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CfT-I: an LTR-retrotransposon in Cladosporium fulvum, a fungal pathogen of tomato

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Summary

A retrotransposon from the fungal tomato pathogen Cladosporium fulvum (syn. Fulvia fulva) has been isolated and characterised. It is 6968 by in length and bounded by identical long terminal repeats of 427 bp; 5 by target-site duplications were found. Putative first- and second-strand primer binding sites were identified. Three long open reading frames (ORFs) are predicted from the sequence. The first has homology to retroviral gag genes. The second includes sequences homologous to protease, reverse transcriptase, RNAse H and integrase, in that order. Sequence comparisons of the predicted ORFs indicate that this element is closely related to the gypsy class of LTR retrotransposons. Races of the pathogen exhibit polymorphisms in their complement of at least 25 copies of the sequence. Virus-like particles which co-sediment with reverse transcriptase activity were observed in homogenates of the fungus. This is the first report of an LTR retrotransposon in a filamentous fungus.

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References

  • Bingham PM, Zachar Z (1989) Retrotransposons and the FB transposon from Drosophila melanogaster. In: Berg DE, Howe MM (eds) Mobile DNA. American Society for Microbiology, Washington DC, pp 485–502

    Google Scholar 

  • Boeke JD, Corces VG (1989) Transcription and reverse transcription of retrotransposons. Annu Rev Microbiol 43:403–434

    Google Scholar 

  • Boeke JD (1989) Transposable elements in Saccharomyces cerevisiae. In: Berg DE, Howe MM (eds) Mobile DNA. American Society for Microbiology, Washington DC, pp 403–434

    Google Scholar 

  • Bozarth RF (1972) A new dimension in microbiology. In: Environmental health perspectives. United States Department of Health Education and Welfare, Washington, pp 23–39

    Google Scholar 

  • Buck KW (1986) Fungal virology — an overview. In: Buck FW (ed) Fungal virology. CRC Press, Boca Raton, Florida, pp 1–84

    Google Scholar 

  • Cappello J, Handelsman K, Lodish HF (1985) Sequence of Dictyostelium DIRS-1: An apparent retrotransposon with inverted terminal repeats and internal circle junction. Cell 43:105–115

    Google Scholar 

  • Clare J, Frabaugh P (1985) Nucleotide sequence of a yeast Ty element: evidence for an unusual mechanism of gene expression. Proc Natl Acad Sci USA 82:2829–2833

    Google Scholar 

  • Clark DJ, Bilanchone VW, Haywood LJ, Dildine SL, Sandmeyer SB (1988) A yeast sigma composite element Ty3 has properties of a retrotransposon. J Biol Chem 263:1413–1423

    Google Scholar 

  • Covey SN (1986) Amino acid sequence homology in gag region of reverse transcribing elements and the coat protein of cauliflower mosaic virus. Nucleic Acids Res 14:623–633

    Google Scholar 

  • de Wit PJGM (1977) A light and scanning-electron microscope study of infection of tomato plants by virulent and avirulent races of Cladosporium fulvum. Neth J Plant Pathol 83:109–122

    Google Scholar 

  • Dinoor A, Eshed N, Nof E (1988) Puccinia coronata crown rust of oats and grasses. In: Sidhu GS (ed) Advances in plant pathology, vol 6. Academic press, New York, pp 333–344

    Google Scholar 

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

    Google Scholar 

  • Dunsmuir P, Brorein WJ, Simon MA, Rubin GM (1980) Insertion of the Drosophila transposable element copia generates a 5 base pair duplication. Cell 21:575–579

    Google Scholar 

  • El-Sherbeini M, Tipper DJ, Mitchell DJ, Bostian KA (1984) Virus-like particle capsid proteins encoded by different L double-stranded RNAs of Saccharomyces cerevisial: their roles in maintenance of M double-stranded killer plasmids. Mol Cell Biol 4:2818–2827

    Google Scholar 

  • Errede B, Company M, Ferchak JD, Hutchinson CA III (1985) Activation regions in a yeast transposon have homology to mating type control sequences and to mammalian enhancers. Proc Natl Acad Sci USA 82:5423–5427

    Google Scholar 

  • Fink GR, Boeke JD, Garfinkel DJ (1986) The mechanism and consequences of retrotransposition. Trends Genet 2:118–123

    Google Scholar 

  • Friesen PD, Nissen MS (1990) Gene organisation and transcription of TED, a lepidopteran retrotransposon integrated within the baculovirus genome. Mol Cell Biol 10:3067–3077

    Google Scholar 

  • Gardner RC, Howarth AJ, Hahn P, Brown-Leudi M, Shepherd RJ, Messing J (1981) The complete nucleotide sequence of an infectious clone of cauliflower mosaic virus by M13mp7 shotgun sequencing. Nucleic Acids Res. 9:2871–2887

    Google Scholar 

  • Garfinkel DJ, Boeke JD, Fink GR (1985) Ty element transposition reverse transcriptase and virus-like particles. Cell 42:507–517

