Intra-genomic GC heterogeneity in sauropsids: Evolutionary insights from cDNA mapping and GC3 profiling in snake

Kazumi Matsubara, Shigehiro Kuraku, Hiroshi Tarui, Osamu Nishimura, Chizuko Nishida, Kiyokazu Agata, Yoshinori Kumazawa, Yoichi Matsuda

    Research output: Contribution to journalArticle

    22 Citations (Scopus)

    Abstract

    Background Extant sauropsids (reptiles and birds) are divided into two major lineages, the lineage of Testudines (turtles) and Archosauria (crocodilians and birds) and the lineage of Lepidosauria (tuatara, lizards, worm lizards and snakes). Karyotypes of these sauropsidan groups generally consist of macrochromosomes and microchromosomes. In chicken, microchromosomes exhibit a higher GC-content than macrochromosomes. To examine the pattern of intra-genomic GC heterogeneity in lepidosaurian genomes, we constructed a cytogenetic map of the Japanese four-striped rat snake (Elaphe quadrivirgata) with 183 cDNA clones by fluorescence in situ hybridization, and examined the correlation between the GC-content of exonic third codon positions (GC3) of the genes and the size of chromosomes on which the genes were localized. Results Although GC3 distribution of snake genes was relatively homogeneous compared with those of the other amniotes, microchromosomal genes showed significantly higher GC3 than macrochromosomal genes as in chicken. Our snake cytogenetic map also identified several conserved segments between the snake macrochromosomes and the chicken microchromosomes. Cross-species comparisons revealed that GC3 of most snake orthologs in such macrochromosomal segments were GC-poor (GC3 < 50%) whereas those of chicken orthologs in microchromosomes were relatively GC-rich (GC3 ≥ 50%). Conclusion Our results suggest that the chromosome size-dependent GC heterogeneity had already occurred before the lepidosaur-archosaur split, 275 million years ago. This character was probably present in the common ancestor of lepidosaurs and but lost in the lineage leading to Anolis during the diversification of lepidosaurs. We also identified several genes whose GC-content might have been influenced by the size of the chromosomes on which they were harbored over the course of sauropsid evolution.
    Original languageEnglish
    Pages (from-to)1-14
    Number of pages14
    JournalBMC Genomics
    Volume13
    DOIs
    Publication statusPublished - 2012

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    Snakes
    Complementary DNA
    Chickens
    Base Composition
    Lizards
    Chromosomes
    Genes
    Cytogenetics
    Birds
    Turtles
    Reptiles
    Gene Order
    Fluorescence In Situ Hybridization
    Karyotype
    Codon
    Clone Cells
    Genome

    Cite this

    Matsubara, K., Kuraku, S., Tarui, H., Nishimura, O., Nishida, C., Agata, K., ... Matsuda, Y. (2012). Intra-genomic GC heterogeneity in sauropsids: Evolutionary insights from cDNA mapping and GC3 profiling in snake. BMC Genomics, 13, 1-14. https://doi.org/10.1186/1471-2164-13-604
    Matsubara, Kazumi ; Kuraku, Shigehiro ; Tarui, Hiroshi ; Nishimura, Osamu ; Nishida, Chizuko ; Agata, Kiyokazu ; Kumazawa, Yoshinori ; Matsuda, Yoichi. / Intra-genomic GC heterogeneity in sauropsids: Evolutionary insights from cDNA mapping and GC3 profiling in snake. In: BMC Genomics. 2012 ; Vol. 13. pp. 1-14.
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    title = "Intra-genomic GC heterogeneity in sauropsids: Evolutionary insights from cDNA mapping and GC3 profiling in snake",
    abstract = "Background Extant sauropsids (reptiles and birds) are divided into two major lineages, the lineage of Testudines (turtles) and Archosauria (crocodilians and birds) and the lineage of Lepidosauria (tuatara, lizards, worm lizards and snakes). Karyotypes of these sauropsidan groups generally consist of macrochromosomes and microchromosomes. In chicken, microchromosomes exhibit a higher GC-content than macrochromosomes. To examine the pattern of intra-genomic GC heterogeneity in lepidosaurian genomes, we constructed a cytogenetic map of the Japanese four-striped rat snake (Elaphe quadrivirgata) with 183 cDNA clones by fluorescence in situ hybridization, and examined the correlation between the GC-content of exonic third codon positions (GC3) of the genes and the size of chromosomes on which the genes were localized. Results Although GC3 distribution of snake genes was relatively homogeneous compared with those of the other amniotes, microchromosomal genes showed significantly higher GC3 than macrochromosomal genes as in chicken. Our snake cytogenetic map also identified several conserved segments between the snake macrochromosomes and the chicken microchromosomes. Cross-species comparisons revealed that GC3 of most snake orthologs in such macrochromosomal segments were GC-poor (GC3 < 50{\%}) whereas those of chicken orthologs in microchromosomes were relatively GC-rich (GC3 ≥ 50{\%}). Conclusion Our results suggest that the chromosome size-dependent GC heterogeneity had already occurred before the lepidosaur-archosaur split, 275 million years ago. This character was probably present in the common ancestor of lepidosaurs and but lost in the lineage leading to Anolis during the diversification of lepidosaurs. We also identified several genes whose GC-content might have been influenced by the size of the chromosomes on which they were harbored over the course of sauropsid evolution.",
    author = "Kazumi Matsubara and Shigehiro Kuraku and Hiroshi Tarui and Osamu Nishimura and Chizuko Nishida and Kiyokazu Agata and Yoshinori Kumazawa and Yoichi Matsuda",
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    Matsubara, K, Kuraku, S, Tarui, H, Nishimura, O, Nishida, C, Agata, K, Kumazawa, Y & Matsuda, Y 2012, 'Intra-genomic GC heterogeneity in sauropsids: Evolutionary insights from cDNA mapping and GC3 profiling in snake', BMC Genomics, vol. 13, pp. 1-14. https://doi.org/10.1186/1471-2164-13-604

