Skip to main content
Log in

Globin evolution in the genusXenopus: Comparative analysis of cDNAs coding for adult globin polypeptides ofXenopus borealis andXenopus tropicalis

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

Summary

Globin mRNAs ofXenopus borealis andXenopus tropicalis have been cloned and sequenced. The nucleotide and derived amino acid sequences were compared with each other and with already available data fromXenopus laevis. This analysis rendered clear evidence that the common ancestor ofX. laevis andX. borealis, but not ofX. tropicalis, had lost one amino acid of the β-globins prior to a genome duplication event that preceded the segregation of the former two species. Replacement-site substitutions were used to calculate a rough time scale of genome duplication and species segregation. The results suggest an ancient separation between theX. laevis and theX. tropicalis groups occurring approximately 110–120 million years ago. Analysis of the amino acid chains demonstrated various alterations. However, some functional domains, like heme-binding sites andα1β2 contact sites, were subject to a high degree of conservation, indicating the existence of functional constraints on them also in the genusXenopus.

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.

Similar content being viewed by others

References

  • Ahl E (1926) Anura; Aglossa, Xenopodidae. In: Kaiser E (ed) Die Diamantenwüste Südwest-Afrikas, vol 2. D Reimer, Berlin, pp 141–142

    Google Scholar 

  • Andres A-C, Hosbach HA, Weber R (1984) Comparative analysis of the cDNA sequences derived from the larval and the adult αI-globin mRNAs ofXenopus laevis. Biochim Biophys Acta 781:294–301

    PubMed  Google Scholar 

  • Aviv H, Leder P (1972) Purification of biologically active globin messenger RNA by chromatography on oligothymidylic acid-cellulose. Proc Natl Acad Sci USA 69:1408–1412

    PubMed  Google Scholar 

  • Birnboim HC, Doly J (1979) A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res 7:1513–1523

    PubMed  Google Scholar 

  • Bisbee CA, Baker MA, Wilson AC, Hadji-Azimi I, Fischberg M (1977) Albumin phylogeny for clawed frogs (Xenopus). Science 195:785–787

    PubMed  Google Scholar 

  • Broin F de, Buffetaut E, Koeniguer J, Rage J, Russel D, Taquet P, Vergnaud-Grazzini C, Wenz S (1974) La faune de vertébrés continentaux du gisement d'In Beceten (Sénonien du Niger). C R Seances Acad Sci 279:469–472

    Google Scholar 

  • Bürki E, Fischberg M (1985) Evolution of globin expression in the genusXenopus (Anura: Pipidae). Mol Biol Evol 2:270–277

    PubMed  Google Scholar 

  • Efstratiadis A, Posakony JW, Maniatis T, Lawn RM, O'Connell C, Spritz RA, deRiel JK, Forget BG, Weissman SM, Slightom JL, Blechl AE, Smithies O, Baralle FE, Shoulders CC, Proudfoot NJ (1980) The structure and evolution of the human β-globin gene family. Cell 21:653–668

    Article  PubMed  Google Scholar 

  • Estes R (1975a) FossilXenopus from the Paleocene of South America and the zoogeography of pipid frogs. Herpetologica 31:263–278

    Google Scholar 

  • Estes R (1975b)Xenopus from the Paleocene of Brazil and its zoogeographic importance. Nature 254:48–50

    Article  Google Scholar 

  • Fermi G (1975) Three-dimensional fourier synthesis of human deoxyhaemoglobin at 2.5 Å resolution: refinement of the atomic model. J Mol Biol 97:237–256

    PubMed  Google Scholar 

  • Goodman M, Moore GW, Barnabas J, Matsuda G (1974) The phylogeny of human globin genes investigated by the maximum parsimony method. J Mol Evol 3:1–48

    Article  PubMed  Google Scholar 

  • Goodman M, Moore GW, Matsuda G (1975) Darwinian evolution in the genealogy of haemoglobin. Nature 253:603–608

    Article  PubMed  Google Scholar 

  • Hosbach HA, Wyler T, Weber R (1983) TheXenopus laevis globin gene family: chromosomal arrangement and gene structure. Cell 32:45–53

    Article  PubMed  Google Scholar 

  • Jeffreys AJ (1981) Recent studies of gene evolution using recombinant DNA. In: Williamson R (ed) Genetic engineering, vol 2. Academic Press, New York, pp 1–48

