Skip to main content
SpringerLink
Log in

Different evolution rates within the lens-specificβ-crystallin gene family

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

Summary

We have determined the sequence of a rat βA3/A1-crystallin complementary DNA (cDNA) clone and the (partial) sequence of the human βB3-crystallin gene. Calculation of the ratio of silent to nonsynonymous substitution between orthologous βA3/A1-, βB3-, and other β- and γ-crystallin sequences revealed that the region encoding the two globular domains of the βA3/A1-crystallin sequence is the best conserved during evolution, much better than the corresponding region of the βB1-, βB3-, or the γ-crystallin sequences, and even better (at least in the rodent/frog comparison) that the well-conserved αA-crystallin sequence. Remarkably, the rate of change of the βA3/A1-crystallin coding sequence does not differ in the rodent and primate lineages, in contrast with previous findings concerning the evolution rates of the αA- or γ-crystallin sequences in these two lineages. Comparison of the regions that encode the four motifs of the β-crystallin between orthologous mammalian sequences showed that the extent of nonsynonymous substitution in each of these four homologous motif regions is the same. However, when the orthologous β-crystallin genes of more distantly related species (mammals vs chicken or frog) are compared, the extent of nonsynonymous substitution is higher in the regions encoding the external motifs I and III than in the regions encoding the internal motifs II and IV. This phenomenon is also observed when paralogous members of the β/γ-crystallin supergene family are compared.

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

  • Aarts HJM, Den Dunnen JT, Lubsen NH, Schoenmakers JGG (1987) Linkage between the βB2 and βB3 crystallin genes in man and rat: a remnant of an ancient β-crystallin gene cluster. Gene 59:127–135

    PubMed  Google Scholar 

  • Aarts HJM, Den Dunnen JT, Leunissen J, Lubsen NH, Schoenmakers JGG (1988) The γ-crystallin gene families: sequence and evolutionary patterns. J Mol Evol 27:163–172

    PubMed  Google Scholar 

  • Berbers GAM, Hoekman WA, Bloemendal H, De Jong WW, Kleinschmidt T, Braunitzer G (1984) Homology between the primary structures of the major bovine β-crystallin chains. Eur J Biochem 139:467–479

    PubMed  Google Scholar 

  • Bloemendal H (1985) Lens research: from protein to gene. Exp Eye Res 41:429–448

    PubMed  Google Scholar 

  • Blundell T, Lindley P, Miller L, Moss D, Slingsby C, Tickle I, Turnell B, Wistow G (1981) The molecular structure and stability of the eye lens: x-ray analysis of γ-crystallin II. Nature 289:771–777

    PubMed  Google Scholar 

  • Dayhoff MO (1972) Atlas of protein sequences and structure, vol 5. National Biomedical Research Foundation, Silver Spring MD

    Google Scholar 

  • De Jong WW (1981) Evolution of lens and crystallins. In: Bloemendal H (ed) Molecular and cellular biology of the eye lens. John Wiley and Sons, New York, pp 221–278

    Google Scholar 

  • Delaye M, Tardieu A (1983) Short-range order of crystallin proteins accounts for eye lens transparency. Nature 302:415–417

    PubMed  Google Scholar 

  • Den Dunnen JT, Moormann RJM, Schoenmakers JGG (1985a) Rat lens β-crystallins are internally duplicated and homologous to γ-crystallins. Biochim Biophys Acta 824:295–303

    PubMed  Google Scholar 

  • Den Dunnen JT, Moormann RJM, Cremers FPM, Schoenmakers JGG (1985b) Two human γ-crystallin genes are linked and riddled with alu-repeats. Gene 38:197–204

    PubMed  Google Scholar 

  • Den Dunnen JT, Moormann RJM, Lubsen NH, Schoenmakers JGG (1986a) Intron insertions and deletions in the β-/γ-crystallin gene family: the rat βB1-gene. Proc Natl Acad Sci USA 83:2855–2859

    PubMed  Google Scholar 

  • Den Dunnen JT, Moormann RJM, Lubsen NH, Schoenmakers JGG (1986b) Concerted and divergent evolution within the rat γ-crystallin gene family. J Mol biol 189:37–46

