Chromosome Research

, Volume 14, Issue 2, pp 187–202 | Cite as

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

  • Shigehiro Kuraku
  • Junko Ishijima
  • Chizuko Nishida-Umehara
  • Kiyokazu Agata
  • Shigeru Kuratani
  • Yoichi Matsuda
Article

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.

Key words

GC-content microchromosome sauropsida turtle 

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References

  1. 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.CrossRefPubMedGoogle Scholar
  2. 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.Google Scholar
  3. 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.CrossRefPubMedGoogle Scholar
  4. Auer H, Mayr B, Lambrou M, Schleger W (1987) An extended chicken karyotype, including the NOR chromosome. Cytogenet Cell Genet 45: 218–221.PubMedGoogle Scholar
  5. 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.CrossRefPubMedGoogle Scholar
  6. Bernardi G (2000) Isochores and the evolutionary genomics of vertebrates. Gene 241: 3–17.PubMedGoogle Scholar
  7. Bernardi G, Olofsson B, Filipski J et al. (1985) The mosaic genome of warm-blooded vertebrates. Science 228: 953–958.PubMedGoogle Scholar
  8. Burt DW (2002) Origin and evolution of avian microchromosomes. Cytogenet Genome Res 96: 97–112.CrossRefPubMedGoogle Scholar
  9. 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.PubMedGoogle Scholar
  10. Clay O, Caccio S, Zoubak S, Mouchiroud D, Bernardi G (1996) Human coding and noncoding DNA: compositional correlations. Mol Phylogenet Evol 5: 2–12.PubMedGoogle Scholar
  11. Cohen MM, Gans C (1970) The chromosomes of the order Crocodilia. Cytogenetics 9: 81–105.PubMedGoogle Scholar
  12. 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
  13. 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.CrossRefPubMedGoogle Scholar
  14. Eyre-Walker A, Hurst LD (2001) The evolution of isochores. Nat Rev, Genet 2: 549–555.CrossRefGoogle Scholar
  15. Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17: 368–376.CrossRefPubMedGoogle Scholar
  16. 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.PubMedGoogle Scholar
  17. Goldman N, Yang Z (1994) A codon-based model of nucleotide substitution for protein-coding DNA sequences. Mol Biol Evol 11: 725–736.PubMedGoogle Scholar
  18. Graves JA, Westerman M (2002) Marsupial genetics and genomics. Trends Genet 18: 517–521.PubMedGoogle Scholar
  19. 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
  20. 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.CrossRefPubMedGoogle Scholar
  21. 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.Google Scholar
  22. 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.Google Scholar
  23. Hedges SB, Poling LL (1999) A molecular phylogeny of reptiles. Science 283: 998–1001.CrossRefPubMedGoogle Scholar
  24. Holmquist GP (1989) Evolution of chromosome bands: molecular ecology of noncoding DNA. J Mol Evol 28: 469–486.PubMedGoogle Scholar
  25. Hubbard T, Andrews D, Caccamo M et al. (2005) Ensembl 2005. Nucleic Acids Res 33: D447–D453.PubMedGoogle Scholar
  26. Hughes S, Zelus D, Mouchiroud D (1999) Warm-blooded isochore structure in Nile crocodile and turtle. Mol Biol Evol 16: 1521–1527.PubMedGoogle Scholar
  27. Hughes S, Clay O, Bernardi G (2002) Compositional patterns in reptilian genomes. Gene 295: 323–329.CrossRefPubMedGoogle Scholar
  28. 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
  29. International Human Genome Sequence Consortium (IHGSC) (2001) Initial sequencing and analysis of the human genome. Nature 409: 860–921.Google Scholar
  30. 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.PubMedGoogle Scholar
  31. 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.CrossRefPubMedGoogle Scholar
  32. 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.CrossRefGoogle Scholar
  33. 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.CrossRefPubMedGoogle Scholar
