scholarly journals Effects of the Sex Chromosome Complement, XX, XO, or XY, on the Transcriptome and Development of Mouse Oocytes During Follicular Growth

2021 ◽  
Vol 12 ◽  
Author(s):  
Wataru Yamazaki ◽  
Dunarel Badescu ◽  
Seang Lin Tan ◽  
Jiannis Ragoussis ◽  
Teruko Taketo

The sex chromosome complement, XX or XY, determines sexual differentiation of the gonadal primordium into a testis or an ovary, which in turn directs differentiation of the germ cells into sperm and oocytes, respectively, in eutherian mammals. When the X monosomy or XY sex reversal occurs, XO and XY females exhibit subfertility and infertility in the mouse on the C57BL/6J genetic background, suggesting that functional germ cell differentiation requires the proper sex chromosome complement. Using these mouse models, we asked how the sex chromosome complement affects gene transcription in the oocytes during follicular growth. An oocyte accumulates cytoplasmic components such as mRNAs and proteins during follicular growth to support subsequent meiotic progression, fertilization, and early embryonic development without de novo transcription. However, how gene transcription is regulated during oocyte growth is not well understood. Our results revealed that XY oocytes became abnormal in chromatin configuration, mitochondria distribution, and de novo transcription compared to XX or XO oocytes near the end of growth phase. Therefore, we compared transcriptomes by RNA-sequencing among the XX, XO, and XY oocytes of 50–60 µm in diameter, which were still morphologically comparable. The results showed that the X chromosome dosage limited the X-linked and autosomal gene transcript levels in XO oocytes whereas many genes were transcribed from the Y chromosome and made the transcriptome in XY oocytes closer to that in XX oocytes. We then compared the transcript levels of 3 X-linked, 3 Y-linked and 2 autosomal genes in the XX, XO, and XY oocytes during the entire growth phase as well as at the end of growth phase using quantitative RT-PCR. The results indicated that the transcript levels of most genes increased with oocyte growth while largely maintaining the X chromosome dosage dependence. Near the end of growth phase, however, transcript levels of some X-linked genes did not increase in XY oocytes as much as XX or XO oocytes, rendering their levels much lower than those in XX oocytes. Thus, XY oocytes established a distinct transcriptome at the end of growth phase, which may be associated with abnormal chromatin configuration and mitochondria distribution.

2021 ◽  
Vol 36 (Supplement_1) ◽  
Author(s):  
W Yamazaki ◽  
D Badescu ◽  
S L Tan ◽  
J Ragoussis ◽  
T Taketo

Abstract Study question How does the sex chromosome complement affect the transcriptome and development of oocytes during follicular growth in the mouse ovary? Summary answer Highly expressed X-linked genes adjust their transcript levels according to the X dosage. Y-linked genes affect the transcript levels of some X-linked and autosomal genes. What is known already Female mice carrying XO and XY chromosomes on the C57BL/6J (B6) genetic background are healthy but encounter subfertility and infertility, respectively. Our previous results have shown that the XY oocyte is defective in its cytoplasm; its replacement with that of an XX oocyte at the GV stage allows for production of healthy offspring after fertilization. Since transcription is shut down in the oocyte by the end of growth phase, the mRNAs and proteins necessary for meiotic progression and early embryonic development are accumulated during follicular growth. Study design, size, duration 30 oocytes of 50–59 μm diameter were pooled for each genotype in biological triplicate and subjected to RNA-Sequencing. Total RNA extracted from 10–30 pooled oocytes of each size range and genotype in biological triplicate were subjected to qRT-PCR. All experiments were performed between 2019–2021. Participants/materials, setting, methods XY and XO females were generated by cross between B6 females with B6.YTIR and B6.XPafY males, respectively. Oocytes in the growth phase were collected at 8–18 days postpartum (dpp), whereas fully-grown oocytes were collected at 27–29 dpp after injection with equine chorionic gonadotropin. Oocytes of 50–59 μm diameter were subjected to RNA-Sequencing using a version of SmartSeq2, followed by DEG analyses. Transcript levels in the oocytes of various diameters were determined by qRT-PCR. Main results and the role of chance Chromatin configuration, mitochondrial distribution, and de novo transcription were largely comparable among the XX, XO, and XY oocytes smaller than 60 µm. Three way comparisons of RNA-Seq data in the oocytes of 50–59 μm revealed; (1) 13.8% of X-linked DEGs showed the transcript levels in correspond to the X chromosome dosage; (2) 9 genes on the Y short arm and 2 genes near the distal end of the Y long arm were highly expressed in XY oocytes; (3) transcript levels of X- or autosomal homologs were affected by the XY complement compared to XX and XO oocytes; and (4) 54 and 39 X-linked and autosomal genes show higher and lower transcript levels, respectively, in XY oocytes compared to XX and XO oocytes. The results of qRT-PCR of selected genes revealed distinct dynamic changes in transcript levels in the oocyte during follicular growth. Data of RNA-Seq were statistically analyzed using R Bioconductor limma package for differentially expressed genes having Benjamini-Hochberg adjusted P values lower than 0.01 and log2 fold change higher than 1. All data of qRT-PCR were statistically analyzed by one-way ANOVA followed by Tukey’s honestly significant difference (HSD) test. Limitations, reasons for caution In humans, most XO females die in utero and those who reach the term suffer from congenital abnormalities and infertility (Turner’s syndrome). However, the severer phenotype can be attributed to somatic cells with a greater number of genes that escape from X chromosome inactivation in humans than mice. Wider implications of the findings: XO and XY mice provide animal models for investigating the consequence of X haplodeficiency in the female germline, independent of somatic defects. Furthermore, XY female mice provide a unique opportunity for examining whether and how Y-linked genes are transcribed outside the male germline. Trial registration number Not applicable


