Comparative genome analyses reveal distinct structure in the saltwater crocodile MHC

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 di...

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Published inPloS one Vol. 9; no. 12; p. e114631
Main Authors Jaratlerdsiri, Weerachai, Deakin, Janine, Godinez, Ricardo M, Shan, Xueyan, Peterson, Daniel G, Marthey, Sylvain, Lyons, Eric, McCarthy, Fiona M, Isberg, Sally R, Higgins, Damien P, Chong, Amanda Y, John, John St, Glenn, Travis C, Ray, David A, Gongora, Jaime
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 11.12.2014
Public Library of Science (PLoS)
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Summary: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.
Bibliography:Conceived and designed the experiments: WJ SRI JG. Performed the experiments: WJ JD TCG. Analyzed the data: WJ RGM SM EL FMM AYC JSJ JG. Contributed reagents/materials/analysis tools: WJ JD XS DGP EL FMM JSJ TCG DAR JG. Wrote the paper: WJ JD RGM XS DGP SM EL FMM SRI DPH AYC JSJ TCG DAR JG. Contributed to the experimental design, undertook primary experiments, performed data analyses and led the writing up of this paper: WJ. Initiated, directed and supervised this work, contributed with the interpretation of the data and preparation of the manuscript and provided extensive feedback: JG. Provided assistance in BAC library screening: JD. Contributed to data of the green anole MHC used in this paper: RGM. Provided saltwater crocodile BAC library, prepared BAC clones containing MHC genes in the USA, and shipped them to Australia: XS DGP. Provided invaluable assistance on data analyses and offered useful suggestions on the manuscript: SM EL FMM. Contributed to supervision of the project and discussions concerning the project plan and manuscript preparation: SRI DPH. Provided assistance in the lab, performed the second run of de novo BAC assemblies for cross-referencing purposes, and contributed useful comments on retroelements: AYC. Offered advice on techniques and analyses of BAC-based sequencing, and provided genome and transcriptome resources of the saltwater crocodile, American alligator and Indian gharial used in the data analyses: JSJ TCG DAR. Read, commented on and approved the drafts of the manuscript: WJ JD RGM XS DGP SM EL FMM SRI DPH AYC JSJ TCG DAR JG.
Current address: Department of Biological Sciences, Texas Tech University, Lubbock, Texas 79409, United States of America.
Competing Interests: The authors have declared that no competing interests exist.
ISSN:1932-6203
1932-6203
DOI:10.1371/journal.pone.0114631