Abstract
The human and mouse X chromosomes have an atypical gene content. These X chromosomes contain more genes involved in reproduction and brain function than would be expected by chance alone. The accumulation of these types of genes may be facilitated by the structure of the X chromosome, which may be conducive to the amplification of genes in particular regions. In addition, as the X chromosome is hemizygous in males and is silenced during male meiosis, this affects both the fixation of male-beneficial and female-beneficial genes, and the expression of X-linked genes during meiosis. A requirement for the expression of X-linked genes during spermatogenesis may have driven retrotransposition of genes both on and off the X, and this has had a role in shaping the gene content of the mammalian X chromosome. Characterisation of the structure and gene content of the marsupial X chromosome is essential to understand whether the features of structure and expression observed on the human and mouse X chromosomes are fundamental to all therian X chromosomes. This will indicate whether the therian X chromosome plays a special role in reproduction and brain functions, and possibly speciation.
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References
Bertrand M, Huijbers I, Chomez P, De Backer O (2004) Comparative expression analysis of the MAGED genes during embryogenesis and brain development. Dev Dyn 230:325–334.
Bininda-Emonds ORP, Cardillo M, Jones KE, et al. (2007) The delayed rise of present-day mammals. Nature 446:507–512.
Chiurazzi P, Schwartz CE, Gecz J, Neri G (2008) XLMR genes: update 2007. Eur J Hum Genet 16:422–434.
Chomez P, De Backer O, Bertrand M, et al. (2001) An overview of the MAGE gene family with the identification of all human members of the family. Cancer Res 61:5544–5551.
Dahl HH, Brown RM, Hutchison WM, Maragos C, Brown GK (1990) A testis-specific form of the human pyruvate dehydrogenase E1 alpha subunit is coded for by an intronless gene on chromosome 4. Genomics 8:225–232.
Deakin JE, Koina E, Waters PD, et al. (2008) Physical map of two tammar wallaby chromosomes: a strategy for mapping in non-model mammals. Chromosome Res 16:1159–1175.
Delbridge ML, Graves JAM (2007) Origin and evolution of spermatogenesis genes on the human sex chromosomes. Soc Reprod Fertil Suppl 65:1–17.
Delbridge ML, Lingenfelter PA, Disteche CM, Graves JAM (1999) The candidate spermatogenesis gene RBMY has a homologue on the human X chromosome. Nat Genet 22:223–224.
Delbridge ML, Longepied G, Depetris D, et al. (2004) TSPY, the candidate gonadoblastoma gene on the human Y chromosome, has a widely expressed homologue on the X – implications for Y chromosome evolution. Chromosome Res 12:345–356.
Delbridge ML, McMillan DA, Doherty RJ, Deakin JE, Graves JAM (2008) Origin and evolution of candidate mental retardation genes on the human X chromosome (MRX). BMC Genomics 9:65.
Emerson JJ, Kaessmann H, Betran E, Long M (2004) Extensive gene traffic on the mammalian X chromosome. Science 303:537–540.
Foster JW, Graves JAM (1994) An SRY-related sequence on the marsupial X chromosome: implications for the evolution of the mammalian testis-determining gene. Proc Natl Acad Sci USA 91:1927–1931.
Franco MJ, Sciurano RB, Solari AJ (2007) Protein immunolocalization supports the presence of identical mechanisms of XY body formation in eutherians and marsupials. Chromosome Res 15:815–824.
Graves JAM (1995) The origin and function of the mammalian Y chromosome and Y-borne genes–an evolving understanding. Bioessays 17:311–320.
Graves JAM (2006) Sex chromosome specialization and degeneration in mammals. Cell 124: 901–914.
Graves JAM, Gecz J, Hameister H (2002) Evolution of the human X–a smart and sexy chromosome that controls speciation and development. Cytogenet Genome Res 99:141–145.
Grützner F, Rens W, Tsend-Ayush E, et al. (2004) In the platypus a meiotic chain of ten sex chromosomes shares genes with the bird Z and mammal X chromosomes. Nature 432:913–917.
Gurbich TA, Bachtrog D (2008) Gene content evolution on the X chromosome. Curr Opin Genet Dev 18:493–498.
Heard E, Disteche CM (2006) Dosage compensation in mammals: fine-tuning the expression of the X chromosome. Genes Dev 20:1848–1867.
