Skip to main content
Log in

Nonrandom Representation of Sex-Biased Genes on Chicken Z Chromosome

  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Abstract

Several lines of evidence suggest that the X chromosome of various animal species has an unusual complement of genes with sex-biased or sex-specific expression. However, the study of the X chromosome gene content in different organisms provided conflicting results. The most striking contrast concerns the male-biased genes, which were reported to be almost depleted from the X chromosome in Drosophila but overrepresented on the X chromosome in mammals. To elucidate the reason for these discrepancies, we analysed the gene content of the Z chromosome in chicken. Our analysis of the publicly available expressed sequence tags (EST) data and genome draft sequence revealed a significant underrepresentation of ovary-specific genes on the chicken Z chromosome. For the brain-expressed genes, we found a significant enrichment of male-biased genes but an indication of underrepresentation of female-biased genes on the Z chromosome. This is the first report on the nonrandom gene content in a homogametic sex chromosome of a species with heterogametic female individuals. Further comparison of gene contents of the independently evolved X and Z sex chromosomes may offer new insight into the evolutionary processes leading to the nonrandom genomic distribution of sex-biased and sex-specific genes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1.

Similar content being viewed by others

References

  • Avner P, Heard E (2001) X-chromosome inactivation: Counting, choice and initiation. Nat Rev Genet 2:59–67

    Article  PubMed  CAS  Google Scholar 

  • Axelsson E, Smith NG, Sundstrom H, Berlin S, Ellegren H (2004) Male-biased mutation rate and divergence in autosomal, z-linked and w-linked introns of chicken and turkey. Mol Biol Evol 21:1538–1547

    Article  PubMed  CAS  Google Scholar 

  • Baker BS, Gorman M, Marin I (1994) Dosage compensation in Drosophila. Annu Rev Genet 28:491–521

    Article  PubMed  CAS  Google Scholar 

  • Betran E, Thornton K, Long M (2002) Retroposed new genes of the X in Drosophila. Genome Res 12:1854–1859

    Article  PubMed  CAS  Google Scholar 

  • Bisoni L, Batlle-Morera L, Bird AP, Suzuki M, McQueen HA (2005) Female-specific hyperacetylation of histone H4 in the chicken Z chromosome. Chromosome Res 13:205–214

    Article  PubMed  CAS  Google Scholar 

  • Bortoluzzi S, Rampoldi L, Simionati B, Zimbello R, Barbon A, d’Alessi F, Tiso N, Pallavicini A, Toppo S, Cannata N, Valle G, Lanfranchi G, Danieli GA (1998) A comprehensive, high-resolution genomic transcript map of human skeletal muscle. Genome Res 8:817–825

    PubMed  CAS  Google Scholar 

  • Divina P, Vlcek C, Strnad P, Paces V, Forejt J (2005) Global transcriptome analysis of the C57BL/6J mouse testis by SAGE: Evidence for nonrandom gene order. BMC Genomics 6:29

    Article  PubMed  CAS  Google Scholar 

  • Ellegren H (2002) Dosage compensation: Do birds do it as well? Trends Genet 18:25–28

    Article  PubMed  CAS  Google Scholar 

  • Ellegren H, Fridolfsson AK (1997) Male-driven evolution of DNA sequences in birds. Nat Genet 17:182–184

    Article  PubMed  CAS  Google Scholar 

  • Emerson JJ, Kaessmann H, Betran E, Long M (2004) Extensive gene traffic on the mammalian X chromosome. Science 303:537–540

    Article  PubMed  CAS  Google Scholar 

  • Gupta V, Parisi M, Sturgill D, Nuttall R, Doctolero M, Dudko OK, Malley JD, Eastman PS, Oliver B (2006) Global analysis of X-chromosome dosage compensation. J Biol 5:3

    Article  PubMed  CAS  Google Scholar 

  • Hurst LD (2001) Evolutionary genomics. Sex and the X. Nature 411:149–150

    Article  PubMed  CAS  Google Scholar 

  • Hurst LD, Randerson JP (1999) An eXceptional chromosome. Trends Genet 15:383–385

    Article  PubMed  CAS  Google Scholar 

  • International Chicken Genome Sequencing Consortium (2004) Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature 432:695–716

    Article  CAS  Google Scholar 

  • Jablonka E, Lamb MJ (1990) The evolution of heteromorphic sex chromosomes. Biol Rev Camb Philos Soc 65:249–276

    Article  PubMed  CAS  Google Scholar 

  • Karolchik D, Baertsch R, Diekhans M, Furey TS, Hinrichs A, Lu YT, Roskin KM, Schwartz M, Sugnet CW, Thomas DJ, Weber RJ, Haussler D, Kent WJ (2003) The UCSC Genome Browser Database. Nucleic Acids Res 31:51–54