Changing DNA methylation patterns during embryonic development are discussed in relation to differential gene expression, changes in X-chromosome activity and genomic imprinting. Sperm DNA is more methylated than oocyte DNA, both overall and for specific sequences. The methylation difference between the gametes could be one of the mechanisms (along with chromatin structure) regulating initial differences in expression of parental alleles in early development. There is a loss of methylation during development from the morula to the blastocyst and a marked decrease in methylase activity. De novo methylation becomes apparent around the time of implantation and occurs to a lesser extent in extra-embryonic tissue DNA. In embryonic DNA, de novo methylation begins at the time of random X-chromosome inactivation but it continues to occur after X-chromosome inactivation and may be a mechanism that irreversibly fixes specific patterns of gene expression and X-chromosome inactivity in the female. The germ line is probably delineated before extensive de novo methylation and hence escapes this process. The marked undermethylation of the germ line DNA may be a prerequisite for X-chromosome reactivation. The process underlying reactivation and removal of parent-specific patterns of gene expression may be changes in chromatin configuration associated with meiosis and a general reprogramming of the germ line to developmental totipotency.


2021 ◽  
Author(s):  
Monica M Sheffer ◽  
Mathilde M Cordellier ◽  
Martin Forman ◽  
Malte Grewoldt ◽  
Katharina Hoffmann ◽  
...  

Differences between sexes in growth, ecology and behavior strongly shape species biology. In some animal groups, such as spiders, it is difficult or impossible to identify the sex of juveniles. This information would be useful for field surveys, behavioral experiments, and ecological studies on e.g. sex ratios and dispersal. In species with sex chromosomes, sex can be determined based on the specific sex chromosome complement. Additionally, information on the sequence of sex chromosomes provides the basis for studying sex chromosome evolution. We combined cytogenetic and genomic data to identify the sex chromosomes in the sexually dimorphic spider Argiope bruennichi, and designed RT-qPCR sex markers. We found that genome size and GC content of this spider falls into the range reported for the majority of araneids. The male karyotype is formed by 24 acrocentric chromosomes with an X1X20 sex chromosome system, with little similarity between X chromosomes, suggesting origin of these chromosomes by X chromosome fission or early duplication of an X chromosome and subsequent independent differentiation of the copies. Our data suggest similarly sized X chromosomes in A. bruennichi. They are smaller chromosomes of the complement. Our findings open the door to new directions in spider evolutionary and ecological research.


2018 ◽  
Vol 2018 ◽  
pp. 1-3 ◽  
Author(s):  
Hanane Latrech ◽  
Houssein Madar ◽  
Ahmed Gaouzi

Turner syndrome is a common sex chromosome disorder characterized by complete or partial absence of an X chromosome. The spectrum of its clinical features and cytogenetics are various. We report new chromosomal formula revealed by DSD and associated with translocation (13,14). To our knowledge, this is the first case of 45X, t(13;14) de novo translocation as a variation of Turner syndrome in a patient with this clinical presentation.


Cells ◽  
2020 ◽  
Vol 9 (6) ◽  
pp. 1436
Author(s):  
Qinwei Kim-Wee Zhuang ◽  
Jose Hector Galvez ◽  
Qian Xiao ◽  
Najla AlOgayil ◽  
Jeffrey Hyacinthe ◽  
...  

Sex biases in the genome-wide distribution of DNA methylation and gene expression levels are some of the manifestations of sexual dimorphism in mammals. To advance our understanding of the mechanisms that contribute to sex biases in DNA methylation and gene expression, we conducted whole genome bisulfite sequencing (WGBS) as well as RNA-seq on liver samples from mice with different combinations of sex phenotype and sex-chromosome complement. We compared groups of animals with different sex phenotypes, but the same genetic sexes, and vice versa, same sex phenotypes, but different sex-chromosome complements. We also compared sex-biased DNA methylation in mouse and human livers. Our data show that sex phenotype, X-chromosome dosage, and the presence of Y chromosome shape the differences in DNA methylation between males and females. We also demonstrate that sex bias in autosomal methylation is associated with sex bias in gene expression, whereas X-chromosome dosage-dependent methylation differences are not, as expected for a dosage-compensation mechanism. Furthermore, we find partial conservation between the repertoires of mouse and human genes that are associated with sex-biased methylation, an indication that gene function is likely to be an important factor in this phenomenon.


