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Diversity in a chorion multigene family created by tandem duplications and a putative gene-conversion event

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Summary

Two families of high-cysteine chorion proteins inBombyx mori are encoded in 15 tandemly arranged nonidentical gene pairs. It is assumed that this locus arose by duplication with subsequent sequence divergence. We have compared DNA sequences from two such neighboring pairs of genes in an attempt to understand the manner in which diversity has been generated and/or removed. A high level of sequence identity (91%–99%) was found between the repeats throughout the transcribed and flanking regions, with two significant exceptions. First, in the DNA segment encoding a conserved region of the chorion proteins, ten substitutions were detected in a 39-base-pair region. This localized region of high variability would suggest an intergene conversion-like event. Second, a length difference of 141 base pairs was detected in a region encoding the carboxy-terminal arm of the protein. This difference can be explained by three separate reiterations of single codons (3 base pairs) separated in time by duplication or triplication events.

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References

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

    Article  PubMed  Google Scholar 

  • Bock SC, Tiemeier DC, Mester K, Wu M, Goldsmith MR (1982) Hybridization selected translation ofBombyx mori high cysteine chorion proteins inXenopus laevis oocytes. Proc Natl Acad Sci USA 79:1032–1036

    PubMed  Google Scholar 

  • Bock SC, Tiemeier DC, Mester K, Goldsmith MR (1983) Differential patterns in the temporal expression ofBombyx mori chorion genes. Rouxs Arch Dev Biol 192:222–227

    Article  Google Scholar 

  • Cohen JB, Effron K, Rechavi G, Ben-Neriah Y, Zakut R, Givol D (1982) Simple DNA sequences in homologous flanking regions near immunoglobulin VH genes: a role in gene interaction? Nucleic Acids Res 10:3353–3370

    PubMed  Google Scholar 

  • Eickbush TH, Kafatos F (1982) A walk in the chorion locus ofBombyx mori. Cell 29:633–643

    Article  PubMed  Google Scholar 

  • Farabaugh P, Schmeissner U, Hofer M, Miller JH (1978) Genetic studies of the lac repressor. VII. On the molecular nature of spontaneous hotspots in the lac I gene ofEscherichia coli. J Mol Biol 126:847–863

    Article  PubMed  Google Scholar 

  • Goldsmith MR, Clermont-Rattner E (1980) Organization of the chorion genes inBombyx mori, a multigene family. III. Detailed composition of three gene clusters. Genetics 96:201–212

    PubMed  Google Scholar 

  • Hamodrakas SJ, Jones CW, Kafatos FC (1982) Secondary structure predictions for silkmoth chorion proteins. Biochim Biophys Acta 700:42–51

    Google Scholar 

  • Iatrou K, Tsitilou SG (1983) Coordinately expressed chorion genes ofBombyx mori: Is developmental specificity determined by secondary structure recognition. EMBO J 2:1431–1440

    PubMed  Google Scholar 

  • Iatrou K, Tsitilou SG, Kafatos FC (1982) Developmental classes and homologous families of chorion genes inBombyx mori. J Mol Biol 157:417–434

    Article  PubMed  Google Scholar 

  • Iatrou K, Tsitilou SG, Kafatos FC (1984) DNA sequence transfer between two high cysteine chorion gene families inBombyx mori. Proc Natl Acad Sci USA (in press)

  • Jones CW, Kafatos FC (1980) Structure, organization and evolution of developmentally regulated chorion genes in a silkmoth. Cell 22:855–867

    Article  PubMed  Google Scholar 

  • Jones CW, Kafatos FC (1982) Accepted mutations in a gene family: evolutionary diversification of duplicated DNA. J Mol Evol 19:87–103

    PubMed  Google Scholar 

  • Jones CW, Rosenthal N, Rodakis GC, Kafatos FC (1979) Evolution of two major chorion multigene families as inferred from cloned cDNA and protein sequences. Cell 18:1317–1332

    Article  PubMed  Google Scholar 

  • Kafatos FC, Reiger JC, Mazur GD, Nadel MR, Blau HM, Petri WH, Wyman AR, Gelinas RE, Moore BP, Paul M, Efstratiadis A, Vournakis JN, Goldsmith MR, Hunsley JR, Baker B, Nardi J, Koehler M (1977) The eggshell of insects: differentiation-specific proteins and the control of their synthesis and accumulation during development. In: Beerman W (ed) Results and problems in cell differentiation, vol 8. Springer-Verlag: Berlin Heidelberg New York, pp 45–145

