Skip to main content

An unusually compact retrotransposon in maize

Plant Molecular Biology volume 12, pages 633–642 (1989)Cite this article

Abstract

Unlike any other known plant transposon, the maize transposable element Bs1 is similar to the retrotransposons previously described in yeast and Drosophila. Bs1 is bounded by 302 bp identical long terminal repeats (LTRs), and it contains open reading frames with apparent amino acid sequence similarity to reverse transcriptase and other retroviral pol gene enzymes. Bs1 is 3203 bp long, very short for a retrotransposon, and the apparent organization of its genetic information is significantly different from any previously described element. Although transcription of Bs1 has not been observed, it is probably an active transposon, since it was observed to transpose in a maize line that contains only two sequences hybridizing to Bs1 probes. Both of these sequences share 35 restriction sites with the cloned Bs1 element, and thus must be very similar or identical with it.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

References

  1. Aeby P, Spicher A, deChastonay Y, Muller F, Tobler H: Structure and genomic organization of proretrovirus-like elements partially eliminated from the somatic genome of Ascaris lumbricoides. EMBO J 5: 3353–3360 (1986).

    Google Scholar 

  2. Adams SE, Mellor J, Gull K, Sim RB, Tuite MF, Kingsman SM, Kingsman AJ: The functions and relationships of Ty-VLP proteins in yeast reflect those of mammalian retroviral proteins. Cell 49: 111–119 (1987).

    Google Scholar 

  3. Canaday J, Guillemaut P, Weil JH: The nucleotide sequences of the initiator tRNAs from bean cytoplasm and chloroplasts. Nucl Acids Res 8: 999–1008 (1980).

    Google Scholar 

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

    Google Scholar 

  5. Copeland TD, Oroszlan S, Kalyanaraman VS, Sarngadharan MG, Gallo RC: Complete amino acid sequence of human T-cell leukemia virus structural protein p15. FEBS Lett 162: 390–395 (1983).

    Google Scholar 

  6. Doolittle RF, Feng D-F, Johnson MS, McClure MA: Origins and evolutionary relationships of retroviruses. Quart Rev Biol, in press (1989).

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

    Google Scholar 

  8. Feinberg AP, Vogelstein B: A technique for radiolabeling DNA restriction fragments to high specific activity. Anal Biochem 132: 6–13 (1983).

    Google Scholar 

  9. Ghosh HP, Ghosh K, Simsek M, RajBhandary UL: Nucleotide sequence of wheat germ cytoplasmic initiator methionine transfer ribonucleic acid. Nucl Acids Res 10: 3241–3247 (1982).

    Google Scholar 

  10. Hiramatsu K, Nishida J, Naito A, Yoshikuri H: Molecular cloning of the closed circular provirus of human T leukaemia virus type I: A new open reading frame in the gag-pol region. J Gen Virol 68: 213–218 (1987).

    Google Scholar 

  11. Holland J, Spinler K, Horodyski F, Grabau E, Nichol S, VandePol S: Rapid evolution of RNA genomes. Science 215: 1577–1585 (1982).

    Google Scholar 

  12. Hull R, Sadler J, Longstaff M: The sequence of carnation etched ring virus DNA: Comparison with cauliflower mosaic virus and retroviruses. EMBO J 5: 3083–3090 (1986).

    Google Scholar 

  13. Inoue J, Watanabe T, Sato M, Oda A, Toyoshima K, Yoshida M, Seiki M: Nucleotide sequence of the protease-coding region in an infectious DNA of simian (STLV) of the HTLV-I family. Virology 150: 187–195 (1986).

    Google Scholar 

  14. Jacks TE, Varmus HE: Expression of the Rous sarcoma virus pol gene by ribosomal frameshifting. Science 230: 1237–1242 (1985).

    Google Scholar 

  15. Johns MA, Mottinger J, Freeling M: A low copy number copia-like transponson in maize. EMBO J 4: 1093–1102 (1985).

    Google Scholar 

  16. Johnson MS, McClure MA, Feng D-F, Gray J, Doolittle RF: Computer analysis of retroviral pol genes: Assignment of enzymatic functions to specific functions and homologies with nonviral enzymes. Proc Natl Acad Sci USA 83; 7648–7652 (1986).

    Google Scholar 

  17. Kamer G, Argos P: Primary structural comparison of RNA-dependent polymerases from plant, animal and bacterial viruses. Nucl Acids Res 12: 7269–7282 (1984).

    Google Scholar 

  18. Loeb DD, Padgett RW, Hardies SC, Shehee WR, Comer MB, Edgell MH, Hutchison CA: The sequence of a large L1Md element reveals a tandemly repeated 5′ end and several features found in retrotransposons. Mol Cell Biol 6: 168–182 (1986).

    Google Scholar 

  19. Lutcke HA, Chow KC, Mickel FS, Moss KA, Kern HF, Scheele GA: Selection of AUG codons differs in plants and animals. EMBO J 6: 43–48 (1987).

    Google Scholar 

  20. Marlor RL, Parkhurst SM, Corces VG: The Drosophila melanogaster gypsy transposoable element encodes putative gene products homologous to retroviral protein. Mol Cell Biol 6: 1129–1134 (1986).