    Article  PubMed  CAS  Google Scholar 

  • Kelley RL (2004) Path to equality strewn with roX. Dev Biol 269:18–25

    Article  PubMed  CAS  Google Scholar 

  • Kent WJ (2002) BLAT—the BLAST-like alignment tool. Genome Res 12:656–664

    Article  PubMed  CAS  Google Scholar 

  • Khil PP, Oliver B, Camerini-Otero RD (2005) X for intersection: Retrotransposition both on and off the X chromosome is more frequent. Trends Genet 21:3–7

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Kirkpatrick M, Hall DW (2004) Male-biased mutation, sex linkage, and the rate of adaptive evolution. Evolution Int J Org Evolution 58:437–40

    PubMed  Google Scholar 

  • Lercher MJ, Urrutia AO, Hurst LD (2003) Evidence that the human X chromosome is enriched for male-specific but not female-specific genes. Mol Biol Evol 20:1113–1116

    Article  PubMed  CAS  Google Scholar 

  • Meyer BJ (2000) Sex in the worm-counting and -compensating X-chromosome dose. Trends Genet 16:247–253

    Article  PubMed  CAS  Google Scholar 

  • Montell H, Fridolfsson AK, Ellegren H (2001) Contrasting levels of nucleotide diversity on the avian Z and W sex chromosomes. Mol Biol Evol 18:2010–2016

    PubMed  CAS  Google Scholar 

  • Parisi M, Nuttall R, Naiman D, Bouffard G, Malley J, Andrews J, Eastman S, Oliver B (2003) Paucity of genes on the Drosophila X chromosome showing male-biased expression. Science 299:697–700

    Article  PubMed  CAS  Google Scholar 

  • Ranz JM, Castillo-Davis CI, Meiklejohn CD, Hartl DL (2003) Sex-dependent gene expression and evolution of the Drosophila transcriptome. Science 300:1742–1745

    Article  PubMed  CAS  Google Scholar 

  • Reeve HK, Pfennig DW (2003) Genetic biases for showy males: Are some genetic systems especially conducive to sexual selection? Proc Natl Acad Sci U S A 100:1089–1094

    Article  PubMed  CAS  Google Scholar 

  • Reinke V (2004) Sex and the genome. Nat Genet 36:548–549

    Article  PubMed  CAS  Google Scholar 

  • Reinke V, Gil IS, Ward S, Kazmer K (2004) Genome-wide germline–enriched and sex-biased expression profiles in Caenorhabditis elegans. Development 131:311–323

    Article  PubMed  CAS  Google Scholar 

  • Rice WR (1984) Sex-chromosomes and the evolution of sexual dimorphism. Evolution 38:735–742

    Article  Google Scholar 

  • Rogers DW, Carr M, Pomiankowski A (2003) Male genes: X-pelled or X-cluded? Bioessays 25:739–741

    Article  PubMed  Google Scholar 

  • Saifi GM, Chandra HS (1999) An apparent excess of sex- and reproduction-related genes on the human X chromosome. Proc Biol Sci 266:203–209

    Article  PubMed  CAS  Google Scholar 

  • Stekel DJ, Git Y, Falciani F (2000) The comparison of gene expression from multiple cDNA libraries. Genome Res 10:2055–2061

    Article  PubMed  CAS  Google Scholar 

  • Wang PJ, McCarrey JR, Yang F, Page DC (2001) An abundance of X-linked genes expressed in spermatogonia. Nat Genet 27:422–426

    Article  PubMed  CAS  Google Scholar 

  • Wheeler DL, Barrett T, Benson DA, Bryant SH, Canese K, Church DM, DiCuccio M, Edgar R, Federhen S, Helmberg W, Kenton DL, Khovayko O, Lipman DJ, Madden TL, Maglott DR, Ostell J, Pontius JU, Pruitt KD, Schuler GD, Schriml LM, Sequeira E, Sherry ST, Sirotkin K, Starchenko G, Suzek TO, Tatusov R, Tatusova TA, Wagner L, Yaschenko E (2005) Database resources of the National Center for Biotechnology Information. Nucleic Acids Res 33:39–45

    Article  Google Scholar 

  • Zechner U, Wilda M, Kehrer-Sawatzki H, Vogel W, Fundele R, Hameister H (2001) A high density of X-linked genes for general cognitive ability: A runaway process shaping human evolution? Trends Genet 17:697–701

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank J. Forejt for continuing support and comments on our work; J. Hejnar, D. Storch, and Z. Trachtulec for valuable suggestions; Š. Takáčová for reading the manuscript; and two anonymous reviewers for insightful comments. This work was supported by the Ministry of Education, Youth and Sports of the Czech Republic Grant No. 1M6837805002, Center for Applied Genomics, and by the Grant Agency of the Academy of Sciences Grant No. AVOZ50520514.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to R. Storchová.

Additional information

[Reviewing Editor: Dr. Manyuan Long]

Electronic Supplementary Material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Storchová, R., Divina, P. Nonrandom Representation of Sex-Biased Genes on Chicken Z Chromosome. J Mol Evol 63, 676–681 (2006). https://doi.org/10.1007/s00239-006-0022-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00239-006-0022-1

Keywords

Navigation