Skip to main content
Log in

Suggestive Association of Major Histocompatibility IB Genetic Markers with Resistance to Bacterial Cold Water Disease in Rainbow Trout (Oncorhynchus mykiss)

  • Original Article
  • Published:
Marine Biotechnology Aims and scope Submit manuscript

Abstract

Genes within the major histocompatibility complex (MHC) are important for both innate and adaptive immune responses in mammals; however, much less is known regarding their contribution in teleost fishes. We examined the involvement of four major histocompatibility (MH) genomic regions in rainbow trout in resistance to the causative agent of bacterial coldwater disease (BCWD), Flavobacterium psychrophilum. Fish from the 2005 NCCCWA brood-year (71 full-sib families) were challenged with F. psychrophilum strain CSF 259–93. The overall mortality rate was 70%, with large variation in mortality between families. Disease resistance was quantified as post-challenge days to death. Phenotypic variation and additive genetic variation were estimated using mixed models of survival analysis. To examine association, eight microsatellite markers were isolated from MH gene-containing BAC clones and mapped onto the rainbow trout genetic linkage map. The parents and grandparents of the 2005 brood-year families were genotyped with these eight markers and another two markers tightly linked to the MH-IB region to assess the extent of linkage disequilibrium (LD) of MH genomic regions MH-IA, MH-IB, TAP1, and MH-II with survival post-challenge. MH-IB and MH-II markers were linked to BCWD survivability when data were analyzed by family. Tests for disease association at the population level substantiated the involvement of MH-IB, but not MH-II, with disease resistance. The impact of selective breeding for disease resistance on MH sequence variation is discussed in the context of aquaculture production.

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

Similar content being viewed by others

References

  • Berg P, Henryon M (1998) A comparison of mating designs for inference on genetic parameters in fish. Proc 6th World Congr Genet Appl Livest Prod 27:115–118

    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 146:129–134

    Article  Google Scholar 

  • Braud VM, Allan DS, McMichael AJ (1999) Functions of nonclassical MHC and non-MHC-encoded class I molecules. Curr Opin Immunol 11:100–108

    Article  PubMed  CAS  Google Scholar 

  • Cipriano RC, Holt RA (2005) Flavobacterium psychrophilum, cause of bacterial cold-water disease and rainbow trout fry syndrome. Fish Disease Leaflet No. 86. United States Dept. of the Interior. U.S. Geological Service, National Fish Health Research Laboratory, Leetown, WV

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Cohen S, Tirindelli J, Gomez-Chiarri M, Nacci D (2006) Functional implications of major histocompatibility (MH) variation using estuarine fish populations. Integr Comp Biol 46:1016–1029

    Article  CAS  Google Scholar 

  • Cuesta A, Esteban MA, Meseguer J (2006) Cloning, distribution and up-regulation of the teleost fish MHC class II alpha suggests a role for granulocytes as antigen-presenting cells. Mol Immun 43:1275–1285

    Article  CAS  Google Scholar 

  • Dijkstra JM, Kiryu I, Yoshiura Y, Kumanovics A, Kohara M, Hayashi N, Ototake M (2006) Polymorphism of two very similar MHC class Ib loci in rainbow trout (Oncorhynchus mykiss). Immunogenetics 58:152–167

    Article  PubMed  CAS  Google Scholar 

  • Dijkstra JM, Katagiri T, Hosomichi K, Yanagiya K, Inoko H, Ototake M, Aoki T, Hashimoto K, Shiina T (2007) A third broad lineage of major histocompatibility complex (MHC) class I in teleost fish; MHC class II linkage and processed genes. Immunogenetics 59:305–321

    Article  PubMed  CAS  Google Scholar 

  • Ducrocq V, Casella G (1996) A Bayesian analysis of mixed survival models. Genet Sel Evol 28:505–529

    Article  Google Scholar 

  • Elgert KD (1996) Immunology: understanding the immune system. Wiley-Liss, New York, p p 441

    Google Scholar 

  • Falconer DS, Mackay TFC (1996) Introduction to quantitative genetics. Pearson Prentice Hall, England, UK

    Google Scholar 

  • Grimholt U, Larsen S, Nordmo R, Midtlyng P, Kjoeglum S, Storset A, Saebø S, Stet RJM (2003) MHC polymorphism and disease resistance in Atlantic salmon (Salmo salar); facing pathogens with single expressed major histocompatibility class I and class II loci. Immunogenetics 55:210–219

    Article  PubMed  CAS  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

    PubMed  CAS  Google Scholar 

  • Hansen TH, Huang S, Arnold PL, Fremont DH (2007) Patterns of nonclassical MHC antigen presentation. Nature Immunol 8:563–568

    Article  CAS  Google Scholar 

  • Hedrick PW, Thomson G (1983) Evidence for balancing selection at HLA. Genetics 104:449–456

    PubMed  CAS  Google Scholar 

  • Hedrick PW, Black FL (1997) HLA and mate selection: no evidence in South Amerindians. Am J Hum Genet 61:494–496

