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Distribution and evolution of introns in drosophila amylase genes

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Abstract

While the two amylase genes ofDrosophila melanogaster are intronless, the three genes ofD. pseudoobscura harbor a short intron. This raises the question of the common structure of theAmy gene in Drosophila species. We have investigated the presence or absence of an intron in the amylase genes of 150 species of Drosophilids. Using polymerase chain reaction (PCR), we have amplified a region that surrounds the intron site reported inD. pseudoobscura and a few other species. The results revealed that most species contain an intron, with a variable size ranging from 50 to 750 bp, although the very majoritary size was around 60–80 bp. Several species belonging to different lineages were found to lack an intron. This loss of intervening sequence was likely due to evolutionarily independent and rather frequent events. Some other species had both types of genes: In theobscura group, and to a lesser extent in theananassae subgroup, intronless copies had much diverged from intron-containing genes. Base composition of short introns was found to be variable and correlated with that of the surrounding exons, whereas long introns were all A-T rich. We have extended our study to non-Drosophilid insects. In species from other orders of Holometaboles, Lepidoptera and Hymenoptera, an intron was found at an identical position in theAmy gene, suggesting that the intron was ancestral.

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References

  • Balm E (1967) Crossing over in the chromosomal region determining amylase isozymes inDrosophila melanogaster. Hereditas 58:1–12

    Google Scholar 

  • Bingham PM, Chou T-B, Mims I, Zachar Z (1988) On/off regulation of gene expression at the level of splicing. Trends Genet 4:134–138

    Article  CAS  PubMed  Google Scholar 

  • Boer PH, Hickey DA (1986) The alpha-amylase gene inDrosophila melanogaster: nucleotide sequence, gene structure and expression motifs. Nucleic Acids Res 14:8399–8411

    CAS  PubMed  Google Scholar 

  • Bowtell DDL, Simon MA, Rubin GM (1988) Nucleotide sequence and structure of thesevenless gene ofDrosophila melanogaster. Genes Dev 2:620–634

    CAS  PubMed  Google Scholar 

  • Brown CJ, Aquadro CF, Anderson WW (1990) DNA sequence evolution of the amylase multigene family inDrosophila pseudoobscura. Genetics 126:131–138

    CAS  PubMed  Google Scholar 

  • Cariou M-L, Lachaise D, Sourdis J, Tsacas L, Krimbas C, Ashbumer M (1988) New African species in theDrosophila obscura species group: genetic variation, differentiation and evolution. Heredity 61: 73–84

    Google Scholar 

  • Cavalier-Smith T (1991) Intron phylogeny: a new hypothesis. Trends Genet 7:145–148

    CAS  PubMed  Google Scholar 

  • Csank C, Taylor FM, Martindale DW (1990) Nuclear pre-mRNA introns: analysis and comparison of intron sequences from Tetrahymena thermophila and other eukaryotes. Nucleic Acids Res 18: 5133–5141

    CAS  PubMed  Google Scholar 

  • Da Lage J-L, Carion M-L, David JR (1989) Geographical polymorphism of amylase inDrosophila ananassae and its relatives. Heredity 63:67–72

    PubMed  Google Scholar 

  • Da Lage J-L, Cariou M-L (1993) Organization and structure of the amylase gene family. In: Tobari YN (ed)Drosophila ananassae, genetical and biological aspects. Japan Scientific Societies Press, Karger, Tokyo, pp 171–181

    Google Scholar 

  • Da Lage J-L, Lemeunier F, Cariou M-L, David JR (1992) Multiple amylase genes inDrosophila ananassae and related species. Genet Res Camb 59:85–92

    Google Scholar 

  • Daïnou O, Cariou M-L, David JR, Hickey D (1987) Amylase gene duplication: an ancestral trait in theDrosophila melanogaster species subgroup. Heredity 59:245–251

    PubMed  Google Scholar 

  • Di Bello PR, Withers DA, Bayer CA, Fristrom JW, Guild GM (1991) TheDrosophila Broad-Complex encodes a family of related proteins containing zinc-fingers. Genetics 129:385–397

    Google Scholar 

  • Doolittle WF (1987) The origin and function of intervening sequences in DNA: a review. Am Nat 130:915–928

