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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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Schematic diagram of six saltwater crocodile gene clusters representing MHC class I and II.Arrows indicate annotated genes and their strands (plus and minus); lines with names in the boxes below the annotation indicate BAC clones corresponding to the MHC gene clusters; and sticky ends show restriction sites of Hind III enzyme, and therefore BAC end sequencing. For retrotransposon sequences and endogenous retrovirus (ERV) sequences, asterisks indicate retrotransposon reverse transcriptase (RT) proteins; hashes indicate Gag-Pol precursor polyproteins; and pluses indicate non-LTR retrotransposon LINE-1 (L1).
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pone-0114631-g001: Schematic diagram of six saltwater crocodile gene clusters representing MHC class I and II.Arrows indicate annotated genes and their strands (plus and minus); lines with names in the boxes below the annotation indicate BAC clones corresponding to the MHC gene clusters; and sticky ends show restriction sites of Hind III enzyme, and therefore BAC end sequencing. For retrotransposon sequences and endogenous retrovirus (ERV) sequences, asterisks indicate retrotransposon reverse transcriptase (RT) proteins; hashes indicate Gag-Pol precursor polyproteins; and pluses indicate non-LTR retrotransposon LINE-1 (L1).

Mentions: Six MHC gene clusters encompassing 452,493 bp were characterised. Among these clusters, the following 20 genes and pseudogenes were predicted using transcript-based homology and ab initio gene prediction: nine for MHC class I, six for MHC class II, three for antigen-processing genes (transporter 2 associated with antigen processing, TAP2), one for TRIM39 and a single actin pseudogene (Table 1; Fig. 1). Among them, five of MHC class I, two of MHC class II, and a single gene of TAP2 showed in-frame stop codons and/or large deletions of entire/partial exons, indicating that they were putative pseudogenes. Four MHC gene clusters (clusters 2, 3, 4 and 6) contained MHC class I genes, and two other gene clusters (clusters 1 and 5) contained MHC class II genes. All the MHC gene clusters sequenced and assembled in the current study had more than 95% identity to genomic scaffolds (∼374 kb in total) of the saltwater crocodile previously generated by ICGWG [28], and showed either large or complete overlapping fragments with them. Genomic sequences and gene annotations were submitted to the ICGWG (ftp://ftp.crocgenomes.org/pub/) and added to ICGWG genome resources for the saltwater crocodile (v0.2). The gene annotation information was incorporated into gff files and integrated into CrocBase for genome viewing.


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)

Schematic diagram of six saltwater crocodile gene clusters representing MHC class I and II.Arrows indicate annotated genes and their strands (plus and minus); lines with names in the boxes below the annotation indicate BAC clones corresponding to the MHC gene clusters; and sticky ends show restriction sites of Hind III enzyme, and therefore BAC end sequencing. For retrotransposon sequences and endogenous retrovirus (ERV) sequences, asterisks indicate retrotransposon reverse transcriptase (RT) proteins; hashes indicate Gag-Pol precursor polyproteins; and pluses indicate non-LTR retrotransposon LINE-1 (L1).
© Copyright Policy
Related In: Results  -  Collection

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

pone-0114631-g001: Schematic diagram of six saltwater crocodile gene clusters representing MHC class I and II.Arrows indicate annotated genes and their strands (plus and minus); lines with names in the boxes below the annotation indicate BAC clones corresponding to the MHC gene clusters; and sticky ends show restriction sites of Hind III enzyme, and therefore BAC end sequencing. For retrotransposon sequences and endogenous retrovirus (ERV) sequences, asterisks indicate retrotransposon reverse transcriptase (RT) proteins; hashes indicate Gag-Pol precursor polyproteins; and pluses indicate non-LTR retrotransposon LINE-1 (L1).
Mentions: Six MHC gene clusters encompassing 452,493 bp were characterised. Among these clusters, the following 20 genes and pseudogenes were predicted using transcript-based homology and ab initio gene prediction: nine for MHC class I, six for MHC class II, three for antigen-processing genes (transporter 2 associated with antigen processing, TAP2), one for TRIM39 and a single actin pseudogene (Table 1; Fig. 1). Among them, five of MHC class I, two of MHC class II, and a single gene of TAP2 showed in-frame stop codons and/or large deletions of entire/partial exons, indicating that they were putative pseudogenes. Four MHC gene clusters (clusters 2, 3, 4 and 6) contained MHC class I genes, and two other gene clusters (clusters 1 and 5) contained MHC class II genes. All the MHC gene clusters sequenced and assembled in the current study had more than 95% identity to genomic scaffolds (∼374 kb in total) of the saltwater crocodile previously generated by ICGWG [28], and showed either large or complete overlapping fragments with them. Genomic sequences and gene annotations were submitted to the ICGWG (ftp://ftp.crocgenomes.org/pub/) and added to ICGWG genome resources for the saltwater crocodile (v0.2). The gene annotation information was incorporated into gff files and integrated into CrocBase for genome viewing.

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