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.
Highlights
The major histocompatibility complex (MHC) is one of the most dynamic genomic regions involved in self/non-self recognition and defense against pathogens in jawed vertebrates [1, 2]
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, one for TRIM39 and a single actin pseudogene (Table 1; Fig. 1)
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 International Crocodilian Genomes Working Group (ICGWG) [28], and showed either large or complete overlapping fragments with them
Summary
The major histocompatibility complex (MHC) is one of the most dynamic genomic regions involved in self/non-self recognition and defense against pathogens in jawed vertebrates [1, 2]. The MHC typically consists of three regions: class I, class II, and class III [3]. The MHC class III region contains genes with a functional role in innate (non-specific) immunity, inflammation, and regulation of the immune response [4]. Gene content and orientation of MHC regions has diverged throughout vertebrate evolution as species evolved and adapted to pathogenic pressures in their environment [5]. Assessment of non-avian reptile MHC is needed for comparisons of gene gain and loss, as well as gene rearrangement (i.e. insertions, deletions, inversion, and gene conversion) between this lineage and others, as it will be crucial to understand species adaption to environmental challenges and provide background information on evolutionary potentials of the lineage to fight against pathogens [16,17,18]
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