    Article  CAS  Google Scholar 

  • Ellsworth DL, Hewett-Emmett D, Li W-H (1994) Evolution of base composition in the insulin and insulin-like growth factor genes. Mol Biol Evol 11:875–885

    CAS  PubMed  Google Scholar 

  • Geiss KT, Abbas GM, Makaroff CA (1994) Intron loss from the NADH dehydrogenase subunit 4 gene of lettuce mitochondrial DNA: evidence for homologous recombination of a cDNA intermediate. Mol Gen Genet 243:97–105

    Article  CAS  PubMed  Google Scholar 

  • Gemmill RM, Levy JN, Doane WW (1985) Molecular cloning of alpha-amylase genes fromDrosophila melanogaster. I Clone isolation by use of a mouse probe. Genetics 110:299–312

    CAS  PubMed  Google Scholar 

  • Gilbert W (1978) Why genes-in-pieces? Nature 271:501

    Article  CAS  PubMed  Google Scholar 

  • Giroux MJ, Clancy M, Baier J, Ingham L, McCarthy D, Hannah LC (1994)De novo synthesis of an intron by the maize transposable elementDissociation. Proc Natl Acad Sci USA 91:12150–12154

    CAS  PubMed  Google Scholar 

  • Gloor G, Engels W (1991) Single fly DNA preps for PCR. Dros Inf Serv 74:148–149

    Google Scholar 

  • Goodall GJ, Filipowicz W (1989) The AU-rich sequences present in the introns of plant nuclear pre-mRNAs are required for splicing. Cell 58:473–483

    Article  CAS  PubMed  Google Scholar 

  • Gumucio DL, Wiebauer K, Caldwell RM, Samuelson L, Meisler MH (1988) Concerted evolution of human amylase genes. Mol Cell Biol 8:1197–1205

    CAS  PubMed  Google Scholar 

  • Guo M, Lo PCH, Mount SM (1993) Species-specific signals for the splicing of a short intron in vitro. Mol Cell Biol 13:1104–1118

    CAS  PubMed  Google Scholar 

  • Hawkins JD (1988) A survey on intron and exon lengths. Nucleic Acids Res 16:9893–9905

    CAS  PubMed  Google Scholar 

  • Heberlein U, Rubin G (1990) Structural and functional comparisons of theDrosophila virilis andDrosophila melanogaster rough genes. Proc Natl Acad Sci USA 87:5916–5920

    CAS  PubMed  Google Scholar 

  • Hickey DA (1979) The geographical pattern of an enzyme polymorphism inD. melanogaster. Genetica 51:1–4

    Article  Google Scholar 

  • Janecek S (1994) Sequence similarities and evolutionary relationships of microbial, plant and animal alpha-amylases. Eur J Biochem 224: 519–524

    Article  CAS  PubMed  Google Scholar 

  • Kassis JA, Poole SJ, Wright DK, O'Farrell PH (1986) Sequence conservation in the protein coding and intron regions of theengrailed transcription unit. EMBO J 5:3583–3589

    CAS  PubMed  Google Scholar 

  • Keller EB, Noon WA (1985) Intron splicing: a conserved internal signal in introns of Drosophila pre-mRNAs. Nucleic Acids Res 13:4971–4981

    CAS  PubMed  Google Scholar 

  • Koelle MR, Talbot WS, Segraves WA, Bender MT, Cherbas P, Hogness DS (1991) The Drosophila EcR gene encodes an ecdysone receptor, a new member of the steroid receptor superfamily. Cell 67:59–77

    Article  CAS  PubMed  Google Scholar 

  • Kristensen NP (1991) Phylogeny of extant Hexapods. In: Nauman ID (ed) The insects of Australia. Carlton, Victoria, Melbourne, Univ. Press, pp 125–140

    Google Scholar 

  • Kukalova-Peck J (1991) Fossil history and the evolution of Hexapod structures. In: Nauman ID (ed) The insects of Australia. Carlton, Victoria, Melbourne, Univ. Press, pp 141–179