2021 ◽  
Author(s):  
Antonio Marco

Genes are often differentially expressed between males and females. In Drosophila melanogaster, the analysis of sex-biased microRNAs (short non-coding regulatory molecules) has revealed striking differences with protein-coding genes. Mainly, the X chromosome is enriched in male-biased microRNA genes, although it is depleted of male-biased protein-coding genes. The paucity of male-biased genes in the X chromosome is generally explained by an evolutionary process called demasculinization. I suggest that the excess of male-biased microRNAs in the X chromosome is due to high-rates of de novo emergence of microRNAs, a tendency of novel microRNAs in the X chromosome to be expressed in testis, and to a lack of a demasculinization process. To test this hypothesis I analysed the expression profile of microRNAs in males, females and gonads in D. pseudoobscura, in which an autosome translocated into the X chromosome effectively becoming part of a sex chromosome (neo-X). I found that the pattern of sex- biased expression is generally conserved between D. melanogaster and D. pseudoobscura. Also, orthologous microRNAs in both species conserve their chromosomal location, indicating that there is no evidence of demasculinization or other inter-chromosomal movement of microRNAs. D. pseudoobscura-specific microRNAs in the neo-X chromosome tend to be male-biased and particularly expressed in testis. In summary, the apparent paradox resulting from male-biased protein-coding genes depleted in the X chromosome and an enrichment in male-biased microRNAs is a consequence of different evolutionary dynamics between coding genes and short RNAs.


1984 ◽  
Vol 37 (2) ◽  
pp. 53 ◽  
Author(s):  
RL Close

An X chromosome disappears from female cells and the Y chromosome from male cells of some somatic tissues of all peramelid bandicoots, leaving cells with a 2n = 13 (i.e. XO) chromosome complement. The patterns of loss, which differ among tissues and species, were studied during development of specimens of P. nasuta and /. macrourus.


1982 ◽  
Vol 30 (5) ◽  
pp. 799 ◽  
Author(s):  
DL Hayman ◽  
P.J. Sharp

Tarsipes spencerae Gray (Marsupialia) has a chromosome complement of 2n = 24 (XX, XY). The chromosomes possess two unusual features. They have both autosomal and sex chromosome sites which are responsive to silver staining (nucleolar organizers), a feature previously found only in the Phalangeroidea, and all autosomes and the X chromosome show pronounced Hoechst 33258 sensitivity, a feature previously found only in the Macropodidae.


2021 ◽  
Author(s):  
Emily Christine Moore ◽  
Gregg W C Thomas ◽  
Sebastian Mortimer ◽  
Emily Emiko Konishi Kopania ◽  
Kelsie E Hunnicutt ◽  
...  

The mammalian X chromosome shows strong conservation among distantly related species, limiting insights into the distinct selective processes that have shaped sex chromosome evolution. We constructed a chromosome-scale de novo genome assembly for the Siberian dwarf hamster (Phodopus sungorus), a species reported to show extensive recombination suppression across an entire arm of the X chromosome. Combining a physical genome assembly based on shotgun and long-range proximity ligation sequencing with a dense genetic map, we detected widespread suppression of female recombination across ~65% of the Phodopus X chromosome. This region of suppressed recombination likely corresponds to the Xp arm, which has previously been shown to be highly heterochromatic. Using additional sequencing data from two closely-related species (P. campbelli and P. roborovskii), we show that recombination suppression on Xp appears to be independent of major structural rearrangements. The suppressed Xp arm was enriched for genes primarily expressed in the placenta and some transposable elements, but otherwise showed similar gene densities, expression patterns, and rates of molecular evolution when compared to the recombinant Xq arm. Phodopus Xp gene content and order was also broadly conserved relative to the more distantly related rat X chromosome. Collectively, these data suggest that widespread suppression of recombination has likely evolved through the transient induction of facultative heterochromatin on the Phodopus Xp arm without major changes in chromosome structure or genetic content. Thus, dramatic changes in the recombination landscape have so far had relatively subtle influences on overall patterns of X-linked molecular evolution.


2021 ◽  
Vol 12 (1) ◽  
Author(s):  
Yisrael Rappaport ◽  
Hanna Achache ◽  
Roni Falk ◽  
Omer Murik ◽  
Oren Ram ◽  
...  

AbstractDuring meiosis, gene expression is silenced in aberrantly unsynapsed chromatin and in heterogametic sex chromosomes. Initiation of sex chromosome silencing is disrupted in meiocytes with sex chromosome-autosome translocations. To determine whether this is due to aberrant synapsis or loss of continuity of sex chromosomes, we engineered Caenorhabditis elegans nematodes with non-translocated, bisected X chromosomes. In early meiocytes of mutant males and hermaphrodites, X segments are enriched with euchromatin assembly markers and active RNA polymerase II staining, indicating active transcription. Analysis of RNA-seq data showed that genes from the X chromosome are upregulated in gonads of mutant worms. Contrary to previous models, which predicted that any unsynapsed chromatin is silenced during meiosis, our data indicate that unsynapsed X segments are transcribed. Therefore, our results suggest that sex chromosome chromatin has a unique character that facilitates its meiotic expression when its continuity is lost, regardless of whether or not it is synapsed.


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