A synaptonemal complex-derived mechanism for meiotic segregation precedes the evolutionary loss of homology between sex chromosomes in arvicolid mammals

Fuente, Roberto de la; Sánchez, Antonio; Marchal, Juan A.; Viera, Alberto; Parra, María Teresa; Rufas, Julio S.; Page, Jesús

doi:10.1007/s00412-012-0374-9

Cited by 21 publications

(27 citation statements)

References 54 publications

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“…The H3K79me3 enrichment at the XY pair takes place during the diplotene/diakinesis transition when the staining for γH2AX and the repressive macroH2A variant becomes weaker. Nevertheless, it is possible that, although undetectable with our spreading technique, at least a fraction of these histone variants remains associated with the sex chromosomes until later meiotic stages, as occurs in other mammalian species (De la Fuente et al 2007; Namekawa et al 2007; De la Fuente et al 2012). Conversely, H2A.Z, which is initially excluded from the sex body, arrives at this location at the same time as H3K79me3 accumulates.…”

Section: Discussionmentioning

confidence: 92%

Dynamics of DOT1L localization and H3K79 methylation during meiotic prophase I in mouse spermatocytes

et al. 2013

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During meiotic prophase I, interactions between maternal and paternal chromosomes, under checkpoint surveillance, establish connections between homologs that promote their accurate distribution to meiotic progeny. In human, faulty meiosis causes aneuploidy resulting in miscarriages and genetic diseases. Meiotic processes occur in the context of chromatin, therefore histone post-translational modifications are expected to play important roles. Here, we report the cytological distribution of the evolutionarily conserved DOT1L methyltransferase and the different H3K79 methylation states resulting from its activity (mono-, di- and tri-methylation; H3K79me1, me2 and me3, respectively) during meiotic prophase I in mouse spermatocytes. In the wild type, whereas low amounts of H3K79me1 are rather uniformly present throughout prophase I, levels of DOT1L, H3K79me2 and H3K79me3 exhibit a notable increase from pachynema onwards, but with differential subnuclear distribution patterns. The heterochromatic centromeric regions and the sex body are enriched for H3K79me3. In contrast, H3K79me2 is present all over the chromatin, but is largely excluded from the sex body despite the accumulation of DOT1L. In meiosis-defective mouse mutants, the increase of DOT1L and H3K79me is blocked at the same stage where meiosis is arrested. H3K79me patterns, combined with the cytological analysis of the H3.3, γH2AX, macroH2A and H2A.Z histone variants, are consistent with a differential role for these epigenetic marks in male mouse meiotic prophase I. We propose that H3K79me2 is related to transcriptional reactivation on autosomes during pachynema, whereas H3K79me3 may contribute to the maintenance of repressive chromatin at centromeric regions and the sex body.

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Section: Discussionmentioning

confidence: 92%

Dynamics of DOT1L localization and H3K79 methylation during meiotic prophase I in mouse spermatocytes

et al. 2013

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“…Noncanonical mechanisms of sex chromosome segregation have been previously described in marsupials (Solari and Bianchi 1975; Page et al 2005, 2006a) and several nonmurid rodent species (de la Fuente et al 2007, 2012). These exceptional species possess sex chromosomes that are fully nonhomologous—with no PAR—yet sex chromosomes segregate reductionally at the first meiotic division.…”

Section: Discussionmentioning

confidence: 98%

Meiotic Consequences of Genetic Divergence Across the Murine Pseudoautosomal Region

Dumont

2017

Genetics

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The production of haploid gametes during meiosis is dependent on the homology-driven processes of pairing, synapsis, and recombination. On the mammalian heterogametic sex chromosomes, these key meiotic activities are confined to the pseudoautosomal region (PAR), a short region of near-perfect sequence homology between the X and Y chromosomes. Despite its established importance for meiosis, the PAR is rapidly evolving, raising the question of how proper X/Y segregation is buffered against the accumulation of homology-disrupting mutations. Here, I investigate the interplay of PAR evolution and function in two interfertile house mouse subspecies characterized by structurally divergent PARs, Mus musculus domesticus and M. m. castaneus. Using cytogenetic methods to visualize the sex chromosomes at meiosis, I show that intersubspecific F1 hybrids harbor an increased frequency of pachytene spermatocytes with unsynapsed sex chromosomes. This high rate of asynapsis is due, in part, to the premature release of synaptic associations prior to completion of prophase I. Further, I show that when sex chromosomes do synapse in intersubspecific hybrids, recombination is reduced across the paired region. Together, these meiotic defects afflict ∼50% of spermatocytes from F1 hybrids and lead to increased apoptosis in meiotically dividing cells. Despite flagrant disruption of the meiotic program, a subset of spermatocytes complete meiosis and intersubspecific F1 males remain fertile. These findings cast light on the meiotic constraints that shape sex chromosome evolution and offer initial clues to resolve the paradox raised by the rapid evolution of this functionally significant locus.

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“…The presence of the PAR has also been acknowledged in all domestic animals and a few wild mammals [Van Laere et al, 2008;Raudsepp et al, 2012;Das et al, 2013] and is thought to be a common feature of eutherian sex chromosomes. The presently known exceptions are some species of arvicoline and gerbilline rodents, such as the Mediterranean pine vole and Mongolian gerbil that, like in marsupials, have asynaptic and achiasmatic sex chromosomes with no PAR [de la Fuente et al, 2012].…”

Section: The Eutherian Parmentioning

confidence: 99%

The Eutherian Pseudoautosomal Region

Raudsepp

Chowdhary²

2015

Cytogenet Genome Res

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The pseudoautosomal region (PAR) is a unique segment of sequence homology between differentiated sex chromosomes where recombination occurs during meiosis. Molecular and functional properties of the PAR are distinctive from the autosomes and the remaining regions of the sex chromosomes. These include a higher rate of recombination than genome average, bias towards GC-substitutions and increased interindividual nucleotide divergence and mutations. As yet, the PAR has been physically demarcated in only 28 eutherian species representing 6 mammalian orders. Murid rodents have the smallest, gene-poorest and most diverged PARs. Other eutherian PARs are largely homologous but differ in size and gene content, being the smallest in equids and human/simian primates and much larger in other eutherians. Because pseudoautosomal genes escape X inactivation, their dosage changes with sex chromosome aneuploidies, whereas phenotypic effects of the latter depend on the size and gene content of the PAR. Thus, X monosomy is more viable in mice, humans and horses than in species with larger PARs. Presently, little is known about the functions of PAR genes in individual species, though human studies suggest their involvement in early embryonic development. The PAR is, thus, of evolutionary, genetic and biomedical significance and a ‘research hotspot' in eutherian genomes.

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A synaptonemal complex-derived mechanism for meiotic segregation precedes the evolutionary loss of homology between sex chromosomes in arvicolid mammals

Cited by 21 publications

References 54 publications

Dynamics of DOT1L localization and H3K79 methylation during meiotic prophase I in mouse spermatocytes

Dynamics of DOT1L localization and H3K79 methylation during meiotic prophase I in mouse spermatocytes

Meiotic Consequences of Genetic Divergence Across the Murine Pseudoautosomal Region

The Eutherian Pseudoautosomal Region

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