1887

Abstract

Hybrids between different species or genera of the single-stranded RNA coliphages have not been found in nature. Here, it has been shown that viable hybrids between different phage species can easily be generated in the laboratory by recombination. cDNA of species I phage MS2 located on a plasmid and lacking part of its 5′ untranslated leader (5′ UTR) was complemented with another plasmid carrying the 5′ half of the genome of fr, a species I phage, or of KU1, a species II representative with low sequence similarity. When the two plasmids were present in the same cell there was spontaneous production of hybrid phages. Interestingly, these hybrids did not arise by a double or single crossover that would replace the missing MS2 sequences with those of fr or KU1. Rather, hybrids arose by attaching the complete 5′ UTR of fr or KU1 to the 5′ terminus of the defective MS2 phage. Several elements of the 5′ UTR then occurred twice, one from KU1 (or fr) and the other from MS2. These redundant elements are in most cases deleted upon evolution of the hybrids. As a result, the 5′ UTR of KU1 (or fr) then replaced that of MS2. It was earlier shown that this 5′ UTR could assume two alternating structures that facilitated transient translation of the proximal maturation gene. Apparently, this timer function of the 5′ UTR was exchangeable and could function independently of the rest of the genome. When hybrids were competed against wild-type, they were quickly outgrown, probably explaining their absence from natural isolates.

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2002-05-01
2019-10-22
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References

