Skip to main content
Log in

Interchromosomal duplication of major histocompatibility complex class I regions in rainbow trout (Oncorhynchus mykiss), a species with a presumably recent tetraploid ancestry

  • Original Paper
  • Published:
Immunogenetics Aims and scope Submit manuscript

Abstract

Salmonid fishes are among the few animal taxa with a probable recent tetraploid ancestor. The present study is the first to compare large (>100 kb) duplicated genomic sequence fragments in such species. Two contiguous stretches with major histocompatibility complex (MHC) class I genes were detected in a rainbow trout BAC library, mapped and sequenced. The MHC class I duplicated regions, mapped by fluorescence in situ hybridization (FISH), were shown to be located on different metaphase chromosomes, Chr 14 and 18. Gene organization in both duplications is similar to that in other fishes, in that the class I loci are tightly linked with the PSMB8, PSMB9, PSMB10 and ABCB3 genes. Whereas one region, Onmy-IA, has a classical MHC class I locus (UBA), Onmy-IB encodes only non-classical class Ib proteins. The nucleotide diversity between the Onmy-IA and Onmy-IB noncoding regions is about 14%. This suggests that the MHC class I duplication event has occurred about 60 mya close to the time of an hypothesized ancestral tetraploid event. The present article is the first convincing report on the co-existence of two closely related MHC class I core regions on two different chromosomes. The interchromosomal duplication and the homology levels are supportive of the tetraploid model.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Allendorf FW, Danzmann RG (1997) Secondary tetrasomic segregation of MDH-B and preferential pairing of homeologues in rainbow trout. Genetics 145:1083–1092

    Google Scholar 

  • Allendorf FW, Thorgaard GH (1984) Tetraploidy and the evolution of salmonid fishes. In: Turner BJ (ed) Evolutionary genetics of fishes. Plenum, New York, pp 1–53

    Google Scholar 

  • Aoyagi K, Dijkstra JM, Xia C, Denda I, Ototake M, Hashimoto K, Nakanishi T (2002) Classical MHC class I genes composed of highly divergent sequence lineages share a single locus in rainbow trout (Oncorhynchus mykiss). J Immunol 168:260–273

    Google Scholar 

  • Arratia G (1997) Basal teleosts and teleostean phylogeny. Palaeo Ichthyologica 7:5–168

    Google Scholar 

  • Beck S, Kelly A, Radley E, Khurshid F, Alderton RP, Trowsdale J (1992) DNA sequence analysis of 66 kb of the human MHC class II region encoding a cluster of genes for antigen processing. J Mol Biol 228:433–441

    CAS  PubMed  Google Scholar 

  • Bingulac-Popovic J, Figueroa F, Sato A, Talbot WS, Johnson SL, Gates M, Postlethwait JH, Klein J (1997) Mapping of Mhc class I and class II regions to different linkage groups in the zebrafish, Danio rerio. Immunogenetics 46:129–134

    Article  CAS  PubMed  Google Scholar 

  • Brunelli JP, Robison BD, Thorgaard GH (2001) Ancient and recent duplications of the rainbow trout Wilms’ tumor gene. Genome 44:455–462

    Article  Google Scholar 

  • Bucher P (1990) Weight matrix descriptions of four eukaryotic RNA polymerase II promoter elements derived from 502 unrelated promoter sequences. J Mol Biol 212:563–578

    CAS  PubMed  Google Scholar 

  • Bury NR, Sturm A, Le Rouzic P, Lethimonier C, Ducouret B, Guiguen Y, Robinson-Rechavi M, Laudet V, Rafestin-Oblin ME, Prunet P (2003) Evidence for two distinct functional glucocorticoid receptors in teleost fish. J Mol Endocrinol 31:141–156

    Article  Google Scholar 

  • Clark MS, Shaw L, Kelly A, Snell P, Elgar G (2001) Characterization of the MHC class I region of the Japanese pufferfish (Fugu rubripes). Immunogenetics 52:174–185