    Google Scholar 

  • Jeffreys AJ, Wilson V, Wood D, Simons JP, Kay RM, Williams JG (1980) Linkage of adult α- and β-globin genes inX. laevis and gene duplication by tetraploidization. Cell 21:555–564

    Article  PubMed  Google Scholar 

  • Kay RM, Harris R, Patient RK, Williams JG (1983) Complete nucleotide sequence of a cloned cDNA derived from the major adult α-globin mRNA ofX. laevis. Nucleic Acids Res 11: 1537–1542

    PubMed  Google Scholar 

  • Kimura M (1977) Preponderance of synonymous changes as evidence for the neutral theory of molecular evolution. Nature 267:275–276

    Article  PubMed  Google Scholar 

  • Knöchel W, Bladauski D (1981) Cloning of cDNA sequences derived from poly(A)+ nuclear RNA ofXenopus laevis at different developmental stages: Evidence for stage specific regulation. Wilhelm Roux's Archives 190:97–102

    Article  Google Scholar 

  • Knöchel W, Wittig B, Wittig S, John ME, Grundmann U, Oberthür W, Godovac J, Braunitzer G (1982) No evidence for “stress” α-globin genes in chicken. Nature 295:710–712

    Article  PubMed  Google Scholar 

  • Knöchel W, Meyerhof W, Hummel S, Grundmann U (1983) Molecular cloning and sequencing of mRNAs coding for minor adult globin polypeptides ofXenopus laevis. Nucleic Acids Res 11:1543–1553

    PubMed  Google Scholar 

  • Kobel HR, Wolff J (1983) Two transitions of haemoglobin expression inXenopus: from embryonic to larval and from larval to adult. Differentiation 24:24–26

    PubMed  Google Scholar 

  • Lee YM, Friedman DJ, Ayala FJ (1985) Superoxide dismutase: an evolutionary puzzle. Proc Natl Acad Sci USA 82:824–828

    PubMed  Google Scholar 

  • Lewin R (1985) Molecular clocks scrutinized. Science 228:571

    PubMed  Google Scholar 

  • Marotta CA, Wilson JT, Forget BG, Weissman SM (1977) Human β-globin messenger RNA. III. Nucleotide sequences derived from complementary DNA. J Biol Chem 252:5040–5053

    PubMed  Google Scholar 

  • Maxam AM, Gilbert W (1980) Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol 65: 499–560

    PubMed  Google Scholar 

  • May FEB, Weber R, Westley BR (1982) Isolation and characterisation of theXenopus laevis albumin genes: loss of 74K albumin gene sequences by library amplification. Nucleic Acids Res 10:2791–2807

    PubMed  Google Scholar 

  • Meyerhof W, Klinger-Mitropoulos S, Stalder J, Weber R, Knöchel W (1984) The primary structure of the larval β1-globin gene ofXenopus laevis and its flanking regions. Nucleic Acids Res 12:7705–7719

    PubMed  Google Scholar 

  • Meyerhof W, Köster M, Stalder J, Weber R, Knöchel W (1986) Sequence analysis of the larval βu-globin gene ofXenopus laevis. Mol Biol Rep, in press

  • Nevo E (1968) Pipid frogs from the early Cretaceous of Israel and pipid evolution. Bull Mus Comp Zool Harvard Univ 136: 255–318

    Google Scholar 

  • Patient RK, Harris R, Walmsley ME, Williams JG (1983) The complete nucleotide sequence of the major adult β-globin gene ofXenopus laevis. J Biol Chem 258:8521–8523

    PubMed  Google Scholar 

  • Perler F, Efstratiadis A, Lomedico P, Gilbert W, Kolodner R, Dodgson J (1980) The evolution of genes: the chicken preproinsulin gene. Cell 20:555–565

    Article  PubMed  Google Scholar 

  • Reig O (1959) Primeros datos descriptivos sobre los anuros del Eocretaceo de la Provincia de Salta (Rep Argentina). Ameghiniana 1:3–7

    Google Scholar 

  • Richards RJ, Shine J, Ullrich A, Wells JRE, Goodman HM (1979) Molecular cloning and sequence analysis of adult chicken β globin cDNA. Nucleic Acids Res 7:1137–1146