  34. 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.PubMedGoogle Scholar
  35. Matsuda Y, Chapman VM (1995) Application of fluorescence in situ hybridization in genome analysis of the mouse. Electrophoresis 16: 261–272.CrossRefPubMedGoogle Scholar
  36. 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.Google Scholar
  37. 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.CrossRefPubMedGoogle Scholar
  38. McQueen HA, Siriaco G, Bird AP (1998) Chicken microchromosomes are hyperacetylated, early replicating, and gene rich. Genome Res 8: 621–630.PubMedGoogle Scholar
  39. 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.CrossRefPubMedGoogle Scholar
  40. 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.CrossRefPubMedGoogle Scholar
  41. Mouse Genome Sequencing Consortium (MGSC) (2002) Initial sequencing and comparative analysis of the mouse genome. Nature 420: 520–562.Google Scholar
  42. Musto H, Romero H, Zavala A, Bernardi G (1999) Compositional correlations in the chicken genome. J Mol Evol 49: 325–329.PubMedGoogle Scholar
  43. Nei M, Gojobori T (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3: 418–426.PubMedGoogle Scholar
  44. 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.CrossRefPubMedGoogle Scholar
  45. Phillips MJ, Penny D (2003) The root of the mammalian tree inferred from whole mitochondrial genomes. Mol Phylogenet Evol 28: 171–185.PubMedGoogle Scholar
  46. 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
  47. 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.PubMedGoogle Scholar
  48. Rodionov AV (1996) Micro vs. macro: structural–functional organization of avian micro- and macrochromosomes. Genetika 32: 597–608.PubMedGoogle Scholar
  49. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406–425.PubMedGoogle Scholar
  50. Schmid M, Nanda I, Guttenbach M et al. (2000) First report on chicken genes and chromosomes 2000. Cytogenet Cell Genet 90: 169–218.CrossRefPubMedGoogle Scholar
  51. Smith J, Bruley CK, Paton IR et al. (2000) Differences in gene density on chicken macrochromosomes and microchromosomes. Anim Genet 31: 96–103.PubMedGoogle Scholar
  52. Stajich JE, Block D, Boulez K et al. (2002) The Bioperl toolkit: Perl modules for the life sciences. Genome Res 12: 1611– 1618.CrossRefPubMedGoogle Scholar
  53. 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.PubMedGoogle Scholar
  54. Thiery JP, Macaya G, Bernardi G (1976) An analysis of eukaryotic genomes by density gradient centrifugation. J Mol Biol 108: 219–235.PubMedGoogle Scholar
  55. 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.Google Scholar
  56. 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.Google Scholar
  57. Yang Z (1997) PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 13: 555–556.PubMedGoogle Scholar
  58. Zardoya R, Meyer A (1998) Complete mitochondrial genome suggests diapsid affinities of turtles. Proc Natl Acad Sci USA 95: 14226–14231.CrossRefPubMedGoogle Scholar
  59. Zardoya R, Meyer A (2001) The evolutionary position of turtles revised. Naturwissenschaften 88: 193–200.CrossRefPubMedGoogle Scholar

Copyright information

© Springer 2006

Authors and Affiliations

  • Shigehiro Kuraku
    • 1
  • Junko Ishijima
    • 2
  • Chizuko Nishida-Umehara
    • 2
    • 3
  • Kiyokazu Agata
    • 4
    • 5
  • Shigeru Kuratani
    • 1
  • Yoichi Matsuda
    • 2
    • 3
  1. 1.Laboratory for Evolutionary MorphologyRIKEN Center for Developmental BiologyChuo-kuJapan
  2. 2.Laboratory of Animal Cytogenetics, Division of Genome Dynamics, Creative Research Initiative “Sousei”Hokkaido UniversityKita-kuJapan
  3. 3.Division of Biological Sciences, Graduate School of ScienceHokkaido UniversitySapporoJapan
  4. 4.Laboratory for Evolutionary Regeneration BiologyRIKEN Center for Developmental BiologyChuo-kuJapan
  5. 5.Laboratory for Molecular Developmental Biology, Department of Biophysics, Graduate School of ScienceKyoto UniversityKyotoJapan

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