    PubMed  Google Scholar 

  • Den Dunnen JT, Van Neck JW, Cremers FPM, Lubsen NH, Schoenmakers JGG (1988) Nucleotide sequence of the rat γ-crystallin gene region and comparison with an orthologous human region. Gene (in press)

  • Hejtmancik JF, Thompson MA, Wistow G, Piatigorsky J (1986) cDNA and deduced protein sequence for the βB1-crystallin polypeptide of the chicken lens. Conservation of the PAPA sequence. J Biol Chem 261:982–987

    PubMed  Google Scholar 

  • Hogg D, Tsui L-C, Gorin M, Breitman ML (1986) Characterization of the human β-crystallin gene Hu\A3/A1 reveals ancestral relationships among the βγ-crystallin superfamily. J Biol Chem 261:12420–12427

    PubMed  Google Scholar 

  • Hogg D, Gorin MB, Heinzmann C, Zollman S, Mohandas T, Klisak I, Sparkes RS, Breitman M, Tsui L-C, Horwitz J (1987) Nucleotide sequence for the cDNA of the bovine βB2 crystallin and assignment of the orthologous human locus to chronosome 22. Curr Eye Res 6:1335–1342

    PubMed  Google Scholar 

  • Inana G, Piatigorsky J, Norman B, Slingsby C, Blundell T (1983) Gene and protein structure of the β-crystallin polypeptide in murine lens: relationship of exons and structural motifs. Nature 302:310–315

    PubMed  Google Scholar 

  • Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HN (ed) Mammalian protein metabolism. Academic Press, New York, pp 21–123

    Google Scholar 

  • King CR, Shinohara T, Piatigorsky J (1982) αA-crystallin mesenger RNA of the mouse lens: more noncoding than coding sequences. Science 215:985–987

    PubMed  Google Scholar 

  • Lapeyre B, Almaric F (1985) A powerful method for the preparation of cDNA libraries: isolation of cDNA encoding a 100-kDal nucleolar protein. Gene 37:215–220

    PubMed  Google Scholar 

  • Law ML, Cai C-Y, Hartz J, Kao F-T, Hogg D, Breitman ML, Tsui L-C (1986) Localization of a β-crystallin gene, the huβ-A3/1 (gene symbol, cryB1), to the long arm of human chromosome-17. Cytogenet Cell Genet 42:202–207

    PubMed  Google Scholar 

  • Li W-H, Tanimura M, Sharp PM (1987) An evaluation of the molecular clock hypothesis using mammalian DNA sequences. J Mol Evol 25:330–342

    PubMed  Google Scholar 

  • Lok S, Tsui L-C, Shinohara T, Piatigorsky J, Gold R, Breitman ML (1984) Analysis of the mouse γ-crystallin gene family: assignment of multiple cDNAs to discrete genomic sequences and characterization of a representative gene. Nucleic Acids Res 12:4517–4529

    PubMed  Google Scholar 

  • Luchin SV, Zinovieva RD, Tomarev SI, Dolgilevich SM, Gause Jr GG, Bax B, Driessen H, Blundell TL (1987) Frog lens βA1-crystallin: the nucleotide sequence of the cloned cDNA and computer graphics modelling of the three-dimensional structure. Biochim Biophys Acta 916:163–171

    PubMed  Google Scholar 

  • Meakin SO, Breitman ML, Tsui L-C (1985) Structural and evolutionary relationships among five members of the human γ-crystallin gene family. Mol Cell Biol 5:1408–1414

    PubMed  Google Scholar 

  • Miyata T, Yasunaga T (1980) Molecular evolution of mRNA: a method for estimating evolutionary rates of synonymous and amino acid substitutions from homologous nucleotide sequences and its application. J Mol Evol 16:23–36

    PubMed  Google Scholar 

  • Moormann RJM, Van der Velden HWM, Dodemont HJ, Andreoli PM, Bloemendal H, Schoenmakers JGG (1981) An unusually long non-coding region in the rat lens α-crystallin messenger RNA. Nucleic Acids Res 9:4813–4822

    PubMed  Google Scholar 

  • Moormann RJM, Den Dunnen JT, Mulleners L, Andreoli PM, Bloemendal H, Schoenmakers JGG (1983) Strict colinearity of genetic and protein folding domains in an intragenically duplicated rat lens γ-crystallin, gene. J Mol Biol 171:353–368