    Google Scholar 

  • Michael WM, Bowtell DDL, Rubin GM (1990) Comparison of the sevenless genes ofDrosophila virilis andDrosophila melanogaster. Proc Natl Acad Sci USA 87:5351–5353

    CAS  PubMed  Google Scholar 

  • Mount SM (1982) A catalogue of splice junction sequences. Nucleic Acids Res 10:459–472

    CAS  PubMed  Google Scholar 

  • Mount SM, Burks C, Hertz G, Stormo GD, White O, Fields C (1992) Splicing signals in Drosophila: inron size, information content, and consensus sequences. Nucleic Acids Res 20:4253–4262

    Google Scholar 

  • Neufeld TP, Carthew RW, Rubin GM (1991) Evolution of gene position: chromosomal arrangement and sequence comparison of theDrosophila melanogaster andDrosophila virilis sina andRh4 genes. Proc Natl Acad Sci USA 88:10203–10207

    CAS  PubMed  Google Scholar 

  • Ohta T (1983) On the evolution of multigene families. Theor Popul Biol 23:216–240

    CAS  PubMed  Google Scholar 

  • Payant V, Abukashawa S, Sasseville M, Benkel BF, Hickey DA, David J (1988) Evolutionary conservation of the chromosomal configuration and regulation of amylase genes among eight species of theDrosophila melanogaster species subgroup. Mol Biol Evol 5:560–567

    CAS  PubMed  Google Scholar 

  • Pélandakis M, Higgins DG, Solignac M (1991) Molecular phylogeny of the subgenusSophophora ofDrosophila derived from large subunit of ribosomal RNA sequences. Genetica 84:87–94

    Article  PubMed  Google Scholar 

  • Purugganan M, Wessler S (1993) The splicing of transposable elements and its role in intron evolution. In: McDonald JF (ed) Transposable elements and evolution. Kluwer Academic, Dordrecht, pp 28–36

    Google Scholar 

  • Riley MA (1989) Nucleotide sequence of theXdh region inDrosophila pseudoobscura and an analysis of the evolution of synonymous codons. Mol Biol Evol 6:33–52

    CAS  PubMed  Google Scholar 

  • Rogers JH (1990) The role of introns in evolution. FEBS Lett 268: 339–343

    Article  CAS  PubMed  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Sharp PA (1985) On the origin of RNA splicing and introns. Cell 42:397–400

    Article  CAS  PubMed  Google Scholar 

  • Shibata H, Yamazaki T (1995) Molecular evolution of the duplicatedAmy locus inDrosophila melanogaster species subgroup: concerted evolution only in coding region and excess of nonsynonymous substitutions in speciation. Genetics 141:223–236

    CAS  PubMed  Google Scholar 

  • Stephan W, Rodriguez VS, Zhou B, Parsch J (1994) Molecular evolution of the metallothionein geneMtn in themelanogaster species group: results fromDrosophila ananassae. Genetics 138:135–143

    CAS  PubMed  Google Scholar 

  • Tadlaoui-Ouafi A (1993) Evolution structurale et moléculaire de la famille mulrigénique Amylase chez quelques Drosophilidae. Thesis, Université Pierre et Marie Curie, Paris, 142 pp

    Google Scholar 

  • Talerico M, Berget SM (1994) Intron definition in splicing of smallDrosophila introns. Mol Cell Biol 14:3434–3445

    CAS  PubMed  Google Scholar 

Download references

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Authors and Affiliations

  1. UPR 9034: Populations, Génétique et Évolution, CNRS, 91198, Gif sur Yvette cedex, France

    Jean-Luc Da Lage & Marie-Louise Cariou

  2. Laboratoire Développement et Morphogenése, UPS centre d'Orsay, Bât. 445, 91405, Orsay cedex, France

    Maurice Wegnez

Authors
  1. Jean-Luc Da Lage
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  2. Maurice Wegnez
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  3. Marie-Louise Cariou
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Correspondence to: J-L. Da Lage

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Da Lage, JL., Wegnez, M. & Cariou, ML. Distribution and evolution of introns in drosophila amylase genes. J Mol Evol 43, 334–347 (1996). https://doi.org/10.1007/BF02339008

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  • DOI: https://doi.org/10.1007/BF02339008

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