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Comparative genome analyses reveal distinct structure in the saltwater crocodile MHC.

Jaratlerdsiri W, Deakin J, Godinez RM, Shan X, Peterson DG, Marthey S, Lyons E, McCarthy FM, Isberg SR, Higgins DP, Chong AY, John JS, Glenn TC, Ray DA, Gongora J - PLoS ONE (2014)

Bottom Line: Here, we studied the MHC region of the saltwater crocodile (Crocodylus porosus) and compared it with that of other taxa.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.

View Article: PubMed Central - PubMed

Affiliation: Faculty of Veterinary Science, University of Sydney, Sydney, New South Wales 2006, Australia.

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 crocodilian-avian 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.

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Bayesian phylogenetic analysis of MHC class II B sequences.The fish MHC class II B sequence (Onmy-DAB; FR688148) is used as an outgroup. Brackets on the right show Clades 1 and 2 of the MHC variants from Crocodylia, and six subclades (A–F) for Clade 1. For Subclades A and B, gene lineages are named with ‘DAB’ (an abbreviation for MHC class II B) and then the identification number, following Klein et al. [86]. Support on branches is indicated by posterior probabilities (PP = 0–1).
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pone-0114631-g006: Bayesian phylogenetic analysis of MHC class II B sequences.The fish MHC class II B sequence (Onmy-DAB; FR688148) is used as an outgroup. Brackets on the right show Clades 1 and 2 of the MHC variants from Crocodylia, and six subclades (A–F) for Clade 1. For Subclades A and B, gene lineages are named with ‘DAB’ (an abbreviation for MHC class II B) and then the identification number, following Klein et al. [86]. Support on branches is indicated by posterior probabilities (PP = 0–1).

Mentions: Bayesian inference of MHC class II B genes identified in this study and those from the previous study described in S3 Table showed two clades (clades 1 and 2) using the fish sequence as an outgroup (PP = 0.85–1.0; Fig. 6). In Clade 1, the tree was found to have six subclades (1A–1F) with low branch support. Subclades 1A and 1B provided two separate clusterings of the saltwater crocodile DAB1 and DAB2 genes, respectively. Subclade 1A clustered the saltwater crocodile DAB1 gene with MHC variants from six other species of Crocodilidae (crocodiles) and a single species of Alligatoridae (alligators and caimans) (pairwise genetic distance, 0.0–0.074), while Subclade 1B clustered the saltwater crocodile DAB2 gene with variants from seven other species of Crocodilidae (pairwise genetic distance, 0.0–0.070). These clusterings appear to suggest orthologous relationships of two gene lineages (DAB1 and DAB2) to which the variants correspond. The remaining subclades (1C–1F) contained MHC variants from different species of Crocodylia: three (1C, 1E and 1F) clustered variants from different species of Alligatoridae and Crocodilidae; and one (1D) clustered variants from different species of Alligatoridae. However, collapsing low branch support (PP<0.50) caused Subclades 1A and 1B to cluster together (PP = 0.51) and the others disappeared, except for Subclade 1E (PP = 0.92), suggesting high identity between DAB1 and DAB2 genes analysed. In addition, Clade 2 consisted of only a putative pseudogene identified in gene cluster 6, and revealed large divergence to other variants compared, with pairwise genetic distances ranging from 0.425 to 0.507. This could suggest that this pseudogene corresponds to a different locus from the other genes from Crocodylia and may have been selected against in the past resulting in the pseudogenisation of the gene.


Comparative genome analyses reveal distinct structure in the saltwater crocodile MHC.

Jaratlerdsiri W, Deakin J, Godinez RM, Shan X, Peterson DG, Marthey S, Lyons E, McCarthy FM, Isberg SR, Higgins DP, Chong AY, John JS, Glenn TC, Ray DA, Gongora J - PLoS ONE (2014)

Bayesian phylogenetic analysis of MHC class II B sequences.The fish MHC class II B sequence (Onmy-DAB; FR688148) is used as an outgroup. Brackets on the right show Clades 1 and 2 of the MHC variants from Crocodylia, and six subclades (A–F) for Clade 1. For Subclades A and B, gene lineages are named with ‘DAB’ (an abbreviation for MHC class II B) and then the identification number, following Klein et al. [86]. Support on branches is indicated by posterior probabilities (PP = 0–1).
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4263668&req=5

pone-0114631-g006: Bayesian phylogenetic analysis of MHC class II B sequences.The fish MHC class II B sequence (Onmy-DAB; FR688148) is used as an outgroup. Brackets on the right show Clades 1 and 2 of the MHC variants from Crocodylia, and six subclades (A–F) for Clade 1. For Subclades A and B, gene lineages are named with ‘DAB’ (an abbreviation for MHC class II B) and then the identification number, following Klein et al. [86]. Support on branches is indicated by posterior probabilities (PP = 0–1).
Mentions: Bayesian inference of MHC class II B genes identified in this study and those from the previous study described in S3 Table showed two clades (clades 1 and 2) using the fish sequence as an outgroup (PP = 0.85–1.0; Fig. 6). In Clade 1, the tree was found to have six subclades (1A–1F) with low branch support. Subclades 1A and 1B provided two separate clusterings of the saltwater crocodile DAB1 and DAB2 genes, respectively. Subclade 1A clustered the saltwater crocodile DAB1 gene with MHC variants from six other species of Crocodilidae (crocodiles) and a single species of Alligatoridae (alligators and caimans) (pairwise genetic distance, 0.0–0.074), while Subclade 1B clustered the saltwater crocodile DAB2 gene with variants from seven other species of Crocodilidae (pairwise genetic distance, 0.0–0.070). These clusterings appear to suggest orthologous relationships of two gene lineages (DAB1 and DAB2) to which the variants correspond. The remaining subclades (1C–1F) contained MHC variants from different species of Crocodylia: three (1C, 1E and 1F) clustered variants from different species of Alligatoridae and Crocodilidae; and one (1D) clustered variants from different species of Alligatoridae. However, collapsing low branch support (PP<0.50) caused Subclades 1A and 1B to cluster together (PP = 0.51) and the others disappeared, except for Subclade 1E (PP = 0.92), suggesting high identity between DAB1 and DAB2 genes analysed. In addition, Clade 2 consisted of only a putative pseudogene identified in gene cluster 6, and revealed large divergence to other variants compared, with pairwise genetic distances ranging from 0.425 to 0.507. This could suggest that this pseudogene corresponds to a different locus from the other genes from Crocodylia and may have been selected against in the past resulting in the pseudogenisation of the gene.

Bottom Line: Here, we studied the MHC region of the saltwater crocodile (Crocodylus porosus) and compared it with that of other taxa.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.

View Article: PubMed Central - PubMed

Affiliation: Faculty of Veterinary Science, University of Sydney, Sydney, New South Wales 2006, Australia.

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 crocodilian-avian 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.

Show MeSH