Skip to main content
SpringerLink
Log in

The organization of the β-globin gene of the bivalve mollusc Anadara trapezia and its evolutionary relationship to other invertebrate and vertebrate globin genes

  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Abstract

Three pairs of oligonucleotide primers based on partial DNA and amino acid sequences were used in a combination of PCR experiments to amplify the β-globin gene of the bivalve mollusc Anadara trapezia. The sequence of 2,139 by presented contains the whole of the β-globin gene with the exception of the 5′ flanking sequence. This gene possesses the three-exon-and-two-intron gene structure typical of vertebrate globin genes but the lengths of the introns (762 by and 690 bp, respectively) are only approximately half the size of those present in a β-variant gene previously characterized from this organism. The encoded amino acid sequence shows two changes when compared to the previously published amino acid sequence.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Antoine M, Niessing J (1984) Intron-less globin genes in the insect Chironomus thummi thummi. Nature 310: 795–798

    Google Scholar 

  • Blake CCF (1981) Exons and the structure, function and evolution of haemoglobin. Nature 291:616

    Google Scholar 

  • Blanchetot A, Wilson V, Wood D, Jeffreys AJ (1983) The seal myoglobin gene: an unusually long globin gene. Nature 301:732–734

    Google Scholar 

  • Blin N, Stafford DW (1976) A general method for isolation of high molecular weight DNA from eukaryotes. Nucleic Acids Res 3:2303–2308

    Google Scholar 

  • Bogusz D, Appleby CA, Landsmann J, Dennis ES, Trinick MJ, Peacock WJ (1988) Functioning haemoglobin genes in non-nodulating plants. Nature 331:178–180

    Google Scholar 

  • Breathnach R, Benoist C, O'Hare K, Gannon F, Chambon P (1978) Ovalbumin gene: evidence for a leader sequence in mRNA anc DNA sequences at the exon-intron boundaries. Proc Nall Acad Sci. USA 75:4853–4857

    Google Scholar 

  • Breathnach R, Chambon P (1981) Organization and expression of eucaryotic split genes coding for proteins. Ann Rev Biochem 50:349–383

    Google Scholar 

  • Chiancone E, Vecchini P, Verzili D, Ascoli F, Antonini E (1981) Dimeric and tetrameric hemoglobins from the mollusc Scapharca inaequivalvis. Structural and functional properties. J Mol Biol 152:577–592

    Google Scholar 

  • Collett LC, O'Gower AK (1972) Molluscan haemoglobins with unusual temperature-dependent characteristics. Comp Biochem Physiol 41A:843–850

    Google Scholar 

  • Como PF, Thompson EOP (1980) Amino acid sequence of the α-chair of the tetrameric haemoglobin of the bivalve mollusc Anadara trapezia. Aust J Biol Sci 33:653–664

    Google Scholar 

  • Dixon B, Walker B, Kimmins W, Pohajdak B (1992) A nematode hemoglobin gene contains an intron previously thought to be unique to plants. J Mol Evol 35:131–136

    Google Scholar 

  • Dixon B, Pohajdak B (1992) Did the ancestral globin gene of plants and animals contain only two introns? Trends Biochem Sci 17: 486–488

    Google Scholar 

  • Dixon PI (1976) The biology of Anadara trapezia with particular reference to its haemoglobin. Malacol Rev 9:139

    Google Scholar 

  • Djangmah IS, Gabbott PA, Wood EJ (1978) Physico-chemical characteristics and oxygen-binding properties of the multiple hemoglobins of the West African blood clam Anadara senilis (L). Comp Biochem Physiol 60B:245–250

    Google Scholar 

  • Fisher WK, Gilbert AT, Thompson EOP (1984) Amino acid sequence of the globin IIB chain of the dimeric haemoglobin of the bivalve mollusc Anadara trapezia. Aust J Biol Sci 37:191–203

    Google Scholar 

  • Furuta H, Ohe M, Kajita A (1977) Subunit structure of hemoglobins from erythrocytes of the blood clam, Anadara broughtonii. J Biochem (Tokyo) 82:1723–1730

