Skip to main content

Advertisement

SpringerLink
Log in

cDNA-based gene mapping and GC3 profiling in the soft-shelled turtle suggest a chromosomal size-dependent GC bias shared by sauropsids

  • Published:
Chromosome Research Aims and scope Submit manuscript

Abstract

Mammalian and avian genomes comprise several classes of chromosomal segments that vary dramatically in GC-content. Especially in chicken, microchromosomes exhibit a higher GC-content and a higher gene density than macrochromosomes. To understand the evolutionary history of the intra-genome GC heterogeneity in amniotes, it is necessary to examine the equivalence of this GC heterogeneity at the nucleotide level between these animals including reptiles, from which birds diverged. We isolated cDNAs for 39 protein-coding genes from the Chinese soft-shelled turtle, Pelodiscus sinensis, and performed chromosome mapping of 31 genes. The GC-content of exonic third positions (GC3) of P. sinensis genes showed a heterogeneous distribution, and exhibited a significant positive correlation with that of chicken and human orthologs, indicating that the last common ancestor of extant amniotes had already established a GC-compartmentalized genomic structure. Furthermore, chromosome mapping in P. sinensis revealed that microchromosomes tend to contain more GC-rich genes than GC-poor genes, as in chicken. These results illustrate two modes of genome evolution in amniotes: mammals elaborated the genomic configuration in which GC-rich and GC-poor regions coexist in individual chromosomes, whereas sauropsids (reptiles and birds) refined the chromosomal size-dependent GC compartmentalization in which GC-rich genomic fractions tend to be confined to microchromosomes.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • 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 

  • Andreozzi L, Federico C, Motta S et al. (2001) Compositional mapping of chicken chromosomes and identification of the gene-richest regions. Chromosom Res 9: 521–532.

    CAS  Google Scholar 

  • Aparicio S, Chapman J, Stupka E et al. (2002) Whole-genome shotgun assembly and analysis of the genome of Fugu rubripes. Science 297: 1301–1310.

    Article  CAS  PubMed  Google Scholar 

  • Auer H, Mayr B, Lambrou M, Schleger W (1987) An extended chicken karyotype, including the NOR chromosome. Cytogenet Cell Genet 45: 218–221.

    CAS  PubMed  Google Scholar 

  • Belle EM, Smith N, Eyre-Walker A (2002) Analysis of the phylogenetic distribution of isochores in vertebrates and a test of the thermal stability hypothesis. J Mol Evol 55: 356–363.

    Article  CAS  PubMed  Google Scholar 

  • Bernardi G (2000) Isochores and the evolutionary genomics of vertebrates. Gene 241: 3–17.

    CAS  PubMed  Google Scholar 

  • Bernardi G, Olofsson B, Filipski J et al. (1985) The mosaic genome of warm-blooded vertebrates. Science 228: 953–958.

    CAS  PubMed  Google Scholar 

  • Burt DW (2002) Origin and evolution of avian microchromosomes. Cytogenet Genome Res 96: 97–112.

    Article  CAS  PubMed  Google Scholar 

  • Cao Y, Sorenson MD, Kumazawa Y, Mindell DP, Hasegawa M (2000) Phylogenetic position of turtles among amniotes: evidence from mitochondrial and nuclear genes. Gene 259: 139–148.

    CAS  PubMed  Google Scholar 

  • Clay O, Caccio S, Zoubak S, Mouchiroud D, Bernardi G (1996) Human coding and noncoding DNA: compositional correlations. Mol Phylogenet Evol 5: 2–12.

    CAS  PubMed  Google Scholar 

  • Cohen MM, Gans C (1970) The chromosomes of the order Crocodilia. Cytogenetics 9: 81–105.

    CAS  PubMed  Google Scholar 

  • De Boer LEM, Sinoo RP (1984) A karyological study of Accipitridae (Aves: Falconiformes), with karyotypic description of 16 species new to cytology. Genetica 65: 89–107.

    Google Scholar 

  • Dehal P, Satou Y, Campbell RK et al. (2002) The draft genome of Ciona intestinalis: insights into chordate and vertebrate origins. Science 298: 2157–2167.

    Article  CAS  PubMed  Google Scholar 

  • Eyre-Walker A, Hurst LD (2001) The evolution of isochores. Nat Rev, Genet 2: 549–555.

    Article  CAS  Google Scholar 

  • Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17: 368–376.

    Article  CAS  PubMed  Google Scholar 

  • Frohman MA, Dush MK, Martin GR (1988) Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer. Proc Natl Acad Sci USA 85: 8998–9002.

    CAS  PubMed  Google Scholar 

  • Goldman N, Yang Z (1994) A codon-based model of nucleotide substitution for protein-coding DNA sequences. Mol Biol Evol 11: 725–736.

    CAS  PubMed  Google Scholar 

  • Graves JA, Westerman M (2002) Marsupial genetics and genomics. Trends Genet 18: 517–521.

    CAS  PubMed  Google Scholar 

  • Grützner F, Deakin J, Rens W, El-Mogharbel N, Marshall Graves JA (2003) The monotreme genome: a patchwork of reptile, mammal and unique features? Comp Biochem Physiol, A Mol Integr Physiol 136: 867–881.

