catalytic subunit of maturation-promoting factor. Recent studies showed that except for cyclin B1, multiple cyclins interact with CDK1 to form complexes, which are involved in the regulation of meiotic progression at different stages. Here, we review and discuss the control of oocyte meiotic progression by cyclins A1, A2, B1, B2, B3, and O.
Topics: Animals; Cell Cycle; Cyclins; Female; Meiosis; Oocytes
PubMed: 31347666
DOI: 10.1093/biolre/ioz143 -
Genes Sep 2021Plant cytogenetic studies have provided essential knowledge on chromosome behavior during meiosis, contributing to our understanding of this complex process. In this... (Review)
Review
Plant cytogenetic studies have provided essential knowledge on chromosome behavior during meiosis, contributing to our understanding of this complex process. In this review, we describe in detail the meiotic process in auto- and allopolyploids from the onset of prophase I through pairing, recombination, and bivalent formation, highlighting recent findings on the genetic control and mode of action of specific proteins that lead to diploid-like meiosis behavior in polyploid species. During the meiosis of newly formed polyploids, related chromosomes (homologous in autopolyploids; homologous and homoeologous in allopolyploids) can combine in complex structures called multivalents. These structures occur when multiple chromosomes simultaneously pair, synapse, and recombine. We discuss the effectiveness of crossover frequency in preventing multivalent formation and favoring regular meiosis. Homoeologous recombination in particular can generate new gene (locus) combinations and phenotypes, but it may destabilize the karyotype and lead to aberrant meiotic behavior, reducing fertility. In crop species, understanding the factors that control pairing and recombination has the potential to provide plant breeders with resources to make fuller use of available chromosome variations in number and structure. We focused on wheat and oilseed rape, since there is an abundance of elucidating studies on this subject, including the molecular characterization of the (wheat) and (oilseed rape) loci, which are known to play a crucial role in regulating meiosis. Finally, we exploited the consequences of chromosome pairing and recombination for genetic map construction in polyploids, highlighting two case studies of complex genomes: (i) modern sugarcane, which has a man-made genome harboring two subgenomes with some recombinant chromosomes; and (ii) hexaploid sweet potato, a naturally occurring polyploid. The recent inclusion of allelic dosage information has improved linkage estimation in polyploids, allowing multilocus genetic maps to be constructed.
Topics: Brassica napus; Chromosomes, Plant; Crossing Over, Genetic; Meiosis; Plant Breeding; Polyploidy; Triticum
PubMed: 34680912
DOI: 10.3390/genes12101517 -
Cells Mar 2020Meiosis is a key event in the manufacturing of an oocyte. During this process, the oocyte creates a set of unique chromosomes by recombining paternal and maternal copies... (Review)
Review
Meiosis is a key event in the manufacturing of an oocyte. During this process, the oocyte creates a set of unique chromosomes by recombining paternal and maternal copies of homologous chromosomes, and by eliminating one set of chromosomes to become haploid. While meiosis is conserved among sexually reproducing eukaryotes, there is a bewildering diversity of strategies among species, and sometimes within sexes of the same species, to achieve proper segregation of chromosomes. Here, we review the very first steps of meiosis in females, when the maternal and paternal copies of each homologous chromosomes have to move, find each other and pair. We explore the similarities and differences observed in , , zebrafish and mouse females.
Topics: Animals; Caenorhabditis elegans; Chromosomes; Meiosis
PubMed: 32178277
DOI: 10.3390/cells9030696 -
Annual Review of Genetics Nov 2021The specialized two-stage meiotic cell division program halves a cell's chromosome complement in preparation for sexual reproduction. This reduction in ploidy requires... (Review)
Review
The specialized two-stage meiotic cell division program halves a cell's chromosome complement in preparation for sexual reproduction. This reduction in ploidy requires that in meiotic prophase, each pair of homologous chromosomes (homologs) identify one another and form physical links through DNA recombination. Here, we review recent advances in understanding the complex morphological changes that chromosomes undergo during meiotic prophase to promote homolog identification and crossing over. We focus on the structural maintenance of chromosomes (SMC) family cohesin complexes and the meiotic chromosome axis, which together organize chromosomes and promote recombination. We then discuss the architecture and dynamics of the conserved synaptonemal complex (SC), which assembles between homologs and mediates local and global feedback to ensure high fidelity in meiotic recombination. Finally, we discuss exciting new advances, including mechanisms for boosting recombination on particular chromosomes or chromosomal domains and the implications of a new liquid crystal model for SC assembly and structure.