    PubMed  Google Scholar 

  • Richardson C, Capello J, Cochran MD, Armentrout RW, Brown RD (1980) Partial sequence analysis ofXenopus α- and β-globin mRNA as determined from recombinant DNA plasmids. Dev Biol 78:161–172

    Article  PubMed  Google Scholar 

  • Rossi-Fanelli A, Antonini E, Caputo A (1958) Studies on the structure of hemoglobin I. Physicochemical properties of human globin. Biochim Biophys Acta 30:608–615

    Article  PubMed  Google Scholar 

  • Stalder J, Meyerhof W, Wirthmüller U, Gruber A, Wyler T, Knöchel W, Weber R (1986) Conserved sequences and cell specific DNase I hypersensitive sites upstream of the coordinately expressed αI and αII-globin genes ofXenopus laevis. J Mol Biol 188:119–128

    Article  PubMed  Google Scholar 

  • Takeshita S, Aoki T, Fukumaki Y, Takagi Y (1984) Cloning and sequence analysis of a cDNA for the α-globin mRNA of carp,Cyprinus carpio. Biochim Biophys Acta 783:265–271

    PubMed  Google Scholar 

  • Thiebaud C-H, Fischberg M (1977) DNA content in the genusXenopus. Chromosoma 59:253–257

    Article  PubMed  Google Scholar 

  • Tymowska J (1973) Karyotype analysis ofXenopus tropicalis Gray, Pipidae. Cytogenet Cell Genet 12:297–304

    PubMed  Google Scholar 

  • Tymowska J, Fischberg M (1980) The karyotype of the hexaploid speciesXenopus ruwenzoriensis Fischberg and Kobel (Anura: Pipidae). Cytogenet Cell Genet 27:39–44

    PubMed  Google Scholar 

  • Tymowska J, Fischberg M (1982) A comparison of the karyotype, constitutive heterochromatin, and nucleolar organizer regions of the new tetraploid speciesXenopus epitropicalis Fischberg and Picard with those ofXenopus tropicalis Gray (Anura, Pipidae). Cytogenet Cell Genet 34:149–157

    PubMed  Google Scholar 

  • Wahli W, Dawid IB (1980) Isolation of two closely related vitellogenin genes, including their flanking regions, from aXenopus laevis gene library. Proc Natl Acad Sci USA 77: 1437–1441

    PubMed  Google Scholar 

  • Westley B, Wyler T, Ryffel G, Weber R (1981)Xenopus laevis serum albumins are encoded in two closely related genes. Nucleic Acids Res 9:3557–3574

    PubMed  Google Scholar 

  • Williams JG, Kay RM, Patient RK (1980) The nucleotide sequence of the major β-globin mRNA fromXenopus laevis. Nucleic Acids Res 8:4247–4258

    PubMed  Google Scholar 

  • Wilson AC, Carlson SS, White TJ (1977) Biochemical evolution. Annu Rev Biochem 46:573–639

    Article  PubMed  Google Scholar 

  • Wilson JT, Wilson LB, deRiel JK, Villa-Komaroff L, Efstratiadis A, Forget BG, Weissman SM (1978) Insertion of synthetic copies of human globin genes into bacterial plasmids. Nucleic Acids Res 5:563–581

    PubMed  Google Scholar 

  • Wilson JT, Wilson LB, Reddy VB, Cavallesco C, Ghosh PK, deRiel JK, Forget BG, Weissman SM (1980) Nucleotide sequence of the coding portion of human α globin messenger RNA. J Biol Chem 255:2807–2815

    PubMed  Google Scholar 

  • Wu C-I, Li W-H (1985) Evidence for higher rates of nucleotide substitution in rodents than in man. Proc Natl Acad Sci USA 82:1741–1745

    PubMed  Google Scholar 

  • Zain S, Sambrook J, Roberts RJ, Keller W, Fried M, Dunn AR (1979) Nucleotide sequence analysis of the leader segments in a cloned copy of adenovirus 2 fiber mRNA. Cell 16:851–861

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Knöchel, W., Korge, E., Basner, A. et al. Globin evolution in the genusXenopus: Comparative analysis of cDNAs coding for adult globin polypeptides ofXenopus borealis andXenopus tropicalis . J Mol Evol 23, 211–223 (1986). https://doi.org/10.1007/BF02115578

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02115578

Key words

Navigation