Functional significance of the sex chromosomes during spermatogenesis

Hu, Yueh Chiang; Namekawa, Satoshi H.

doi:10.1530/rep-14-0613

Cited by 17 publications

(9 citation statements)

References 129 publications

(193 reference statements)

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“…Several studies have concluded that the X chromosome is still under the influence of MSCI after meiosis since they observed that only a small number of genes are expressed from the X chromosome in post-meiotic cells [25, 50, 51]. These studies were based on microarray analyses and either ignored multicopy genes or considered all genes of the same family (all copies of the same gene) as one gene.…”

Section: Discussionmentioning

confidence: 99%

Expression and epigenomic landscape of the sex chromosomes in mouse post-meiotic male germ cells

Moretti

Vaiman

Torès

et al. 2016

Epigenetics & Chromatin

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Background During meiosis, the X and Y chromosomes are transcriptionally silenced. The persistence of repressive chromatin marks on the sex chromatin after meiosis initially led to the assumption that XY gene silencing persists to some extent in spermatids. Considering the many reports of XY-linked genes expressed and needed in the post-meiotic phase of mouse spermatogenesis, it is still unclear whether or not the mouse sex chromatin is a repressive or permissive environment, after meiosis.Results To determine the transcriptional and chromatin state of the sex chromosomes after meiosis, we re-analyzed ten ChIP-Seq datasets performed on mouse round spermatids and four RNA-seq datasets from male germ cells purified at different stages of spermatogenesis. For this, we used the last version of the genome (mm10/GRCm38) and included reads that map to several genomic locations in order to properly interpret the high proportion of sex chromosome-encoded multicopy genes. Our study shows that coverage of active epigenetic marks H3K4me3 and Kcr is similar on the sex chromosomes and on autosomes. The post-meiotic sex chromatin nevertheless differs from autosomal chromatin in its enrichment in H3K9me3 and its depletion in H3K27me3 and H4 acetylation. We also identified a posttranslational modification, H3K27ac, which specifically accumulates on the Y chromosome. In parallel, we found that the X and Y chromosomes are enriched in genes expressed post-meiotically and display a higher proportion of spermatid-specific genes compared to autosomes. Finally, we observed that portions of chromosome 14 and of the sex chromosomes share specific features, such as enrichment in H3K9me3 and the presence of multicopy genes that are specifically expressed in round spermatids, suggesting that parts of chromosome 14 are under the same evolutionary constraints than the sex chromosomes.ConclusionsBased on our expression and epigenomic studies, we conclude that, after meiosis, the mouse sex chromosomes are no longer silenced but are nevertheless regulated differently than autosomes and accumulate different chromatin marks. We propose that post-meiotic selective constraints are at the basis of the enrichment of spermatid-specific genes and of the peculiar chromatin composition of the sex chromosomes and of parts of chromosome 14.Electronic supplementary materialThe online version of this article (doi:10.1186/s13072-016-0099-8) contains supplementary material, which is available to authorized users.

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Section: Discussionmentioning

confidence: 99%

Expression and epigenomic landscape of the sex chromosomes in mouse post-meiotic male germ cells

Moretti

Vaiman

Torès

et al. 2016

Epigenetics & Chromatin

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“…Nevertheless, this finding was also proven to be imprecise by other contemporaries (Curtsinger et al, 1983;Martin et al, 1995a,b). Apart from the debate, it has been reported that an active gene transcription occurs selectively in the chromosomes (including sex chromosomes) of haploid round spermatids (Hu and Namekawa, 2015). Therefore, if the composition of sex chromosomes has changed due to the post-meiotic modifications in the gene expression and differential survival of spermatozoa during epididymal maturation, these may affect the expected ratio (Bean, 1990).…”

Section: Ratiomentioning

confidence: 99%

New Biological Insights on X and Y Chromosome-Bearing Spermatozoa

Rahman

Pang

2020

Front. Cell Dev. Biol.