    Google Scholar 

  • Cresswell P, Bangia N, Dick T, Diedrich G (1999) The nature of the MHC class I peptide loading complex. Immunol Rev 172:21–28

    Google Scholar 

  • Deininger PL (1983) Random subcloning of sonicated DNA: application to shotgun DNA sequence analysis. Anal Biochem 129:216–223

    Article  Google Scholar 

  • Dijkstra JM, Yoshiura Y, Kiryu I, Aoyagi K, Kollner B, Fischer U, Nakanishi T, Ototake M (2003) The promoter of the classical MHC class I locus in rainbow trout (Oncorhynchus mykiss). Fish Shellfish Immunol 14:177–182

    Article  Google Scholar 

  • Dixon B, Shum B, Adams EJ, Magor KE, Hedrick RP, Muir DG, Parham P (1998) CK-1, a putative chemokine of rainbow trout (Oncorhynchus mykiss). Immunol Rev 166:341–348

    CAS  PubMed  Google Scholar 

  • Dorschner MO, Phillips RB (1999) Comparative analysis of two Nramp loci from rainbow trout. DNA Cell Biol 18:573–583

    Article  Google Scholar 

  • Elsen PJ van den, Peijnenburg A, van Eggermond MC, Gobin SJ (1998) Shared regulatory elements in the promoters of MHC class I and class II genes. Immunol Today 19:308–312

    Google Scholar 

  • Erp SH van, Dixon B, Figueroa F, Egberts E, Stet RJ (1996) Identification and characterization of a new major histocompatibility complex class I gene in carp (Cyprinus carpio L.). Immunogenetics 44:49–61

    Article  Google Scholar 

  • Flajnik MF, Ohta Y, Namikawa-Yamada C, Nonaka M (1999a) Insight into the primordial MHC from studies in ectothermic vertebrates. Immunol Rev 167:59–67

    Google Scholar 

  • Flajnik MF, Ohta Y, Greenberg AS, Salter-Cid L, Carrizosa A, Du Pasquier L, Kasahara M (1999b) Two ancient allelic lineages at the single classical class I locus in the Xenopus MHC. J Immunol 163:3826–3833

    Google Scholar 

  • Fujiwara A, Nishida-Umehara C, Sakamoto T, Okamoto N, Nakayama I, Abe S (2001) Improved fish lymphocyte culture for chromosome preparation. Genetica 111:77–89

    Article  Google Scholar 

  • Fujiwara A, Kiryu I, Dijkstra JM, Yoshiura Y, Nishida-Umehara C, Ototake M (2003) Chromosome mapping of MHC class I in rainbow trout (Oncorhynchus mykiss). Fish Shellfish Immunol 14:171–175

    Article  Google Scholar 

  • Griffin TA, Nandi D, Cruz M, Fehling HJ, Kaer LV, Monaco JJ, Colbert RA (1998) Immunoproteasome assembly: cooperative incorporation of interferon gamma (IFN-gamma)-inducible subunits. J Exp Med 187:97–104

    Article  Google Scholar 

  • Grimholt U (1997) Transport-associated proteins in Atlantic salmon (Salmo salar). Immunogenetics 46:213–221

    Article  Google Scholar 

  • Grimholt U, Drablos F, Jorgensen SM, Hoyheim B, Stet RJ (2002) The major histocompatibility class I locus in Atlantic salmon (Salmo salar L.): polymorphism, linkage analysis and protein modelling. Immunogenetics 54:570–581

    Article  Google Scholar 

  • Hansen JD, La Patra S (2002) Induction of the rainbow trout MHC class I pathway during acute IHNV infection. Immunogenetics 54:654–661

    Article  Google Scholar 

  • Hansen JD, Strassburger P, Du Pasquier L (1996) Conservation of an alpha 2 domain within the teleostean world, MHC class I from the rainbow trout Oncorhynchus mykiss. Dev Comp Immunol 20:417–425

