An apparent excess of sex– and reproduction–related genes on the human X chromosome

Saifi, Gulam Mustafa; Chandra, H. Sharat

doi:10.1098/rspb.1999.0623

Cited by 141 publications

(113 citation statements)

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“…The accumulation of both male-and female-biased genes on the X chromosome is consistent with the predictions of W. Rice 3 and previous reports on mice and humans [6][7][8] . We believe that the paucity of testis-enriched genes on the mouse X is mainly attributable to the effects of MSCI 19,20 .…”

supporting

confidence: 91%

“…One model predicts that genes with sexbiased expression should be enriched on the X chromosome [2][3][4][5] . In agreement with Rice's hypothesis 3 , spermatogonial genes are over-represented on the X chromosome of mice 6 and sex-and reproduction-related genes are over-represented on the human X chromosome 7,8 . Male-biased genes are under-represented on the X chromosome in worms and flies [9][10][11] , however.…”

supporting

confidence: 86%

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The mouse X chromosome is enriched for sex-biased genes not subject to selection by meiotic sex chromosome inactivation

et al. 2004

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Sex chromosomes are subject to sex-specific selective evolutionary forces 1,2 . One model predicts that genes with sexbiased expression should be enriched on the X chromosome 2-5 . In agreement with Rice's hypothesis 3 , spermatogonial genes are over-represented on the X chromosome of mice 6 and sex-and reproduction-related genes are over-represented on the human X chromosome 7,8 . Male-biased genes are under-represented on the X chromosome in worms and flies 9-11 , however. Here we show that mouse spermatogenesis genes are relatively underrepresented on the X chromosome and female-biased genes are enriched on it. We used Spo11 -/-mice blocked in spermatogenesis early in meiosis 12 to evaluate the temporal pattern of gene expression in sperm development. Genes expressed before the Spo11 block are enriched on the X chromosome, whereas those expressed later in spermatogenesis are depleted. Inactivation of the X chromosome in male meiosis may be a universal driving force for X-chromosome demasculinization.To investigate the genomic distribution of mouse genes with patterns of sex-biased expression, we analyzed the chromosomal distribution of genes expressed in sexually dimorphic tissues. We consider genes that are preferentially expressed in such tissues as testis, ovary and placenta to be sex-biased genes. We used two approaches to define the tissue specificity of genes expressed in mice: analysis of large-scale microarray-based gene expression data and analysis of the distribution of expressed-sequence tags (ESTs) in different cDNA libraries. Instead of focusing on transcripts restricted to a single tissue, our analysis targeted the identification of tissue-enriched transcripts using a 'preferential expression measure' (PEM) 13 . As an uniform source of expression data, we used publicly available data sets of mouse RNA samples representing 49 tissues hybridized to Affymetrix mouse U74A microarrays (GNF data set) 14 and 20 tissues analyzed with RIKEN cDNA microarrays (RIKEN data set) 15 .In the GNF data set 14 , expression of 624 genes (∼7% of all analyzed) in testis was three times greater than the median expression in other tissues, and expression of 361 genes in testis was five times greater (PEM values >1.58 and >2.32, respectively). These genes are considered testis-enriched genes. The chromosomal distribution of testisenriched genes was significantly different from uniform (χ 2 = 30.8, P = 0.05; Fig. 1a and Supplementary Table 1 online). The most significant deviation from the average gene density was on the X chromosome, where testis-enriched genes were 2.5 times less dense (the ratio of the density of testis-enriched genes on the X chromosome to the average density on all chromosomes, ρ X , was 0.40; χ 2 = 7.7, P = 0.006). The depletion of testis-enriched genes on the X chromosome was independent of the cut-off (three or five times greater expression) used in the selection process (Table 1). In addition, genes that were expressed most highly in testis and all the genes detected in testis were underrepresen...