    Google Scholar 

  21. Mellor J, Fulton SM, Dobson MJ, Wilson W, Kingsman SM, Kingsman AJ: A retrovirus-like strategy for expression of a fusion protein encoded by yeast transposon Ty1. Nature 313: 243–246 (1985).

    Google Scholar 

  22. Messing J, Geraghty D, Heidecker G, Hu N-T, Kridl J, Rubenstein I: Plant gene structure. In: Kosuge T, Meredith CP, Hollaender A (eds) Genetic Engineering of Plants. Plenum Press, New York (1983).

    Google Scholar 

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

    Google Scholar 

  24. Michel F, Lang BF: Mitochondrial class II introns encode proteins related to the reverse transcriptases of retroviruses. Nature 316: 641–643 (1985).

    Google Scholar 

  25. Miller RH, Robinson WS: Common evolutionary origin of hepatitis B virus and retroviruses. Proc Natl Acad Sci USA 83: 2531–2535 (1986).

    Google Scholar 

  26. Mottinger JP, Johns MA, Freeling M: Mutations of the Adh1 gene in maize following infection with barley stripe mosaic virus. Mol Gen Genet 195: 367–369 (1984).

    Google Scholar 

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

    Google Scholar 

  28. Murray MG, Thompson WF: Rapid isolation of high molecular weight plant DNA. Nucl Acids Res 8: 4321–4325 (1980).

    Google Scholar 

  29. Nevers P, Shepherd NS, Saedler H: Plant transposable elements. Adv Bot Res 12: 103–203 (1986).

    Google Scholar 

  30. Pearl LH, Taylor WR: Sequence specificity of retroviral proteases. Nature 328: 482 (1987).

    Google Scholar 

  31. Saghai-Maroof MA, Soliman KM, Jorgensen RA, Allard RW: Ribosomal DNA spacer-length polymorphisms in barley: Mendelian inheritance, chromosomal location, and population dynamics. Proc Natl Acad Sci USA 81: 8014–8018 (1984).

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  34. Schwarz-Sommer Z, Leclercq L, Gobel E, Saedler H: Cin4, an insert altering the structure of the A1 gene in Zea mays, exhibits properties of nonviral retrotransposons. EMBO J 6: 3873–3880 (1987).

    Google Scholar 

  35. Sonigo P, Alizon M, Staskus K, Klatzmann D, Cole S, Danos O, Retzel E, Tiollais P, Haase A, Wain-Hobson S: Nucleotide sequence of the visna lentivirus: Relationship to the AIDS virus. Cell 42: 369–382 (1985).

    Google Scholar 

  36. Sprague GF, McKinney HH, Greeley L: Virus as a mutagenic agent in maize. Science 141: 1052–1053 (1963).

    Google Scholar 

  37. Temin HM: Evolution of retroviruses and other retrotranscripts. In: Bolognesi D (ed) Human Retroviruses, Cancer and AIDS. UCLA Symposia on Molecular and Cellular Biology, New Series, vol. 71, pp. 1–28. Alan R. Liss, New York (1987).

    Google Scholar 

  38. Toh H, Hayashida H, Miyata T: Sequence homology between retroviral reverse transcriptease and putative polymerases of hepatitis B virus and cauliflower mosaic virus. Nature 305: 827–829 (1983).

    Google Scholar 

  39. Toh H, Kikuno R, Hayashida H, Miyata T, Kugimiya W, Inouye S, Yuki S, Saigo K: Close structural resemblence between putative polymerase of a Drosophila transponsable genetic element 17.6 and pol gene product of Moloney murine leukaemia virus. EMBO J 4: 1267–1272 (1985).

    Google Scholar 

  40. Varmus HE: Retroviruses. In: Shapiro JA (ed) Mobile Genetic Elements, pp. 411–503. Academic Press, New York (1983).

    Google Scholar 

  41. Yuki S, Ishimaru S, Inouye S, Saigo K: Identification of genes for reverse transcriptase-like enzymes in two Drosophila retrotransposons, 412 and gypsy: A rapid detection method of reverse transcriptase genes using YXDD box probes. Nucl Acids Res 14: 3017–3030 (1986).

    Google Scholar 

Download references

Author information

Author notes

  1. Marla S. Babcock

    Present address: Department of Chemistry, Rutgers University, 08855, Piscataway, NJ, USA

  2. Sally M. Fuerstenberg

    Present address: Karolinska Institute, Stockholm, Sweden

Affiliations

  1. Plant Molecular Biology Center, Northern Illinois University, 60115, DeKalb, IL, USA

    Mitrick A. Johns, Sally M. Fuerstenberg & Susan I. Fuerstenberg

  2. Plant Cell Research Institute, 94568, Dublin, CA, USA

    Marla S. Babcock & Robert B. Simpson

  3. Department of Genetics, University of California, 94720, Berkeley, CA, USA

    Michael Freeling

Authors
  1. Mitrick A. Johns
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marla S. Babcock
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sally M. Fuerstenberg
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Susan I. Fuerstenberg
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Michael Freeling
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Robert B. Simpson
    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

Johns, M.A., Babcock, M.S., Fuerstenberg, S.M. et al. An unusually compact retrotransposon in maize. Plant Mol Biol 12, 633–642 (1989). https://doi.org/10.1007/BF00044154

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00044154

Key words

  • reverse transcriptase
  • sequence similarity
  • transposable element
  • Zea mays