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A W-linked palindrome and gene conversion in New World sparrows and blackbirds

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Abstract

A hallmark feature of the male-specific region of the human Y chromosome is the presence of large and near-identical palindromes. These palindromes are maintained in a state of near identity via gene conversion between the arms of the palindrome, and both neutral and selection-based theories have been proposed to explain their enrichment on the human Y and X chromosomes. While those proposed theories would be applicable to sex chromosomes in other species, it has not been established whether near-identical palindromes are a common feature of sex chromosomes in a broader range of taxa, including other tetrapods. Here, we report the genomic sequencing and features of a 279-kb region of the non-recombining portion of the W chromosome spanning the CHD1W locus in a New World sparrow, the white-throated sparrow (Zonotrichia albicollis), and the corresponding region on the Z chromosome. As has been observed for other Y and W chromosomes, we detected a high repetitive element content (51%) and low gene content on the white-throated sparrow W chromosome. In addition, we identified a 22-kb near-identical (>99%) palindrome on the W chromosome that flanks the 5′ end of the CHD1W gene. Signatures of gene conversion were readily detected between the arms of this palindrome, as was the presence of this palindrome in other New World sparrows and blackbirds. Near-identical palindromes are therefore present on the avian W chromosome and may persist due to the same forces proposed for the enrichment of these elements on the human sex chromosomes.

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Abbreviations

BAC:

Bacterial artificial chromosome

CHD1W:

Chromo-helicase DNA-binding protein, W chromosome

CHD1Z:

Chromo-helicase DNA-binding protein, Z chromosome

CHORI:

Children’s Hospital Oakland Research Institute

dNTP:

deoxy-nucleotide triphosphate

HINTW:

Histidine triad nucleotide binding protein W

kb:

Kilobase pairs

MSCI:

Meiotic sex chromosome inactivation

MSY:

Male-specific region of the Y chromosome

PCR:

Polymerase chain reaction

RASA1:

RAS p21 protein activator (GTPase activating protein) 1

RGMB:

RGM domain family, member B

UWBM:

University of Washington Burke Museum

References

  • Agate RJ, Choe M, Arnold AP (2004) Sex differences in structure and expression of the sex chromosome genes CHD1Z and CHD1W in zebra finches. Mol Biol Evol 21:384–396

    Article  CAS  PubMed  Google Scholar 

  • Altschul SF, Madden TL, Schaffer AA et al (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  CAS  PubMed  Google Scholar 

  • Bachtrog D, Hom E, Wong KM, Maside X, De Jong P (2008) Genomic degradation of a young Y chromosome in Drosophila miranda. Genome Biol 9:R30

    Article  PubMed  Google Scholar 

  • Backstrom N, Ceplitis H, Berlin S, Ellegren H (2005) Gene conversion drives the evolution of HINTW, an ampliconic gene on the female-specific avian W chromosome. Mol Biol Evol 22:1992–1999

    Article  PubMed  Google Scholar 

  • Bagnall RD, Ayres KL, Green PM, Giannelli F (2005) Gene conversion and evolution of Xq28 duplicons involved in recurring inversions causing severe hemophilia A. Genome Res 15:214–223

    Article  CAS  PubMed  Google Scholar 

  • Balakrishnan CN, Edwards SV (2009) Nucleotide variation, linkage disequilibrium and founder-facilitated speciation in wild populations of the zebra finch (Taeniopygia guttata). Genetics 181:645–660

    Article  PubMed  Google Scholar 

  • Blakesley RW, Hansen NF, Mullikin JC et al (2004) An intermediate grade of finished genomic sequence suitable for comparative analyses. Genome Res 14:2235–2244

    Article  CAS  PubMed  Google Scholar 

  • Burge C, Karlin S (1997) Prediction of complete gene structures in human genomic DNA. J Mol Biol 268:78–94

    Article  CAS  PubMed  Google Scholar 

  • Caceres M, Sullivan RT, Thomas JW (2007) A recurrent inversion on the eutherian X chromosome. Proc Natl Acad Sci USA 104:18571–18576

    Article  CAS  PubMed  Google Scholar 

  • Charlesworth B, Charlesworth D (2000) The degeneration of Y chromosomes. Philos Trans R Soc Lond B Biol Sci 355:1563–1572

    Article  CAS  PubMed  Google Scholar 

  • Charlesworth D, Charlesworth B, Marais G (2005) Steps in the evolution of heteromorphic sex chromosomes. Heredity 95:118–128

