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Organization of a β and α Globin Gene Set in the Teleost Atlantic Cod, Gadus morhua

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Abstract

Developmental globin gene expression and gene switching in vertebrates have been extensively studied. Globin gene regions have been characterized in some fish species and show linked α and β loci. Understanding coordinated expression between α and β globin genes in fish is of importance for further insights into globin gene regulation in teleosts and higher vertebrates. We characterize linked β and α globin genes in Atlantic cod, pulled from the Atlantic cod genome with a PCR research strategy, by screening a genomic λ library and primer walking. The genes are oriented tail-to-head (5′–3′), differing from the head-to-head orientation in transcriptional polarity characteristic of teleostean globin genes. Four tandem repeats are found in an intergenic region of 1500 base pairs. One microsatellite, which consists primarily of atg tandem repeats, has an open reading frame. The globin genes and open reading frame have a CCAAT promoter element and TATA boxes. The promoters of the open reading frame and the β gene share an 89-bp block (with 100% identity) that probably regulates transcription.

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References

  • Agarwall S, Arya V, Stolle C, Pradhan M (2006) A novel Indian β-thalassemia mutation in the CACCC box of the promoter region. Eur J Heamat 77:530–532

    Article  Google Scholar 

  • Altschul S, Gish W, Miller W, Myers E, Lipman D (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    CAS  PubMed  Google Scholar 

  • Árnason E (2004) Mitochondrial cytochrome b DNA variation in the high fecundity Atlantic cod: Trans-atlantic clines and shallow gene-genealogy. Genetics 166:1871–1885

    Article  PubMed  Google Scholar 

  • Ashe H, Monks J, Wijgerde M, Fraser P, Proudfoot N (1997) Intergenic transcription and transinduction of the human β-globin locus. Genes Dev 249:4–2509

    Google Scholar 

  • Berenbrink M, Koldkjær P, Kepp O, Cossins AR (2005) Evolution of oxygen secretion in fishes and the emergence of a complex physiological system. Science 307:1752–1757

    Article  CAS  PubMed  Google Scholar 

  • Brownlie A, Hersey C, Oates AC, Paw BH, Falick AM, Witkowska HE, Flint J, Higgs D, Jessen J, Bahary N, Zhu H, Lin S, Zon L (2003) Characterization of embryonic globin genes of the zebrafish. Dev Biol 255:48–61

    Article  CAS  PubMed  Google Scholar 

  • Bulger M, Doorninck J, Saitoh N, Telling A, Farrell C, Bender M, Felsenfeld G, Axel R, Groudine M (1999) Conservation of sequence and structure flanking the mouse and human β-globin loci: The β-globin genes are embedded within an array of odorant receptor genes. Proc Natl Acad Sci USA 96:5129–5134

    Article  CAS  PubMed  Google Scholar 

  • Burge C, Karlin S (1997) Prediction of complete gene structures in human genomic DNA. J Mol Biol 268:78–94

    Article  CAS  PubMed  Google Scholar 

  • Chan F, Robinson J, Brownlie A, Shivdasani RA, Donovan A, Brugnara C, Kim J, Lau B, Witkowska HE, Zon LI (1997) Characterization of adult α- and β-globin genes in the zebrafish. Blood 89:688–700

    CAS  PubMed  Google Scholar 

  • Cohen R, Sheffery M, Kim C (1986) Partial purification of a nuclear protein that binds to the CCAAT box of the mouse alpha 1-globin gene. Mol Cell Biol 6:821–832

    CAS  PubMed  Google Scholar 

  • Dickerson RE, Geis I (1983) Hemoglobin: structure, function, evolution and pathology. The Benjamin/Cummings Publishing Company, Inc, Menlo Park, California

    Google Scholar 

  • Ewing B, Green P (1998) Basecalling of automated sequencer traces using phred. II. Error probabilities. Genome Res 8:186–194

    CAS  PubMed  Google Scholar 

  • Ewing B, Hillier L, Wendl M, Green P (1998) Base-calling of automated sequencer traces using phred. I. accuracy assessment. Genome Res 8:175–185

