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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 I genes.The fish MHC class I sequence (Onmy-UBA; AF287487) is used as an outgroup. Brackets on the right show Clades 1 to 4 of the MHC genes/pseudogenes from Crocodylia identified in the current study and previous publications as described in Materials and Methods. For Clades 1 and 3, gene lineages are named with ‘U’ for unknown families of MHC class I and then the locus name, following Klein et al. [86]. Support on branches is indicated by posterior probabilities (PP = 0–1).
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pone-0114631-g004: Bayesian phylogenetic tree of MHC class I genes.The fish MHC class I sequence (Onmy-UBA; AF287487) is used as an outgroup. Brackets on the right show Clades 1 to 4 of the MHC genes/pseudogenes from Crocodylia identified in the current study and previous publications as described in Materials and Methods. For Clades 1 and 3, gene lineages are named with ‘U’ for unknown families of MHC class I and then the locus name, following Klein et al. [86]. Support on branches is indicated by posterior probabilities (PP = 0–1).

Mentions: Bayesian inference of MHC class I genes from the current study and those from the previous study described in S3 Table showed that they clustered into four clades (Clades 1–4; PP = 0.79–1.00) when a fish sequence (Oncorhynchus mykiss) was used as an outgroup (Fig. 4). All these clades contained MHC genes/pseudogenes from the saltwater crocodile, American alligator and/or Indian gharial identified herein. Clades 2–4 each clustered MHC genes/pseudogenes (PP = 1.00) that were assigned to the same MHC locus in the three crocodilian taxa studied. Therefore, orthologous relationships could be suggested for these three clades corresponding to the cluster 3.2 pseudogene, UA gene and cluster 4.1 pseudogene respectively, with between-clade pairwise distance ranging from 0.466 to 0.703 showing great divergence between them. Cluster 4.1 pseudogenes from the saltwater crocodile and American alligator within Clade 4 showed dramatic divergence from the rest of MHC genes in Crocodylia analysed here with pairwise genetic distance of exons ranging from 0.564 to 0.744. These MHC class I pseudogenes formed a paraphyletic clade with currently analysed MHC genes from crocodilians, fowl, and the tuatara (Sphenodon punctatus), indicating that they are expected to predate the divergence of these vertebrate groups. However, Clade 1 clustered five loci of saltwater crocodile MHC class I identified here (the UB gene, UC gene, cluster 1 pseudogene, cluster 2 pseudogene and partial MHC class I gene) and all previously sequenced variants (PP = 0.79). This clustering indicated that the Clade 1 variants corresponded to UB and UC gene lineages, where their loci were detected at different sites on the saltwater crocodile genome. Since the topology in Clade 1 did not allow a clear subdivision of these two genes, we proposed this clade as a representation of UB and UC gene lineages. The saltwater crocodile UB gene clustered well (PP = 1.00) with other five MHC class I sequences from four species of crocodiles (the saltwater crocodile, mugger crocodile, Philippine crocodile and Siamese crocodile), suggesting that they may represent orthologs to the UB gene in the saltwater crocodile.


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 I genes.The fish MHC class I sequence (Onmy-UBA; AF287487) is used as an outgroup. Brackets on the right show Clades 1 to 4 of the MHC genes/pseudogenes from Crocodylia identified in the current study and previous publications as described in Materials and Methods. For Clades 1 and 3, gene lineages are named with ‘U’ for unknown families of MHC class I and then the locus name, 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-g004: Bayesian phylogenetic tree of MHC class I genes.The fish MHC class I sequence (Onmy-UBA; AF287487) is used as an outgroup. Brackets on the right show Clades 1 to 4 of the MHC genes/pseudogenes from Crocodylia identified in the current study and previous publications as described in Materials and Methods. For Clades 1 and 3, gene lineages are named with ‘U’ for unknown families of MHC class I and then the locus name, following Klein et al. [86]. Support on branches is indicated by posterior probabilities (PP = 0–1).
Mentions: Bayesian inference of MHC class I genes from the current study and those from the previous study described in S3 Table showed that they clustered into four clades (Clades 1–4; PP = 0.79–1.00) when a fish sequence (Oncorhynchus mykiss) was used as an outgroup (Fig. 4). All these clades contained MHC genes/pseudogenes from the saltwater crocodile, American alligator and/or Indian gharial identified herein. Clades 2–4 each clustered MHC genes/pseudogenes (PP = 1.00) that were assigned to the same MHC locus in the three crocodilian taxa studied. Therefore, orthologous relationships could be suggested for these three clades corresponding to the cluster 3.2 pseudogene, UA gene and cluster 4.1 pseudogene respectively, with between-clade pairwise distance ranging from 0.466 to 0.703 showing great divergence between them. Cluster 4.1 pseudogenes from the saltwater crocodile and American alligator within Clade 4 showed dramatic divergence from the rest of MHC genes in Crocodylia analysed here with pairwise genetic distance of exons ranging from 0.564 to 0.744. These MHC class I pseudogenes formed a paraphyletic clade with currently analysed MHC genes from crocodilians, fowl, and the tuatara (Sphenodon punctatus), indicating that they are expected to predate the divergence of these vertebrate groups. However, Clade 1 clustered five loci of saltwater crocodile MHC class I identified here (the UB gene, UC gene, cluster 1 pseudogene, cluster 2 pseudogene and partial MHC class I gene) and all previously sequenced variants (PP = 0.79). This clustering indicated that the Clade 1 variants corresponded to UB and UC gene lineages, where their loci were detected at different sites on the saltwater crocodile genome. Since the topology in Clade 1 did not allow a clear subdivision of these two genes, we proposed this clade as a representation of UB and UC gene lineages. The saltwater crocodile UB gene clustered well (PP = 1.00) with other five MHC class I sequences from four species of crocodiles (the saltwater crocodile, mugger crocodile, Philippine crocodile and Siamese crocodile), suggesting that they may represent orthologs to the UB gene in the saltwater crocodile.

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
Related in: MedlinePlus