Inference of the Protokaryotypes of Amniotes and Tetrapods and the Evolutionary Processes of Microchromosomes from Comparative Gene Mapping

Yoshinobu Uno, Chizuko Nishida, Hiroshi Tarui, Satoshi Ishishita, Chiyo Takagi, Osamu Nishimura, Junko Ishijima, Hidetoshi Ota, Ayumi Kosaka, Kazumi Matsubara, Yasunori Murakami, Shigeru Kuratani, Naoto Ueno, Kiyokazu Agata, Yoichi Matsuda

    Research output: Contribution to journalArticle

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    Abstract

    Comparative genome analysis of non-avian reptiles and amphibians provides important clues about the process of genome evolution in tetrapods. However, there is still only limited information available on the genome structures of these organisms. Consequently, the protokaryotypes of amniotes and tetrapods and the evolutionary processes of microchromosomes in tetrapods remain poorly understood. We constructed chromosome maps of functional genes for the Chinese soft-shelled turtle (Pelodiscus sinensis), the Siamese crocodile (Crocodylus siamensis), and the Western clawed frog (Xenopus tropicalis) and compared them with genome and/or chromosome maps of other tetrapod species (salamander, lizard, snake, chicken, and human). This is the first report on the protokaryotypes of amniotes and tetrapods and the evolutionary processes of microchromosomes inferred from comparative genomic analysis of vertebrates, which cover all major non-avian reptilian taxa (Squamata, Crocodilia, Testudines). The eight largest macrochromosomes of the turtle and chicken were equivalent, and 11 linkage groups had also remained intact in the crocodile. Linkage groups of the chicken macrochromosomes were also highly conserved in X. tropicalis, two squamates, and the salamander, but not in human. Chicken microchromosomal linkages were conserved in the squamates, which have fewer microchromosomes than chicken, and also in Xenopus and the salamander, which both lack microchromosomes; in the latter, the chicken microchromosomal segments have been integrated into macrochromosomes. Our present findings open up the possibility that the ancestral amniotes and tetrapods had at least 10 large genetic linkage groups and many microchromosomes, which corresponded to the chicken macro- and microchromosomes, respectively. The turtle and chicken might retain the microchromosomes of the amniote protokaryotype almost intact. The decrease in number and/or disappearance of microchromosomes by repeated chromosomal fusions probably occurred independently in the amphibian, squamate, crocodilian, and mammalian lineages
    Original languageEnglish
    Pages (from-to)1-12
    Number of pages12
    JournalPLoS One
    Volume7
    Issue number12
    DOIs
    Publication statusPublished - 2012

    Fingerprint

    Chromosome Mapping
    chromosome mapping
    Chickens
    Genes
    chickens
    Squamata
    Urodela
    Turtles
    Crocodylus siamensis
    Chromosomes
    Pelodiscus sinensis
    salamanders and newts
    linkage groups
    Crocodylia
    Genome
    Alligators and Crocodiles
    genome
    Amphibians
    Xenopus
    turtles