    Article  CAS  PubMed  Google Scholar 

  • Ellegren H, Carmichael A (2001) Multiple and independent cessation of recombination between avian sex chromosomes. Genetics 158:325–331

    CAS  PubMed  Google Scholar 

  • Ezaz T, Moritz B, Waters P, Marshall Graves JA, Georges A, Sarre SD (2009) The ZW sex microchromosomes of an Australian dragon lizard share no homology with those of other reptiles or birds. Chromosome Res 17:965–973

    Article  CAS  PubMed  Google Scholar 

  • Fridolfsson AK, Ellegren H (2000) Molecular evolution of the avian CHD1 genes on the Z and W sex chromosomes. Genetics 155:1903–1912

    CAS  PubMed  Google Scholar 

  • Griffiths R, Double MC, Orr K, Dawson RJ (1998) A DNA test to sex most birds. Mol Ecol 7:1071–1075

    Article  CAS  PubMed  Google Scholar 

  • Hillier LW, Miller W, Birney E et al (2004) Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature 432:695–716

    Article  CAS  Google Scholar 

  • Hori T, Asakawa S, Itoh Y, Shimizu N, Mizuno S (2000) Wpkci, encoding an altered form of PKCI, is conserved widely on the avian W chromosome and expressed in early female embryos: implication of its role in female sex determination. Mol Biol Cell 11:3645–3660

    CAS  PubMed  Google Scholar 

  • Hughes JF, Skaletsky H, Pyntikova T et al (2010) Chimpanzee and human Y chromosomes are remarkably divergent in structure and gene content. Nature 463:536–539

    Article  CAS  PubMed  Google Scholar 

  • Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23:254–267

    Article  CAS  PubMed  Google Scholar 

  • Itoh Y, Kampf K, Arnold AP (2008) Molecular cloning of zebra finch W chromosome repetitive sequences: evolution of the avian W chromosome. Chromosoma 117:111–121

    Article  CAS  PubMed  Google Scholar 

  • Itoh Y, Kampf K, Arnold AP (2009) Disruption of FEM1C-W gene in zebra finch: evolutionary insights on avian ZW genes. Chromosoma 118:323–334

    Article  CAS  PubMed  Google Scholar 

  • Jeanmougin F, Thompson JD, Gouy M, Higgins DG, Gibson TJ (1998) Multiple sequence alignment with Clustal X. Trends Biochem Sci 23:403–405

    Article  CAS  PubMed  Google Scholar 

  • Kondo M, Hornung U, Nanda I et al (2006) Genomic organization of the sex-determining and adjacent regions of the sex chromosomes of medaka. Genome Res 16:815–826

    Article  CAS  PubMed  Google Scholar 

  • Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163

    Article  CAS  PubMed  Google Scholar 

  • Lahn BT, Page DC (1999) Four evolutionary strata on the human X chromosome. Science 286:964–967

    Article  CAS  PubMed  Google Scholar 

  • Lakich D, Kazazian HH Jr, Antonarakis SE, Gitschier J (1993) Inversions disrupting the factor VIII gene are a common cause of severe haemophilia A. Nat Genet 5:236–241

    Article  CAS  PubMed  Google Scholar 

  • Lange J, Skaletsky H, Van Daalen SK et al (2009) Isodicentric Y chromosomes and sex disorders as byproducts of homologous recombination that maintains palindromes. Cell 138:855–869

    Article  CAS  PubMed  Google Scholar 

  • Mank JE, Ellegren H (2007) Parallel divergence and degradation of the avian W sex chromosome. Trends Ecol Evol 22:389–391

    Article  PubMed  Google Scholar 

  • Marshall Graves JA (2008) Weird animal genomes and the evolution of vertebrate sex and sex chromosomes. Annu Rev Genet 42:565–586

    Article  CAS  PubMed  Google Scholar 

  • Matsubara K, Tarui H, Toriba M et al (2006) Evidence for different origin of sex chromosomes in snakes, birds, and mammals and step-wise differentiation of snake sex chromosomes. Proc Natl Acad Sci USA 103:18190–18195

    Article  CAS  PubMed  Google Scholar 

  • Nam K, Ellegren H (2008) The chicken (Gallus gallus) Z chromosome contains at least three nonlinear evolutionary strata. Genetics 180:1131–1136

    Article  CAS  PubMed  Google Scholar 

  • Ohno S (1967) Sex chromosomes and sex-linked genes. Springer-Verlag, New York

    Google Scholar 

  • Rossiter JP, Young M, Kimberland ML et al (1994) Factor VIII gene inversions causing severe hemophilia A originate almost exclusively in male germ cells. Hum Mol Genet 3:1035–1039