    Article  Google Scholar 

  • Henryon M, Berg P, Olesen NJ, Kjaer TE, Slierendrecht WJ, Jokumsen A, Lund I (2005) Selective breeding provides an approach to increase resistance of rainbow trout (Onchorhynchus mykiss) to the diseases, enteric redmouth disease, rainbow trout fry syndrome, and viral haemorrhagic septicaemia. Aquaculture 250:621–636

    Article  Google Scholar 

  • Hughes AL, Yeager M (1998) Natural selection at major histocompatibility complex loci of vertebrates. Annu Rev Genet 32:415–435

    Article  PubMed  CAS  Google Scholar 

  • Johnson NA, Rexroad III CE, Hallerman EM, Vallejo RL, Palti Y (2007) Development and evaluation of a new microsatellite multiplex system for parental allocation and management of rainbow trout (Oncorhynchus mykiss) broodstocks. Aquaculture 266:53–62

    Article  CAS  Google Scholar 

  • Khakoo SI, Rajalingam R, Shum BP, Weidenbach K, Flodin L, Muir DG, Canavez F, Cooper SL, Valiante NM, Lanier LL, Parham P (2000) Rapid evolution of NK cell receptor systems demonstrated by comparison of chimpanzees and humans. Immunity 12:687–698

    Article  PubMed  CAS  Google Scholar 

  • Kiryu I, Dijkstra JM, Sarder RI, Fujiwara A, Toshiura Y, Ototake M (2005) New MHC class Ia domain lineages in rainbow trout (Oncorhynchus mykiss) which are shared with other fish species. Fish Shellfish Immunol 18:243–254

    PubMed  CAS  Google Scholar 

  • Laird NM, Horvath S, Xu X (2000) Implementing a unified approach to family-based tests of association. Genet Epidemiol 19:S36–S42

    Article  PubMed  Google Scholar 

  • Landis ED, Palti Y, Dekoning J, Drew R, Phillips RB, Hansen JD (2006) Identification and regulatory analysis of rainbow trout tapasin and tapasin-related genes. Immunogenetics 58:56–69

    Article  PubMed  CAS  Google Scholar 

  • Lange C, Silverman EK, Xu X, Weiss ST, Laird NM (2003) A multivariate transmission disequilibrium test. Biostatistics 71:195–206

    Article  Google Scholar 

  • Langefors A, Lohm J, Grahn M, Andersen O, Schantz TV (2001) Association between major histocompatibility complex class IIB alleles and resistance to Aeromonas salmonicida in Atlantic salmon. Proc R Soc Lond 268:479–485

    Article  CAS  Google Scholar 

  • Liu ZJ, Cordes JF (2004) DNA marker technologies and their applications in aquaculture genetics. Aquaculture 238:1–37

    Article  CAS  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  PubMed  CAS  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

    PubMed  CAS  Google Scholar 

  • Miller KM, Winton JR, Schulze AD, Purcell MK, Ming TJ (2004) Major histocompatibility complex loci are associated with susceptibility of Atlantic salmon to infectious hematopoietic necrosis virus. Environ Biol Fishes 69:307–316

    Article  Google Scholar 

  • Milliken GA, Johnson DE (1984) Analysis of messy data: designed experiments, vol 1. Belmont, CA, Lifetime Learning Publications

    Google Scholar 

  • Naruse K, Fukamachi S, Mitani H, Kondo M, Matsuoka T, Kondo S, Hanamura N, Morita Y, Hasegawa K, Nishigaki R, Shimada A, Wada H, Kusakabe T, Suzuki N, Kinoshita M, Kanamori A, Terado T, Kimura H, Nonaka M, Shima A (2000) A detailed linkage map of medaka, Oryzias latipes: comparative genomics and genome evolution. Genetics 154:1773–1784

    PubMed  CAS  Google Scholar 

  • Ozaki A, Sakamoto T, Khoo S-K, Nakamura K, Coimbra MRM, Akutsu T, Okamoto N (2001) Quantitative trait loci (QTLs) associated with resistance/susceptibility to infectious pancreatic necrosis virus (IPNV) in rainbow trout (Oncorhynchus mykiss). Mol Genet Genom 265:23–31

    Article  CAS  Google Scholar 

  • Ozaki A, Khoo S-K, Yoshiura Y, Ototake M, Sakamoto T, Dijkstra JM, Okamoto N (2007) Identification of additional quantitative trait loci (QTL) responsible for susceptibility to infectious pancreatic necrosis virus in rainbow trout. Fish Pathol 42:131–140

    Article  Google Scholar 

  • Palti Y, Nichols KM, Waller KI, Parsons JE, Thorgaard GH (2001) Association between DNA polymorphisms tightly linked to MHC class II genes and IHN virus resistance in backcrosses of rainbow and cutthroat trout. Aquaculture 194:283–289

    Article  CAS  Google Scholar 

  • Palti Y, Silverstein JT, Wieman H, Phillips JG, Barrows FT, Parsons JE (2006) Evaluation of family growth response to fishmeal and gluten-based diets in rainbow trout (Oncorhynchus mykiss). Aquaculture 255:548–556