    Cite this

    Uno, Yoshinobu ; Nishida, Chizuko ; Tarui, Hiroshi ; Ishishita, Satoshi ; Takagi, Chiyo ; Nishimura, Osamu ; Ishijima, Junko ; Ota, Hidetoshi ; Kosaka, Ayumi ; Matsubara, Kazumi ; Murakami, Yasunori ; Kuratani, Shigeru ; Ueno, Naoto ; Agata, Kiyokazu ; Matsuda, Yoichi. / Inference of the Protokaryotypes of Amniotes and Tetrapods and the Evolutionary Processes of Microchromosomes from Comparative Gene Mapping. In: PLoS One. 2012 ; Vol. 7, No. 12. pp. 1-12.
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    abstract = "Comparative genome analysis of non-avian reptiles and amphibians provides important clues about the process of genome evolution in tetrapods. However, there is still only limited information available on the genome structures of these organisms. Consequently, the protokaryotypes of amniotes and tetrapods and the evolutionary processes of microchromosomes in tetrapods remain poorly understood. We constructed chromosome maps of functional genes for the Chinese soft-shelled turtle (Pelodiscus sinensis), the Siamese crocodile (Crocodylus siamensis), and the Western clawed frog (Xenopus tropicalis) and compared them with genome and/or chromosome maps of other tetrapod species (salamander, lizard, snake, chicken, and human). This is the first report on the protokaryotypes of amniotes and tetrapods and the evolutionary processes of microchromosomes inferred from comparative genomic analysis of vertebrates, which cover all major non-avian reptilian taxa (Squamata, Crocodilia, Testudines). The eight largest macrochromosomes of the turtle and chicken were equivalent, and 11 linkage groups had also remained intact in the crocodile. Linkage groups of the chicken macrochromosomes were also highly conserved in X. tropicalis, two squamates, and the salamander, but not in human. Chicken microchromosomal linkages were conserved in the squamates, which have fewer microchromosomes than chicken, and also in Xenopus and the salamander, which both lack microchromosomes; in the latter, the chicken microchromosomal segments have been integrated into macrochromosomes. Our present findings open up the possibility that the ancestral amniotes and tetrapods had at least 10 large genetic linkage groups and many microchromosomes, which corresponded to the chicken macro- and microchromosomes, respectively. The turtle and chicken might retain the microchromosomes of the amniote protokaryotype almost intact. The decrease in number and/or disappearance of microchromosomes by repeated chromosomal fusions probably occurred independently in the amphibian, squamate, crocodilian, and mammalian lineages",
    keywords = "Chickens, Chromosome mapping, Homologous chromosomes, Amniotes, Genetic linkage, Amphibian genomics, Reptile genomics, Salamanders",
    author = "Yoshinobu Uno and Chizuko Nishida and Hiroshi Tarui and Satoshi Ishishita and Chiyo Takagi and Osamu Nishimura and Junko Ishijima and Hidetoshi Ota and Ayumi Kosaka and Kazumi Matsubara and Yasunori Murakami and Shigeru Kuratani and Naoto Ueno and Kiyokazu Agata and Yoichi Matsuda",
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    Uno, Y, Nishida, C, Tarui, H, Ishishita, S, Takagi, C, Nishimura, O, Ishijima, J, Ota, H, Kosaka, A, Matsubara, K, Murakami, Y, Kuratani, S, Ueno, N, Agata, K & Matsuda, Y 2012, 'Inference of the Protokaryotypes of Amniotes and Tetrapods and the Evolutionary Processes of Microchromosomes from Comparative Gene Mapping', PLoS One, vol. 7, no. 12, pp. 1-12. https://doi.org/10.1371/journal.pone.0053027

    Inference of the Protokaryotypes of Amniotes and Tetrapods and the Evolutionary Processes of Microchromosomes from Comparative Gene Mapping. / Uno, Yoshinobu; Nishida, Chizuko; Tarui, Hiroshi; Ishishita, Satoshi; Takagi, Chiyo; Nishimura, Osamu; Ishijima, Junko; Ota, Hidetoshi; Kosaka, Ayumi; Matsubara, Kazumi; Murakami, Yasunori; Kuratani, Shigeru; Ueno, Naoto; Agata, Kiyokazu; Matsuda, Yoichi.

    In: PLoS One, Vol. 7, No. 12, 2012, p. 1-12.

    Research output: Contribution to journalArticle

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    T1 - Inference of the Protokaryotypes of Amniotes and Tetrapods and the Evolutionary Processes of Microchromosomes from Comparative Gene Mapping

