The Germline-Restricted Chromosome of Male Zebra Finches in Meiotic Prophase I: A Proteinaceous Scaffold and Chromatin Modifications.

Simple Summary: In most animals, the genome does not undergo radical changes during ontogenesis. However, in some species, a programmed loss of a portion of the genome has been identified, such as the elimination of entire chromosomes during meiosis in passerine birds; this chromosome is termed the germline-restricted chromosome (GRC). The discovery of the GRC in 1998 in the zebra finch opened new avenues for understanding the phenomenon of DNA elimination. It is now known that the GRC is predominantly maternally inherited, as this chromosome is lost in males at the end of meiosis. In spermatocytes, the GRC univalent forms a distinct chromatin domain at the nuclear periphery. In the present study, immunocytochemistry showed that the components of the proteinaceous scaffold of the prophase I GRC and other chromosomes most likely load asynchronously. This is possibly due to unique aspects of chromatin conformation and transcriptional silencing in the GRC domain, where repressive chromatin marks are present, while transcriptional markers are absent. Nonetheless, some studies indicate gene expression in the GRC of several species. In this study, the molecular machinery of meiotic repair and recombination was found to be functional, as RPA and RAD51 proteins (involved in double-strand break processing) were detected at certain GRC sites. Notably, some RPA foci in the GRC univalent showed telomeric localization. It is in these chromosomal regions that female GRC homologs recombine. The observed meiotic phenomena associated with the GRC make this chromosome unique and a target for further research. Among eukaryotes, there are many examples of partial genome elimination during ontogenesis. A striking example of this phenomenon is the loss of entire avian chromosomes during meiosis, called a germline-restricted chromosome (GRC). The GRC is absent in somatic tissues but present in germ cells. It has been established that a prophase I male GRC is usually represented by a univalent surrounded by heterochromatin. In the present study, an immunocytochemical analysis of zebra finch spermatocytes was performed to focus on some details of this chromosome's organization. For the first time, it was shown that a prophase I GRC contains the HORMAD1 protein, which participates in the formation of a full axial element. This GRC axial element has signs of a delay of core protein loading, probably owing to peculiarities of meiotic silencing of chromatin. The presence of repressive marks (H3K9me3 and H3K27me3) and the lack of RNA polymerase II, typically associated with active transcription, indicate transcriptional inactivation in the GRC body, despite the known activity of some genes of the GRC. Nevertheless, RPA and RAD51 proteins were found at some GRC sites, indicating the formation and repair of double-strand breaks on this chromosome. Our results provide new insights into the meiotic behavior and structure of a GRC. [ABSTRACT FROM AUTHOR]

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