XY and ZW: Is Meiotic Sex Chromosome Inactivation the Rule in Evolution?

Howard Hughes Medical Institute, Department of Molecular Biology, Massachusetts General Hospital, Boston, Massachusetts, USA.
PLoS Genetics (Impact Factor: 7.53). 06/2009; 5(5):e1000493. DOI: 10.1371/journal.pgen.1000493
Source: PubMed

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    • "This error-free repair pathway may thus protect X-linked genes from (intron) deletions at transcription-induced DSBs. Although mechanisms of sex-chromosome inactivation have been observed for nematodes, flies, and mammals (Namekawa and Lee, 2009; Meiklejohn et al. 2011), it is currently unknown whether they protect the sex chromosomes from mutations such as deletion of intronic sequences. "
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    ABSTRACT: How introns are lost from eukaryotic genomes during evolution remains an enigmatic question in biology. By comparative genome analysis of five Caenorhabditis and eight Drosophila species, we found that the likelihood of intron loss is highly influenced by the degree of sequence homology at exon–intron junctions: a significant elevated degree of microhomology was observed for sequences immediately flanking those introns that were eliminated from the genome of one or more subspecies. This determinant was significant even at individual nucleotides. We propose that microhomology-mediated DNA repair underlies this phenomenon, which we termed microhomology-mediated intron loss. This hypothesis is further supported by the observations that in both species 1) smaller introns are preferentially lost over longer ones and 2) genes that are highly transcribed in germ cells, and are thus more prone to DNA double strand breaks, display elevated frequencies of intron loss. Our data also testify against a prominent role for reverse transcriptase-mediated intron loss in metazoans.
    Full-text · Article · Jun 2013 · Genome Biology and Evolution
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    • "Two competing models have been proposed to explain the lower overall X-linked gene expression levels in Drosophila testes. The first is that MSCI occurs in Drosophila as it does in mammals and C. elegans (Namekawa and Lee 2009), leading to reduced expression from the X chromosome versus the autosomes in the testes (Vibranovski et al. 2009). Under this hypothesis, the lower X chromosome expression in whole testis is the read-out of a mixed population of cells, including those in which the X is expressed at levels equal to the autosomes (implying X chromosome dosage compensation) and a small subset of cells, presumably early meiotic spermatocytes, in which the X is transcriptionally inactive (Vibranovski et al. 2009). "
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    ABSTRACT: Male-biased genes—those expressed at higher levels in males than in females—are underrepresented on the X chromosome of Drosophila melanogaster. Several evolutionary models have been posited to explain this so-called demasculinization of the X. Here, we show that the apparent paucity of male-biased genes on the X chromosome is attributable to global X-autosome differences in expression in Drosophila testes, owing to a lack of sex chromosome dosage compensation in the male germline, but not to any difference in the density of testis-specific or testis-biased genes on the X chromosome. First, using genome-wide gene expression data from 20 tissues, we find no evidence that genes with testis-specific expression are underrepresented on the X chromosome. Second, using contrasts in gene expression profiles among pairs of tissues, we recover a statistical underrepresentation of testis-biased genes on the X but find that the pattern largely disappears once we account for the lack of dosage compensation in the Drosophila male germline. Third, we find that computationally “demasculinizing” the autosomes is not sufficient to produce an expression profile similar to that of the X chromosome in the testes. Our findings thus show that the lack of sex chromosome dosage compensation in Drosophila testes can explain the apparent signal of demasculinization on the X, whereas evolutionary demasculinization of the X cannot explain its overall reduced expression in the testes.
    Full-text · Article · Sep 2012 · Genome Biology and Evolution
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    • "Similar complementary expression for retrogenes and parental genes has been also shown to occur in Drosophila mitotic and meiotic phases of the male germline (Vibranovski et al. 2009a) in agreement with the MSCI model. In birds, the MSCI observed in the synapsed ZW chromosomes during chicken oogenesis (Schoenmakers et al. 2009; Namekawa and Lee 2009) could explain the ovary-biased expression pattern found for ''out of Z'' duplicate genes (Ellegren 2011). In silkworm, it is still unknown whether MSCI exists and if it plays a role on the retrogene traffic between chromosomes. "
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    ABSTRACT: Previous studies on organisms with well-differentiated X and Y chromosomes, such as Drosophila and mammals, consistently detected an excess of genes moving out of the X chromosome and gaining testis-biased expression. Several selective evolutionary mechanisms were shown to be associated with this nonrandom gene traffic, which contributed to the evolution of the X chromosome and autosomes. If selection drives gene traffic, such traffic should also exist in species with Z and W chromosomes, where the females are the heterogametic sex. However, no previous studies on gene traffic in species with female heterogamety have found any nonrandom chromosomal gene movement. Here, we report an excess of retrogenes moving out of the Z chromosome in an organism with the ZW sex determination system, Bombyx mori. In addition, we showed that those "out of Z" retrogenes tended to have ovary-biased expression, which is consistent with the pattern of non-retrogene traffic recently reported in birds and symmetrical to the retrogene movement in mammals and fruit flies out of the X chromosome evolving testis functions. These properties of gene traffic in the ZW system suggest a general role for the heterogamety of sex chromosomes in determining the chromosomal locations and the evolution of sex-biased genes.
    Preview · Article · Apr 2012 · Journal of Molecular Evolution
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