    AU - Uno, Yoshinobu

    AU - Nishida, Chizuko

    AU - Tarui, Hiroshi

    AU - Ishishita, Satoshi

    AU - Takagi, Chiyo

    AU - Nishimura, Osamu

    AU - Ishijima, Junko

    AU - Ota, Hidetoshi

    AU - Kosaka, Ayumi

    AU - Matsubara, Kazumi

    AU - Murakami, Yasunori

    AU - Kuratani, Shigeru

    AU - Ueno, Naoto

    AU - Agata, Kiyokazu

    AU - Matsuda, Yoichi

    PY - 2012

    Y1 - 2012

    N2 - Comparative genome analysis of non-avian reptiles and amphibians provides important clues about the process of genome evolution in tetrapods. However, there is still only limited information available on the genome structures of these organisms. Consequently, the protokaryotypes of amniotes and tetrapods and the evolutionary processes of microchromosomes in tetrapods remain poorly understood. We constructed chromosome maps of functional genes for the Chinese soft-shelled turtle (Pelodiscus sinensis), the Siamese crocodile (Crocodylus siamensis), and the Western clawed frog (Xenopus tropicalis) and compared them with genome and/or chromosome maps of other tetrapod species (salamander, lizard, snake, chicken, and human). This is the first report on the protokaryotypes of amniotes and tetrapods and the evolutionary processes of microchromosomes inferred from comparative genomic analysis of vertebrates, which cover all major non-avian reptilian taxa (Squamata, Crocodilia, Testudines). The eight largest macrochromosomes of the turtle and chicken were equivalent, and 11 linkage groups had also remained intact in the crocodile. Linkage groups of the chicken macrochromosomes were also highly conserved in X. tropicalis, two squamates, and the salamander, but not in human. Chicken microchromosomal linkages were conserved in the squamates, which have fewer microchromosomes than chicken, and also in Xenopus and the salamander, which both lack microchromosomes; in the latter, the chicken microchromosomal segments have been integrated into macrochromosomes. Our present findings open up the possibility that the ancestral amniotes and tetrapods had at least 10 large genetic linkage groups and many microchromosomes, which corresponded to the chicken macro- and microchromosomes, respectively. The turtle and chicken might retain the microchromosomes of the amniote protokaryotype almost intact. The decrease in number and/or disappearance of microchromosomes by repeated chromosomal fusions probably occurred independently in the amphibian, squamate, crocodilian, and mammalian lineages

    AB - Comparative genome analysis of non-avian reptiles and amphibians provides important clues about the process of genome evolution in tetrapods. However, there is still only limited information available on the genome structures of these organisms. Consequently, the protokaryotypes of amniotes and tetrapods and the evolutionary processes of microchromosomes in tetrapods remain poorly understood. We constructed chromosome maps of functional genes for the Chinese soft-shelled turtle (Pelodiscus sinensis), the Siamese crocodile (Crocodylus siamensis), and the Western clawed frog (Xenopus tropicalis) and compared them with genome and/or chromosome maps of other tetrapod species (salamander, lizard, snake, chicken, and human). This is the first report on the protokaryotypes of amniotes and tetrapods and the evolutionary processes of microchromosomes inferred from comparative genomic analysis of vertebrates, which cover all major non-avian reptilian taxa (Squamata, Crocodilia, Testudines). The eight largest macrochromosomes of the turtle and chicken were equivalent, and 11 linkage groups had also remained intact in the crocodile. Linkage groups of the chicken macrochromosomes were also highly conserved in X. tropicalis, two squamates, and the salamander, but not in human. Chicken microchromosomal linkages were conserved in the squamates, which have fewer microchromosomes than chicken, and also in Xenopus and the salamander, which both lack microchromosomes; in the latter, the chicken microchromosomal segments have been integrated into macrochromosomes. Our present findings open up the possibility that the ancestral amniotes and tetrapods had at least 10 large genetic linkage groups and many microchromosomes, which corresponded to the chicken macro- and microchromosomes, respectively. The turtle and chicken might retain the microchromosomes of the amniote protokaryotype almost intact. The decrease in number and/or disappearance of microchromosomes by repeated chromosomal fusions probably occurred independently in the amphibian, squamate, crocodilian, and mammalian lineages

    KW - Chickens

    KW - Chromosome mapping

    KW - Homologous chromosomes

    KW - Amniotes

    KW - Genetic linkage

    KW - Amphibian genomics

    KW - Reptile genomics

    KW - Salamanders

    U2 - 10.1371/journal.pone.0053027

    DO - 10.1371/journal.pone.0053027

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    JO - PLoS One

    JF - PLoS One

    SN - 1932-6203

    IS - 12

    ER -