Demasculinization of X chromosomes in the Drosophila genus

Laboratory of Cellular and Developmental Biology, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Department of Health and Human Services, Bethesda Maryland 20892, USA.
Nature (Impact Factor: 41.46). 12/2007; 450(7167):238-41. DOI: 10.1038/nature06330
Source: PubMed


X chromosomes evolve differently from autosomes, but general governing principles have not emerged. For example, genes with male-biased expression are under-represented on the X chromosome of D. melanogaster, but are randomly distributed in the genome of Anopheles gambiae. In direct global profiling experiments using species-specific microarrays, we find a nearly identical paucity of genes with male-biased expression on D. melanogaster, D. simulans, D. yakuba, D. ananassae, D. virilis and D. mojavensis X chromosomes. We observe the same under-representation on the neo-X of D. pseudoobscura. It has been suggested that precocious meiotic silencing of the X chromosome accounts for reduced X chromosome male-biased expression in nematodes, mammals and Drosophila. We show that X chromosome genes with male-biased expression are under-represented in somatic cells and in mitotic male germ cells. These data are incompatible with simple X chromosome inactivation models. Using expression profiling and comparative sequence analysis, we show that selective gene extinction on the X chromosome, creation of new genes on autosomes and changed genomic location of existing genes contribute to the unusual X chromosome gene content.

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    • "Despite all the debate about meiotic sex chromosome inactivation (MSCI) in Drosophila, a lot of discussion regarding the status of X chromosome dosage compensation (DC) in the D. melanogaster male germline has recently intensified in the literature 31, 37, 49. However, only a few studies have tried to assess and disentangle the contribution of both mechanisms to the evolution of gene expression in the germline 31, 37. "
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    ABSTRACT: In several different taxa, there is indubitable evidence of transcriptional silencing of the X and Y chromosomes in male meiotic cells of spermatogenesis. However, the so called meiotic sex chromosome inactivation (MSCI) has been recently a hot bed for debate in Drosophila melanogaster. This review covers cytological and genetic observations, data from transgenic constructs with testis-specific promoters, global expression profiles obtained from mutant, wild-type, larvae and adult testes as well as from cells of different stages of spermatogenesis. There is no dispute on that D. melanogaster spermatogenesis presents a down-regulation of X chromosome that does not result from the lack of dosage compensation. However, the issue is currently focused on the level of reduction of X-linked expression, the precise time it occurs and how many genes are affected. The deep examination of data and experiments in this review exposes the limitations intrinsic to the methods of studying MSCI in D. melanogaster. The current methods do not allow us to affirm anything else than the X chromosome down-regulation in meiosis (MSCI). Therefore, conclusion about level, degree or precise timing is inadequate until new approaches are implemented to know the details of MSCI or other processes involved for D. melanogaster model.
    Preview · Article · Jun 2014
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    • "This result suggests that X upregulation is restricted to dosage-sensitive genes. Much of the comparative work regarding evolution of sex-biased gene expression and the X chromosome has been performed in Drosophila and mammals (Wang et al. 2001; Lercher et al. 2003; Parisi et al. 2003; Khil et al. 2004; Parisi et al. 2004; Yang et al. 2006; Sturgill et al. 2007; Vicoso and Charlesworth 2009; Ellegren 2011; Meisel et al. 2012a; Allen et al. 2013; Parsch and Ellegren 2013). Here, to expand our understanding of X evolution, we compared X-linked gene expression in five nematode species that include both gonochoristic (outcrossing) and hermaphroditic mating systems (Figure 1A). "
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    ABSTRACT: Studies of X chromosome evolution in various organisms have indicated that sex-biased genes are non-randomly distributed between the X and autosomes. Here, to extend these studies to nematodes, we annotated and analyzed X chromosome gene content in four Caenorhabditis species and in Pristionchus pacificus. Our gene expression analyses comparing young adult male and female mRNA-seq data indicate that, in general, nematode X chromosomes are enriched for genes with high female-biased expression and depleted of genes with high male-biased expression. Genes with low sex-biased expression do not show the same trend of X chromosome enrichment and depletion. Combined with the observation that highly sex-biased genes are primarily expressed in the gonad, differential distribution of sex-biased genes reflects differences in evolutionary pressures linked to tissue-specific regulation of X chromosome transcription. Our data also indicate that X dosage imbalance between males (XO) and females (XX) is influential in shaping both expression and gene content of the X chromosome. Predicted upregulation of the single male X to match autosomal transcription (Ohno's hypothesis) is supported by our observation that overall transcript levels from the X and autosomes are similar for highly expressed genes. However, comparison of differentially located one-to-one orthologs between C. elegans and P. pacificus indicates lower expression of X-linked orthologs, arguing against X upregulation. These contradicting observations may be reconciled if X-upregulation is not a global mechanism but instead acts locally on a subset of tissues and X-linked genes that are dosage sensitive.
    Preview · Article · May 2014 · Genetics
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    • "Evolved sex chromosomes have a highly diverged gene content [1,5,27]. Ancient Y chromosomes have usually lost most of their ancestral genes, and the few remaining genes often have testis-specific functions [1,5]. "
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    ABSTRACT: The Drosophila miranda neo-sex chromosome system is a useful resource for studying recently evolved sex chromosomes. However, the neo-Y genomic assembly is fragmented due to the accumulation of repetitive sequence. Furthermore, the separate assembly of the neo-X and neo-Y chromosomes into genomic scaffolds has proven to be difficult, due to their low level of sequence divergence, which in coding regions is about 1.5%. Here, we de novo assemble the transcriptome of D. miranda using RNA-seq data from several male and female tissues, and develop a bioinformatic pipeline to separately reconstruct neo-X and neo-Y transcripts. We obtain 2,141 transcripts from the neo-X and 1,863 from the neo-Y. Neo-Y transcripts are generally shorter than their homologous neo-X transcripts (N50 of 2,048-bp vs. 2,775-bp) and expressed at lower levels. We find that 24% of expressed neo-Y transcripts harbor nonsense mutation within their open reading frames, yet most non-functional neo-Y genes are expressed throughout all of their length. We find evidence of gene loss of male-specific genes on the neo-X chromosome, and transcriptional silencing of testis-specific genes from the neo-X. Nonsense mediated decay (NMD) has been implicated to degrade transcripts containing pre-mature termination codons (PTC) in Drosophila, but rampant description of neo-Y genes with pre-mature stop codons suggests that it does not play a major role in down-regulating transcripts from the neo-Y. Loss or transcriptional down-regulation of genes from the neo-X with male-biased function provides evidence for beginning demasculinization of the neo-X. Thus, evolving sex chromosomes can rapidly shift their gene content or patterns of gene expression in response to their sex-biased transmission, supporting the idea that sex-specific or sexually antagonistic selection plays a major role in the evolution of heteromorphic sex chromosomes.
    Full-text · Article · Mar 2014 · BMC Genomics
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