-
Development (Cambridge, England) Jul 2023Retinoic acid (RA) is the proposed mammalian 'meiosis inducing substance'. However, evidence for this role comes from studies in the fetal ovary, where germ cell...
Retinoic acid (RA) is the proposed mammalian 'meiosis inducing substance'. However, evidence for this role comes from studies in the fetal ovary, where germ cell differentiation and meiotic initiation are temporally inseparable. In the postnatal testis, these events are separated by more than 1 week. Exploiting this difference, we discovered that, although RA is required for spermatogonial differentiation, it is dispensable for the subsequent initiation, progression and completion of meiosis. Indeed, in the absence of RA, the meiotic transcriptome program in both differentiating spermatogonia and spermatocytes entering meiosis was largely unaffected. Instead, transcripts encoding factors required during spermiogenesis were aberrant during preleptonema, and the subsequent spermatid morphogenesis program was disrupted such that no sperm were produced. Taken together, these data reveal a RA-independent model for male meiotic initiation.
Topics: Animals; Female; Male; Testis; Tretinoin; Spermatogenesis; Spermatogonia; Spermatozoa; Meiosis; Mammals
PubMed: 37350382
DOI: 10.1242/dev.201638 -
Chromosoma Sep 2019Meiosis is the special division that produces haploid gametes, such as sperm and eggs. It involves a complex series of events that integrate large structural changes at...
Meiosis is the special division that produces haploid gametes, such as sperm and eggs. It involves a complex series of events that integrate large structural changes at the chromosome scale with fine regulation of recombination events in localized regions. To evaluate the complexity of these processes, the meiosis field covers a variety of disciplines and model organisms, making it an exciting and rapidly changing area of research. The field as a whole highlights both the conserved aspects of meiosis, as well as the marked diversity of the means taken to ensure that, ultimately, gametes will contain a balanced number of chromosomes and genetic diversity will have been produced. Studying meiosis is also critically important for the improvement of our human condition as errors of meiosis are a leading cause of infertility, miscarriage, and developmental disabilities. Finally, the complex chromosome behavior of meiosis is a genetically tractable paradigm, the study of which improves our understanding of many fundamental cellular processes including DNA repair, genome stability, cancer etiology, chromatin structure, and chromosome dynamics.This special issue on meiosis contains twenty-two papers, of which five are in-depth reviews that complement and put in context the experimental data presented in the seventeen original research articles. The content of this issue illustrates the diversity of topics covered by researchers in the field, ranging from the effects of environment and external factors on the success of meiosis, the cell cycle actors that control the meiotic divisions, the mechanism of chromosome segregation, and the mechanisms that ensure proper homologous chromosome pairing, recombination, and synapsis. Multiple organisms are covered. Also evident is the fact that more and more studies use multicellular organisms as a model system, in large part due to the increased availability of tools that were previously restricted to studies in budding and fission yeasts.
Topics: Animals; Chromosome Segregation; DNA Replication; Humans; Meiosis
PubMed: 31616989
DOI: 10.1007/s00412-019-00726-4 -
Nature Reviews. Genetics May 2024Sexually reproducing eukaryotes use recombination between homologous chromosomes to promote chromosome segregation during meiosis. Meiotic recombination is almost... (Review)
Review
Sexually reproducing eukaryotes use recombination between homologous chromosomes to promote chromosome segregation during meiosis. Meiotic recombination is almost universally conserved in its broad strokes, but specific molecular details often differ considerably between taxa, and the proteins that constitute the recombination machinery show substantial sequence variability. The extent of this variation is becoming increasingly clear because of recent increases in genomic resources and advances in protein structure prediction. We discuss the tension between functional conservation and rapid evolutionary change with a focus on the proteins that are required for the formation and repair of meiotic DNA double-strand breaks. We highlight phylogenetic relationships on different time scales and propose that this remarkable evolutionary plasticity is a fundamental property of meiotic recombination that shapes our understanding of molecular mechanisms in reproductive biology.
Topics: DNA Repair; Phylogeny; Homologous Recombination; Meiosis; DNA Breaks, Double-Stranded
PubMed: 38036793
DOI: 10.1038/s41576-023-00669-8 -
Genes Mar 2022The origin and inheritance of chromosome changes provide the essential foundation for natural selection and evolution. The evolutionary fate of chromosome changes... (Review)
Review
The origin and inheritance of chromosome changes provide the essential foundation for natural selection and evolution. The evolutionary fate of chromosome changes depends on the place and time of their emergence and is controlled by checkpoints in mitosis and meiosis. Estimating whether the altered genome can be passed to subsequent generations should be central when we consider a particular genome rearrangement. Through comparative analysis of chromosome rearrangements in soma and germ line, the potential impact of macromutations such as chromothripsis or chromoplexy appears to be fascinating. What happens with chromosomes during the early development, and which alterations lead to mosaicism are other poorly studied but undoubtedly essential issues. The evolutionary impact can be gained most effectively through chromosome rearrangements arising in male meiosis I and in female meiosis II, which are the last divisions following fertilization. The diversity of genome organization has unique features in distinct animals; the chromosome changes, their internal relations, and some factors safeguarding genome maintenance in generations under natural selection were considered for mammals.