    Google Scholar 

  • Kimura M (1968) Evolutionary rate at the molecular level. Nature 217:624–626

    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 

  • King JL, Jukes TH (1969) Non-Darwinian evolution: random fixation of selectively neutral mutations. Science 164:788–798

    PubMed  Google Scholar 

  • Krawinkel U, Zoebelein G, Bruggemann M, Radbruch A, Rajewsky K (1983) Recombination between antibody heavy chain variable-region genes: evidence for gene conversion. Proc Natl Acad Sci USA 80:4997–5001

    PubMed  Google Scholar 

  • Lecanidou R, Eickbush TH, Rodakis GC, Kafatos FC (1983) Novel B family sequence from an early chorion cDNA library ofBombyx mori. Proc Natl Acad Sci USA 80:1955–1959

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Maxam A, Gilbert W (1977) A new method for sequencing DNA. Proc Natl Acad Sci USA 74:560–564

    PubMed  Google Scholar 

  • Messing J, Vieira J (1982) A new pair of M13 vectors for selecting either DNA strand of double-digested restriction fragments. Gene 19:269–276

    Article  PubMed  Google Scholar 

  • Miyata T, Yasunaga T, Nishida T (1980) Nucleotide sequence divergence and functional constraint in mRNA evolution. Proc Natl Acad Sci USA 77:7328–7332

    PubMed  Google Scholar 

  • Nadel MR, Kafatos FC (1980) Specific protein synthesis in cellular differentiation. IV. The chorion proteins ofBombyx mori and their program of synthesis. Dev Biol 75:26–40

    Article  PubMed  Google Scholar 

  • Pease LR, Schulze DH, Pfaffenbach GM, Nathenson SG (1983) Spontaneous H-2 mutants provide evidence that a copy mechanism analogous to gene conversion generates polymorphism in the major histocompatibility complex. Proc Natl Acad Sci USA 80:242–246

    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 20:555–566

    Article  PubMed  Google Scholar 

  • Proudfoot NJ, Brownlee GG (1976) 3′ Non-coding region sequences in eukaryotic messenger RNA. Nature 263:211–214

    Article  PubMed  Google Scholar 

  • Pustell J, Kafatos FC (1982) A convenient and adaptable pack-age of DNA sequence analysis programs for microcomputers. Nucleic Acids Res 10:51–60

    PubMed  Google Scholar 

  • Regier JC, Kafatos FC, Hamodrakis SJ (1983) Silkmoth chorion multigene families constitute a superfamily: comparison of C and B family sequences. Proc Natl Acad Sci USA 80: 1043–1047

    PubMed  Google Scholar 

  • Rodakis GC, Kafatos FC (1982) Origin of evolutionary novelty in proteins: how a high-cysteine chorion protein has evolved. Proc Natl Acad Sci USA 79:3551–3555

    PubMed  Google Scholar 

  • Rodakis GC, Moschonas NK, Kafatos FC (1982) Evolution of a multigene family of chorion proteins in silkmoths. Mol Cell Biol 2:554–563

    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 

  • Smith GP (1973) Unequal crossover and the evolution of multigene families. Cold Spring Harbor Symp Quant Biol 38: 507–513

    Google Scholar 

  • Smith HO, Birnstiel ML (1976) A simple method for DNA restriction site mapping. Nucleic Acids Res 3:2387–2398

    PubMed  Google Scholar 

  • Tsitilou SG, Rodakis GC, Alexopoulou M, Kafatos FC, Ito K, Iatrou K (1983) Structural features of B family chorion sequences in the silkmothBombyx mori, and their evolutionary implications. EMBO J 2:1845–1852

    PubMed  Google Scholar 

  • Weiss EH, Mellor A, Golden L, Fahrner K, Simpson E, Hurst J, Flavell RA (1983) The structure of a mutant H-2 gene suggests that the generation of polymorphism in H-2 genes may occur by gene conversion-like events. Nature 301:671–674

    Article  PubMed  Google Scholar 

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Rodakis, G.C., Lecanidou, R. & Eickbush, T.H. Diversity in a chorion multigene family created by tandem duplications and a putative gene-conversion event. J Mol Evol 20, 265–273 (1984). https://doi.org/10.1007/BF02104732

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