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Seminars in Cell & Developmental Biology Aug 2022Despite the universal requirement for faithful chromosome segregation, eukaryotic centromeres are rapidly evolving. It is hypothesized that rapid centromere evolution... (Review)
Review
Despite the universal requirement for faithful chromosome segregation, eukaryotic centromeres are rapidly evolving. It is hypothesized that rapid centromere evolution represents an evolutionary arms race between selfish genetic elements that drive, or propagate at the expense of organismal fitness, and mechanisms that suppress fitness costs. Selfish centromere DNA achieves preferential inheritance in female meiosis by recruiting more effector proteins that alter spindle microtubule interaction dynamics. Parallel pathways for effector recruitment are adaptively evolved to suppress functional differences between centromeres. Opportunities to drive are not limited to female meiosis, and selfish transposons, plasmids and B chromosomes also benefit by maximizing their inheritance. Rapid evolution of selfish genetic elements can diversify suppressor mechanisms in different species that may cause hybrid incompatibility.
Topics: Centromere; Chromosome Segregation; Eukaryota; Female; Humans; Meiosis; Microtubules
PubMed: 35346579
DOI: 10.1016/j.semcdb.2022.03.026 -
Cell Jun 2020Meiosis is the specialized cell division that generates haploid gametes and is therefore essential for sexual reproduction. This SnapShot encompasses key events taking...
Meiosis is the specialized cell division that generates haploid gametes and is therefore essential for sexual reproduction. This SnapShot encompasses key events taking place during prophase I of meiosis that are required for achieving proper chromosome segregation and highlights how these are both conserved and diverged throughout five different species. To view this SnapShot, open or download the PDF.
Topics: Animals; Arabidopsis; Caenorhabditis elegans; Chromosome Segregation; Drosophila melanogaster; Meiosis; Meiotic Prophase I; Mice; Saccharomyces cerevisiae
PubMed: 32531249
DOI: 10.1016/j.cell.2020.04.038 -
Nature Communications Mar 2023Spindle formation in male meiosis relies on the canonical centrosome system, which is distinct from acentrosomal oocyte meiosis, but its specific regulatory mechanisms...
Spindle formation in male meiosis relies on the canonical centrosome system, which is distinct from acentrosomal oocyte meiosis, but its specific regulatory mechanisms remain unknown. Herein, we report that DYNLRB2 (Dynein light chain roadblock-type-2) is a male meiosis-upregulated dynein light chain that is indispensable for spindle formation in meiosis I. In Dynlrb2 KO mouse testes, meiosis progression is arrested in metaphase I due to the formation of multipolar spindles with fragmented pericentriolar material (PCM). DYNLRB2 inhibits PCM fragmentation through two distinct pathways; suppressing premature centriole disengagement and targeting NuMA (nuclear mitotic apparatus) to spindle poles. The ubiquitously expressed mitotic counterpart, DYNLRB1, has similar roles in mitotic cells and maintains spindle bipolarity by targeting NuMA and suppressing centriole overduplication. Our work demonstrates that two distinct dynein complexes containing DYNLRB1 or DYNLRB2 are separately used in mitotic and meiotic spindle formations, respectively, and that both have NuMA as a common target.
Topics: Mice; Animals; Male; Dyneins; Spindle Apparatus; Centrosome; Meiosis; Metaphase
PubMed: 36973253
DOI: 10.1038/s41467-023-37370-7 -
Development (Cambridge, England) Sep 2022Gametogenesis in mammals encompasses highly regulated developmental transitions. These are associated with changes in transcription that cause characteristic patterns of...
Gametogenesis in mammals encompasses highly regulated developmental transitions. These are associated with changes in transcription that cause characteristic patterns of gene expression observed during distinct stages of gamete development, which include specific activities with critical meiotic functions. SWI/SNF chromatin remodelers are recognized regulators of gene transcription and DNA repair, but their composition and functions in meiosis are poorly understood. We have generated gamete-specific conditional knockout mice for ARID2, a specific regulatory subunit of PBAF, and have compared its phenotype with BRG1 knockouts, the catalytic subunit of PBAF/BAF complexes. While Brg1Δ/Δ knockout acts at an early stage of meiosis and causes cell arrest at pachynema, ARID2 activity is apparently required at the end of prophase I. Striking defects in spindle assembly and chromosome-spindle attachment observed in Arid2Δ/Δ knockouts are attributed to an increase in aurora B kinase, a master regulator of chromosome segregation, at centromeres. Further genetic and biochemical analyses suggest the formation of a canonical PBAF and a BRG1-independent complex containing ARID2 and PBRM1 as core components. The data support a model in which different PBAF complexes regulate different stages of meiosis and gametogenesis.