    CAS  PubMed  Google Scholar 

  • Fang X, Han H, Stamatoyannopoulos G, Li Q (2004) Developmentally specific role of the CCAAT box in regulation of human γ-globin gene expression. J Biol Chem 279(7):5444–5449

    Article  CAS  PubMed  Google Scholar 

  • Feng Y, Warin R, Li T, Olivier E, Besse A, Lobell A, Fu H, Lin C, Aladjem M, Bouhassira E (2005) The human β-globin locus control region can silence as well as activate gene expression. Mol Cell Biol 25:3864–3874

    Article  CAS  PubMed  Google Scholar 

  • Filipe A, Li Q, Deveaux S, Godin I, Roméo P, Stamatoyannopoulos G, Mignotte V (1999) Regulation of embryonic/fetal globin genes by nuclear hormone receptors: a novel perspective on hemoglobin switching. EMBO J 18:687–697

    Article  CAS  PubMed  Google Scholar 

  • Gillemans N, McMorrow T, Tewari R, Wai A, Burgtorf C, Drabek D, Ventress N, Langeveld A, Higgs D, Tan-Un K, Grosveld F, Philipsen S (2003) Functional and comparative analysis of globin loci in pufferfish and humans. Blood 101(7):2842–2849

    Google Scholar 

  • Gish W, States D (1993) Identification of protein coding regions by database similarity search. Nat Genet 3:266–272

    Article  CAS  PubMed  Google Scholar 

  • Gordon D, Abajian C, Green P (1998) Consed: A graphical tool for sequence finishing. Genome Res 8:195–202

    CAS  PubMed  Google Scholar 

  • Hardison R (1998) Hemoglobins from bacteria to man: evolution of different patterns of gene expression. J Exp Biol 201:1099–1117

    CAS  PubMed  Google Scholar 

  • Harju S, Navas P, Stamatoyannopoulos G, KR P (2005) Genome architecture of the human β-globin locus affects developmental regulation of gene expression. Mol Cell Biol 25:8765–8778

    Article  CAS  PubMed  Google Scholar 

  • Hoegg S, Brinkmann H, Taylor J, Meyer A (2004) Phylogenetic timing of the fish-specific genome duplication correlates with the diversification of teleost fish. J Mol Evol 59:190–203

    Article  CAS  PubMed  Google Scholar 

  • Hosbach H, Wyler T, Weber R (1983) The Xenopus laevis globin gene family: Chromosomal arrangement and gene structure. Cell 32:45–53

    Article  CAS  PubMed  Google Scholar 

  • Ji X, Liu D, Xu D, Li L, Wang J, Liang C (2000) Both locus control region and proximal regulatory elements direct the developmental regulation of β-globin gene cluster. J Cell Biochem 76:376–385

    Article  CAS  PubMed  Google Scholar 

  • Johnson R, Prychitko T, Gumucio D, Wildman D, Uddin M, Goodman M (2005) Phylogenetic comparisons suggest that distance from the locus control region guides developmental expression of primate β-type globin genes. Proc Natl Acad Sci USA 103:3186–3191

    Article  Google Scholar 

  • Karlsson S, Nienhuis A (1985) Developmental regulation of human globin genes. Annu Rev Biochem 54:1071–1108

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Korol A, Fahima T, Nevo E (2004) Microsatellites within genes: structure, function, and evolution. Mol Biol Evol 21:991–1007

    Article  CAS  PubMed  Google Scholar 

  • Lynch M, Force A (2000) The probability of duplicate-gene preservation by subfunctionalization. Genetics 154:459–473

    CAS  PubMed  Google Scholar 

  • Maruyama K, Yasumasu S, Naruse K, Mitani H, Shima A, Iuchi I (2004) Genomic organization and developmental expression of globin genes in the teleost Oryzias latipes. Gene 335:89–100

    Article  CAS  PubMed  Google Scholar 

  • Maruyama K, Ishikawa Y, Yasumasu S, Iuchi I (2007) Globin gene enhancer activity of a dnase-i hypersensitivesite-40 homolog in medaka, Oryzias latipes. Zool Sci 24:997–1004

