Centromere Associations in Meiotic Chromosome Pairing

Ines, Olivier Da; White, Charles I.

doi:10.1146/annurev-genet-112414-055107

Cited by 41 publications

(33 citation statements)

References 146 publications

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“…The classic example of chromosome movements and telomere clustering is provided by Schizosaccharomyces pombe , in which the telomeres cluster at the spindle pole body and the entire nucleus oscillates between the cell poles, a movement often described as the horsetail (46, 114). Centromere association appears to be important also, at least in certain species, including S. cerevisiae , S. pombe , A. thaliana , and D. melanogaster (reviewed by 58). …”

Section: Initiation Of Synapsis and Recombinationmentioning

confidence: 99%

Control of Meiotic Crossovers: From Double-Strand Break Formation to Designation

2016

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Meiosis, the mechanism of creating haploid gametes, is a complex cellular process observed across sexually reproducing organisms. Fundamental to meiosis is the process of homologous recombination, whereby DNA double-strand breaks are introduced into the genome and are subsequently repaired to generate either noncrossovers or crossovers. Although homologous recombination is essential for chromosome pairing during prophase I, the resulting crossovers are critical for maintaining homolog interactions and enabling accurate segregation at the first meiotic division. Thus, the placement, timing, and frequency of crossover formation must be exquisitely controlled. In this review, we discuss the proteins involved in crossover formation, the process of their formation and designation, and the rules governing crossovers, all within the context of the important landmarks of prophase I. We draw together crossover designation data across organisms, analyze their evolutionary divergence, and propose a universal model for crossover regulation.

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Section: Initiation Of Synapsis and Recombinationmentioning

confidence: 99%

Control of Meiotic Crossovers: From Double-Strand Break Formation to Designation

2016

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“…Because of the presence of multiple similar chromosomes, polyploid wheat requires specific mechanisms to correctly pair homologous chromosomes and thus avoid the formation of unbalanced gametes during meiosis. Centromeres are essential for genome stability, and centromere coupling before the onset of homologous chromosome pairing during meiosis is critical for the faithful segregation of monocentric eukaryotic chromosomes to daughter cells (Pluta et al, 1995;Zhang et al, 2013b;Fukagawa and Earnshaw, 2014;Da Ines and White, 2015). These observations suggest that the centromeres in the subgenomes of polyploid species may function during meiosis to ensure genome stability via effects on chromosome pairing, in addition to mediating kinetochore organization and the attachment of spindle microtubules.…”

Section: Introductionmentioning

confidence: 99%

Centromere Satellite Repeats Have Undergone Rapid Changes in Polyploid Wheat Subgenomes

Liu

et al. 2019

Plant Cell

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Centromeres mediate the pairing of homologous chromosomes during meiosis; this pairing is particularly challenging for polyploid plants such as hexaploid bread wheat (Triticum aestivum), as their meiotic machinery must differentiate homologs from similar homoeologs. However, the sequence compositions (especially functional centromeric satellites) and evolutionary history of wheat centromeres are largely unknown. Here, we mapped T. aestivum centromeres by chromatin immunoprecipitation sequencing using antibodies to the centromeric-specific histone H3 variant (CENH3); this identified two types of functional centromeric satellites that are abundant in two of the three subgenomes. These centromeric satellites had unit sizes greater than 500 bp and contained specific sites with highly phased binding to CENH3 nucleosomes. Phylogenetic analysis revealed that the satellites have diverged in the three T. aestivum subgenomes, and the more homogeneous satellite arrays are associated with CENH3. Satellite signals decreased and the degree of satellites variation increased from diploid to hexaploid wheat. Moreover, several T. aestivum centromeres lack satellite repeats. Rearrangements, including local expansion and satellite variations, inversions, and changes in gene expression, occurred during the evolution from diploid to tetraploid and hexaploid wheat. These results reveal the asymmetry in centromere organization among the wheat subgenomes, which may play a role in proper homolog pairing during meiosis.

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“…As expected from its structure, bouquet formation restricts chromosome mobility at telomeres and telomere-led chromosome oscillation promotes pairing of homologous regions followed by synapsis and meiotic recombination between homologues [ 4 , 5 ]. In some organisms chromosomes form contacts with the LINC complex via the centromeres or specific domains called pairing centres [ 5–7 ]. In mammals, this anchoring of telomeres as a bouquet, and the dynamic movement of chromosomes, are both essential processes for gametogenesis, suggesting a crucial role for the bouquet in meiotic progression [ 8–16 ].…”

Section: Introductionmentioning

confidence: 99%

The telomere bouquet facilitates meiotic prophase progression and exit in fission yeast

et al. 2017

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During meiotic prophase, chromosome arrangement and oscillation promote the pairing of homologous chromosomes for meiotic recombination. This dramatic movement involves clustering of telomeres at the nuclear membrane to form the so-called telomere bouquet. In fission yeast, the telomere bouquet is formed near the spindle pole body (SPB), which is the microtubule organising centre, functionally equivalent to the metazoan centrosome. Disruption of bouquet configuration impedes homologous chromosome pairing, meiotic recombination and spindle formation. Here, we demonstrate that the bouquet is maintained throughout meiotic prophase and promotes timely prophase exit in fission yeast. Persistent DNA damages, induced during meiotic recombination, activate the Rad3 and Chk1 DNA damage checkpoint kinases and extend the bouquet stage beyond the chromosome oscillation period. The auxin-inducible degron system demonstrated that premature termination of the bouquet stage leads to severe extension of prophase and consequently spindle formation defects. However, this delayed exit from meiotic prophase was not caused by residual DNA damage. Rather, loss of chromosome contact with the SPB caused delayed accumulation of CDK1-cyclin B at the SPB, which correlated with impaired SPB separation. In the absence of the bouquet, CDK1-cyclin B localised near the telomeres but not at the SPB at the later stage of meiotic prophase. Thus, bouquet configuration is maintained throughout meiotic prophase, by which this spatial organisation may facilitate local and timely activation of CDK1 near the SPB. Our findings illustrate that chromosome contact with the nuclear membrane synchronises meiotic progression of the nucleoplasmic chromosomes with that of the cytoplasmic SPB.

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Centromere Associations in Meiotic Chromosome Pairing

Cited by 41 publications

References 146 publications

Control of Meiotic Crossovers: From Double-Strand Break Formation to Designation

Control of Meiotic Crossovers: From Double-Strand Break Formation to Designation

Centromere Satellite Repeats Have Undergone Rapid Changes in Polyploid Wheat Subgenomes

The telomere bouquet facilitates meiotic prophase progression and exit in fission yeast

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