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. 1995 Jun 1;14(11):2670–2678. doi: 10.1002/j.1460-2075.1995.tb07265.x

Sequence variability within the tobacco retrotransposon Tnt1 population.

J M Casacuberta 1, S Vernhettes 1, M A Grandbastien 1
PMCID: PMC398381  PMID: 7781619

Abstract

Retroviruses consist of populations of different but closely related genomes referred to as quasispecies. A high mutation rate coupled with extremely rapid replication cycles allows these sequences to be highly interconnected in a rapid equilibrium. It is not known if other retroelements can show a similar population structure. We show here that when the tobacco Tnt1 retrotransposon is expressed, its RNA is not a unique sequence but a population of different but closely related sequences. Nevertheless, this highly variable population is not in a rapid equilibrium and could not be considered as a quasispecies. We have thus named the structure presented by Tnt1 RNA quasispecies-like. We show that the expression of Tnt1 in different situations gives rise to different populations of Tnt1 RNA sequences, suggesting an adaptive capacity for this element. The analysis of the variability within the total genomic population of Tnt1 elements shows that mutations frequently occur in important regulatory elements and that defective elements are often produced. We discuss the implications that this population structure could have for Tnt1 regulation and evolution.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Boeke J. D., Corces V. G. Transcription and reverse transcription of retrotransposons. Annu Rev Microbiol. 1989;43:403–434. doi: 10.1146/annurev.mi.43.100189.002155. [DOI] [PubMed] [Google Scholar]
  2. Boeke J. D., Eichinger D., Castrillon D., Fink G. R. The Saccharomyces cerevisiae genome contains functional and nonfunctional copies of transposon Ty1. Mol Cell Biol. 1988 Apr;8(4):1432–1442. doi: 10.1128/mcb.8.4.1432. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Boeke J. D., Garfinkel D. J., Styles C. A., Fink G. R. Ty elements transpose through an RNA intermediate. Cell. 1985 Mar;40(3):491–500. doi: 10.1016/0092-8674(85)90197-7. [DOI] [PubMed] [Google Scholar]
  4. Casacuberta J. M., Grandbastien M. A. Characterisation of LTR sequences involved in the protoplast specific expression of the tobacco Tnt1 retrotransposon. Nucleic Acids Res. 1993 May 11;21(9):2087–2093. doi: 10.1093/nar/21.9.2087. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Coffin J. M. Genetic variation in AIDS viruses. Cell. 1986 Jul 4;46(1):1–4. doi: 10.1016/0092-8674(86)90851-2. [DOI] [PubMed] [Google Scholar]
  6. Domingo E., Martínez-Salas E., Sobrino F., de la Torre J. C., Portela A., Ortín J., López-Galindez C., Pérez-Breña P., Villanueva N., Nájera R. The quasispecies (extremely heterogeneous) nature of viral RNA genome populations: biological relevance--a review. Gene. 1985;40(1):1–8. doi: 10.1016/0378-1119(85)90017-4. [DOI] [PubMed] [Google Scholar]
  7. Domingo E. RNA virus evolution and the control of viral disease. Prog Drug Res. 1989;33:93–133. doi: 10.1007/978-3-0348-9146-2_5. [DOI] [PubMed] [Google Scholar]
  8. Flavell A. J., Smith D. B., Kumar A. Extreme heterogeneity of Ty1-copia group retrotransposons in plants. Mol Gen Genet. 1992 Jan;231(2):233–242. doi: 10.1007/BF00279796. [DOI] [PubMed] [Google Scholar]
  9. Grandbastien M. A., Audeon C., Casacuberta J. M., Grappin P., Lucas H., Moreau C., Pouteau S. Functional analysis of the tobacco Tnt1 retrotransposon. Genetica. 1994;93(1-3):181–189. doi: 10.1007/BF01435250. [DOI] [PubMed] [Google Scholar]
  10. Grandbastien M. A. Retroelements in higher plants. Trends Genet. 1992 Mar;8(3):103–108. doi: 10.1016/0168-9525(92)90198-d. [DOI] [PubMed] [Google Scholar]
  11. Grandbastien M. A., Spielmann A., Caboche M. Tnt1, a mobile retroviral-like transposable element of tobacco isolated by plant cell genetics. Nature. 1989 Jan 26;337(6205):376–380. doi: 10.1038/337376a0. [DOI] [PubMed] [Google Scholar]