Topics: Animals; Chromosome Aberrations; Chromosomes; Chromothripsis; Female; Germ Cells; Male; Mammals; Meiosis; Mitosis
PubMed: 35456408
DOI: 10.3390/genes13040602 -
Seminars in Cell & Developmental Biology Jul 2022Centromeres are specialized chromosomal regions that recruit kinetochore proteins and mediate spindle microtubule attachment to ensure faithful chromosome segregation... (Review)
Review
Centromeres are specialized chromosomal regions that recruit kinetochore proteins and mediate spindle microtubule attachment to ensure faithful chromosome segregation during mitosis and meiosis. Centromeres can be restricted to one region of the chromosome. Named "monocentromere", this type represents the most commonly found centromere organization across eukaryotes. Alternatively, centromeres can also be assembled at sites chromosome-wide. This second type is called "holocentromere". Despite their early description over 100 years ago, research on holocentromeres has lagged behind that of monocentromeres. Nevertheless, the application of next generation sequencing approaches and advanced microscopic technologies enabled recent advances understanding the molecular organization and regulation of holocentromeres in different organisms. Here we review the current state of research on holocentromeres focusing on evolutionary considerations. First, we provide a brief historical perspective on the discovery of holocentric chromosomes. We then discuss models/drivers that have been proposed over the years to explain the evolutionary transition from mono- to holocentric chromosomes. We continue to review the description of holocentric chromosomes in diverse eukaryotic groups and then focus our discussion on a specific and recently characterized type of holocentromere organization in insects that functions independently of the otherwise essential centromeric marker protein CenH3, thus providing novel insights into holocentromere evolution in insects. Finally, we propose reasons to explain why the holocentric trait is not more frequent across eukaryotes despite putative selective advantages.
Topics: Animals; Centromere; Chromosome Segregation; Insecta; Meiosis; Mitosis
PubMed: 35031207
DOI: 10.1016/j.semcdb.2022.01.003 -
Annual Review of Genetics Nov 2021Sex, as well as meiotic recombination between homologous chromosomes, is nearly ubiquitous among eukaryotes. In those species that use it, recombination is important for... (Review)
Review
Sex, as well as meiotic recombination between homologous chromosomes, is nearly ubiquitous among eukaryotes. In those species that use it, recombination is important for chromosome segregation during gamete production, and thus for fertility. Strikingly, although in most species only one crossover event per chromosome is required to ensure proper segregation, recombination rates vary considerably above this minimum and show variation within and among species. However, whether this variation in recombination is adaptive or neutral and what might shape it remain unclear. Empirical studies and theory support the idea that recombination is generally beneficial but can also have costs. Here, we review variation in genome-wide recombination rates, explore what might cause this, and discuss what is known about its mechanistic basis. We end by discussing the environmental sensitivity of meiosis and recombination rates, how these features may relate to adaptation, and their implications for a broader understanding of recombination rate evolution.
Topics: Chromosome Segregation; Chromosomes; Genome; Homologous Recombination; Meiosis
PubMed: 34310193
DOI: 10.1146/annurev-genet-021721-033821 -
Journal of Advanced Research Sep 2023The R-loop is a naturally formed three-strand nucleic acid structure that recently has been reported to participate in multiple biological processes and helped answer...
INTRODUCTION
The R-loop is a naturally formed three-strand nucleic acid structure that recently has been reported to participate in multiple biological processes and helped answer some previously unexplained scientific questions. Meiosis process involves multiple chromatin-related events such as DNA double-stranded breaks (DSB) formation, repairing and transcriptional dynamics.
OBJECTIVES
Explore the regulatory roles and physiological functions of R-loops in the mammalian meiosis process.
METHODS
In our study, using genome-wide S9.6 CUT & Tag seq, we first mapped the genomic distribution and dynamic changes of R-loop during the meiotic process in mice, from spermatogonia to secondary spermatocytes. And we further explore the role of R-loop in physiological conditions by constructing conditional knockout mice of Rnaseh1, which deleted the R-loop endonuclease before meiosis entry.
RESULTS
R-loop predominantly distributes at promoter-related regions and varies across different meiotic stages. By joint analysis with the corresponding transcriptome, we found that the R-loop was closely related to transcription during the meiotic process. The high frequency of promoter-related R-loop in meiotic cells is usually accompanied by high transcription activity, and we further verified this in the leptotene/zygotene to the pachytene transition process. Moreover, the lack of RNase H1 caused sterility in male mice with R-loop accumulation and abnormal DSB repair in spermatocytes. Further analysis showed that abnormal R-loop accumulation in the leptotene/zygotene stages influenced transcriptional regulation in the pachytene stage.
