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Evolutionary analysis of two classical MHC class I loci of the medaka fish, Oryzias latipes: haplotype-specific genomic diversity, locus-specific polymorphisms, and interlocus homogenization

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Abstract

The major histocompatibility complex (MHC) region of the teleost medaka (Oryzias latipes) contains two classical class I loci, UAA and UBA, whereas most lower vertebrates possess or express a single locus. To elucidate the allelic diversification and evolutionary relationships of these loci, we compared the BAC-based complete genomic sequences of the MHC class I region of three medaka strains and the PCR-based cDNA sequences of two more strains and two wild individuals, representing nine haplotypes. These were derived from two geographically distinct medaka populations isolated for four to five million years. Comparison of the genomic sequences showed a marked diversity in the region encompassing UAA and UBA even between the strains derived from the same population, and also showed an ancient divergence of these loci. cDNA analysis indicated that the peptide-binding domains of both UAA and UBA are highly polymorphic and that most of the polymorphisms were established in a locus-specific manner before the divergence of the two populations. Interallelic recombination between exons 2 and 3 encoding these domains was observed. The second intron of the UAA genes contains a highly conserved region with a palindromic sequence, suggesting that this region contributed to the recombination events. In contrast, the α3 domain is extremely homogenized not only within each locus but also between UAA and UBA regardless of populations. Two lineages of the transmembrane and cytoplasmic regions are also shared by UAA and UBA, suggesting that these two loci evolved with intimate genetic interaction through gene conversion or unequal crossing over.

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Acknowledgments

We thank Ms. Kazuyo Takada for technical assistance in sequencing. This work was supported by KAKENHI (Grant-in-Aid for Scientific Research) on Priority Areas Comparative Genomics from Ministry of Education, Culture, Sports, Science and Technology, Japan (20017009).

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  1. Department of Biological Sciences, Graduate School of Science, The University of Tokyo, Hongo 7-3-1, Bunkyo-ku, Tokyo, 113-0033, Japan

    Mayumi I. Nonaka & Masaru Nonaka

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  1. Mayumi I. Nonaka
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  2. Masaru Nonaka
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Correspondence to Mayumi I. Nonaka.

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Supplementary Fig. 1

(a) Alignment of nucleotide sequences of exon 4 encoding the α3 domain. Identical nucleotides with the first sequence are indicated by dots. The deduced amino acid sequence of the first sequence is shown above the nucleotide sequences. Only one synonymous substitution at the 32nd nucleotide is shown in gray color. Asterisks show the nucleotide substitutions shared by UAA and UBA. HNI and Kaga shown in bold are derived from the N population and others are from the S population. (b) Alignment of the regions from intron 4 to exon 7 encoding two lineages of the TM and CY region. Identical nucleotides with the first sequence are indicated by dots, and gaps are shown by dashes. Exon regions are boxed and shown in upper case, while intron regions are shown in lower case. Horizontal double-headed arrows show the duplicated regions. Brackets in introns 4 show the continuous insertions/deletions found commonly in UAA and UBA. Open box in intron 6 of Hd-rR-UAA and HNI-UAA shows the position of the insertion of ∼1.2-kb DNA transposon (sequences are not shown) (PDF 72.8 kb)

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Nonaka, M.I., Nonaka, M. Evolutionary analysis of two classical MHC class I loci of the medaka fish, Oryzias latipes: haplotype-specific genomic diversity, locus-specific polymorphisms, and interlocus homogenization. Immunogenetics 62, 319–332 (2010). https://doi.org/10.1007/s00251-010-0426-3

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