    Google Scholar 

  • Guttenbach M, Nanda I, Brickell PM et al. (2000) Chromosomal localization of the genes encoding ALDH, BMP-2, R-FABP, IFN-gamma, RXR-gamma, and VIM in chicken by fluorescence in situ hybridization. Cytogenet Cell Genet 88: 266–271.

    Article  CAS  PubMed  Google Scholar 

  • Hamada K, Horiike T, Kanaya S et al. (2002) Changes in body temperature pattern in vertebrates do not influence the codon usages of alpha-globin genes. Genes & Genet Syst 77: 197–207.

    CAS  Google Scholar 

  • Hamada K, Horiike T, Ota H, Mizuno K, Shinozawa T (2003) Presence of isochore structures in reptile genomes suggested by the relationship between GC contents of intron regions and those of coding regions. Genes & Genet Syst 78: 195–198.

    CAS  Google Scholar 

  • Hedges SB, Poling LL (1999) A molecular phylogeny of reptiles. Science 283: 998–1001.

    Article  CAS  PubMed  Google Scholar 

  • Holmquist GP (1989) Evolution of chromosome bands: molecular ecology of noncoding DNA. J Mol Evol 28: 469–486.

    CAS  PubMed  Google Scholar 

  • Hubbard T, Andrews D, Caccamo M et al. (2005) Ensembl 2005. Nucleic Acids Res 33: D447–D453.

    PubMed  Google Scholar 

  • Hughes S, Zelus D, Mouchiroud D (1999) Warm-blooded isochore structure in Nile crocodile and turtle. Mol Biol Evol 16: 1521–1527.

    CAS  PubMed  Google Scholar 

  • Hughes S, Clay O, Bernardi G (2002) Compositional patterns in reptilian genomes. Gene 295: 323–329.

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • International Human Genome Sequence Consortium (IHGSC) (2001) Initial sequencing and analysis of the human genome. Nature 409: 860–921.

    Google Scholar 

  • Iwabe N, Hara Y, Kumazawa Y et al. (2005) Sister group relationship of turtles to the bird–crocodilian clade revealed by nuclear DNA-coded proteins. Mol Biol Evol 22: 810–813.

    CAS  PubMed  Google Scholar 

  • Jaillon O, Aury JM, Brunet F et al. (2004) Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype. Nature 431: 946–957.

    Article  PubMed  Google Scholar 

  • Kadi F, Mouchiroud D, Sabeur G, Bernardi G (1993) The compositional patterns of the avian genomes and their evolutionary implications. J Mol Evol 37: 544–551.

    Article  CAS  Google Scholar 

  • Katoh K, Misawa K, Kuma K, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30: 3059–3066.

    Article  CAS  PubMed  Google Scholar 

  • Kumazawa Y, Nishida M (1999) Complete mitochondrial DNA sequences of the green turtle and blue-tailed mole skink: statistical evidence for archosaurian affinity of turtles. Mol Biol Evol 16: 784–792.

    CAS  PubMed  Google Scholar 

  • Matsuda Y, Chapman VM (1995) Application of fluorescence in situ hybridization in genome analysis of the mouse. Electrophoresis 16: 261–272.

    Article  CAS  PubMed  Google Scholar 

  • Matsuda Y, Nishida-Umehara C, Tarui H et al. (2005) Highly conserved linkage homology between birds and turtles: Bird and turtle chromosomes are precise counterparts of each other. Chromosom Res 13: 601–615.

    CAS  Google Scholar 

  • McQueen HA, Fantes J, Cross SH, Clark VH, Archibald AL, Bird AP (1996) CpG islands of chicken are concentrated on microchromosomes. Nat Genet 12: 321–324.

    Article  CAS  PubMed  Google Scholar 

  • McQueen HA, Siriaco G, Bird AP (1998) Chicken microchromosomes are hyperacetylated, early replicating, and gene rich. Genome Res 8: 621–630.

    CAS  PubMed  Google Scholar 

  • Miyata T, Yasunaga T (1980) Molecular evolution of mRNA: a method for estimating evolutionary rates of synonymous and amino acid substitutions from homologous nucleotide sequences and its application. J Mol Evol 16: 23–36.

    Article  CAS  PubMed  Google Scholar 

  • Mouchiroud D, Gautier C, Bernardi G (1988) The compositional distribution of coding sequences and DNA molecules in humans and murids. J Mol Evol 27: 311–320.

    Article  CAS  PubMed  Google Scholar 

  • Mouse Genome Sequencing Consortium (MGSC) (2002) Initial sequencing and comparative analysis of the mouse genome. Nature 420: 520–562.

    Google Scholar 

  • Musto H, Romero H, Zavala A, Bernardi G (1999) Compositional correlations in the chicken genome. J Mol Evol 49: 325–329.

    CAS  PubMed  Google Scholar 

  • Nei M, Gojobori T (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3: 418–426.