    Article  CAS  PubMed  Google Scholar 

  • Hansen JD, Strassburger P, Thorgaard GH, Young WP, Du Pasquier L (1999) Expression, linkage, and polymorphism of MHC-related genes in rainbow trout, Oncorhynchus mykiss. J Immunol 163:774–786

    Google Scholar 

  • Hashimoto K, Okamura K, Yamaguchi H, Ototake M, Nakanishi T, Kurosawa Y (1999) Conservation and diversification of MHC class I and its related molecules in vertebrates. Immunol Rev 167:81–100

    Google Scholar 

  • Hordvik I (1998) The impact of ancestral tetraploidy on antibody heterogeneity in salmonid fishes. Immunol Rev 166:153–157

    Google Scholar 

  • Hughes AL, Nei M (1989) Evolution of the major histocompatibility complex: independent origin of nonclassical class I genes in different groups of mammals. Mol Biol Evol 6:559–579

    CAS  PubMed  Google Scholar 

  • Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HN (ed) Mammalian protein metabolism, vol. III. Academic, New York, pp 21–132

    Google Scholar 

  • Kasahara M (1998) What do the paralogous regions in the genome tell us about the origin of the adaptive immune system? Immunol Rev 166:159–175

    Google Scholar 

  • Katagiri T, Asakawa S, Hirono I, Aoki T, Shimizu N (2000) Genomic bacterial artificial chromosome library of the Japanese flounder Paralichthys olivaceus. Mar Biotechnol 2:571–576

    Article  CAS  PubMed  Google Scholar 

  • Katagiri T, Asakawa S, Minagawa S, Shimizu N, Hirono I, Aoki T (2001) Construction and characterization of BAC libraries for three fish species; rainbow trout, carp and tilapia. Anim Genet 32:200–204

    Article  CAS  PubMed  Google Scholar 

  • Kruiswijk CP, Hermsen TT, Westphal AH, Savelkoul HF, Stet RJ (2002) A novel functional class I lineage in zebrafish (Danio rerio), carp (Cyprinus carpio), and large barbus (Barbus intermedius) showing an unusual conservation of the peptide binding domains. J Immunol 169:1936–1947

    Google Scholar 

  • Kulski JK, Dunn DS, Gaudieri S, Shiina T, Inoko H (2001) Genomic and phylogenetic analysis of the human CD1 and HLA class I multicopy genes. J Mol Evol 53:642–650

    Article  Google Scholar 

  • Kulski JK, Shiina T, Anzai T, Kohara S, Inoko H (2002) Comparative genomic analysis of the MHC: the evolution of class I duplication blocks, diversity and complexity from shark to man. Immunol Rev 190:95–122

    Article  CAS  PubMed  Google Scholar 

  • Larsen F, Solheim J, Kristensen T, Kolsto AB, Prydz H (1993) A tight cluster of five unrelated human genes on chromosome 16q22.1. Hum Mol Genet 2:1589–1595

    Google Scholar 

  • Lawlor DA, Zemmour J, Ennis PD, Parham P (1990) Evolution of class-I MHC genes and proteins: from natural selection to thymic selection. Annu Rev Immunol 8:23–63

    Article  Google Scholar 

  • Leaver MJ (2001) A family of Tc1-like transposons from the genomes of fishes and frogs: evidence for horizontal transmission. Gene 271:203–214

    Article  Google Scholar 

  • Madden DR (1995) The three-dimensional structure of peptide-MHC complexes. Annu Rev Immunol 13:587–622

    Article  CAS  PubMed  Google Scholar 

  • Magor KE, Taylor EJ, Shen SY, Martinez-Naves E, Valiante NM, Wells RS, Gumperz JE, Adams EJ, Little AM, Williams F, Middleton D, Gao X, McCluskey J, Parham P, Lienert-Weidenbach K (1997) Natural inactivation of a common HLA allele (A*2402) has occurred on at least three separate occasions. J Immunol 158:5242–5250

    Google Scholar 

  • Matsuo MY, Asakawa S, Shimizu N, Kimura H, Nonaka M (2002) Nucleotide sequence of the MHC class I genomic region of a teleost, the medaka (Oryzias latipes). Immunogenetics 53:930–940