Topics: Animals; Aurora Kinase B; Chromatin; Chromatin Assembly and Disassembly; Chromosomal Proteins, Non-Histone; Meiosis; Mice; Transcription Factors
PubMed: 36111709
DOI: 10.1242/dev.199967 -
Current Opinion in Genetics &... Dec 2023Gametogenesis is vulnerable to selfish genetic elements that bias their transmission to the next generation by cheating meiosis. These so-called meiotic drivers are... (Review)
Review
Gametogenesis is vulnerable to selfish genetic elements that bias their transmission to the next generation by cheating meiosis. These so-called meiotic drivers are widespread in plants, animals, and fungi and can impact genome evolution. Here, we summarize recent progress on the causes and consequences of meiotic drive in males, where selfish elements attack vulnerabilities in spermatogenesis. Advances in genomics provide new insights into the organization and dynamics of driving chromosomes in natural populations. Common themes, including small RNAs, gene duplications, and heterochromatin, emerged from these studies. Interdisciplinary approaches combining evolutionary genomics with molecular and cell biology are beginning to unravel the mysteries of drive and suppression mechanisms. These approaches also provide insights into fundamental processes in spermatogenesis and chromatin regulation.
Topics: Animals; Male; Chromosomes; Meiosis
PubMed: 37704518
DOI: 10.1016/j.gde.2023.102111 -
Current Opinion in Genetics &... Dec 2021DNA breaks may arise accidentally in vegetative cells or in a programmed manner in meiosis. The usage of a DNA template makes homologous recombination potentially... (Review)
Review
DNA breaks may arise accidentally in vegetative cells or in a programmed manner in meiosis. The usage of a DNA template makes homologous recombination potentially error-free, however, recombination is not always accurate. Cells possess a remarkable capacity to tailor processing of recombination intermediates to fulfill a particular need. Vegetatively growing cells aim to maintain genome stability and therefore repair accidental breaks largely accurately, using sister chromatids as templates, into mostly non-crossovers products. Recombination in meiotic cells is instead more likely to employ homologous chromosomes as templates and result in crossovers to allow proper chromosome segregation and promote genetic diversity. Here we review models explaining the processing of recombination intermediates in vegetative and meiotic cells and its regulation, with a focus on MLH1-MLH3-dependent crossing-over during meiotic recombination.
Topics: Chromatids; Chromosome Segregation; DNA Breaks, Double-Stranded; DNA Repair; Homologous Recombination; Meiosis
PubMed: 34293660
DOI: 10.1016/j.gde.2021.06.012 -
Scientific Reports Sep 2021Dinoflagellates in the family Symbiodiniaceae are obligate endosymbionts of diverse marine invertebrates, including corals, and impact the capacity of their hosts to...
Dinoflagellates in the family Symbiodiniaceae are obligate endosymbionts of diverse marine invertebrates, including corals, and impact the capacity of their hosts to respond to climate change-driven ocean warming. Understanding the conditions under which increased genetic variation in Symbiodiniaceae arises via sexual recombination can support efforts to evolve thermal tolerance in these symbionts and ultimately mitigate coral bleaching, the breakdown of the coral-Symbiodiniaceae partnership under stress. However, direct observations of meiosis in Symbiodiniaceae have not been reported, despite various lines of indirect evidence that it occurs. We present the first cytological evidence of sex in Symbiodiniaceae based on nuclear DNA content and morphology using Image Flow Cytometry, Cell Sorting and Confocal Microscopy. We show the Symbiodiniaceae species, Cladocopium latusorum, undergoes gamete conjugation, zygote formation, and meiosis within a dominant reef-building coral in situ. On average, sex was detected in 1.5% of the cells analyzed (N = 10,000-40,000 cells observed per sample in a total of 20 samples obtained from 3 Pocillopora colonies). We hypothesize that meiosis follows a two-step process described in other dinoflagellates, in which diploid zygotes form dyads during meiosis I, and triads and tetrads as final products of meiosis II. This study sets the stage for investigating environmental triggers of Symbiodiniaceae sexuality and can accelerate the assisted evolution of a key coral symbiont in order to combat reef degradation.
