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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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Comparative MHC organisations of the fugu, chicken, saltwater crocodile and human.MHC mapping in the fugu, chicken, and human is generated using data from Clark et al. [87], AL023516 (plus Shiina et al. [29] for a framework region), and NT_007592, respectively. Gene cluster 2 of the saltwater crocodile, where a gene model of coding sequences is absent, is omitted in this figure. Graphics in the first row of each vertebrate represent genes in the MHC based on schematic representation in GEvo [88], where all graphics are automatically created if applicable. Unlinked MHC genes and regions in the fugu and saltwater crocodile presented by the absence of line connection indicate that their order is arbitrary and is not based on the current data. Gray arrows indicate gene models; green arrows indicate protein coding sequences (CDS); blue arrows (on top of gray genes) indicate mRNA; and yellow arrows indicate approximately 50% GC content in codon wobble positions. Scales above the graphics show different sizes of MHC regions in kilo base pairs (K) or mega base pairs (M).
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pone-0114631-g003: Comparative MHC organisations of the fugu, chicken, saltwater crocodile and human.MHC mapping in the fugu, chicken, and human is generated using data from Clark et al. [87], AL023516 (plus Shiina et al. [29] for a framework region), and NT_007592, respectively. Gene cluster 2 of the saltwater crocodile, where a gene model of coding sequences is absent, is omitted in this figure. Graphics in the first row of each vertebrate represent genes in the MHC based on schematic representation in GEvo [88], where all graphics are automatically created if applicable. Unlinked MHC genes and regions in the fugu and saltwater crocodile presented by the absence of line connection indicate that their order is arbitrary and is not based on the current data. Gray arrows indicate gene models; green arrows indicate protein coding sequences (CDS); blue arrows (on top of gray genes) indicate mRNA; and yellow arrows indicate approximately 50% GC content in codon wobble positions. Scales above the graphics show different sizes of MHC regions in kilo base pairs (K) or mega base pairs (M).

Mentions: The comparative MHC analysis of the saltwater crocodile, fugu (Fugu rubripes), chicken (or red jungle fowl, Gallus gallus), and human showed that the present saltwater crocodile genome structure consisted of two independent regions of MHC class I and two of MHC class II (Fig. 3). Based upon the current crocodile sequencing and gene annotation, it is not clear if the crocodile MHC class I and II regions are separated like MHC class I and II regions in the chicken and human, or intermingled like those of the fugu. MHC class I regions of both the saltwater crocodile and chicken showed a close linkage between MHC class I gene and antigen processing gene (TAP), reflecting an associate role of the TAP genes in peptide loading into MHC class I molecules [44]. This was in contrast with the human MHC, where the TAP genes were located closely with MHC class II genes. One difference of MHC organisation between the saltwater crocodile and chicken was linkage between TRIM39 and MHC class I gene in the saltwater crocodile (18,575 bp distant between TRIM39 and MHC class I pseudogene in gene cluster 4.1). In the chicken, it was reported that framework genes, such as TRIM genes, were located 41 kb upstream of the core B locus with TRIM-class II-class I-class III orientation [29]. Identifying collinear sets of MHC regions/genes of sequence similarity to infer synteny between the saltwater crocodile and the chicken (plus the human), using SynMap [45], did not show significant large conserved sequences among these comparisons, even though the two species are closely related within Archosauria. It is likely, because the saltwater crocodile compared had much larger MHC regions (452,493 bp in total) and the greater number of MHC class I and II genes/pseudogenes than the fowl B locus (92 Kbp). Only a single gene, the saltwater crocodile TAP2, was shown to present a synteny to TAP2 coding sequences of the fowl B locus (S3 Figure), suggesting their orthologous relationships between the two species.


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)

Comparative MHC organisations of the fugu, chicken, saltwater crocodile and human.MHC mapping in the fugu, chicken, and human is generated using data from Clark et al. [87], AL023516 (plus Shiina et al. [29] for a framework region), and NT_007592, respectively. Gene cluster 2 of the saltwater crocodile, where a gene model of coding sequences is absent, is omitted in this figure. Graphics in the first row of each vertebrate represent genes in the MHC based on schematic representation in GEvo [88], where all graphics are automatically created if applicable. Unlinked MHC genes and regions in the fugu and saltwater crocodile presented by the absence of line connection indicate that their order is arbitrary and is not based on the current data. Gray arrows indicate gene models; green arrows indicate protein coding sequences (CDS); blue arrows (on top of gray genes) indicate mRNA; and yellow arrows indicate approximately 50% GC content in codon wobble positions. Scales above the graphics show different sizes of MHC regions in kilo base pairs (K) or mega base pairs (M).
© Copyright Policy
Related In: Results  -  Collection

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

pone-0114631-g003: Comparative MHC organisations of the fugu, chicken, saltwater crocodile and human.MHC mapping in the fugu, chicken, and human is generated using data from Clark et al. [87], AL023516 (plus Shiina et al. [29] for a framework region), and NT_007592, respectively. Gene cluster 2 of the saltwater crocodile, where a gene model of coding sequences is absent, is omitted in this figure. Graphics in the first row of each vertebrate represent genes in the MHC based on schematic representation in GEvo [88], where all graphics are automatically created if applicable. Unlinked MHC genes and regions in the fugu and saltwater crocodile presented by the absence of line connection indicate that their order is arbitrary and is not based on the current data. Gray arrows indicate gene models; green arrows indicate protein coding sequences (CDS); blue arrows (on top of gray genes) indicate mRNA; and yellow arrows indicate approximately 50% GC content in codon wobble positions. Scales above the graphics show different sizes of MHC regions in kilo base pairs (K) or mega base pairs (M).
Mentions: The comparative MHC analysis of the saltwater crocodile, fugu (Fugu rubripes), chicken (or red jungle fowl, Gallus gallus), and human showed that the present saltwater crocodile genome structure consisted of two independent regions of MHC class I and two of MHC class II (Fig. 3). Based upon the current crocodile sequencing and gene annotation, it is not clear if the crocodile MHC class I and II regions are separated like MHC class I and II regions in the chicken and human, or intermingled like those of the fugu. MHC class I regions of both the saltwater crocodile and chicken showed a close linkage between MHC class I gene and antigen processing gene (TAP), reflecting an associate role of the TAP genes in peptide loading into MHC class I molecules [44]. This was in contrast with the human MHC, where the TAP genes were located closely with MHC class II genes. One difference of MHC organisation between the saltwater crocodile and chicken was linkage between TRIM39 and MHC class I gene in the saltwater crocodile (18,575 bp distant between TRIM39 and MHC class I pseudogene in gene cluster 4.1). In the chicken, it was reported that framework genes, such as TRIM genes, were located 41 kb upstream of the core B locus with TRIM-class II-class I-class III orientation [29]. Identifying collinear sets of MHC regions/genes of sequence similarity to infer synteny between the saltwater crocodile and the chicken (plus the human), using SynMap [45], did not show significant large conserved sequences among these comparisons, even though the two species are closely related within Archosauria. It is likely, because the saltwater crocodile compared had much larger MHC regions (452,493 bp in total) and the greater number of MHC class I and II genes/pseudogenes than the fowl B locus (92 Kbp). Only a single gene, the saltwater crocodile TAP2, was shown to present a synteny to TAP2 coding sequences of the fowl B locus (S3 Figure), suggesting their orthologous relationships between the two species.

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