    Article  CAS  PubMed  Google Scholar 

  • McKay SJ, Devlin RH, Smith MJ (1996) Phylogeny of Pacific salmon and trout based on growth hormone type-2 and mitochondrial NADH dehydrogenase subunit 3 DNA sequences. Can J Fish Aquatic Sci 53:1165–1176

    Article  Google Scholar 

  • Michalova V, Murray BW, Sultmann H, Klein J (2000) A contig map of the Mhc class I genomic region in the zebrafish reveals ancient synteny. J Immunol 164:5296–5305

    Google Scholar 

  • Miller KM, Withler RE (1998) The salmonid class I MHC: limited diversity in a primitive teleost. Immunol Rev 166:279–293

    Google Scholar 

  • Momburg F, Roelse J, Howard JC, Butcher GW, Hammerling GJ, Neefjes JJ (1994) Selectivity of MHC-encoded peptide transporters from human, mouse and rat. Nature 367:648–651

    Article  Google Scholar 

  • Murray BW, Busby ER, Mommsen TP, Wright PA (2003) Evolution of glutamine synthetase in vertebrates: multiple glutamine synthetase genes expressed in rainbow trout (Oncorhynchus mykiss). J Exp Biol 206:1511–1521

    Article  Google Scholar 

  • Namikawa C, Salter-Cid L, Flajnik MF, Kato Y, Nonaka M, Sasaki M (1995) Isolation of Xenopus LMP-7 homologues. Striking allelic diversity and linkage to MHC. J Immunol 155:1964–1971

    Google Scholar 

  • Nichols KM, Young WP, Danzmann RG, Robison BD, Rexroad C, Noakes M, Phillips RB, Bentzen P, Spies I, Knudsen K, Allendorf FW, Cunningham BM, Brunelli J, Zhang H, Ristow S, Drew R, Brown KH, Wheeler PA, Thorgaard GH (2003) A consolidated linkage map for rainbow trout (Oncorhynchus mykiss). Anim Genet 34:102–115

    CAS  PubMed  Google Scholar 

  • Ohta Y, Okamura K, McKinney EC, Bartl S, Hashimoto K, Flajnik MF (2000) Primitive synteny of vertebrate major histocompatibility complex class I and class II genes. Proc Natl Acad Sci USA 97:4712–4727

    Google Scholar 

  • Ohta Y, McKinney EC, Criscitiello MF, Flajnik MF (2002) Proteasome, transporter associated with antigen processing, and class I genes in the nurse shark Ginglymostoma cirratum: evidence for a stable class I region and MHC haplotype lineages. J Immunol 168:771–781

    Google Scholar 

  • Ohta Y, Powis SJ, Lohr RL, Nonaka M, Pasquier LD, Flajnik MF (2003) Two highly divergent ancient allelic lineages of the transporter associated with antigen processing (TAP) gene in Xenopus: further evidence for co-evolution among MHC class I region genes. Eur J Immunol 33:3017–3027

    Google Scholar 

  • Okamura K, Ototake M, Nakanishi T, Kurosawa Y, Hashimoto K (1997) The most primitive vertebrates with jaws possess highly polymorphic MHC class I genes comparable to those of humans. Immunity 7:777–790

    Article  CAS  PubMed  Google Scholar 

  • Onozato H (1984) Diploidization of gynogenetically activated salmonid eggs using hydrostatic pressure. Aquaculture 43:91–97

    Article  Google Scholar 

  • Phillips RB, Zimmerman A, Noakes MA, Palti Y, Morasch MR, Eiben L, Ristow SS, Thorgaard GH, Hansen JD (2003) Physical and genetic mapping of the rainbow trout major histocompatibility regions: evidence for duplication of the class I region. Immunogenetics 55:561–569

    Article  CAS  PubMed  Google Scholar 

  • Pond L, Kuhn LA, Teyton L, Schutze MP, Tainer JA, Jackson MR, Peterson PA (1995) A role for acidic residues in di-leucine motif-based targeting to the endocytic pathway. J Biol Chem 270:19989–19997

