Abstract
Heterozygous chromosomal rearrangements can result in failures during the meiotic cycle and the apoptosis of germline, making carrier individuals infertile. The Amazon frog Leptodactylus pentadactylus has a meiotic multivalent, composed of 12 sex chromosomes. The mechanisms by which this multi-chromosome system maintains fertility in males of this species remain undetermined. In this study we investigated the meiotic behavior of this multivalent to understand how synapse, recombination and epigenetic modifications contribute to maintaining fertility and chromosomal sexual determination in this species. Our sample had 2n = 22, with a ring formed by ten chromosomes in meiosis, indicating a new system of sex determination for this species (X1Y1X2Y2X3Y3X4Y4X5Y5). Synapsis occurs in the homologous terminal portion of the chromosomes, while part of the heterologous interstitial regions performed synaptic adjustment. The multivalent center remains asynaptic until the end of pachytene, with interlocks, gaps and rich-chromatin in histone H2A phosphorylation at serine 139 (γH2AX), suggesting transcriptional silence. In late pachytene, paired regions show repair of double strand-breaks (DSBs) with RAD51 homolog 1 (Rad51). These findings suggest that Rad51 persistence creates positive feedback at the pachytene checkpoint, allowing meiosis I to progress normally. Additionally, histone H3 trimethylation at lysine 27 in the pericentromeric heterochromatin of this anuran can suppress recombination in this region, preventing failed chromosomal segregation. Taken together, these results indicate that these meiotic adaptations are required for maintenance of fertility in L. pentadactylus.
Highlights
During the evolution of vertebrates, the XY and ZW chromosomes developed independently through translocations and fusion/fission rearrangements, generating multiple sex c hromosomes[1,2,3]
The present study investigated the meiotic behavior of this multivalent system in males of L. pentadactylus by immunocytogenetic analysis to determine the mechanisms by which synapse, recombination and epigenetic modifications contribute to the maintenance of fertility and the determination of sex chromosomes in this species
The meiotic behavior of L. pentadactylus chromosomes was investigated by immunodetection of structural maintenance of chromosomes protein 3 (SMC3) that marks the axis of cohesins associated with the complex synaptonemal
Summary
During the evolution of vertebrates, the XY and ZW chromosomes developed independently through translocations and fusion/fission rearrangements, generating multiple sex c hromosomes[1,2,3]. Other factors, including the kinase ataxia telangiectasia and Rad[3] related (ATR), are recruited and promote formation of γH2AX, which silences autosomal and sex chromosome associated sequences[22,23] Others epigenetic modifications, such as H3K27me[3] and histone H3 tri-methylation at lysine 9 (H3K9me3) are observed during early phases prophase I and contribute to MSUC24. Heterozygous chromosomal rearrangements, as observed in this anuran species, can promote serious damage to the meiotic process, including synapsis, recombination, chromatin remodeling and chromosomal segregation[19] These failures may be recognized by the pachytene checkpoint during prophase I, activating chain apoptosis in germ lines and reducing the fertility of carriers of individual rearrangements[35]. The present study investigated the meiotic behavior of this multivalent system in males of L. pentadactylus by immunocytogenetic analysis to determine the mechanisms by which synapse, recombination and epigenetic modifications contribute to the maintenance of fertility and the determination of sex chromosomes in this species
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