Comparative Genome Analyses Reveal Distinct Structure in the Saltwater Crocodile MHC

Weerachai Jaratlerdsiri, Janine DEAKIN, Ricardo Godinez.M, Xueyan Shan, Daniel Peterson, Sylvain Marthey, Eric Lyons, Fiona McCarthy, Sally Isberg, Damien Higgins, Amanda Chong, John St John, Travis Glenn, David A. Ray, Jaime Gongora

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    Abstract

    The major histocompatibility complex (MHC) is a dynamic genome region with an essential role in the adaptive immunity of vertebrates, especially antigen presentation. The MHC is generally divided into subregions (classes I, II and III) containing genes of similar function across species, but with different gene number and organisation. Crocodylia (crocodilians) are widely distributed and represent an evolutionary distinct group among higher vertebrates, but the genomic organisation of MHC within this lineage has been largely unexplored. Here, we studied the MHC region of the saltwater crocodile (Crocodylus porosus) and compared it with that of other taxa. We characterised genomic clusters encompassing MHC class I and class II genes in the saltwater crocodile based on sequencing of bacterial artificial chromosomes. Six gene clusters spanning ,452 kb were identified to contain nine MHC class I genes, six MHC class II genes, three TAP genes, and a TRIM gene. These MHC class I and class II genes were in separate scaffold regions and were greater in length (2–6 times longer) than their counterparts in well-studied fowl B loci, suggesting that the compaction of avian MHC occurred after the crocodilianavian split. Comparative analyses between the saltwater crocodile MHC and that from the alligator and gharial showed large syntenic areas (.80% identity) with similar gene order. Comparisons with other vertebrates showed that the saltwater crocodile had MHC class I genes located along with TAP, consistent with birds studied. Linkage between MHC class I and TRIM39 observed in the saltwater crocodile resembled MHC in eutherians compared, but absent in avian MHC, suggesting that the saltwater crocodile MHC appears to have gene organisation intermediate between these two lineages. These observations suggest that the structure of the saltwater crocodile MHC, and other crocodilians, can help determine the MHC that was present in the ancestors of archosaurs.
    Original languageEnglish
    Pages (from-to)1-33
    Number of pages33
    JournalPLoS One
    Volume9
    Issue number12
    DOIs
    Publication statusPublished - 2014

    Fingerprint

    Crocodylus porosus
    Alligators and Crocodiles
    major histocompatibility complex
    Major Histocompatibility Complex
    Genes
    Genome
    genome
    Crocodylia
    genes
    MHC Class II Genes
    MHC Class I Genes
    Vertebrates
    vertebrates
    Alligator (Alligatoridae)
    Birds
    Chromosomes
    genomics
    Bacterial Artificial Chromosomes
    Scaffolds
    antigen presentation

    Cite this

    Jaratlerdsiri, W., DEAKIN, J., Godinez.M, R., Shan, X., Peterson, D., Marthey, S., ... Gongora, J. (2014). Comparative Genome Analyses Reveal Distinct Structure in the Saltwater Crocodile MHC. PLoS One, 9(12), 1-33. https://doi.org/10.1371/journal.pone.0114631
    Jaratlerdsiri, Weerachai ; DEAKIN, Janine ; Godinez.M, Ricardo ; Shan, Xueyan ; Peterson, Daniel ; Marthey, Sylvain ; Lyons, Eric ; McCarthy, Fiona ; Isberg, Sally ; Higgins, Damien ; Chong, Amanda ; St John, John ; Glenn, Travis ; Ray, David A. ; Gongora, Jaime. / Comparative Genome Analyses Reveal Distinct Structure in the Saltwater Crocodile MHC. In: PLoS One. 2014 ; Vol. 9, No. 12. pp. 1-33.
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    title = "Comparative Genome Analyses Reveal Distinct Structure in the Saltwater Crocodile MHC",
    abstract = "The major histocompatibility complex (MHC) is a dynamic genome region with an essential role in the adaptive immunity of vertebrates, especially antigen presentation. The MHC is generally divided into subregions (classes I, II and III) containing genes of similar function across species, but with different gene number and organisation. Crocodylia (crocodilians) are widely distributed and represent an evolutionary distinct group among higher vertebrates, but the genomic organisation of MHC within this lineage has been largely unexplored. Here, we studied the MHC region of the saltwater crocodile (Crocodylus porosus) and compared it with that of other taxa. We characterised genomic clusters encompassing MHC class I and class II genes in the saltwater crocodile based on sequencing of bacterial artificial chromosomes. Six gene clusters spanning ,452 kb were identified to contain nine MHC class I genes, six MHC class II genes, three TAP genes, and a TRIM gene. These MHC class I and class II genes were in separate scaffold regions and were greater in length (2–6 times longer) than their counterparts in well-studied fowl B loci, suggesting that the compaction of avian MHC occurred after the crocodilianavian split. Comparative analyses between the saltwater crocodile MHC and that from the alligator and gharial showed large syntenic areas (.80{\%} identity) with similar gene order. Comparisons with other vertebrates showed that the saltwater crocodile had MHC class I genes located along with TAP, consistent with birds studied. Linkage between MHC class I and TRIM39 observed in the saltwater crocodile resembled MHC in eutherians compared, but absent in avian MHC, suggesting that the saltwater crocodile MHC appears to have gene organisation intermediate between these two lineages. These observations suggest that the structure of the saltwater crocodile MHC, and other crocodilians, can help determine the MHC that was present in the ancestors of archosaurs.",
    keywords = "major histocompatibility complex (MHC), crocodiles, antigen presentation, MHC class I genes, bird genomics, genome evolution, genomic library screening, genetic loci",
    author = "Weerachai Jaratlerdsiri and Janine DEAKIN and Ricardo Godinez.M and Xueyan Shan and Daniel Peterson and Sylvain Marthey and Eric Lyons and Fiona McCarthy and Sally Isberg and Damien Higgins and Amanda Chong and {St John}, John and Travis Glenn and Ray, {David A.} and Jaime Gongora",
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    Jaratlerdsiri, W, DEAKIN, J, Godinez.M, R, Shan, X, Peterson, D, Marthey, S, Lyons, E, McCarthy, F, Isberg, S, Higgins, D, Chong, A, St John, J, Glenn, T, Ray, DA & Gongora, J 2014, 'Comparative Genome Analyses Reveal Distinct Structure in the Saltwater Crocodile MHC', PLoS One, vol. 9, no. 12, pp. 1-33. https://doi.org/10.1371/journal.pone.0114631