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confidence: 91%

supporting

confidence: 86%

The mouse X chromosome is enriched for sex-biased genes not subject to selection by meiotic sex chromosome inactivation

et al. 2004

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“…A large body of literature suggests that the influence of X-linked genes should be greater on sexually selected (often sex-limited) traits than autosomal genes, and in some studies this has been the case (Reinhold, 1998;Hurst and Randerson, 1999;Saifi and Chandra, 1999). When sexual selection favors trait expression in hemizygous males, but not in females, X-linked loci evolve more quickly (Rice, 1984;Charlesworth et al, 1987) and are more likely to persist than autosomal loci (Reinhold, 1999).…”

Section: Discussionmentioning

confidence: 99%

Rapid evolutionary change in a sexual signal: genetic control of the mutation ‘flatwing’ that renders male field crickets (Teleogryllus oceanicus) mute

Tinghitella

2007

Heredity

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Colonizing events may expose organisms to physical and ecological environments found nowhere else in their range. Novel selection pressures can then influence subsequent rapid evolutionary changes. Here, I investigate the genetics of one such rapid change in the sexual signal of Polynesian field crickets, Teleogryllus oceanicus, that recently colonized the Hawaiian Islands. In Hawaii, T. oceanicus encounter a deadly parasitoid fly found nowhere else in their range. In o20 generations, a wing mutation, flatwing, that eliminates the crickets' song, an important sexual signal, but protects them from the fly, spread to 490% of males on the island of Kauai. I show, using crosses between flatwing males and females from a population that has never contained flatwings, that the song-suppressing mutation is due to a change in a single sex-linked locus. Contemporary evolution of secondary sexual characteristics has only rarely been identified as the result of single-gene changes and never before as a single sex-linked locus, but sex-linked inheritance is thought to facilitate the rapid evolution of these types of traits. Because divergence of sexual signals can influence reproductive isolation, understanding how colonization events and subsequent selection affect signals, and the genetic mechanisms of such change, can shed light on processes likely to play a role in speciation.

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“…The human X encodes a mixture of widely expressed housekeeping genes, as well as genes that have specialized functions such as visual pigments and blood clotting factors. However, there is an elevated frequency (compared with the autosomes) of genes with sex and reproduction-related functions (Saifi and Chandra, 1999). It was suggested that the accumulation of male advantage genes on the human X chromosome is the result of rapid selection in the hemizygous male (Rice, 1987).…”

Section: Eutherian Sex Chromosomesmentioning

confidence: 99%

The origin and evolution of vertebrate sex chromosomes and dosage compensation

2011

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In mammals, birds, snakes and many lizards and fish, sex is determined genetically (either male XY heterogamy or female ZW heterogamy), whereas in alligators, and in many reptiles and turtles, the temperature at which eggs are incubated determines sex. Evidently, different sex-determining systems (and sex chromosome pairs) have evolved independently in different vertebrate lineages. Homology shared by Xs and Ys (and Zs and Ws) within species demonstrates that differentiated sex chromosomes were once homologous, and that the sex-specific non-recombining Y (or W) was progressively degraded. Consequently, genes are left in single copy in the heterogametic sex, which results in an imbalance of the dosage of genes on the sex chromosomes between the sexes, and also relative to the autosomes. Dosage compensation has evolved in diverse species to compensate for these dose differences, with the stringency of compensation apparently differing greatly between lineages, perhaps reflecting the concentration of genes on the original autosome pair that required dosage compensation. We discuss the organization and evolution of amniote sex chromosomes, and hypothesize that dosage insensitivity might predispose an autosome to evolving function as a sex chromosome.

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An apparent excess of sex– and reproduction–related genes on the human X chromosome

Cited by 141 publications

References 40 publications

The mouse X chromosome is enriched for sex-biased genes not subject to selection by meiotic sex chromosome inactivation

The mouse X chromosome is enriched for sex-biased genes not subject to selection by meiotic sex chromosome inactivation

Rapid evolutionary change in a sexual signal: genetic control of the mutation ‘flatwing’ that renders male field crickets (Teleogryllus oceanicus) mute

The origin and evolution of vertebrate sex chromosomes and dosage compensation

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