    PubMed  Google Scholar 

  • Moormann RJM, Jongbloed R, Schoenmakers JGG (1984) Isolation and characterization of β- and γ-crystallin genes from rat genomic cosmid libraries. Gene 29:1–9

    PubMed  Google Scholar 

  • Moormann RJM, Den Dunnen JT, Heuyerjans J, Jongloed, RJE, Van Leen RW, Lubsen NH, Schoenmakers JGG (1985) Characterization of the rat γ-crystallin gene family and its expression in the eye lens. J Mol Biol 182:419–430

    PubMed  Google Scholar 

  • Peterson CA, Piatigorsky J (1986) Preferential conservation of the globular domains of the βA3/A1-crystallin polypeptide of the chicken eye lens. Gene 45:139–147

    PubMed  Google Scholar 

  • Quax-Jeuken Y, Janssen G, Quax W, van den Heuvel R, Bloemendal H (1984) Bovine β-crystallin complementary DNA clones. Alternating proline/alanine sequence of βB1 subunit originates from a repetitive DNA sequence. J Mol Biol 180: 457–472

    PubMed  Google Scholar 

  • Quax-Jeuken Y, Driessen H, Leunissen J, Quax W, De Jong W, Bloemendal H (1985) βs-crystallin: structure and evolution of a distinct member of the β/gg-superfamily. EMBO J 4:2597–2602

    PubMed  Google Scholar 

  • Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74: 5463–5467

    PubMed  Google Scholar 

  • Soares MB, Schon E, Henderson A, Karathanasis SK, Cata R, Zeitlin S, chirgwin J, Efstratiadis A (1985) RNA-mediated gene duplication: the rat preproinsulin gene is a functional retroposon. Mol Cell Biol 5:2090–2103

    PubMed  Google Scholar 

  • Tautz D, Trick M, Dover GA (1986) Cryptic simplicity in DNA is a major source of genetic variation. Nature 322:652–656

    PubMed  Google Scholar 

  • Tomarev SI, Zinovieva RD, Dolgilevich SM, Krayev AS, Skryabin KG, Gause Jr GG (1983) The absence of the long 3′-non-translated region in mRNA coding for eye lens αA2-crystallin of the frog (Rana temporaria). FEBS Lett 162:47–51

    PubMed  Google Scholar 

  • Tomarev SI, Zinovieva RD, Chalovka P, Krayev AS, Skryabin KG, Gausse Jr GG (1984) Multiple genes coding for the frog eye lens γ-crystallin. Gene 27:301–308

    PubMed  Google Scholar 

  • Van Leen RW, Van Roozendaal KEP, Lubsen NH, Schoenmakers JGG (1987) Differential expression of crystallin genes during development of the rat eye lens. Dev Biol 120:457–464

    PubMed  Google Scholar 

  • Wistow GJ, Piatigorsky J (1988) Lens crystallins: the evolution and expression of proteins for a highly specialized tissue. Annu Rev Biochem 57:479–504

    PubMed  Google Scholar 

  • Wistow GJ, Slingsby C, Blundell TL, Driessen HPC, De Jong WW, Bloemendal H (1981) Eye lens proteins: the three dimensional structure of β-crystallin predicted from monomeric γ-crystallin. FEBS Lett 133:9–16

    PubMed  Google Scholar 

  • Wistow G, Turnell B, Summers L, Slingsby C, Moss D, Miller L, Lindley P, Blundell T (1983) X-ray analysis of the lens protein γ-II crystallin at 1.9 Å resolution. J Mol Biol 170: 175–202

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratory of Molecular Biology, University of Nijmegen, Toernooiveld, 6525 ED, Nijmegen, The Netherlands

    Henk J. M. Aarts, Eldine H. M. Jacobs, Gijsbert van Willigen, Nicolette H. Lubsen & John G. G. Schoenmakers

Authors
  1. Henk J. M. Aarts
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Eldine H. M. Jacobs
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gijsbert van Willigen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Nicolette H. Lubsen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. John G. G. Schoenmakers
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Aarts, H.J.M., Jacobs, E.H.M., van Willigen, G. et al. Different evolution rates within the lens-specificβ-crystallin gene family. J Mol Evol 28, 313–321 (1989). https://doi.org/10.1007/BF02103427

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02103427

Key words

Search

Navigation