    Google Scholar 

  • Geever RF, Case ME, Tyler BM, Buxton F, Giles NH (1983) Point mutations and DNA rearrangements 5′ to the inducible ga-2 gene of Neurospora allow activator protein-independent transcription. Proc Natl Acad Sci USA 80:7298–7302

    Google Scholar 

  • Gilliquet V, Legrain M, Hilger F (1987) Sequence of the region 5′ to the negative regulatory gene PHO80 of Saccharomyces cerevisiae. Nucleic Acids Res 15:5893

    Google Scholar 

  • Goreleva TV, Resnik NL, Schuppe NG (1989) Retrotransposon transposition intermediates are encapsidated into virus-like particles. FEBS Lett 244:307–310

    Google Scholar 

  • Grandbastien MA, Spielman A, Caboche M (1988) Tnt-1, a mobile retroviral-like element of tobacco isolated by plant cell genetics. Nature 337:376–380

    Google Scholar 

  • Gurr SJ, Unkles SE, Kinghorn JR (1987) The structure and organisation of nuclear genes of filamentous fungi. In: Kinghorn JR (ed) Gene structure in eukaryotic microbes. IRL Press, Washington, pp 117–127

    Google Scholar 

  • Hansen LJ, Chalker DL, Sandmeyer SB (1988) Ty3, a yeast retrotransposon associated with tRNA genes has homology to animal retroviruses. Mol Cell Biol 8:5245–5256

    Google Scholar 

  • Harting R, Kenyon L, Lewis BG, Oliver RP, Turner JG, Coddington A (1988) Conditions for efficient isolation and regeneration of protoplasts from Fulvia fulva. J Phytopathol 122:143–146

    Google Scholar 

  • Hodgson CP, Fisk RZ (1987) Hybridization probe size control: optimised “oligolabelling”. Nucleic Acid Res 5:6295–6296

    Google Scholar 

  • Hull R, Sadler J, Longstaff M (1986) The sequence of the Carnation Etched Ring Virus DNA: comparison with cauliflower mosaic virus and retroviruses. EMBO J 5:3083–3090

    Google Scholar 

  • Inouye S, Yuki S, Saigo K (1986) Complete nucleotide sequence and genome organisation of a Drosophila transposable element 297. Eur J Biochem 154:417–425

    Google Scholar 

  • Kikuchi Y, Ando Y, Shiba T (1986) Unusual priming mechanism of RNA-directed DNA synthesis in copia retrovirus-like particles of Drosophila. Nature 323:824–826

    Google Scholar 

  • Kingsman AJ, Kingsman SM (1988) Ty: a retroelement moving forward Cell 53:333–334

    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 

  • Kohli J, Munz P, Aebi R, Amstutzt H, Gysler C, Heyer WD, Lehmann L, Schuchert P, Thurianx P, Leupold U, Bell J, Gamulin V, Hottinger H, Pearson D, Soell D (1984) Interallelic and intergeneic conversion in three serine tRNA genes of Schizosaccharomyces pombe. Cold Spring Harbor Symp Quant Biol 49:31–40

    Google Scholar 

  • Levin HL, Weaver DC, Boeke JD (1990) Two related families of retrotransposans from Schizosaccharomyces pombe. Mol Cell Biol 10:6791–6798

    Google Scholar 

  • Lindhout P, Korta W, Cislik M, Vos I, Gerlagh T (1989) Further identification of races of Cladosporium fulvum (Fulvia fulva) on tomato originating from the Netherlands, France and Poland. Neth J Plant Pathol 95:43–148

    Google Scholar 

  • Maniatis T, Fritsch EF, Sambrook J (1982) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York

    Google Scholar 

  • Marlor R, Parkhurst S, Corces V (1986) The Drosophila melanogaster gypsy transposable element encodes putative gene products homologous to retroviral proteins. Mol Cell Biol 6:1129–1134

    Google Scholar 

  • McHale MT, Roberts IN, Talbot NJ, Oliver RP (1989) Expression of reverse transcriptase genes in Fulvia fulva. Mol Plant-Microbe Interact 4:165–168

    Google Scholar 

  • Mellor J, Malim MH, Gull K, Tuite MF, McCready S, Dibbayawan T, Kingsman SM, Kingsman AJ (1985) Reverse transcriptase activity and Ty RNA are associated with virus-like particles in yeast. Nature 318:583–586

    Google Scholar 

  • Michel F, Lang BF (1985) Mitochondrial class II introns encode proteins related to the reverse transcriptases of retroviruses. Nature 316:641–642

    Google Scholar 

  • Mount SM, Rubin GM (1985) Complete nucleotide sequence of the Drosophila transposable element copia: homology between copia and retroviral proteins. Mol Cell Biol 5:1630–1638

    Google Scholar 

  • Norrander J, Kemp T, Messing J (1983) Construction of improved M13 vectors using oligodeoxynucleotide-directed mutagenesis. Gene 26:101–106

    Google Scholar 

  • Poch O, Sauvaget I, Delarue M, Tordo N (1989) Identification of four conserved motifs among the RNA-dependent polymerase encoding elements. EMBO J 8:3867–3874

