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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 tree of MHC class II A genes.The fish MHC class II A sequence (Onmy-DAA; AFP94173) is used as an outgroup. A bracket on the right shows the DAA gene lineage of the MHC genes from Crocodylia identified in the current study and previous publications as described in Materials and Methods. This gene lineage is named with ‘DAA’ (an abbreviation for MHC class II A), following Klein et al. [86]. Support on branches is indicated by posterior probabilities (PP = 0–1).
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pone-0114631-g005: Bayesian phylogenetic tree of MHC class II A genes.The fish MHC class II A sequence (Onmy-DAA; AFP94173) is used as an outgroup. A bracket on the right shows the DAA gene lineage of the MHC genes from Crocodylia identified in the current study and previous publications as described in Materials and Methods. This gene lineage is named with ‘DAA’ (an abbreviation for MHC class II A), following Klein et al. [86]. Support on branches is indicated by posterior probabilities (PP = 0–1).

Mentions: Bayesian inference of MHC class II A genes identified among the saltwater crocodile, American alligator and Indian gharial studied here and those from other 16 species of Crocodylia in the previous study (S3 Table) showed that they formed a monophyletic clade (PP = 1.0) without clear subdivision in the clade when the fish sequence was used as an outgroup (Fig. 5). All the genes, including Crpo-DAA, Almi-DAA and Gaga-DAA showed high aa identity with an overall genetic distance of 0.004, indicating that they are orthologous to each other. The analysis of introns 1 to 3 among the full-length DAA genes identified in the current study was consistent showing little pairwise genetic distance ranging from 0.034–0.057. Using this phylogeny, the DAA locus identified on the saltwater crocodile genome enabled us to assign the previously sequenced variants from the other 16 species of Crocodylia to this locus. In addition, all the genes from Crocodylia clustered as a sister clade to mallard and chicken MHC class II A, Anpl-DRA and BLA, respectively, suggesting that these avian genes are orthologs to DAA genes among crocodilians.


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 tree of MHC class II A genes.The fish MHC class II A sequence (Onmy-DAA; AFP94173) is used as an outgroup. A bracket on the right shows the DAA gene lineage of the MHC genes from Crocodylia identified in the current study and previous publications as described in Materials and Methods. This gene lineage is named with ‘DAA’ (an abbreviation for MHC class II A), 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-g005: Bayesian phylogenetic tree of MHC class II A genes.The fish MHC class II A sequence (Onmy-DAA; AFP94173) is used as an outgroup. A bracket on the right shows the DAA gene lineage of the MHC genes from Crocodylia identified in the current study and previous publications as described in Materials and Methods. This gene lineage is named with ‘DAA’ (an abbreviation for MHC class II A), following Klein et al. [86]. Support on branches is indicated by posterior probabilities (PP = 0–1).
Mentions: Bayesian inference of MHC class II A genes identified among the saltwater crocodile, American alligator and Indian gharial studied here and those from other 16 species of Crocodylia in the previous study (S3 Table) showed that they formed a monophyletic clade (PP = 1.0) without clear subdivision in the clade when the fish sequence was used as an outgroup (Fig. 5). All the genes, including Crpo-DAA, Almi-DAA and Gaga-DAA showed high aa identity with an overall genetic distance of 0.004, indicating that they are orthologous to each other. The analysis of introns 1 to 3 among the full-length DAA genes identified in the current study was consistent showing little pairwise genetic distance ranging from 0.034–0.057. Using this phylogeny, the DAA locus identified on the saltwater crocodile genome enabled us to assign the previously sequenced variants from the other 16 species of Crocodylia to this locus. In addition, all the genes from Crocodylia clustered as a sister clade to mallard and chicken MHC class II A, Anpl-DRA and BLA, respectively, suggesting that these avian genes are orthologs to DAA genes among crocodilians.

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