Topics: Coral Reefs; DNA; Dinoflagellida; Flow Cytometry; Meiosis; Microscopy, Confocal; Mitosis; Recombination, Genetic; Reproduction; Zygote
PubMed: 34552138
DOI: 10.1038/s41598-021-98148-9 -
Molecular Biology of the Cell Apr 2024Chromosomes and karyotypes are particularly rich in oddities and extremes. Described below are 10 remarkable chromosomes and karyotypes sprinkled throughout the tree of... (Review)
Review
Chromosomes and karyotypes are particularly rich in oddities and extremes. Described below are 10 remarkable chromosomes and karyotypes sprinkled throughout the tree of life. These include variants in chromosome number, structure, and dynamics both natural and engineered. This versatility highlights the robustness and tolerance of the mitotic and meiotic machinery to dramatic changes in chromosome and karyotype architecture. These examples also illustrate that the robustness comes at a cost, enabling the evolution of chromosomes that subvert mitosis and meiosis.
Topics: Chromosomes; Karyotype; Karyotyping; Meiosis; Mitosis
PubMed: 38517328
DOI: 10.1091/mbc.E23-12-0498 -
EMBO Reports Feb 2023Following meiotic recombination, each pair of homologous chromosomes acquires at least one crossover, which ensures accurate chromosome segregation and allows reciprocal...
Following meiotic recombination, each pair of homologous chromosomes acquires at least one crossover, which ensures accurate chromosome segregation and allows reciprocal exchange of genetic information. Recombination failure often leads to meiotic arrest, impairing fertility, but the molecular basis of recombination remains elusive. Here, we report a homozygous M1AP splicing mutation (c.1074 + 2T > C) in patients with severe oligozoospermia owing to meiotic metaphase I arrest. The mutation abolishes M1AP foci on the chromosome axes, resulting in decreased recombination intermediates and crossovers in male mouse models. M1AP interacts with the mammalian ZZS (an acronym for yeast proteins Zip2-Zip4-Spo16) complex components, SHOC1, TEX11, and SPO16. M1AP localizes to chromosomal axes in a SPO16-dependent manner and colocalizes with TEX11. Ablation of M1AP does not alter SHOC1 localization but reduces the recruitment of TEX11 to recombination intermediates. M1AP shows cytoplasmic localization in fetal oocytes and is dispensable for fertility and crossover formation in female mice. Our study provides the first evidence that M1AP acts as a copartner of the ZZS complex to promote crossover formation and meiotic progression in males.
Topics: Animals; Female; Male; Mice; Meiosis; Microtubule-Associated Proteins; DNA-Binding Proteins; Cell Cycle Proteins; Multiprotein Complexes
PubMed: 36440627
DOI: 10.15252/embr.202255778 -
Journal of Experimental Zoology. Part... Dec 2021The germline is unique and immortal (or at least its genome is). It is able to perform unique jobs (meiosis) and is selected for genetic changes. Part of being this... (Review)
Review
The germline is unique and immortal (or at least its genome is). It is able to perform unique jobs (meiosis) and is selected for genetic changes. Part of being this special also means that entry into the germline club is restricted and cells of the soma are always left out. However, the recent evidence from multiple animals now suggests that somatic cells may join the club and become germline cells in an animal when the original germline is removed. This "violation" may have garnered acceptance by the observation that iPScells, originating experimentally from somatic cells of an adult, can form reproductively successful eggs and sperm, all in vitro. Each of the genes and their functions used to induce pluripotentiality are found normally in the cell and the in vitro conditions to direct germline commitment replicate conditions in vivo. Here, we discuss evidence from three different animals: an ascidian, a segmented worm, and a sea urchin; and that the cells of a somatic cell lineage can convert into the germline in vivo. We discuss the consequences of such transitions and provide thoughts as how this process may have equal precision to the original germline formation of an embryo.
Topics: Animals; Annelida; Cell Lineage; Germ Cells; Meiosis; Sea Urchins; Urochordata
PubMed: 32445519
DOI: 10.1002/jez.b.22952