    Article  Google Scholar 

  • Rexroad CE III, Lee Y, Keele JW, Karamycheva S, Brown G, Koop B, Gahr SA, Palti Y, Quackenbush J (2003) Sequence analysis of a rainbow trout cDNA library and creation of a gene index. Cytogenet Genome Res 102:347–354

    Article  Google Scholar 

  • Rise ML, von Schalburg KR, Brown GD, Mawer MA, Devlin RH, Kuipers N, Busby M, Beetz-Sargent M, Alberto R, Gibbs AR, Hunt P, Shukin R, Zeznik JA, Nelson C, Jones SR, Smailus DE, Jones SJ, Schein JE, Marra MA, Butterfield YS, Stott JM, Ng SH, Davidson WS, Koop BF (2004) Development and application of a salmonid EST database and cDNA microarray: data mining and interspecific hybridization characteristics. Genome Res 14:478–490

    Article  Google Scholar 

  • Robinson-Rechavi M, Marchand O, Escriva H, Bardet PL, Zelus D, Hughes S, Laudet V (2001) Euteleost fish genomes are characterized by expansion of gene families. Genome Res 11:781–788

    Article  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–525

    CAS  PubMed  Google Scholar 

  • Sakamoto T, Danzmann RG, Gharbi K, Howard P, Ozaki A, Khoo SK, Woram RA, Okamoto N, Ferguson MM, Holm LE, Guyomard R, Hoyheim B (2000) A microsatellite linkage map of rainbow trout (Oncorhynchus mykiss) characterized by large sex-specific differences in recombination rates. Genetics 155:1331–1345

    CAS  PubMed  Google Scholar 

  • Sambrook JG, Russell R, Umrania Y, Edwards YJ, Campbell RD, Elgar G, Clark MS (2002) Fugu orthologues of human major histocompatibility complex genes: a genome survey. Immunogenetics 54:367–380

    Article  CAS  PubMed  Google Scholar 

  • Sammut B, Marcuz A, Pasquier LD (2002) The fate of duplicated major histocompatibility complex class Ia genes in a dodecaploid amphibian, Xenopus ruwenzoriensis. Eur J Immunol 32:2698–2709

    Google Scholar 

  • Saper MA, Bjorkman PJ, Wiley DC (1991) Refined structure of the human histocompatibility antigen HLA-A2 at 2.6 A resolution. J Mol Biol 219:277–319

    CAS  PubMed  Google Scholar 

  • Sato A, Figueroa F, Murray BW, Malaga-Trillo E, Zaleska-Rutczynska Z, Sultmann H, Toyosawa S, Wedekind C, Steck N, Klein J (2000) Nonlinkage of major histocompatibility complex class I and class II loci in bony fishes. Immunogenetics 51:108–116

    Article  CAS  PubMed  Google Scholar 

  • Shand R, Dixon B (2001) Teleost major histocompatibility genes: diverse but not complex. Mod Asp Immunobiol 2:66–72

    Google Scholar 

  • Shiina T, Tamiya G, Oka A, Yamagata T, Yamagata N, Kikkawa E, Goto K, Mizuki N, Watanabe K, Fukuzumi Y, Taguchi S, Sugawara C, Ono A, Chen L, Yamazaki M, Tashiro H, Ando A, Ikemura T, Kimura M, Inoko H (1998) Nucleotide sequencing analysis of the 146 kb segment around the IkBL and MICA genes at the centromeric end of the HLA class I region. Genomics 47:372–382

    Article  Google Scholar 

  • Shum BP, Azumi K, Zhang S, Kehrer SR, Raison RL, Detrich HW, Parham P (1996) Unexpected beta2-microglobulin sequence diversity in individual rainbow trout. Proc Natl Acad Sci USA 93:2779–2784

    Article  Google Scholar 

  • Shum BP, Rajalingam R, Magor KE, Azumi K, Carr WH, Dixon B, Stet RJ, Adkison MA, Hedrick RP, Parham P (1999) A divergent non-classical class I gene conserved in salmonids. Immunogenetics 49:479–490