Topics: Chromosome Pairing; Chromosomes; Homologous Recombination; Meiosis; Synaptonemal Complex
PubMed: 34530636
DOI: 10.1146/annurev-genet-071719-020235 -
Asian Journal of Andrology 2021Repairing DNA double-strand breaks (DSBs) with homologous chromosomes as templates is the hallmark of meiosis. The critical outcome of meiotic homologous recombination... (Review)
Review
Repairing DNA double-strand breaks (DSBs) with homologous chromosomes as templates is the hallmark of meiosis. The critical outcome of meiotic homologous recombination is crossovers, which ensure faithful chromosome segregation and promote genetic diversity of progenies. Crossover patterns are tightly controlled and exhibit three characteristics: obligatory crossover, crossover interference, and crossover homeostasis. Aberrant crossover patterns are the leading cause of infertility, miscarriage, and congenital disease. Crossover recombination occurs in the context of meiotic chromosomes, and it is tightly integrated with and regulated by meiotic chromosome structure both locally and globally. Meiotic chromosomes are organized in a loop-axis architecture. Diverse evidence shows that chromosome axis length determines crossover frequency. Interestingly, short chromosomes show different crossover patterns compared to long chromosomes. A high frequency of human embryos are aneuploid, primarily derived from female meiosis errors. Dramatically increased aneuploidy in older women is the well-known "maternal age effect." However, a high frequency of aneuploidy also occurs in young women, derived from crossover maturation inefficiency in human females. In addition, frequency of human aneuploidy also shows other age-dependent alterations. Here, current advances in the understanding of these issues are reviewed, regulation of crossover patterns by meiotic chromosomes are discussed, and issues that remain to be investigated are suggested.
Topics: Cell Division; Chromosome Segregation; Humans; Meiosis; Recombination, Genetic
PubMed: 33533735
DOI: 10.4103/aja.aja_86_20 -
Journal of Genetics 2022Gerrymandering, the structuring of voting districts to favour certain politicians and political groups, undermines fair elections and presents a serious challenge to...
Gerrymandering, the structuring of voting districts to favour certain politicians and political groups, undermines fair elections and presents a serious challenge to democracy. We introduce a solution to gerrymandering inspired by the biological process of cell division in sexually reproducing organisms, meiosis, in which the boundaries of electorates are frequently redrawn by randomizing algorithms. By demonstrating the deep parallels between meiosis and John Rawls's concept of a 'veil of ignorance', we also show how one of the biggest threats to the integrity of meiosis-selfish genetic elements, genes that promote their own transmission at the expense of organismal fitness-can inspire another potential advantage to frequent random redistricting.
Topics: Meiosis; Politics
PubMed: 36156509
DOI: No ID Found -
Journal of Cellular Biochemistry Dec 2023The correct assembly of the spindle apparatus directly regulates the precise separation of chromosomes in mouse oocytes, which is crucial for obtaining high-quality...
The correct assembly of the spindle apparatus directly regulates the precise separation of chromosomes in mouse oocytes, which is crucial for obtaining high-quality oocytes capable of successful fertilization. The localization, assembly, migration, and disassembly of the spindle are regulated by a series of spindle-associated proteins, which exhibit unique expression level variations and specific localization in oocytes. Proteomic analysis revealed that among many representative spindle-associated proteins, the expression level of nucleolar and spindle-associated protein 1 (NUSAP1) significantly increased after meiotic resumption, with a magnitude of change higher than that of other proteins. However, the role of NUSAP1 during oocyte meiosis maturation has not been reported. Here, we report that NUSAP1 is distributed within the cell nucleus during the germinal vesicle (GV) oocytes with non-surrounded nucleolus stage and is not enriched in the nucleus during the GV-surrounded nucleolus stage. Interestingly, NUSAP1 forms distinct granular aggregates near the spindle poles during the prophase of the first meiotic division (Pro-MI), metaphase I, and anaphase I/telophase I stages. Nusap1 depletion leads to chromosome misalignment, increased aneuploidy, and abnormal spindle assembly, particularly a decrease in spindle pole width. Correspondingly, RNA-seq analysis revealed significant suppression of the "establishment of spindle orientation" signaling pathway. Additionally, the attenuation of F-actin in NUSAP1-deficient oocytes may affect the asymmetric division process. Gene ontology analysis of NUSAP1 interactomes, identified through mass spectrometry here, revealed significant enrichment for RNA binding. As an RNA-binding protein, NUSAP1 is likely involved in the regulation of messenger RNA homeostasis by influencing the dynamics of processing (P)-body components. Overall, our results demonstrate the critical importance of precise regulation of NUSAP1 expression levels and protein localization for maintaining mouse oocyte meiosis.
Topics: Animals; Mice; Meiosis; Metaphase; Microtubule-Associated Proteins; Oocytes; Oogenesis; Proteomics; Spindle Apparatus
PubMed: 37992207
DOI: 10.1002/jcb.30498 -
Biology of Reproduction Jul 2022Meiosis is the foundation of sexual reproduction, and crossover recombination is one hallmark of meiosis. Crossovers establish the physical connections between homolog...
Meiosis is the foundation of sexual reproduction, and crossover recombination is one hallmark of meiosis. Crossovers establish the physical connections between homolog chromosomes (homologs) for their proper segregation and exchange DNA between homologs to promote genetic diversity in gametes and thus progenies. Aberrant crossover patterns, e.g., absence of the obligatory crossover, are the leading cause of infertility, miscarriage, and congenital disease. Therefore, crossover patterns have to be tightly controlled. During meiosis, loop/axis organized chromosomes provide the structural basis and regulatory machinery for crossover patterning. Accumulating evidence shows that chromosome axis length regulates the numbers and the positions of crossovers. In addition, recent studies suggest that alterations in axis length and the resultant alterations in crossover frequency may contribute to evolutionary adaptation. Here, current advances regarding these issues are reviewed, the possible mechanisms for axis length regulating crossover frequency are discussed, and important issues that need further investigations are suggested.
Topics: Chromosome Segregation; Chromosomes; Meiosis; Recombination, Genetic
PubMed: 35191959
DOI: 10.1093/biolre/ioac040