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Organization of Mhc class II A and B genes in the tilapiine fish Oreochromis

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Abstract

Perch-like fishes of the family Cichlidae are models for the study of speciation. An important tool in these studies is the major histocompatibility complex (Mhc) and its organization. The present study takes the first step toward the elucidation of the Mhc class II gene organization in the tilapiine fish Oreochromis niloticus (Orni). Using class II A- and class II B-specific probes, Mhc-bearing clones were identified and isolated from a bacterial artificial chromosome (BAC) library. The analysis of these clones by a combination of molecular, genetic-mapping, and phylogenetic methods led to the identification of nine class II A and 15 class II B loci. Genes at these loci constitute two families, which we designate as class IIa and class IIb families. Each of the families contains A and B loci. Some genes in both families are expressed and functional. The two families differ in their chromosomal location (they are unlinked) and their mode of evolution. The class IIa family genes are conserved across different teleost taxonomical orders, whereas the class IIb family genes are apparently products of multiple, more recent, rounds of gene duplications. The rounds established at least five monophyletic groups of genes. The founding unit of each monophyletic group might have been a pair of class II A and B loci.

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Acknowledgments

We thank Dr. T. Aoki (Laboratory of Genetics and Biochemistry, Tokyo University of Fisheries, Tokyo) for giving us access to the O. niloticus BAC library.

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Correspondence to Akie Sato.

Additional information

This work had been carried out in part at the Max-Planck-Institut für Biologie, Abteilung Immungenetik, Tübingen, Germany (A.S., R.D., S.S.).

The sequences reported in this paper have been deposited in the GenBank database (accession nos. AB677247- AB677312).

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ESM Table 1

(PDF 216 kb)

Fig. ESM 5

Class II regions on genomic contigs. Genomic contigs are numbered in the order of contig length and sorted by regions. An ellipse represents Mhc class II A locus and a rectangle a class II B locus. The dot inside the locus symbol indicates that the locus is a pseudogene: truncated, fragmented, or an incomplete sequence. An arrow shows the orientation of the gene. The location of a locus on a contig is indicated as k (kilobase). Loci orthologous to those present on BAC clones are designated by the names of the latter. The pairs of A and B on the contigs are numbered in cases in which more than one pair is present on the same contig (i.e., A1, A2, B1, B2, etc.). In the case of only one pair on a contig, the A or B genes are without numbers (PDF 156 kb)

Fig. ESM 6

Phylogenetic tree of class II A exon 3 and 4 translated into amino acid sequences: O. niloticus and other species (see Online resource 2). O. niloticus sequences of region B, C from the linkage study (Murray et al. 2000) are underlined. Each Orni genomic sequence name is followed by contig number. Numbers above the selected nodes indicate the percent recovery of that node in 500 bootstrap replications. The tree was prepared using pairwise-deletion method (PDF 32 kb)

Fig. ESM 7

Phylogenetic trees of class II B exon 2 translated into amino acid sequences: O. niloticus and other species, including Oreochromis alcalicus (Oral) (see “Materials and methods”). Unique sequences from Oral were designated as G1 through G11. O. niloticus sequences of regions B, C, and D are highlighted. Orni locus 1, 4, 6, 9, 12, and 15 sequences are from the linkage study (Malaga-Trillo et al. 1998). Orni B11 is the unique sequence from O. niloticus genomic DNA and Orni B8 is from cDNA library. Each genomic Orni sequence name is followed by region name, contig number, and pair number of A and B genes (see Online resource 5). Region B sequences are indicated by capital letter B at the end of the sequence name. Numbers above the selected nodes indicate the percent recovery of that node in 1,000 bootstrap replications. The tree was prepared using pairwise-deletion method (PDF 37 kb)

Fig. ESM 8

Phylogenetic tree of class II A full gene translated into amino acid sequences: O. niloticus and other species. (see Online resource 2). Each Orni genomic sequence name is followed by region name, contig number, and A and B pair number (Online resource 5); each region is indicated in different color. Numbers above selected nodes indicate the percent recovery of that node in 1,000 bootstrap replications. The tree was prepared using complete–deletion method (PDF 46 kb)

Fig. ESM 9

Phylogenetic tree of class II B full gene translated into amino acid sequences: O. niloticus and other species (see Online resource 3). Each Orni genomic sequence name is followed by region name, contig number, and the A and B pair number (Online resource 5); each region is indicated in different color. Numbers above selected nodes indicate the percent recovery of that node in 1,000 bootstrap replications. The tree was prepared using pairwise-deletion method (PDF 53 kb)

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Sato, A., Dongak, R., Hao, L. et al. Organization of Mhc class II A and B genes in the tilapiine fish Oreochromis . Immunogenetics 64, 679–690 (2012). https://doi.org/10.1007/s00251-012-0618-0

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  • DOI: https://doi.org/10.1007/s00251-012-0618-0

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