  1. Aaziz, R. & Tepfer, M. ( 1999; ). Recombination between genomic RNAs of two cucumovirus under conditions of minimal selection pressure. Virology 263, 282-289.[CrossRef]
    [Google Scholar]
  2. Adhin, M. R. (1989). A comparative analysis of RNA coliphages. Structural and regulatory features. PhD thesis, Leiden University, The Netherlands.
  3. Beekwilder, M. J. (1996). Secondary structure of the RNA genome of bacteriophage Q β. PhD thesis, Leiden University, The Netherlands.
  4. Biebricher, C. K. & Luce, R. ( 1992; ). In vitro recombination and terminal elongation of RNA by Qβ replicase. EMBO Journal 11, 5129-5135.
    [Google Scholar]
  5. Canto, T., Choi, S. K. & Palukaitis, P. ( 2001; ). A subpopulation of RNA 1 of cucumber mosaic virus contains 3′ termini originating from RNAs 2 or 3. Journal of General Virology 82, 941-945.
    [Google Scholar]
  6. Chetverin, A. B., Chetverina, H. V., Demidenko, A. A. & Ugarov, V. I. ( 1997; ). Nonhomologous RNA recombination in a cell-free system: evidence for a transesterfication mechanism guided by secondary structure. Cell 88, 503-513.[CrossRef]
    [Google Scholar]
  7. Furuse, K. ( 1987; ). Distribution of coliphages in the environment: general considerations. In Phage Ecology , pp. 87-124. Edited by S. M. Goyal. New York:John Wiley & Sons.
  8. Groeneveld, H. (1997). Secondary structure of bacteriophage MS2 RNA. PhD thesis, Leiden University, The Netherlands.
  9. Groeneveld, H., Thimon, H. & van Duin, J. ( 1995; ). Translational control of maturation-protein synthesis in phage MS2: a role for the kinetics of RNA folding? RNA 1, 79-88.
    [Google Scholar]
  10. Groeneveld, H., Oudot, F. & van Duin, J. ( 1996; ). RNA phage KU1 has an insertion of 18 nucleotides in the start codon of its lysis gene. Virology 218, 141-147.[CrossRef]
    [Google Scholar]
  11. Inokuchi, Y., Takahashi, R., Hirose, T., Inayama, S., Jacobson, A. B. & Hirashima, A. ( 1986; ). The complete nucleotide sequence of group II RNA coliphage GA. Journal of Biochemistry (Tokyo) 99, 1169-1180.
    [Google Scholar]
  12. Inokuchi, Y., Jacobson, A. B., Hirose, T., Inayama, S. & Hirashima, A. ( 1988; ). Analysis of the complete nucleotide sequence of the group IV coliphage SP. Nucleic Acids Research 16, 6205-6221.[CrossRef]
    [Google Scholar]
  13. Klovins, J., Tsareva, N. V., de Smit, M. H., Berzins, V. & van Duin, J. ( 1997; ). Rapid evolution of translational control mechanisms in RNA genomes. Journal of Molecular Biology 265, 372-384.[CrossRef]
    [Google Scholar]
  14. Klovins, J., Berzins, V. & van Duin, J. ( 1998; ). A long-range interaction in Qβ RNA that bridges the thousand nucleotides between the M-site and the 3′ end is required for replication. RNA 4, 948-957.[CrossRef]
    [Google Scholar]
  15. Masuta, C., Ueda, S., Suzuki, M. & Uyeda, I. ( 1998; ). Evolution of a quadripartite hybrid virus by interspecific exchange and recombination between replicase components of two related tripartite RNA viruses. Proceedings of the National Academy of Sciences, USA 95, 10487-10492.[CrossRef]
    [Google Scholar]
  16. Miller, J. H., Ganem, D., Lu, P. & Schmitz, A. ( 1977; ). Genetic studies of the lac repressor. Journal of Molecular Biology 109, 275-301.[CrossRef]
    [Google Scholar]
  17. Olsthoorn, R. C. L. (1996). Structure and evolution of RNA phages. PhD thesis, Leiden University, The Netherlands.
  18. Olsthoorn, R. C. L., Licis, N. & van Duin, J. ( 1994; ). Leeway and constraints in the forced evolution of a regulatory RNA helix. EMBO Journal 13, 2660-2668.
    [Google Scholar]
  19. Poot, R. A., Tsareva, N. V., Boni, I. V. & van Duin, J. ( 1997; ). RNA folding kinetics regulates translation of phage MS2 maturation gene. Proceedings of the National Academy of Sciences, USA 94, 10110-10115.[CrossRef]
    [Google Scholar]
  20. Remaut, E., Stanssens, P. & Fiers, W. ( 1981; ). Plasmid vectors for high efficiency expression controlled by the PL promoter of coliphage lambda. Gene 15, 81-93.[CrossRef]
    [Google Scholar]
  21. Shaklee, P. N., Miglietta, J. J., Palmenberg, A. C. & Kaesberg, P. ( 1988; ). Infectious positive- and negative-strand transcript RNAs from bacteriophage Qβ cDNA clones. Virology 163, 209-213.[CrossRef]
    [Google Scholar]
  22. Taniguchi, T., Palmieri, M. & Weissmann, C. ( 1978; ). Qβ DNA-containing hybrid plasmids give rise to Qβ phage formation in the bacterial host. Nature 274, 223-228.[CrossRef]
    [Google Scholar]
  23. van Meerten, D., Zelwer, M., Régnier, P. & van Duin, J. ( 1999; ). In vivo oligo(A) insertions in phage MS2: role of Escherichia coli poly(A) polymerase. Nucleic Acids Research 27, 3891-3898.[CrossRef]
    [Google Scholar]
  24. van Meerten, D., Girard, G. & van Duin, J. ( 2001; ). Translational control by delayed RNA folding: identification of the kinetic trap. RNA 7, 483-494.[CrossRef]
    [Google Scholar]
  25. White, A. K. & Morris, J. T. ( 1995; ). RNA determinants of junction site selection in RNA virus recombinants and defective interfering RNAs. RNA 1, 1029-1040.
    [Google Scholar]
  26. Worobey, M., Rambaut, A. & Holmes, E. C. ( 1999; ). Widespread intra-serotype recombination in natural populations of dengue virus. Proceedings of the National Academy of Sciences, USA 96, 7352-7357.[CrossRef]
    [Google Scholar]
  27. Yuan, S., Nelsen, C. J., Murtaugh, M. P., Schmitt, B. J. & Faaberg, K. S. ( 1999; ). Recombination between North American strains of porcine reproductive and respiratory syndrome virus. Virus Research 61, 87-98.[CrossRef]
    [Google Scholar]
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