    Google Scholar 

  • Furuta H, Kajita A (1983) Dimeric hemoglobin of the bivalve mollusc Anadara broughtonii: complete amino acid sequence of the globin chain. Biochemistry 22:917–922

    Google Scholar 

  • Furuta H, Kajita A (1991) Primary structure of the beta chain of the tetrameric hemoglobin from Anadara broughtonii. In: Vinogradov SN, Kapp OH (eds) Structure and function of invertebrate oxygen carriers. Springer-Verlag, New York, pp 257–260

    Google Scholar 

  • Gilbert AT, Thompson EOP (1985) Amino acid sequence of the β-chain of the tetrameric haemoglobin of the bivalve mollusc, Anadara trapezia. Aust J Biol Sci 38:221–236

    Google Scholar 

  • Glenn WK, Titchen DA, Thompson EOP, Mackinlay AG (1993) Characterization of a repeated sequence occurring within an intron of a globin gene in the bivalve mollusc Anadara trapezia. (manuscript in preparation)

  • Heery DM, Gannon F, Powell R (1990) A simple method for subcloning DNA fragments from gel slices. Trends Genet 6:173

    Google Scholar 

  • Ish-Horowicz D, Burke JF (1981) Rapid and efficient cosmid cloning. Nucleic Acids Res 9:2989–2998

    Google Scholar 

  • Jensen EØ Paludan K, Hyldig-Nielsen JJ, Jørgensen P, Marcker KA (1981) The structure of a chromosomal leghemoglobin gene from soybean. Nature 291:677–679

    Google Scholar 

  • Jhiang SM, Garey JR, Riggs AF (1988) Exon-intron organization in genes of earthworm and vertebrate globins. Science 240:334–336

    Google Scholar 

  • Jhiang SM, Riggs AF (1989) The structure of the gene encoding chain c of the hemoglobin of the earthworm, Lumbricus terrestris. J Biol Chem 264:19003–19008

    Google Scholar 

  • Keller EB, Noon WA (1984) Intron splicing: a conserved internal signal in introns of animal pre-mRNAs. Proc Natl Acad Sci USA 81: 7417–7420

    Google Scholar 

  • Landsmann J, Dennis ES, Higgins TJV, Appleby CA, Kortt AA, Peacock WJ (1986) Common evolutionary origin of legume and nonlegume plant haemoglobins. Nature 324:166–168

    Google Scholar 

  • Mann RG, Fisher WK, Gilbert AT, Thompson EOP (1986) Genetic variation of the dimeric hemoglobin of the bivalve mollusc Anadara trapezia. Aust J Biol Sci 39:109–115

    Google Scholar 

  • Moens L, Vanfleteren J, De Baere I, Jellie AM, Tate W, Trotman CNA (1992) Unexpected intron location in non-vertebrate globin genes. FEBS Lett 312:105–109

    Google Scholar 

  • Morris SC, George JD, Gibson R, Platt HM (1985) The Origins and relationships of lower invertebrates. Oxford University Press, Oxford

    Google Scholar 

  • Mount SM (1982) A catalogue of splice junction sequences. Nucleic Acids Res 10:459–473

    CAS  PubMed  Google Scholar 

  • Naito Y, Riggs CK, Vandergon TL, Riggs AF (1991) Origin of a “bridge” intron in the gene for a two-domain globin. Proc Natl Acad Sci USA 88:6672–6676

    Google Scholar 

  • Nicol PI, O'Gower AK (1967) Haemoglobin variation in Anadara trapezia. Nature 216:684

    Google Scholar 

  • Nassif NT, Mackinlay AG, Thompson EOP (1993) PCR amplification of partial mRNA sequences encoding the α- and β-globin chains of the bivalve mollusc Anadara trapezia: correction of the C-terminal amino acid sequence of the α chain. Comp Biochem Physiol 105B:283–287

    Google Scholar 

  • O'Gower AK, Nicol PI (1968) A latitudinal cline of haemoglobins in a bivalve mollusc. Heredity 23:458–491