    Article  Google Scholar 

  • Shum BP, Guethlein L, Flodin LR, Adkison MA, Hedrick RP, Nehring RB, Stet RJ, Secombes C, Parham P (2001) Modes of salmonid MHC class I and II evolution differ from the primate paradigm. J Immunol 166:3297–3308

    CAS  PubMed  Google Scholar 

  • Shum BP, Mason PM, Magor KE, Flodin LR, Stet RJ, Parham P (2002) Structures of two major histocompatibility complex class I genes of the rainbow trout (Oncorhynchus mykiss). Immunogenetics 54:193–199

    Article  Google Scholar 

  • Solheim JC, Carreno BM, Hansen TH (1997) Are transporter associated with antigen processing (TAP) and tapasin class I MHC chaperones? J Immunol 158:541–543

    Google Scholar 

  • Sonnhammer EL, Durbin R (1995) A dot-matrix program with dynamic threshold control suited for genomic DNA and protein sequence analysis. Gene 167:1–10

    Article  Google Scholar 

  • Sun J, Leahy DJ, Kavathas PB (1995) Interaction between CD8 and major histocompatibility complex (MHC) class I mediated by multiple contact surfaces that include the alpha 2 and alpha 3 domains of MHC class I. J Exp Med 182:1275–1280

    Article  Google Scholar 

  • Sunyer JO, Zarkadis I, Sarrias MR, Hansen JD, Lambris JD (1998) Cloning, structure, and function of two rainbow trout Bf molecules. J Immunol 161:4106–4114

    CAS  PubMed  Google Scholar 

  • Taylor JS, Braasch I, Frickey T, Meyer A, Van de Peer Y (2003) Genome duplication, a trait shared by 22,000 species of ray-finned fish. Genome Res 13:382–390

    CAS  PubMed  Google Scholar 

  • Trowsdale J (1995) “Both man & bird & beast.” Comparative organization of MHC genes. Immunogenetics 41:1–17

    Google Scholar 

  • Von Schalburg KR, Sherwood NM (1999) Regulation and expression of gonadotropin-releasing hormone gene differs in brain and gonads in rainbow trout. Endocrinology 140:3012–3024

    Article  Google Scholar 

  • Yoshizaki G, Oshiro T, Takashima F (1991) Introduction of carp a-globin gene into rainbow trout. Nippon Suisan Gakkaishi 57:819–824

    Google Scholar 

  • Zou J, Wang T, Hirono I, Aoki T, Inagawa H, Honda T, Soma GI, Ototake M, Nakanishi T, Ellis AE, Secombes CJ (2002) Differential expression of two tumor necrosis factor genes in rainbow trout, Oncorhynchus mykiss. Dev Comp Immunol 26:161–172

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank David Dunn for his assistance with Dotter. This study was supported by The Promotion of Basic Research Activities for Innovative Biosciences funded by Bio-oriented Technology Research Advancement Institution (BRAIN), Japan, and also by a Grant-in-Aid for Scientific Research on Priority Areas (C) Genome Science from the Ministry of Education, Culture, Sports, Science and Technology of Japan. All of the work reported here was performed in compliance with all applicable institutional and federal regulations. Takashi Shiina and Johannes Martinus Dijkstra contributed equally to this work.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Takashi Shiina.

Additional information

Nucleotide sequence data reported are available in the DDBJ/EMBL/GenBank database under the accession numbers AB162342, AB162343 and from AY525774 to AY525776.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Shiina, T., Dijkstra, J.M., Shimizu, S. et al. Interchromosomal duplication of major histocompatibility complex class I regions in rainbow trout (Oncorhynchus mykiss), a species with a presumably recent tetraploid ancestry. Immunogenetics 56, 878–893 (2005). https://doi.org/10.1007/s00251-004-0755-1

Download citation

  • Received:

  • Revised:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00251-004-0755-1

Keywords

Navigation