CONCLUSION
The mutual regulation of the R-loop and transcription plays an essential role in spermatogenesis. And R-loop is also important for the normal repair process of DSB during meiosis.
Topics: Male; Mice; Animals; R-Loop Structures; DNA Breaks, Double-Stranded; Meiosis; Spermatogenesis; Spermatocytes; Mice, Knockout; Mammals
PubMed: 36396044
DOI: 10.1016/j.jare.2022.10.016 -
Biological Reviews of the Cambridge... Jun 2021The separation of germ cell populations from the soma is part of the evolutionary transition to multicellularity. Only genetic information present in the germ cells will... (Review)
Review
The separation of germ cell populations from the soma is part of the evolutionary transition to multicellularity. Only genetic information present in the germ cells will be inherited by future generations, and any molecular processes affecting the germline genome are therefore likely to be passed on. Despite its prevalence across taxonomic kingdoms, we are only starting to understand details of the underlying micro-evolutionary processes occurring at the germline genome level. These include segregation, recombination, mutation and selection and can occur at any stage during germline differentiation and mitotic germline proliferation to meiosis and post-meiotic gamete maturation. Selection acting on germ cells at any stage from the diploid germ cell to the haploid gametes may cause significant deviations from Mendelian inheritance and may be more widespread than previously assumed. The mechanisms that affect and potentially alter the genomic sequence and allele frequencies in the germline are pivotal to our understanding of heritability. With the rise of new sequencing technologies, we are now able to address some of these unanswered questions. In this review, we comment on the most recent developments in this field and identify current gaps in our knowledge.
Topics: Biological Evolution; Genome; Germ Cells; Meiosis; Mutation
PubMed: 33615674
DOI: 10.1111/brv.12680 -
Molecules and Cells May 2022During meiosis, homologous chromosomes (homologs) pair and undergo genetic recombination via assembly and disassembly of the synaptonemal complex. Meiotic recombination... (Review)
Review
During meiosis, homologous chromosomes (homologs) pair and undergo genetic recombination via assembly and disassembly of the synaptonemal complex. Meiotic recombination is initiated by excess formation of DNA double-strand breaks (DSBs), among which a subset are repaired by reciprocal genetic exchange, called crossovers (COs). COs generate genetic variations across generations, profoundly affecting genetic diversity and breeding. At least one CO between homologs is essential for the first meiotic chromosome segregation, but generally only one and fewer than three inter-homolog COs occur in plants. CO frequency and distribution are biased along chromosomes, suppressed in centromeres, and controlled by pro-CO, anti-CO, and epigenetic factors. Accurate and high-throughput detection of COs is important for our understanding of CO formation and chromosome behavior. Here, we review advanced approaches that enable precise measurement of the location, frequency, and genomic landscapes of COs in plants, with a focus on .
Topics: Arabidopsis; Crossing Over, Genetic; DNA Breaks, Double-Stranded; Homologous Recombination; Meiosis; Plants
PubMed: 35444069
DOI: 10.14348/molcells.2022.2054 -
The Plant Journal : For Cell and... Aug 2022Polyploidy is a major force shaping eukaryote evolution but poses challenges for meiotic chromosome segregation. As a result, first-generation polyploids often suffer...
Polyploidy is a major force shaping eukaryote evolution but poses challenges for meiotic chromosome segregation. As a result, first-generation polyploids often suffer from more meiotic errors and lower fertility than established wild polyploid populations. How established polyploids adapt their meiotic behaviour to ensure genome stability and accurate chromosome segregation remains an active research question. We present here a cytological description of meiosis in the model allopolyploid species Arabidopsis suecica (2n = 4x = 26). In large part meiosis in A. suecica is diploid-like, with normal synaptic progression and no evidence of synaptic partner exchanges. Some abnormalities were seen at low frequency, including univalents at metaphase I, anaphase bridges and aneuploidy at metaphase II; however, we saw no evidence of crossover formation occurring between non-homologous chromosomes. The crossover number in A. suecica is similar to the combined number reported from its diploid parents Arabidopsis thaliana (2n = 2x = 10) and Arabidopsis arenosa (2n = 2x = 16), with an average of approximately 1.75 crossovers per chromosome pair. This contrasts with naturally evolved autotetraploid A. arenosa, where accurate chromosome segregation is achieved by restricting crossovers to approximately 1 per chromosome pair. Although an autotetraploid donor is hypothesized to have contributed the A. arenosa subgenome to A. suecica, A. suecica harbours diploid A. arenosa variants of key meiotic genes. These multiple lines of evidence suggest that meiosis in the recently evolved allopolyploid A. suecica is essentially diploid like, with meiotic adaptation following a very different trajectory to that described for autotetraploid A. arenosa.
Topics: Arabidopsis; Diploidy; Genome, Plant; Meiosis; Polyploidy
PubMed: 35759495
DOI: 10.1111/tpj.15879