    Google Scholar 

  • Punt PJ, Oliver RP, Dingemanse MA, Pouwels PH, van den Hondel CAMJJ (1987) Transformation of Aspergillus based on the hygromycin B resistance marker from Escherichia coli. Gene 56:117–124

    Google Scholar 

  • Raeder U, Broda P (1985) Rapid preparation of DNA from filamentous fungi. Lett Appl Microbiol 1:17–20

    CAS  Google Scholar 

  • Ratner L, Haseltine W, Patarca R, Livak KJ, Starciach B, Josephs SF, Doran ER, Rafalski JA, Whitehorn EA, Baumeister K, Ivanoff L, Petteway SR, Pearson ML, Lautenberger JA, Papas TS, Ghrayeb J, Chang NT, Gallo RC, Wong-Stahl F (1985) Complete nucleotide sequence of the AIDS virus, HTLV-III. Nature 313:277–283

    Google Scholar 

  • Saigo K, Kugimiya W, Matsuo Y, Inouye S, Yoshioka K, Yuki S (1984) The identification of the coding sequence for a reverse transcriptase-like enzyme in a transposable genetic element in Drosophila melanogaster. Nature 312:659–661

    Google Scholar 

  • Sentry JW, Smyth DR (1989) An element with LTRs and its variant arrangements in the genome of Lilium henryi. Mol Gen Genet 215:349–354

    Google Scholar 

  • Shiba T, Saigo K (1983) Retreovirus-like particles containing RNA homologous to the transposable element copia in Drosophila melanogaster. Nature 302:119–123

    Google Scholar 

  • Smyth DR, Kalitsis P, Joseph JL, Sentry JW (1989) A plant retrotransposon from Lilium henryi is related to Ty3 of yeast and the gypsy group of Drosophila. Proc Natl Acad Sci USA 86:5015–5019

    Google Scholar 

  • Swofford DL (1990) PAUP: Phylogenetic analysis using parsimory. Version 3.0. Computer program distributed by the Illinois Natural History Survey, Champaign, Illinois

    Google Scholar 

  • Talbot NJ, Coddington A, Oliver RP (1991) Pulsed field gel electrophoresis reveals chromosome length polymorphisms between strains of Cladosporium fulvum (syn. Fulvia fulva). Mol Gen Genet 229:267–272

    Google Scholar 

  • Tanda S, Shrimpton AE, Ling-Ling C, Itayama H, Matsubayashi K, Saigo K, Tobari YN, Langley CH (1988) Retrovirus-like features and site specific insertions of a transposable element tom in Drosophila ananassae. Mol Gen Genet 214:405–411

    Google Scholar 

  • van Kan JAL, Van den Ackerveken GFJM, De Wit PJGM (1991) Cloning and characterisation of a cDNA of avirulence gene avr9 of the fungal pathogen C. fulvum; causal agent of tomato leaf mold. Mol Plant Microbe Interact 4:52–60

    Google Scholar 

  • Voytas DF, Ausubel FM (1988) A copia-like transposable element family in Arabidopsis thaliana. Nature 336:242–244

    Google Scholar 

  • Weber F, De Villiers J, Schaffner W (1984) An SV40 “enhancer trap” incorporates exogenous enhancers or generates enhancers from its own sequences. Cell 36:983–992

    Google Scholar 

  • Xiong Y, Eickbush HT (1988) Similarity of reverse transcriptase-like sequences of viruses, transposable elements and mitochondrial introns. Mol Biol Evol 6:675–690

    Google Scholar 

  • Xu H, Boeke JD (1990) Localisation of sequences required in cis for yeast Tyl element transposition near the long teminal repeats — analysis of mini-Tyl elements. Mol Cell Biol 10:2695–2702

    Google Scholar 

  • Yuki S, Inouye Y, Ishimaru S, Saigo K (1986) Nucleotide sequence characterisation of a Drosophila retrotransposon 412. Eur J Biochem 158:403–410

    Google Scholar 

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Author notes

  1. Mark T. McHale

    Present address: SmithKline Beecham, The Frythe, Welwyn, Herts, UK

  2. Ian N. Roberts

    Present address: Institute of Food Research Norwich, Colney Lane, Norwich, UK

  3. Devanshi Seth

    Present address: Biotech International, Technology Park, Bentley, Western Australia

Authors and Affiliations

  1. Norwich Molecular Plant Pathology Group, University of East Anglia, School of Biological Sciences, NR4 7TJ, Norwich, UK

    Mark T. McHale, Ian N. Roberts, Stuart M. Noble, Christine Beaumont, Michael P. Whitehead, Devanshi Seth & Richard P. Oliver

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  1. Mark T. McHale
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Communicated by D.J. Finnegan

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McHale, M.T., Roberts, I.N., Noble, S.M. et al. CfT-I: an LTR-retrotransposon in Cladosporium fulvum, a fungal pathogen of tomato. Molec. Gen. Genet. 233, 337–347 (1992). https://doi.org/10.1007/BF00265429

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