    Google Scholar 

  • Petruzzelli R, Goffredo BM, Barra D, Bossa F, Boffi A, Verzili D, Ascoli F, Chiancone E (1985) Amino acid sequence of the cooperative homodimeric hemoglobin from the mollusc Scapharca inaequivalvis and topology of the intersubunit contacts. FEBS Lett 184:328–332

    Google Scholar 

  • Petruzzelli R, Boffi A, Barra D, Bossa F, Ascoli F, Chiancone E (1989) Scapharca hemoglobins, type cases of a novel mode of chain assembly and heme-heme communication. Amino acid sequence and subunit interactions of the tetrameric component. FEBS Lett 259:133–136

    Google Scholar 

  • Purchon RD (1978) The Biology of the mollusca, 2nd ed. Pergamon Press Ltd, Oxford

    Google Scholar 

  • Royer WE, Love WE, Fenderson FF (1985) Cooperative dimeric and tetrameric clam haemoglobins are novel assemblages of myoglobin folds. Nature 316:277–280

    Google Scholar 

  • Sherman DR, Kloek AP, Krishnan BR, Guinn B, Goldberg DE (1992) Ascaris hemoglobin gene: plant-like structure reflects the ancestral globin gene. Proc Natl Acad Sci USA 89:11696–11700

    Google Scholar 

  • Spritz RA, Forget BG (1983) The thalassemias: molecular mechanisms of human genetic disease. Am J Hum Gen 35:333–361

    Google Scholar 

  • Stoltzfus A, Doolittle WF (1993) Slippery introns and globin gene evolution. Curr Biol 3:215–217

    Google Scholar 

  • Sulston J, Du Z, Thomas K, Wilson R, Hillier L, Staden R, Halloran N, Green P, Thierry-Mieg J, Qiu L, Dear S, Coulson A, Craxton M, Durbin R, Berks M, Metzstein M, Hawkins T, Ainscough R, Waterston R (1992) The C. elegans genome sequencing project: a beginning. Nature 356:37–40

    Google Scholar 

  • Titchen DA, Glenn WK, Nassif N, Thompson AR, Thompson EOP (1991) A minor globin gene of the bivalve mollusc Anadara trapezia. Biochim Biophys Acta 1089:61–67

    Google Scholar 

  • Triglia T, Peterson MG, Kemp DJ (1988) A procedure for in vitro amplification of DNA segments that lie outside the boundaries of known sequences. Nucleic Acids Res 16:81–86

    Google Scholar 

  • Weller P, Jeffreys AJ, Wilson V, Blanchetot A (1984) Organization of the human myoglobin gene. EMBO J 3:439–446

    Google Scholar 

  • Yagi Y, Mishima T, Tsujimura T, Sato K, Egami F (1957) Studies on the hemoglobin of Anadara inflata (Reeve). 1. Purification and properties of the crystalline hemoglobin. J Biochem (Tokyo) 44:1–10

    Google Scholar 

  • Yamauchi K, Ochiai T, Usuki I (1992) The unique structure of the Paramecium caudatum hemoglobin gene: the presence of one intron in the middle of the coding region. Biochim Biophys Acta 1171:81–87

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. School of Biochemistry and Molecular Genetics, University of New South Wales, P.O. Box 1, Kensington, N.S.W. 2033, Australia

    N. T. Nassif, W. K. Glenn & A. G. Mackinlay

Authors
  1. N. T. Nassif
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. W. K. Glenn
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. G. Mackinlay
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Correspondence to: A.G. Mackinlay

Rights and permissions

Reprints and permissions

About this article

Cite this article

Nassif, N.T., Glenn, W.K. & Mackinlay, A.G. The organization of the β-globin gene of the bivalve mollusc Anadara trapezia and its evolutionary relationship to other invertebrate and vertebrate globin genes. J Mol Evol 39, 47–55 (1994). https://doi.org/10.1007/BF00178248

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00178248

Key words

Search

Navigation