    CAS  PubMed  Google Scholar 

  • Norris TB, Rickards GK, Daugherty CH (2004) Chromosomes of tuatara, Sphenodon, a chromosome heteromorphism and an archaic reptilian karyotype. Cytogenet Genome Res 105: 93– 99.

    Article  CAS  PubMed  Google Scholar 

  • Phillips MJ, Penny D (2003) The root of the mammalian tree inferred from whole mitochondrial genomes. Mol Phylogenet Evol 28: 171–185.

    CAS  PubMed  Google Scholar 

  • Rat Genome Sequencing Project Consortium (RGSPC) (2004) Genome sequence of the Brown Norway rat yields insights into mammalian evolution. Nature 428: 493–521.

    Google Scholar 

  • Rest JS, Ast JC, Austin CC et al. (2003) Molecular systematics of primary reptilian lineages and the tuatara mitochondrial genome. Mol Phylogenet Evol 29: 289–297.

    CAS  PubMed  Google Scholar 

  • Rodionov AV (1996) Micro vs. macro: structural–functional organization of avian micro- and macrochromosomes. Genetika 32: 597–608.

    CAS  PubMed  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406–425.

    CAS  PubMed  Google Scholar 

  • Schmid M, Nanda I, Guttenbach M et al. (2000) First report on chicken genes and chromosomes 2000. Cytogenet Cell Genet 90: 169–218.

    Article  CAS  PubMed  Google Scholar 

  • Smith J, Bruley CK, Paton IR et al. (2000) Differences in gene density on chicken macrochromosomes and microchromosomes. Anim Genet 31: 96–103.

    CAS  PubMed  Google Scholar 

  • Stajich JE, Block D, Boulez K et al. (2002) The Bioperl toolkit: Perl modules for the life sciences. Genome Res 12: 1611– 1618.

    Article  CAS  PubMed  Google Scholar 

  • Suzuki T, Kurosaki T, Shimada K et al. (1999) Cytogenetic mapping of 31 functional genes on chicken chromosomes by direct R-banding FISH. Cytogenet Cell Genet 87: 32–40.

    CAS  PubMed  Google Scholar 

  • Thiery JP, Macaya G, Bernardi G (1976) An analysis of eukaryotic genomes by density gradient centrifugation. J Mol Biol 108: 219–235.

    CAS  PubMed  Google Scholar 

  • Yamada K, Nishida-Umehara C, Matsuda Y (2002) Characterization and chromosomal distribution of novel satellite DNA sequences of the lesser rhea (Pterocnemia pennata) and the greater rhea (Rhea americana). Chromosom Res 10: 513–523.

    CAS  Google Scholar 

  • Yamada K, Nishida-Umehara C, Matsuda Y (2005) Molecular and cytogenetic characterization of site-specific repetitive DNA sequences in the Chinese soft-shelled turtle (Pelodiscus sinensis, Trionychidae). Chromosom Res 13: 33–46.

    CAS  Google Scholar 

  • Yang Z (1997) PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 13: 555–556.

    CAS  PubMed  Google Scholar 

  • Zardoya R, Meyer A (1998) Complete mitochondrial genome suggests diapsid affinities of turtles. Proc Natl Acad Sci USA 95: 14226–14231.

    Article  CAS  PubMed  Google Scholar 

  • Zardoya R, Meyer A (2001) The evolutionary position of turtles revised. Naturwissenschaften 88: 193–200.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Author notes

  1. Kiyokazu Agata

    Present address: Laboratory for Molecular Developmental Biology, Department of Biophysics, Graduate School of Science, Kyoto University, Kyoto, 606-8502, Japan

Authors and Affiliations

  1. Laboratory for Evolutionary Morphology, RIKEN Center for Developmental Biology, 2-2-3 Minatojima-minamimachi, Chuo-ku, Kobe, 650-0047, Japan

    Shigehiro Kuraku & Shigeru Kuratani

  2. Laboratory of Animal Cytogenetics, Division of Genome Dynamics, Creative Research Initiative “Sousei”, Hokkaido University, North 10 West 8, Kita-ku, Sapporo, 060-0810, Japan

    Junko Ishijima, Chizuko Nishida-Umehara & Yoichi Matsuda

  3. Division of Biological Sciences, Graduate School of Science, Hokkaido University, Sapporo, 060-0810, Japan

    Chizuko Nishida-Umehara & Yoichi Matsuda

  4. Laboratory for Evolutionary Regeneration Biology, RIKEN Center for Developmental Biology, 2-2-3 Minatojima-minamimachi, Chuo-ku, Kobe, 650-0047, Japan

    Kiyokazu Agata

Authors
  1. Shigehiro Kuraku
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Junko Ishijima
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Chizuko Nishida-Umehara
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kiyokazu Agata
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Shigeru Kuratani
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yoichi Matsuda
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Shigehiro Kuraku.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kuraku, S., Ishijima, J., Nishida-Umehara, C. et al. cDNA-based gene mapping and GC3 profiling in the soft-shelled turtle suggest a chromosomal size-dependent GC bias shared by sauropsids. Chromosome Res 14, 187–202 (2006). https://doi.org/10.1007/s10577-006-1035-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10577-006-1035-8

Key words

Search

Navigation