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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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Model of the evolution of the saltwater crocodile MHC.The MHC of crocodiles is compared with that of fowl, eutherians, and anoles (A) or opossums (B). Each coloured box indicates different genes consistent with the legend in Fig. 2. Broken lines indicate absence of linkage between genes; and dashed boxes indicate unknown linkage as a result of unmapped scaffolds in the saltwater crocodile and green anole. MHC gene mapping in fowl (chicken, quail, black grouse, golden pheasant, and turkey), eutherians (human, chimpanzee, gorilla, rat, mouse, dog, cat, cattle, sheep, pig, and horse), green anoles, and opossums is generated using data from Kelley et al. [5], Wang et al. [31], Ye et al. [13], Chaves et al. [12], Wilming et al. [61], Yuhki et al. [92], Gao et al. [14], Gonidez et al. (manuscript in revision), and Belov et al. [15].
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pone-0114631-g007: Model of the evolution of the saltwater crocodile MHC.The MHC of crocodiles is compared with that of fowl, eutherians, and anoles (A) or opossums (B). Each coloured box indicates different genes consistent with the legend in Fig. 2. Broken lines indicate absence of linkage between genes; and dashed boxes indicate unknown linkage as a result of unmapped scaffolds in the saltwater crocodile and green anole. MHC gene mapping in fowl (chicken, quail, black grouse, golden pheasant, and turkey), eutherians (human, chimpanzee, gorilla, rat, mouse, dog, cat, cattle, sheep, pig, and horse), green anoles, and opossums is generated using data from Kelley et al. [5], Wang et al. [31], Ye et al. [13], Chaves et al. [12], Wilming et al. [61], Yuhki et al. [92], Gao et al. [14], Gonidez et al. (manuscript in revision), and Belov et al. [15].

Mentions: The saltwater crocodile MHC (evolution model; Fig. 7A) appears to have a gene organisation intermediate between the fowl B locus and the eutherian MHC. The saltwater crocodile shows the same linkage between TAP and MHC class I genes as the fowl (but not eutherians), whilst in contrast TRIM is placed near MHC class I genes in the saltwater crocodile and eutherians (but not fowl). Inclusion of the recently generated green anole MHC in this comparison shows that the gene organisation identified in the saltwater crocodile BACs and the scaffolds from the American alligator and Indian gharial resemble that of the anole with the exception of the close linkage of TRIM and MHC class I among the crocodilians (Godinez et al., manuscript in revision) (Fig. 7A). Given that crocodilians and lizards comprise two major orders of non-avian reptiles (out of 4), it is possible that these immune genes and their organisation, which are conserved between them, also exist across other non-avian reptiles and may suggest putative functional immune/genetic advantages. For instance, the proximity of TAP to MHC class I genes observed in the saltwater crocodile and anole might cause minimal recombination [56], allowing co-evolution between both genes to symbiotically process and present specific peptides consistent with the hypothesis of co-evolving genes observed in the chicken [56]–[58].


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)

Model of the evolution of the saltwater crocodile MHC.The MHC of crocodiles is compared with that of fowl, eutherians, and anoles (A) or opossums (B). Each coloured box indicates different genes consistent with the legend in Fig. 2. Broken lines indicate absence of linkage between genes; and dashed boxes indicate unknown linkage as a result of unmapped scaffolds in the saltwater crocodile and green anole. MHC gene mapping in fowl (chicken, quail, black grouse, golden pheasant, and turkey), eutherians (human, chimpanzee, gorilla, rat, mouse, dog, cat, cattle, sheep, pig, and horse), green anoles, and opossums is generated using data from Kelley et al. [5], Wang et al. [31], Ye et al. [13], Chaves et al. [12], Wilming et al. [61], Yuhki et al. [92], Gao et al. [14], Gonidez et al. (manuscript in revision), and Belov et al. [15].
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4263668&req=5

pone-0114631-g007: Model of the evolution of the saltwater crocodile MHC.The MHC of crocodiles is compared with that of fowl, eutherians, and anoles (A) or opossums (B). Each coloured box indicates different genes consistent with the legend in Fig. 2. Broken lines indicate absence of linkage between genes; and dashed boxes indicate unknown linkage as a result of unmapped scaffolds in the saltwater crocodile and green anole. MHC gene mapping in fowl (chicken, quail, black grouse, golden pheasant, and turkey), eutherians (human, chimpanzee, gorilla, rat, mouse, dog, cat, cattle, sheep, pig, and horse), green anoles, and opossums is generated using data from Kelley et al. [5], Wang et al. [31], Ye et al. [13], Chaves et al. [12], Wilming et al. [61], Yuhki et al. [92], Gao et al. [14], Gonidez et al. (manuscript in revision), and Belov et al. [15].
Mentions: The saltwater crocodile MHC (evolution model; Fig. 7A) appears to have a gene organisation intermediate between the fowl B locus and the eutherian MHC. The saltwater crocodile shows the same linkage between TAP and MHC class I genes as the fowl (but not eutherians), whilst in contrast TRIM is placed near MHC class I genes in the saltwater crocodile and eutherians (but not fowl). Inclusion of the recently generated green anole MHC in this comparison shows that the gene organisation identified in the saltwater crocodile BACs and the scaffolds from the American alligator and Indian gharial resemble that of the anole with the exception of the close linkage of TRIM and MHC class I among the crocodilians (Godinez et al., manuscript in revision) (Fig. 7A). Given that crocodilians and lizards comprise two major orders of non-avian reptiles (out of 4), it is possible that these immune genes and their organisation, which are conserved between them, also exist across other non-avian reptiles and may suggest putative functional immune/genetic advantages. For instance, the proximity of TAP to MHC class I genes observed in the saltwater crocodile and anole might cause minimal recombination [56], allowing co-evolution between both genes to symbiotically process and present specific peptides consistent with the hypothesis of co-evolving genes observed in the chicken [56]–[58].

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