Hore TA, Koina E, Wakefield MJ, Graves JAM (2007) The region homologous to the X-chromosome inactivation centre has been disrupted in marsupial and monotreme mammals. Chromosome Res 15:147–161.
Hornecker JL, Samollow PB, Robinson ES, Vandeberg JL, McCarrey JR (2007) Meiotic sex chromosome inactivation in the marsupial Monodelphis domestica. Genesis 45:696–708.
Huynh KD, Lee JT (2003) Inheritance of a pre-inactivated paternal X chromosome in early mouse embryos. Nature 426:857–862.
Khil PP, Smirnova NA, Romanienko PJ, Camerini-Otero RD (2004) The mouse X chromosome is enriched for sex-biased genes not subject to selection by meiotic sex chromosome inactivation. Nat Genet 36:642–646.
Kohn M, Kehrer-Sawatzki H, Vogel W, Graves JAM, Hameister H (2004) Wide genome comparisons reveal the origins of the human X chromosome. Trends Genet 20:598–603.
Kohn M, Kehrer-Sawatzki H, Steinbach P, Graves JAM, Hameister H (2007) Recruitment of old genes to new functions: evidences obtained by comparing the orthologues of human XLMR genes in mouse and chicken. Cytogenet Genome Res 116:173–180.
Koslowski M, Sahin U, Huber C, Tureci O (2006) The human X chromosome is enriched for germline genes expressed in premeiotic germ cells of both sexes. Hum Mol Genet 15: 2392–2399.
Kouprina N, Mullokandov M, Rogozin IB, et al. (2004) The SPANX gene family of cancer/testis-specific antigens: rapid evolution and amplification in African great apes and hominids. Proc Natl Acad Sci USA 101:3077–3082.
Kouprina N, Pavlicek A, Noskov VN, et al. (2005) Dynamic structure of the SPANX gene cluster mapped to the prostate cancer susceptibility locus HPCX at Xq27. Genome Res 15:1477–1486.
Lingenfelter PA, Delbridge ML, Thomas S, et al. (2001) Expression and conservation of processed copies of the RBMX gene. Mamm Genome 12:538–545.
Loriot A, Boon T, De Smet C (2003) Five new human cancer-germline genes identified among 12 genes expressed in spermatogonia. Int J Cancer 105:371–376.
Lubs HA, Chiurazzi P, Arena JF, et al. (1996) XLMR genes: update 1996. Am J Med Genet 64:147–157.
Mahadevaiah SK, Turner JM, Baudat F, et al. (2001) Recombinational DNA double-strand breaks in mice precede synapsis. Nat Genet 27:271–276.
Mahadevaiah SK, Royo H, Vandeberg JL, et al. (2009) Key features of the X inactivation process are conserved between marsupials and eutherians. Curr Biol 19:1478–1484.
McCarrey JR, Kumari M, Aivaliotis MJ, et al. (1996) Analysis of the cDNA and encoded protein of the human testis-specific PGK-2 gene. Dev Genet 19:321–332.
Mikkelsen TS, Wakefield MJ, Aken B, et al. (2007) Genome of the marsupial Monodelphis domestica reveals innovation in non-coding sequences. Nature 447:167–177.
Mueller JL, Mahadevaiah SK, Park PJ, et al. (2008) The mouse X chromosome is enriched for multicopy testis genes showing postmeiotic expression. Nat Genet 40:794–799.
Namekawa SH, Park PJ, Zhang LF, et al. (2006) Postmeiotic sex chromatin in the male germline of mice. Curr Biol 16:660–667.
Namekawa SH, VandeBerg JL, McCarrey JR, Lee JT (2007) Sex chromosome silencing in the marsupial male germ line. Proc Natl Acad Sci USA 104:9730–9735.
Nguyen DK, Disteche CM (2006a) Dosage compensation of the active X chromosome in mammals. Nat Genet 38:47–53.
Nguyen DK, Disteche CM (2006b) High expression of the mammalian X chromosome in brain. Brain Res 1126:46–49.
Orr HA, Coyne JA (1989) The genetics of postzygotic isolation in the Drosophila virilis group. Genetics 121:527–537.