    Comparative Genome Analyses Reveal Distinct Structure in the Saltwater Crocodile MHC. / Jaratlerdsiri, Weerachai; DEAKIN, Janine; Godinez.M, Ricardo; Shan, Xueyan; Peterson, Daniel; Marthey, Sylvain; Lyons, Eric; McCarthy, Fiona; Isberg, Sally; Higgins, Damien; Chong, Amanda; St John, John; Glenn, Travis; Ray, David A.; Gongora, Jaime.

    In: PLoS One, Vol. 9, No. 12, 2014, p. 1-33.

    Research output: Contribution to journalArticle

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    T1 - Comparative Genome Analyses Reveal Distinct Structure in the Saltwater Crocodile MHC

    AU - Jaratlerdsiri, Weerachai

    AU - DEAKIN, Janine

    AU - Godinez.M, Ricardo

    AU - Shan, Xueyan

    AU - Peterson, Daniel

    AU - Marthey, Sylvain

    AU - Lyons, Eric

    AU - McCarthy, Fiona

    AU - Isberg, Sally

    AU - Higgins, Damien

    AU - Chong, Amanda

    AU - St John, John

    AU - Glenn, Travis

    AU - Ray, David A.

    AU - Gongora, Jaime

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    N2 - The major histocompatibility complex (MHC) is a dynamic genome region with an essential role in the adaptive immunity of vertebrates, especially antigen presentation. The MHC is generally divided into subregions (classes I, II and III) containing genes of similar function across species, but with different gene number and organisation. Crocodylia (crocodilians) are widely distributed and represent an evolutionary distinct group among higher vertebrates, but the genomic organisation of MHC within this lineage has been largely unexplored. Here, we studied the MHC region of the saltwater crocodile (Crocodylus porosus) and compared it with that of other taxa. We characterised genomic clusters encompassing MHC class I and class II genes in the saltwater crocodile based on sequencing of bacterial artificial chromosomes. Six gene clusters spanning ,452 kb were identified to contain nine MHC class I genes, six MHC class II genes, three TAP genes, and a TRIM gene. These MHC class I and class II genes were in separate scaffold regions and were greater in length (2–6 times longer) than their counterparts in well-studied fowl B loci, suggesting that the compaction of avian MHC occurred after the crocodilianavian split. Comparative analyses between the saltwater crocodile MHC and that from the alligator and gharial showed large syntenic areas (.80% identity) with similar gene order. Comparisons with other vertebrates showed that the saltwater crocodile had MHC class I genes located along with TAP, consistent with birds studied. Linkage between MHC class I and TRIM39 observed in the saltwater crocodile resembled MHC in eutherians compared, but absent in avian MHC, suggesting that the saltwater crocodile MHC appears to have gene organisation intermediate between these two lineages. These observations suggest that the structure of the saltwater crocodile MHC, and other crocodilians, can help determine the MHC that was present in the ancestors of archosaurs.

    AB - The major histocompatibility complex (MHC) is a dynamic genome region with an essential role in the adaptive immunity of vertebrates, especially antigen presentation. The MHC is generally divided into subregions (classes I, II and III) containing genes of similar function across species, but with different gene number and organisation. Crocodylia (crocodilians) are widely distributed and represent an evolutionary distinct group among higher vertebrates, but the genomic organisation of MHC within this lineage has been largely unexplored. Here, we studied the MHC region of the saltwater crocodile (Crocodylus porosus) and compared it with that of other taxa. We characterised genomic clusters encompassing MHC class I and class II genes in the saltwater crocodile based on sequencing of bacterial artificial chromosomes. Six gene clusters spanning ,452 kb were identified to contain nine MHC class I genes, six MHC class II genes, three TAP genes, and a TRIM gene. These MHC class I and class II genes were in separate scaffold regions and were greater in length (2–6 times longer) than their counterparts in well-studied fowl B loci, suggesting that the compaction of avian MHC occurred after the crocodilianavian split. Comparative analyses between the saltwater crocodile MHC and that from the alligator and gharial showed large syntenic areas (.80% identity) with similar gene order. Comparisons with other vertebrates showed that the saltwater crocodile had MHC class I genes located along with TAP, consistent with birds studied. Linkage between MHC class I and TRIM39 observed in the saltwater crocodile resembled MHC in eutherians compared, but absent in avian MHC, suggesting that the saltwater crocodile MHC appears to have gene organisation intermediate between these two lineages. These observations suggest that the structure of the saltwater crocodile MHC, and other crocodilians, can help determine the MHC that was present in the ancestors of archosaurs.

    KW - major histocompatibility complex (MHC)

    KW - crocodiles

    KW - antigen presentation

    KW - MHC class I genes

    KW - bird genomics

    KW - genome evolution

    KW - genomic library screening

    KW - genetic loci

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