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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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Comparison of the saltwater crocodile, American alligator and Indian gharial MHC class I and II.Scaffold ID is indicated on the left of each genomic scaffold with S (an abbreviation of a scaffold) or GC (an abbreviation of a gene cluster) followed by number. MHC gene clusters identified in the current saltwater crocodile genome assembly are illustrated in Fig. 1. Scaffolds from the American alligator (unmasked v0.2.1, id 19558) and Indian gharial (unmasked v0.2, id 19547) are retrieved from CoGe database. Annotation for each row of genes across these three species is indicated on the last column. Dark areas within the MHC class I region indicates ambiguous sites. Plus and minus signs indicate sequence strand. A question mark suggests uncertainty of identifying a single gene or separate genes of MHC class I due to a sequence gap; asterisks indicate genes of which only α or β domains are available to assess intact open reading fragments.
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pone-0114631-g002: Comparison of the saltwater crocodile, American alligator and Indian gharial MHC class I and II.Scaffold ID is indicated on the left of each genomic scaffold with S (an abbreviation of a scaffold) or GC (an abbreviation of a gene cluster) followed by number. MHC gene clusters identified in the current saltwater crocodile genome assembly are illustrated in Fig. 1. Scaffolds from the American alligator (unmasked v0.2.1, id 19558) and Indian gharial (unmasked v0.2, id 19547) are retrieved from CoGe database. Annotation for each row of genes across these three species is indicated on the last column. Dark areas within the MHC class I region indicates ambiguous sites. Plus and minus signs indicate sequence strand. A question mark suggests uncertainty of identifying a single gene or separate genes of MHC class I due to a sequence gap; asterisks indicate genes of which only α or β domains are available to assess intact open reading fragments.

Mentions: Comparisons between the saltwater crocodile MHC characterised here and genome sequences available for the American alligator and Indian gharial showed that their sequences corresponded to two MHC regions, class I and class II (Fig. 2). The MHC class I region contained MHC class I genes, framework genes (TRIM39) and antigen processing genes (TAP), while the MHC class II region contained MHC class II genes and, in the alligator only, a bromodomain containing 2 (BRD2). Twenty of these genes/pseudogenes were characterised in the saltwater crocodile MHC regions, but only eight and ten of them accounting for 40% and 50% of the saltwater crocodile genes identified in this analysis were observed in the gharial and alligator scaffolds, respectively (S2 Table). In addition, three genes/pseudogenes within the MHC class I region of the alligator and four from the gharial homologous region showed small and large regions of ambiguity. These ambiguous nucleotide sites and genes could reflect differences in sequencing methods used in the three species of Crocodylia. Particularly, sequence assembly using whole genome sequencing, such as that used to generate the alligator and gharial sequences, is prone to errors caused by the extensive repetitive DNA content and duplicated fragments in a sequence [43].


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)

Comparison of the saltwater crocodile, American alligator and Indian gharial MHC class I and II.Scaffold ID is indicated on the left of each genomic scaffold with S (an abbreviation of a scaffold) or GC (an abbreviation of a gene cluster) followed by number. MHC gene clusters identified in the current saltwater crocodile genome assembly are illustrated in Fig. 1. Scaffolds from the American alligator (unmasked v0.2.1, id 19558) and Indian gharial (unmasked v0.2, id 19547) are retrieved from CoGe database. Annotation for each row of genes across these three species is indicated on the last column. Dark areas within the MHC class I region indicates ambiguous sites. Plus and minus signs indicate sequence strand. A question mark suggests uncertainty of identifying a single gene or separate genes of MHC class I due to a sequence gap; asterisks indicate genes of which only α or β domains are available to assess intact open reading fragments.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0114631-g002: Comparison of the saltwater crocodile, American alligator and Indian gharial MHC class I and II.Scaffold ID is indicated on the left of each genomic scaffold with S (an abbreviation of a scaffold) or GC (an abbreviation of a gene cluster) followed by number. MHC gene clusters identified in the current saltwater crocodile genome assembly are illustrated in Fig. 1. Scaffolds from the American alligator (unmasked v0.2.1, id 19558) and Indian gharial (unmasked v0.2, id 19547) are retrieved from CoGe database. Annotation for each row of genes across these three species is indicated on the last column. Dark areas within the MHC class I region indicates ambiguous sites. Plus and minus signs indicate sequence strand. A question mark suggests uncertainty of identifying a single gene or separate genes of MHC class I due to a sequence gap; asterisks indicate genes of which only α or β domains are available to assess intact open reading fragments.
Mentions: Comparisons between the saltwater crocodile MHC characterised here and genome sequences available for the American alligator and Indian gharial showed that their sequences corresponded to two MHC regions, class I and class II (Fig. 2). The MHC class I region contained MHC class I genes, framework genes (TRIM39) and antigen processing genes (TAP), while the MHC class II region contained MHC class II genes and, in the alligator only, a bromodomain containing 2 (BRD2). Twenty of these genes/pseudogenes were characterised in the saltwater crocodile MHC regions, but only eight and ten of them accounting for 40% and 50% of the saltwater crocodile genes identified in this analysis were observed in the gharial and alligator scaffolds, respectively (S2 Table). In addition, three genes/pseudogenes within the MHC class I region of the alligator and four from the gharial homologous region showed small and large regions of ambiguity. These ambiguous nucleotide sites and genes could reflect differences in sequencing methods used in the three species of Crocodylia. Particularly, sequence assembly using whole genome sequencing, such as that used to generate the alligator and gharial sequences, is prone to errors caused by the extensive repetitive DNA content and duplicated fragments in a sequence [43].

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