    Intra-genomic GC heterogeneity in sauropsids: Evolutionary insights from cDNA mapping and GC3 profiling in snake. / Matsubara, Kazumi; Kuraku, Shigehiro; Tarui, Hiroshi; Nishimura, Osamu; Nishida, Chizuko; Agata, Kiyokazu; Kumazawa, Yoshinori; Matsuda, Yoichi.

    In: BMC Genomics, Vol. 13, 2012, p. 1-14.

    Research output: Contribution to journalArticle

    TY - JOUR

    T1 - Intra-genomic GC heterogeneity in sauropsids: Evolutionary insights from cDNA mapping and GC3 profiling in snake

    AU - Matsubara, Kazumi

    AU - Kuraku, Shigehiro

    AU - Tarui, Hiroshi

    AU - Nishimura, Osamu

    AU - Nishida, Chizuko

    AU - Agata, Kiyokazu

    AU - Kumazawa, Yoshinori

    AU - Matsuda, Yoichi

    PY - 2012

    Y1 - 2012

    N2 - Background Extant sauropsids (reptiles and birds) are divided into two major lineages, the lineage of Testudines (turtles) and Archosauria (crocodilians and birds) and the lineage of Lepidosauria (tuatara, lizards, worm lizards and snakes). Karyotypes of these sauropsidan groups generally consist of macrochromosomes and microchromosomes. In chicken, microchromosomes exhibit a higher GC-content than macrochromosomes. To examine the pattern of intra-genomic GC heterogeneity in lepidosaurian genomes, we constructed a cytogenetic map of the Japanese four-striped rat snake (Elaphe quadrivirgata) with 183 cDNA clones by fluorescence in situ hybridization, and examined the correlation between the GC-content of exonic third codon positions (GC3) of the genes and the size of chromosomes on which the genes were localized. Results Although GC3 distribution of snake genes was relatively homogeneous compared with those of the other amniotes, microchromosomal genes showed significantly higher GC3 than macrochromosomal genes as in chicken. Our snake cytogenetic map also identified several conserved segments between the snake macrochromosomes and the chicken microchromosomes. Cross-species comparisons revealed that GC3 of most snake orthologs in such macrochromosomal segments were GC-poor (GC3 < 50%) whereas those of chicken orthologs in microchromosomes were relatively GC-rich (GC3 ≥ 50%). Conclusion Our results suggest that the chromosome size-dependent GC heterogeneity had already occurred before the lepidosaur-archosaur split, 275 million years ago. This character was probably present in the common ancestor of lepidosaurs and but lost in the lineage leading to Anolis during the diversification of lepidosaurs. We also identified several genes whose GC-content might have been influenced by the size of the chromosomes on which they were harbored over the course of sauropsid evolution.

    AB - Background Extant sauropsids (reptiles and birds) are divided into two major lineages, the lineage of Testudines (turtles) and Archosauria (crocodilians and birds) and the lineage of Lepidosauria (tuatara, lizards, worm lizards and snakes). Karyotypes of these sauropsidan groups generally consist of macrochromosomes and microchromosomes. In chicken, microchromosomes exhibit a higher GC-content than macrochromosomes. To examine the pattern of intra-genomic GC heterogeneity in lepidosaurian genomes, we constructed a cytogenetic map of the Japanese four-striped rat snake (Elaphe quadrivirgata) with 183 cDNA clones by fluorescence in situ hybridization, and examined the correlation between the GC-content of exonic third codon positions (GC3) of the genes and the size of chromosomes on which the genes were localized. Results Although GC3 distribution of snake genes was relatively homogeneous compared with those of the other amniotes, microchromosomal genes showed significantly higher GC3 than macrochromosomal genes as in chicken. Our snake cytogenetic map also identified several conserved segments between the snake macrochromosomes and the chicken microchromosomes. Cross-species comparisons revealed that GC3 of most snake orthologs in such macrochromosomal segments were GC-poor (GC3 < 50%) whereas those of chicken orthologs in microchromosomes were relatively GC-rich (GC3 ≥ 50%). Conclusion Our results suggest that the chromosome size-dependent GC heterogeneity had already occurred before the lepidosaur-archosaur split, 275 million years ago. This character was probably present in the common ancestor of lepidosaurs and but lost in the lineage leading to Anolis during the diversification of lepidosaurs. We also identified several genes whose GC-content might have been influenced by the size of the chromosomes on which they were harbored over the course of sauropsid evolution.

    U2 - 10.1186/1471-2164-13-604

    DO - 10.1186/1471-2164-13-604

    M3 - Article

    VL - 13

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    EP - 14

    JO - BMC Genomics

    JF - BMC Genomics

    SN - 1471-2164

    ER -