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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Available from: Michael Parisi, Sep 29, 2015
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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.
    06/2014; 2:104-17. DOI:10.7150/jgen.8178
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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.
    BMC Genomics 03/2014; 15(1):241. DOI:10.1186/1471-2164-15-241 · 3.99 Impact Factor
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    • ") Fruit fly ( Meisel et al . , 2012 ) Mouse ( Khil et al . , 2004 ) Mosquito ( Magnusson et al . , 2012 ) Fruit fly ( Parisi et al . , 2003 ; Sturgill et al . , 2007 ; Bachtrog et al . , 2010 ) Z chromosome Chicken ( Wright et al . , 2012 ) Silk worm ( Arunkumar et al . , 2009 )"
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    ABSTRACT: In addition to initial sex determination, genes on the sex chromosomes are theorized to play a particularly important role in phenotypic differences between males and females. Sex chromosomes in many species display molecular signatures consistent with these theoretical predictions, particu-larly through sex-specific gene expression. However, the phenotypic implications of this molecular signature are unresolved, and the role of the sex chromosomes in quantitative genetic studies of phenotypic sex differences is largely equivocal. In this article, we examine molecular and phenotypic data in the light of theoretical predictions about masculinization and feminiza-tion of the sex chromosomes. Additionally, we discuss the role of genetic and regulatory complexities in the genome–phenotype relationship, and ultimately how these affect the overall role of the sex chromosomes in sex differences.
    Journal of Evolutionary Biology 02/2014; 27(7). DOI:10.1111/jeb.12345 · 3.23 Impact Factor
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