    Article  CAS  PubMed  Google Scholar 

  • Omori A, Tanabe O, Engel J, Fukamizu A, Tanimoto K (2005) Adult stage γ-globin silencing is mediated by a promoter direct repeat element. Mol Cell Biol 25:3443–3451

    Article  CAS  PubMed  Google Scholar 

  • Paradis E, Strimmer K, Claude J, Jobb G, Opgen-Rhein R, Dutheil J, Noel Y, Bolker B (2005) Ape: analyses of phylogenetics and evolution R package version 1.6

  • R Development Core Team (2006) R: a language and environment for statistical computing R foundation for statistical computing Vienna, Austria ISBN 3-900051-07-0

  • Rice P, Longden I, Bleasby A (2000) Emboss: The European molecular biology open software suite. Trends Genet 16:276–277

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Sambrook J, Fritsch E, Maniatis T (1989) Molecular cloning a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, New York, NY

    Google Scholar 

  • Sandelin A, Bailey P, Bruce S, Engstrom P, Klos J, Wasserman W, Ericson J, Lenhard B (2004) Arrays of ultraconserved non-coding regions span the loci of key developmental genes in vertebrate genomes BMC. Genomics 5:99

    Article  PubMed  Google Scholar 

  • Shen W, Liu D, Liang C (2002) The regulatory network controlling β-globin gene switching. Mol Biol Rep 28:175–183

    Article  Google Scholar 

  • Shimeld S (1999) Gene function, gene networks and the fate of duplicated genes. Cell Devel Biol 10:549–553

    Article  CAS  Google Scholar 

  • Sick K (1965) Hemoglobin polymorphisms of cod in the Baltic and the Danish Belt sea. Hereditas 54:19–48

    Article  CAS  PubMed  Google Scholar 

  • Sjakste N, Sjakste T (2002) Structure of globin gene domains in mammals and birds. Russ J Genet 38:1343–1358

    Article  CAS  Google Scholar 

  • Wagner A, Deryckere F, McMorrow T, Gannon F (1994) Tail-to-tail orientation of the Atlantic salmon alpha- and beta-globin genes. J Mol Evol 38:28–35

    Article  CAS  PubMed  Google Scholar 

  • Walsh PS, Metzger DA, Higuchi R (1991) Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. BioTechniques 10:506–513

    CAS  PubMed  Google Scholar 

  • Woolfe A, Goodson M, Goode D, Snell P, McEwen G, Vavouri T, Smith S, North P, Callaway H, Kelly K, Walter K, Abnizova I, Gilks W, Edwards Y, Cooke J, Elgar G (2005) Highly conserved non-coding sequences are associated with vertebrate development. PLoS Biol 3:116–130

    Article  CAS  Google Scholar 

  • Zhang J (2003) Evolution by gene duplication: an update. Trends Ecol Evol 18:292–299

    Article  Google Scholar 

  • Zhang Z, Schwartz S, Wagner L, Miller W (2000) A greedy algorithm for aligning DNA sequences. J Comput Biol 7:203–214

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Prof. Lars Pilström, Uppsala University, for giving us copies of a λ genomic library, and Prof. Jarle Mork at NTNU in Trondheim for tissue samples of genotyped individuals. The study was supported by a grant from the Icelandic Research Fund. We thank Dr. Petur Henry Petersen, and an anonymous reviewer for critical and helpful comments on the manuscript.

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  1. Institute of Biology, University of Iceland, Sturlugata 7, Reykjavík, Iceland

    Katrín Halldórsdóttir & Einar Árnason

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  1. Katrín Halldórsdóttir
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  2. Einar Árnason
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Correspondence to Katrín Halldórsdóttir.

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Halldórsdóttir, K., Árnason, E. Organization of a β and α Globin Gene Set in the Teleost Atlantic Cod, Gadus morhua . Biochem Genet 47, 817–830 (2009). https://doi.org/10.1007/s10528-009-9280-0

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  • DOI: https://doi.org/10.1007/s10528-009-9280-0

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