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A spermatozoon is a male germ cell capable of fertilizing an oocyte and carries genetic information for determining the sex of the offspring. It comprises autosomes and an X (X spermatozoa) or a Y chromosome (Y spermatozoa). The origin and maturation of both X and Y spermatozoa are the same, however, certain differences may exist. Previous studies proposed a substantial difference between X and Y spermatozoa, however, recent studies suggest negligible or no differences between these spermatozoa with respect to ratio, shape and size, motility and swimming pattern, strength, electric charge, pH, stress response, and aneuploidy. The only difference between X and Y spermatozoa lies in their DNA content. Moreover, recent proteomic and genomic studies have identified a set of proteins and genes that are differentially expressed between X and Y spermatozoa. Therefore, the difference in DNA content might be responsible for the differential expression of certain genes and proteins between these cells. In this review, we have compiled our present knowledge to compare X and Y spermatozoa with respect to their structural, functional, and molecular features. In addition, we have highlighted several areas that could be explored in future studies in this field.

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“…During spermatogenesis, the sex chromosomes are tightly regulated through the generally repressive epigenetic environments of MSCI and PSCR (Turner 2007;Hu and Namekawa 2015). For example, PSCR in mice is partially maintained by the multicopy Y-linked Sly gene (Cocquet et al 2009(Cocquet et al , 2010.…”

Section: Regulatory Evolution and Spermatogenesismentioning

confidence: 99%

Contrasting Levels of Molecular Evolution on the Mouse X Chromosome

et al. 2016

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The mammalian X chromosome has unusual evolutionary dynamics compared to autosomes. Faster-X evolution of spermatogenic protein-coding genes is known to be most pronounced for genes expressed late in spermatogenesis, but it is unclear if these patterns extend to other forms of molecular divergence. We tested for faster-X evolution in mice spanning three different forms of molecular evolution-divergence in protein sequence, gene expression, and DNA methylation-across different developmental stages of spermatogenesis. We used FACS to isolate individual cell populations and then generated cell-specific transcriptome profiles across different stages of spermatogenesis in two subspecies of house mice (Mus musculus), thereby overcoming a fundamental limitation of previous studies on whole tissues. We found faster-X protein evolution at all stages of spermatogenesis and faster-late protein evolution for both X-linked and autosomal genes. In contrast, there was less expression divergence late in spermatogenesis (slower late) on the X chromosome and for autosomal genes expressed primarily in testis (testis-biased). We argue that slower-late expression divergence reflects strong regulatory constraints imposed during this critical stage of sperm development and that these constraints are particularly acute on the tightly regulated sex chromosomes. We also found slower-X DNA methylation divergence based on genome-wide bisulfite sequencing of sperm from two species of mice (M. musculus and M. spretus), although it is unclear whether slower-X DNA methylation reflects development constraints in sperm or other X-linked phenomena. Our study clarifies key differences in patterns of regulatory and protein evolution across spermatogenesis that are likely to have important consequences for mammalian sex chromosome evolution, male fertility, and speciation.KEYWORDS faster X evolution; gene expression; DNA methylation; fluorescence-activated cell sorting; postmeiotic sex chromosome repression (PSCR) T HE X chromosome plays a disproportionately large role in adaptation and speciation (Bachtrog et al. 2011;Ellegren 2011;Charlesworth 2013), but the underlying molecular and evolutionary drivers of these patterns remain unclear. On one hand, the X chromosome often shows strong signatures of evolutionary constraint. For example, the evolution of dosage compensation via epigenetic X-chromosome inactivation (XCI) in females (Lyon 1961(Lyon , 1962 imposes regulatory constraints that select for strong conservation of X-linked gene content in placental mammals (Ohno 1967;Kohn et al. 2004). On the other hand, these inherent constraints are punctuated by strong specialization in X-linked gene content (Emerson et al. 2004;Mueller et al. 2008Mueller et al. , 2013Potrzebowski et al. 2008;Zhang et al. 2010;Sin et al. 2012) and numerous examples of rapid X-linked evolution Singh 2003, 2006;Baines and Harr 2007;Kousathanas et al. 2014;Nam et al. 2015).The X chromosome is predicted to evolve faster than the autosomes if beneficial mutations...

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Functional significance of the sex chromosomes during spermatogenesis

Cited by 17 publications

References 129 publications

Expression and epigenomic landscape of the sex chromosomes in mouse post-meiotic male germ cells

Expression and epigenomic landscape of the sex chromosomes in mouse post-meiotic male germ cells

New Biological Insights on X and Y Chromosome-Bearing Spermatozoa

Contrasting Levels of Molecular Evolution on the Mouse X Chromosome

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