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Sawyer S (1989) Statistical tests for detecting gene conversion. Mol Biol Evol 6:526–538

    CAS  PubMed  Google Scholar 

  • Schoenmakers S, Wassenaar E, Hoogerbrugge JW, Laven JS, Grootegoed JA, Baarends WM (2009) Female meiotic sex chromosome inactivation in chicken. PLoS Genet 5:e1000466

    Article  PubMed  Google Scholar 

  • Schwartz S, Zhang Z, Frazer KA et al (2000) PipMaker—a web server for aligning two genomic DNA sequences. Genome Res 10:577–586

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Sperber G, Lovgren A, Eriksson NE, Benachenhou F, Blomberg J (2009) RetroTector online, a rational tool for analysis of retroviral elements in small and medium size vertebrate genomic sequences. BMC Bioinform 10(6):S4

    Article  Google Scholar 

  • Sullivan RT, Morehouse CB, Thomas JW (2008) Uprobe 2008: an online resource for universal overgo hybridization-based probe retrieval and design. Nucleic Acids Res 36:W149–W153

    Article  CAS  PubMed  Google Scholar 

  • Thomas JW (2008) Comparative physical mapping: universal overgo hybridization probe design and BAC library hybridization. In: Murphy WJ (ed) Methods in molecular biology: phylogenomics. Humana Press, Totowa, pp 119–132

    Chapter  Google Scholar 

  • Thomas JW, Prasad AB, Summers TJ et al (2002) Parallel construction of orthologous sequence-ready clone contig maps in multiple species. Genome Res 12:1277–1285

    Article  CAS  PubMed  Google Scholar 

  • Vibranovski MD, Koerich LB, Carvalho AB (2008) Two new Y-linked genes in Drosophila melanogaster. Genetics 179:2325–2357

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Warren WC, Clayton DF, Ellegren H et al (2010) The genome of a songbird. Nature 464:757–762

    Article  CAS  PubMed  Google Scholar 

  • Wheelan SJ, Church DM, Ostell JM (2001) Spidey: a tool for mRNA-to-genomic alignments. Genome Res 11:1952–1957

    CAS  PubMed  Google Scholar 

  • Wilson MA, Makova KD (2009) Genomic analyses of sex chromosome evolution. Annu Rev Genomics Hum Genet 10:333–354

    Article  CAS  PubMed  Google Scholar 

  • Yu Q, Hou S, Hobza R et al (2007) Chromosomal location and gene paucity of the male specific region on papaya Y chromosome. Mol Genet Genomics 278:177–185

    Article  CAS  PubMed  Google Scholar 

  • Yuri T, Mindell DP (2002) Molecular phylogenetic analysis of Fringillidae, “New World nine-primaried oscines” (Aves: Passeriformes). Mol Phylogenet Evol 23:229–243

    Article  CAS  PubMed  Google Scholar 

  • Zhang Z, Schwartz S, Wagner L, Miller W (2000) A greedy algorithm for aligning DNA sequences. J Comput Biol 7:203–214

    Article  CAS  PubMed  Google Scholar 

  • Zink RM, Dittmann DL, Rootes WL (1991) Mitochrondrial DNA variation and the phylogeny of Zonotrichia. Auk 108:578–584

    Google Scholar 

Internet references

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Acknowledgements

The authors thank Judith E. Mank for helpful comments and discussions, Mario Cáceres for comments, Cheryl T. Strauss for technical writing edits, Donna L. Maney for the dark-eyed junco DNA, Greg K. Tharp for computer support, the BC Cancer Agency Genome Sciences Centre, Vancouver, Canada, for generation of the BAC-end sequences, and members of the NIH Sequencing Center including E.D. Green, R. Blakesley, G. Bouffard, and J. McDowell. DNA samples (excluding the dark-eyed junco) were provided by The Burke Museum of Natural History and Culture. J.K.D. and J.W.T. were supported by a grant from the National Institutes of Health (1R21MH082046), and the NIH Intramural Sequencing Center was supported in part by the Intramural Research Program of the National Human Genome Research Institute of the National Institutes of Health.

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Correspondence to James W. Thomas.

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Responsible Editor: Mary E. Delany

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Davis, J.K., Thomas, P.J., NISC Comparative Sequencing Program. et al. A W-linked palindrome and gene conversion in New World sparrows and blackbirds. Chromosome Res 18, 543–553 (2010). https://doi.org/10.1007/s10577-010-9134-y

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