Potrzebowski L, Vinckenbosch N, Marques AC, et al. (2008) Chromosomal gene movements reflect the recent origin and biology of therian sex chromosomes. PLoS Biol 6:e80.
Rens W, Grützner F, O’Brien PC, et al. (2004) Resolution and evolution of the duck-billed platypus karyotype with an X1Y1X2Y2X3Y3X4Y4X5Y5 male sex chromosome constitution. Proc Natl Acad Sci USA 101:16257–16261.
Ropers HH, Hamel BC (2005) X-linked mental retardation. Nat Rev Genet 6:46–57.
Ross MT, Grafham DV, Coffey AJ, et al. (2005) The DNA sequence of the human X chromosome. Nature 434:325–337.
Rozen S, Skaletsky H, Marszalek JD, et al. (2003) Abundant gene conversion between arms of palindromes in human and ape Y chromosomes. Nature 423:873–876.
Saifi GM, Chandra HS (1999) An apparent excess of sex- and reproduction-related genes on the human X chromosome. Proc R Soc Lond B Biol Sci 266:203–209.
Schoenmakers S, Wassenaar E, Hoogerbrugge JW, et al. (2009) Female meiotic sex chromosome inactivation in chicken. PLoS Genet 5:e1000466.
Simpson AJ, Caballero OL, Jungbluth A, Chen YT, Old LJ (2005) Cancer/testis antigens, gametogenesis and cancer. Nat Rev Cancer 5:615–625.
Skaletsky H, Kuroda-Kawaguchi T, Minx PJ, et al. (2003) The male-specific region of the human Y chromosome is a mosaic of discrete sequence classes. Nature 423:825–837.
Small K, Iber J, Warren ST (1997) Emerin deletion reveals a common X-chromosome inversion mediated by inverted repeats. Nat Genet 16:96–99.
Soullier S, Hanni C, Catzeflis F, Berta P, Laudet V (1998) Male sex determination in the spiny rat Tokudaia osimensis (Rodentia: Muridae) is not Sry dependent. Mamm Genome 9:590–592.
Sutou S, Mitsui Y, Tsuchiya K (2001) Sex determination without the Y chromosome in two Japanese rodents Tokudaia osimensis osimensis and Tokudaia osimensis spp. Mamm Genome 12:17–21.
Veyrunes F, Waters PD, Miethke P, et al. (2008) Bird-like sex chromosomes of platypus imply recent origin of mammal sex chromosomes. Genome Res 18:965–973.
Vicoso B, Charlesworth B (2006) Evolution on the X chromosome: unusual patterns and processes. Nat Rev Genet 7:645–653.
Vogel W, Jainta S, Rau W, et al. (1998) Sex determination in Ellobius lutescens: the story of an enigma. Cytogenet Cell Genet 80:214–221.
Wang PJ, McCarrey JR, Yang F, Page DC (2001) An abundance of X-linked genes expressed in spermatogonia. Nat Genet 27:422–426.
Warburton PE, Giordano J, Cheung F, Gelfand Y, Benson G (2004) Inverted repeat structure of the human genome: the X-chromosome contains a preponderance of large, highly homologous inverted repeats that contain testes genes. Genome Res 14:1861–1869.
Waters PD, Delbridge ML, Deakin JE, et al. (2005) Autosomal location of genes from the conserved mammalian X in the platypus (Ornithorhynchus anatinus): implications for mammalian sex chromosome evolution. Chromosome Res 13:401–410.
Waters PD, Wallis MC, Graves JAM (2007) Mammalian sex–Origin and evolution of the Y chromosome and SRY. Semin Cell Dev Biol 18:389–400.
Wilda M, Bachner D, Zechner U, et al. (2000) Do the constraints of human speciation cause expression of the same set of genes in brain, testis, and placenta? Cytogenet Cell Genet 91:300–302.
Zechner U, Wilda M, Kehrer-Sawatzki H, et al. (2001) A high density of X-linked genes for general cognitive ability: a run-away process shaping human evolution? Trends Genet 17:697–701.
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Delbridge, M.L. (2010). Gene Content of the Mammalian X Chromosome. In: Deakin, J., Waters, P., Marshall Graves, J. (eds) Marsupial Genetics and Genomics. Springer, Dordrecht. https://doi.org/10.1007/978-90-481-9023-2_9
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