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Tadl-1, an active LINE-like element of Neurospora crassa

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Abstract

Tad is a LINE-like retrotransposon of Neurospora crassa. The element was originally detected and cloned using the am gene as a transposon trap in hybrid strains derived from a cross of Adiopodoume (a wild collected strain) and a laboratory strain devoid of Tad elements. We report the cloning and sequencing of an active Tad element, Tadl-1, which is capable of independent transposition. Transposition was demonstrated by screening for transfer of the element from a donor nucleus that contained the Tadl-1 element as the only active Tad, into a naive nucleus within a forced heterokaryon. We also report here the sequence analysis of Tadl-1, and its comparison with the sequence of another active element, Tad3-2. These elements are approximately 7 kb in length. They contain two long open reading frames (ORFs) encoded on the strand of the same polarity as the full-length transcript. ORF1 encodes a putative protein of 486 amino acids. Homology to the first ORF of other LINE elements is confined to three cysteine-rich motifs, located near the carboxy-terminus, that are thought to be involved in binding nucleic acids. The second ORF is 1156 amino acids in length and shows homology to the reverse transcriptase domains of various retroviruses and retrotransposons. Tadl-1 and Tad3-2 differ in only ten positions over their whole length.

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References

  • Abad P, Vaury C, Pelisson A, Chaboissier M-C, Busseau I, Bucheton A (1989) A long interspersed repetitive element, the I factor of Drosophila teissieri, is able to transpose in different Drosophila species. Proc Natl Acad Sci USA 86:8887–8891

    Google Scholar 

  • Atkins JF, Weiss RB, Gesteland RF (1990) Ribosome gymnastics-degree of difficulty 9.5, style 10.00. Cell 62:413–423

    Google Scholar 

  • Besansky NJ (1990) A retrotransposable element from the mosquito Anopheles gambiae. Mol Cell Biol 10:863–871

    Google Scholar 

  • Birnboim HC, Doly J (1979) A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res 7:1513–1522

    Google Scholar 

  • Brooks RR, Huang PC (1972) Redundant DNA of Neurospora crassa. Biochem Genet 6:41–49

    Google Scholar 

  • Bucheton A (1990) I transposable elements and I-R hybrid dysgenesis in Drosophila. Trends Genet 6:16–21

    Google Scholar 

  • Burke WD, Calalang CC, Eickbush TH (1987) The site-specific ribosomal insertion element type II of Bombyx mori (R2Bm) contains the coding sequence for a reverse transcriptase enzyme. Mol Cell Biol 7:2221–2230

    Google Scholar 

  • Cambareri EB, Jensen B, Schabtach E, Selker E (1989) Repeat-induced GC to AT mutation in Neurospora. Science 244:1571–1575

    Google Scholar 

  • Di Nocera PP (1988) Close relationship between non-viral retroposons in Drosophila melanogaster. Nucleic Acids Res 16:4041–4052

    Google Scholar 

  • Di Nocera PP, Casari G (1987) Related polypeptides are encoded by Drosophila F elements, I factors, and mammalian Ll sequences. Proc Natl Acad Sci USA 88:5843–5847

    Google Scholar 

  • Dombroski BA, Mathias SL, Nanthakumar E, Scott AF, Kazazian HH Jr (1991) Isolation of an active human transposable element. Science 354:1805–1808

    Google Scholar 

  • Doolittle RF, Feng D-F, Johnson MS, McClure MA (1989) Origins and evolutionary relationships of retroviruses. Q Rev Biol 64:1–30

    Google Scholar 

  • Fawcett DH, Lister CK, Kellett E, Finnegan DJ (1986) Transposable elements controlling I-R hybrid dysgenesis in D. melanogaster are similar to mammalian LINEs. Cell 47:1007–1015

    Google Scholar 

  • Felger I, Hunt JA (1992) A non-LTR retrotransposon from Hawaiian Drosophila: the LOA element. Genetica 85:119–130

    Google Scholar 

  • Field DJ, Sommerfield A, Saville BJ, Collins RA (1989) A group II intron in the Neurospora mitochondrial col gene: nucleotide sequence and implications for splicing and molecular evolution. Nucleic Acids Res 17:9087

    Google Scholar 

  • Finnegan DJ (1989) The I factor and I-R hybrid dysgenesis in Drosophila melanogaster. In: Berg DE, Howe MM (eds) Mobile DNA. American Society for Microbiology, Washington, DC, pp 503–517

    Google Scholar 

  • Gurr SJ, Unkles SE, Kinghorn JR (1987) The structure and organization of nuclear genes of filamentous fungi. In: Kinghorn JR (ed) Gene structure in eukaryotic microbes. IRL Press, pp 93–139

  • Henikoff S (1984) Unidirectional digestion with exonuclease III creates targeted breakpoints for DNA sequencing. Gene 28:351–359

    Google Scholar 

  • Hutchinson CA, Hardies SC, Loeb DD, Shehee WR, Edgell MH (1989) LINEs and related retrotransposons: long interspersed repeated sequences in the eukaryotic genome. In: Berg DE, Howe MM (eds) Mobile DNA. American Society for Microbiology, Washington, DC, pp 593–617

    Google Scholar 

  • Ilves H, Kahre O, Speck M (1992) Translation of the rat LINE bicistronic RNAs in vitro involves ribosomal reinitiation instead of frameshifting. Mol Cell Biol 12:4242–4248

    Google Scholar 

  • Jakubczak JL, Xiong Y, Eickbush TH (1990) Type I (R1) and type II (R2) ribosomal DNA insertion of Drosophila melanogaster are retrotransposable elements closely related to those of Bombyx mori. J Mol Biol 212:37–52