  12. Hu W. S., Temin H. M. Genetic consequences of packaging two RNA genomes in one retroviral particle: pseudodiploidy and high rate of genetic recombination. Proc Natl Acad Sci U S A. 1990 Feb;87(4):1556–1560. doi: 10.1073/pnas.87.4.1556. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hu W. S., Temin H. M. Retroviral recombination and reverse transcription. Science. 1990 Nov 30;250(4985):1227–1233. doi: 10.1126/science.1700865. [DOI] [PubMed] [Google Scholar]
  14. Katz R. A., Skalka A. M. Generation of diversity in retroviruses. Annu Rev Genet. 1990;24:409–445. doi: 10.1146/annurev.ge.24.120190.002205. [DOI] [PubMed] [Google Scholar]
  15. Marchuk D., Drumm M., Saulino A., Collins F. S. Construction of T-vectors, a rapid and general system for direct cloning of unmodified PCR products. Nucleic Acids Res. 1991 Mar 11;19(5):1154–1154. doi: 10.1093/nar/19.5.1154. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Meyerhans A., Cheynier R., Albert J., Seth M., Kwok S., Sninsky J., Morfeldt-Månson L., Asjö B., Wain-Hobson S. Temporal fluctuations in HIV quasispecies in vivo are not reflected by sequential HIV isolations. Cell. 1989 Sep 8;58(5):901–910. doi: 10.1016/0092-8674(89)90942-2. [DOI] [PubMed] [Google Scholar]
  17. Meyerhans A., Vartanian J. P., Wain-Hobson S. DNA recombination during PCR. Nucleic Acids Res. 1990 Apr 11;18(7):1687–1691. doi: 10.1093/nar/18.7.1687. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Needleman S. B., Wunsch C. D. A general method applicable to the search for similarities in the amino acid sequence of two proteins. J Mol Biol. 1970 Mar;48(3):443–453. doi: 10.1016/0022-2836(70)90057-4. [DOI] [PubMed] [Google Scholar]
  19. Oldstone M. B. Molecular anatomy of viral persistence. J Virol. 1991 Dec;65(12):6381–6386. doi: 10.1128/jvi.65.12.6381-6386.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Pathak V. K., Temin H. M. 5-Azacytidine and RNA secondary structure increase the retrovirus mutation rate. J Virol. 1992 May;66(5):3093–3100. doi: 10.1128/jvi.66.5.3093-3100.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Pathak V. K., Temin H. M. Broad spectrum of in vivo forward mutations, hypermutations, and mutational hotspots in a retroviral shuttle vector after a single replication cycle: deletions and deletions with insertions. Proc Natl Acad Sci U S A. 1990 Aug;87(16):6024–6028. doi: 10.1073/pnas.87.16.6024. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Pouteau S., Huttner E., Grandbastien M. A., Caboche M. Specific expression of the tobacco Tnt1 retrotransposon in protoplasts. EMBO J. 1991 Jul;10(7):1911–1918. doi: 10.1002/j.1460-2075.1991.tb07717.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Rhode B. W., Emerman M., Temin H. M. Instability of large direct repeats in retrovirus vectors. J Virol. 1987 Mar;61(3):925–927. doi: 10.1128/jvi.61.3.925-927.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Steinhauer D. A., Holland J. J. Rapid evolution of RNA viruses. Annu Rev Microbiol. 1987;41:409–433. doi: 10.1146/annurev.mi.41.100187.002205. [DOI] [PubMed] [Google Scholar]
  25. Temin H. M. Retrovirus variation and reverse transcription: abnormal strand transfers result in retrovirus genetic variation. Proc Natl Acad Sci U S A. 1993 Aug 1;90(15):6900–6903. doi: 10.1073/pnas.90.15.6900. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Varela-Echavarría A., Prorock C. M., Ron Y., Dougherty J. P. High rate of genetic rearrangement during replication of a Moloney murine leukemia virus-based vector. J Virol. 1993 Nov;67(11):6357–6364. doi: 10.1128/jvi.67.11.6357-6364.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Wain-Hobson S. The fastest genome evolution ever described: HIV variation in situ. Curr Opin Genet Dev. 1993 Dec;3(6):878–883. doi: 10.1016/0959-437x(93)90008-d. [DOI] [PubMed] [Google Scholar]
  28. Xiong Y., Eickbush T. H. Origin and evolution of retroelements based upon their reverse transcriptase sequences. EMBO J. 1990 Oct;9(10):3353–3362. doi: 10.1002/j.1460-2075.1990.tb07536.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Xu H., Boeke J. D. High-frequency deletion between homologous sequences during retrotransposition of Ty elements in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1987 Dec;84(23):8553–8557. doi: 10.1073/pnas.84.23.8553. [DOI] [PMC free article] [PubMed] [Google Scholar]

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