    Article  CAS  Google Scholar 

  • Palti Y, Rodriguez MF, Gahr SA, Hansen JD (2007) Evolutionary history of the ABCB2 genomic region in teleosts. Develop Comp Immunol 31:483–498

    Article  CAS  Google Scholar 

  • Phillips RB, Zimmerman A, Noakes MA, Palti Y, Morasch MRW, 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  PubMed  CAS  Google Scholar 

  • Rexroad CE, Palti Y (2003) Development of ninety-seven polymorphic microsatellite markers for rainbow trout. Trans Am Fish Soc 132:1214–1221

    Article  CAS  Google Scholar 

  • Rexroad CE, Danzmann RG, Palti Y, Vallejo RL (2006) The NCCCWA genetic linkage map for rainbow trout. Plant & Animal Genome XIV, The International Conference on the Status of Plant and Animal Genome Research, San Diego, CA, p 261

  • Rodriguez F, Rexroad CE, Palti Y (2003) Characterization of twenty-four microsatellite markers for rainbow trout (Oncorhynchus mykiss). Mol Ecol Notes 3:619–622

    Article  CAS  Google Scholar 

  • Rodriguez M, Gahr S, Rexroad C, Palti Y (2006) A polymerase chain reaction screening method for rapid detection of microsatellites in bacterial artificial chromosomes. Mar Biotech 8:346–350

    Article  CAS  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  PubMed  CAS  Google Scholar 

  • Shiina T, Dijkstra JM, Shimizu S, Watanabe A, Yanagiya K, Kiryu I, Fujiwara A, Nishida-Umehara C, Kaba Y, Hirono I, Yoshiura Y, Aoki T, Inoko H, Kulski JK, Ototake M (2005) 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

    Article  PubMed  CAS  Google Scholar 

  • Stephens M, Smith NJ, Donnelly P (2001) A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 68:978–989

    Article  PubMed  CAS  Google Scholar 

  • Stephens M, Scheet P (2005) Accounting for decay of linkage disequilbrium in haplotype inference and missing-data imputation. Am J Hum Genet 76:449–462

    Article  PubMed  CAS  Google Scholar 

  • Stet RJ, Kruiswijk CP, Dixon B (2003) Major histocompatibility lineages and immune gene function in teleost fishes: the road not taken. Crit Rev Immunol 23:441–471

    Article  PubMed  CAS  Google Scholar 

  • Thankappan A, Fuller JR, Godwin UB, Kearse KP, McConnell TJ (2006) Characterization of glycans on major histocompatibility complex class II molecules in channel catfish, Ictalurus punctatus. Dev Comp Immunol 30:772–782

    Article  PubMed  CAS  Google Scholar 

  • Thorsen JB, Zhu E, Frengen K, Osegawa PJ, deJong PJ, Koop BF, Davidson WS, Hoyhein BA (2005) A highly redundant BAC library of Atlantic salmon (Salmo salar): an important tool for salmon projects. BMC Genomics 6:50

    Article  PubMed  CAS  Google Scholar 

  • Yazdi MH, Visscher PM, Ducrocq V, Thompson R (2002) Heritability, reliability of genetic evaluations and response to selection in proportional hazards models. J Dairy Sci 85:1563–1577

    Article  PubMed  CAS  Google Scholar 

  • Zhang YX, Chen SL, Liu YG, Sha ZX, Liu ZJ (2006) Major histocompatibility complex class IIB allele polymorphism and its association with resistance/susceptibility to Vibrio anguillarum in Japanese flounder (Paralichthys olivaceus). Mar Biotechnol 8:600–610

    Article  PubMed  CAS  Google Scholar 

  • Zhang YX, Chen SL (2006) Molecular identification, polymorphism, and expression analysis of major histocompatibility complex class IIA and B genes of turbot (Scophthalmus maximus). Mar Biotechnol 8:611–623

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank Dr. Caird Rexroad III, M. Renee Fincham, Melissa Johnson, Kristy Shewbridge, and Roseanna Long for their technical contribution and assistance, Dr. Scott Gahr for his guidance during RNA extraction and cDNA synthesis (supplement A), Dr. J. M. (Hans) Dijkstra for suggestions and for sharing findings from his own research, and Dr. John Hansen for sharing unpublished sequences of the MH-IA and MH-IB genomic regions in rainbow trout.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yniv Palti.

Electronic Supplementary Materials

Below is the link for the electronic supplementary materials

ESM 1

(DOC 56 kb)

ESM 2

(DOC 43 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Johnson, N.A., Vallejo, R.L., Silverstein, J.T. et al. Suggestive Association of Major Histocompatibility IB Genetic Markers with Resistance to Bacterial Cold Water Disease in Rainbow Trout (Oncorhynchus mykiss). Mar Biotechnol 10, 429–437 (2008). https://doi.org/10.1007/s10126-007-9080-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10126-007-9080-7

Keywords

Navigation