    Google Scholar 

  • Jakubczak JL, Burke WD, Eickbush TH (1991) Retrotransposable elements R1 and R2 interrupt the rRNA genes of most insects. Proc Natl Acad Sci USA 88:3295–3299

    Google Scholar 

  • Kimmel BE, Ole-Moiyol OK, Yourn JR (1987) Ingi, a 5.2 kb dispersed sequence element from Trypanosoma brucei that carries half a smaller mobile element at either end and has homology with mammalian LINEs. Mol Cell Biol 7:1465–1475

    Google Scholar 

  • Kinsey JA (1989a) Restricted distribution of the Tad transposon in strains of Neurospora. Curr Genet 15:271–275

    Google Scholar 

  • Kinsey JA (1989b) A simple colony blot procedure for Neurospora. Fungal Genet Newslett 36:45–46

    Google Scholar 

  • Kinsey JA (1990) Tad, a LINE-like transposable element of Neurospora, can transpose between nuclei in heterokaryons. Genetics 126:317–323

    Google Scholar 

  • Kinsey JA (1993) Transnuclear retrotransposition of the Tad element of Neurospora. Proc Natl Acad Sci USA 90:9384–9387

    Google Scholar 

  • Kinsey JA, Helber J (1989) Isolation of a transposable element from Neurospora crassa. Proc Natl Acad Sci USA 86:1929–1933

    Google Scholar 

  • Kulkosky J, Jones KS, Katz RA, Mack JPG, Skalka AM (1992) Residues critical for retroviral integrative recombination in a region that is highly conserved among retroviral/retrotrasposon integrases and bacterial insertion sequence transposases. Mol Cell Biol 12:2331–2338

    Google Scholar 

  • Leeton PRJ, Smyth DR (1993) An abundant LINE-like element amplified in the genome of Lilium speciosum. Mol Gen Genet 237:97–104

    Google Scholar 

  • Legerton TL, Yanofsky C (1985) Cloning and characterisation of the multifunctional his-3 gene of Neurospora crassa. Gene 39:129–140

    Google Scholar 

  • Lipman DJ, Pearson WR (1985) Rapid and sensitive protein similarity searches. Science 227:1435–1441

    Google Scholar 

  • McClure MA (1991) Evolution of retroposons by acquisition or deletion of retrovirus-like genes. Mol Biol Evol 8:835–857

    Google Scholar 

  • McHale MT, Roberts IN, Noble SM, Beaumont C, Whitehead MP, Seth D, Oliver RP (1992) CfT-I: an LTR-retrotransposon in Cladosporium fulvum, a fungal pathogen of tomato. Mol Gen Genet 233:337–347

    Google Scholar 

  • Metzenberg RL, Baisch TR (1981) An easy method for preparing Neurospora DNA. Neurospora Newslett 28:20–21

    Google Scholar 

  • Metzenberg RL, Grotelueschen J (1987) A restriction polymorphism map of Neurospora crassa: more data. Fungal Genet Newslett 34:39–44

    Google Scholar 

  • Metzenberg RL, Stevens JN, Selker EU, Morzycka-Wroblewska E (1984) A method for finding the genetic map position of cloned DNA fragments. Neurospora Newslett 31:35–40

    Google Scholar 

  • Murphy NB, Pays A, Tebabi P, Coquelet H, Guyaux M, Steinert M, Pays E (1987) Trypanosoma brucei repeated element with unusual structural and transcriptional properties. J Mol Biol 195:855–871

    Google Scholar 

  • Nargang FE, Bell JB, Stohl LL, Lambowitz AM (1984) The DNA sequence and genetic organization of a Neurospora mitochondrial plasmid suggest a relationship to introns and mobile elements. Cell 38:441–453

    Google Scholar 

  • O'Hare K, Alley MR, Cullingford TE, Driver A, Sanderson MJ (1991) DNA sequence of the Doc retroposon in the white-one mutant of Drosophila melaogaster and of secondary insertions in the phenotypically altered derivatives white-honey and white-eosin. Mol Gen Genet 225:17–24

    Google Scholar 

  • Priimagi AF, Mizrokhi LJ, Ilyin YV (1988) The Drosophila mobile element jockey belongs to LINEs and contains coding sequences homologous to some retroviral proteins. Gene 70:253–262

    Google Scholar 

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

    Google Scholar 

  • Schwarz-Sommer A, Leclercq L, Gobel E, Saedler H (1987) Cin4, an insert altering the structure of the Al gene in Zea mays, exhibits properties of nonviral retrotransposons. EMBO J 6:3873–3880

    Google Scholar 

  • Selker E, Cambareri E, Jensen B, Haack K (1987) Rearrangement of duplicated DNA in specialized cells of Neurospora. Cell 51:741–752

    Google Scholar 

  • Stevens JN, Metzenberg RL (1982) Preparing Neurospora DNA: some improvements. Neurospora Newslett 29:27–28

    Google Scholar 

  • Vogel HJ (1964) Distribution of lysine pathways among fungi: evolutionary implications. Am Nat 98:435–446

    Google Scholar 

  • Vollmer SJ, Yanofsky C (1986) Efficient cloning of genes of Neurospora crassa. Proc Natl Acad Sci USA 83:4869–4873

    Google Scholar 

  • Xiong Y, Eickbush TH (1988) The site-specific ribosomal DNA insertion element R1Bm belongs to a class of non-long-terminal-repeat retrotransposons. Mol Cell Biol 8:114–123

    Google Scholar 

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Communicated by D.J. Finnegan

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Cambareri, E.B., Helber, J. & Kinsey, J.A. Tadl-1, an active LINE-like element of Neurospora crassa . Molec. Gen. Genet. 242, 658–665 (1994). https://doi.org/10.1007/BF00283420

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