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. 2005 Jul 13;6(1):75–83. doi: 10.1016/S1044-5773(05)80011-3

Heterologous recombination in the segmented dsRNA genome of bacteriophage Φ6

Leonard Mindich 1
PMCID: PMC7129777  PMID: 32288440

Abstract

The genome of bacteriophage Φ6 is composed of three unique segments of double-stranded RNA packaged within a procapsid. One segment can recombine with another in regions that share little sequence similarity. Although the recombination is therefore heterologous, the crossover points usually consist of two to six identical nucleotides. The frequency of recombinants is enhanced by conditions that prevent or hinder the minus strand synthesis of a single plus strand segment. Recombination serves as a repair system as well as a means of changing the genetic structure of the virus. The reaction can be studied in an in-vitro packaging and replication system involving purified procapsids and ssRNA. Although there are striking differences in the mechanisms of recombination in RNA viruses, there are also strong similarities. All seem to use a copy-choice template switching action for recombination. The Φ6 system is a useful model for the recombination of other segmented double-stranded RNA viruses such as the Reoviridae.

Key words: heterologous recombination, segmented genome, bacteriophage Φ6, dsRNA

References

  • 1.Ledinko N. Genetic recombination with poliovirus type I. Studies of crosses between a normal horse serum-resistant mutant and several guanidine-resistant mutants of the same strain. Virology. 1963;20:107–119. doi: 10.1016/0042-6822(63)90145-4. [DOI] [PubMed] [Google Scholar]
  • 2.Hirst GK. Vol. 27. 1962. Genetic recombination with Newcastle disease virus, polioviruses and influenza; pp. 303–308. (Cold Spring Harbor Symp. Quant. Biol). [DOI] [PubMed] [Google Scholar]
  • 3.Cooper PD. A genetic map of poliovirus temperature-sensitive mutants. Virology. 1968;35:584–596. doi: 10.1016/0042-6822(68)90287-0. [DOI] [PubMed] [Google Scholar]
  • 4.Kirkegaard K, Baltimore D. The mechanism of RNA recombination in poliovirus. Cell. 1986;47:433–443. doi: 10.1016/0092-8674(86)90600-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 5.King AMQ. Genetic recombination in positive strand RNA viruses. In: Domingo E, Holland JJ, Ahlquist P, editors. RNA Genetics, Volume II, Retroviruses, viroids, and RNA recombination. CRC Press; Albany, NY: 1988. pp. 149–165. [Google Scholar]
  • 6.Jarvis TC, Kirkegaard K. The polymerase in its labyrinth. TIG. 1991;7:186–191. doi: 10.1016/0168-9525(91)90434-R. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 7.Lai MMC, Baric RS, Makino S, Keck JG, Egbert J, Leibowitz JL, Stohlman SA. Recombination between nonsegmented RNA genomes of murine coronaviruses. J Virol. 1985;56:449–456. doi: 10.1128/jvi.56.2.449-456.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 8.Lai MMC. RNA recombination in animal and plant viruses. Microbiol Revs. 1992;56:61–79. doi: 10.1128/mr.56.1.61-79.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 9.Makino S, Keck JG, Stohlman SA, Lai MMC. High-frequency RNA recombination of murine coronaviruses. J Virol. 1986;57:729–737. doi: 10.1128/jvi.57.3.729-737.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 10.Keck JG, Stohlman SA, Soe LH, Makino S, Lai MMC. Multiple recombination sites at the 5′-end of murine coronavirus RNA. Virology. 1987;156:331–341. doi: 10.1016/0042-6822(87)90413-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 11.Rott ME, Tremaine JH, Rochon DM. Comparison of the 5′ and 3′ termini of tomato ringspot virus RNA1 and RNA2: Evidence for RNA recombination. Virology. 1991;185:468–472. doi: 10.1016/0042-6822(91)90801-H. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 12.Bergmann M, Garcia-Sastre A, Palese P. Transfection-mediated recombination of Influenza A virus. J Virol. 1992;66:7576–7580. doi: 10.1128/jvi.66.12.7576-7580.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 13.Hahn CS, Lustig S, Strauss EG, Strauss JH. Vol. 85. 1988. Western equine encephalitis virus is a recombinant virus; pp. 5997–6001. (Proc Natl Acad Sci USA). [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 14.Fields S, Winter G. Nucleotide sequences of influenza virus segments 1 and 3 reveal mosaic structure of a small viral RNA segment. Cell. 1982;28:303–313. doi: 10.1016/0092-8674(82)90348-8. [DOI] [PubMed] [Google Scholar]
  • 15.Munishkin AV, Voronin LA, Chetverin AB. An in vivo recombinant RNA capable of autocatalytic synthesis by Qβ replicase. Nature. 1988;333:473–475. doi: 10.1038/333473a0. [DOI] [PubMed] [Google Scholar]
  • 16.Monroe SS, Schlesinger S. Vol. 80. 1983. RNAs from two independently isolated defective-interfering particles of Sindbis virus contain a cellular tRNA sequence at their 5′ ends; pp. 3279–3283. (Proc Natl Acad Sci USA). [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 17.Palasingam K, Shaklee PN. Reversion of Qβ RNA phage mutants by homologous RNA recombination. J Virol. 1992;66:2435–2442. doi: 10.1128/jvi.66.4.2435-2442.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 18.Green AE, Allison RF. Recombination between viral RNA and transgenic plant transcripts. Science. 1994;263:1423–1425. doi: 10.1126/science.8128222. [DOI] [PubMed] [Google Scholar]
  • 19.Bujarski JJ, Kaesberg P. Genetic recombination between RNA components of a multipartite plant virus. Nature. 1986;321:528–531. doi: 10.1038/321528a0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 20.Vidaver AK, Koski RK, Van Etten JL. Bacteriophage Φ6: a lipid-containing virus of Pseudomonas phaseolicola. J Virol. 1973;11:799–805. doi: 10.1128/jvi.11.5.799-805.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 21.Day LA, Mindich L. The molecular weight of bacteriophage Φ6 and its nucleocapsid. Virology. 1980;103:376–385. doi: 10.1016/0042-6822(80)90196-8. [DOI] [PubMed] [Google Scholar]
  • 22.Mindich L, Abelson RD. The characterization of a 120 S particle formed during Φ6 infection. Virology. 1980;103:386–391. doi: 10.1016/0042-6822(80)90197-x. [DOI] [PubMed] [Google Scholar]
  • 23.Koonin EV, Gorbalenya EE, Chumakov KM. Tentative identification of RNA-dependent RNA polymerases of dsRNA viruses and their relationship to positive strand RNA viral polymerases. FEBS Lett. 1989;252:42–46. doi: 10.1016/0014-5793(89)80886-5. [DOI] [PubMed] [Google Scholar]
  • 24.Gottlieb P, Qiao X, Strassman J, Frilander M, Mindich L. Identification of the packaging regions within the genomic RNA segments of bacteriophage Φ6. Virology. 1994;200:42–47. doi: 10.1006/viro.1994.1160. [DOI] [PubMed] [Google Scholar]
  • 25.Mindich L, Qiao X, Onodera S, Gottlieb P, Strassman J. Heterologous recombination in the dsRNA bacteriophage Φ6. J Virol. 1992;66:2605–2610. doi: 10.1128/jvi.66.5.2605-2610.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 26.Mindich L. Bacteriophage Φ6: A unique virus having a lipid-containing membrane and a genome composed of three dsRNA segments. In: Maramorosch K, Murphy FA, Shatkin AJ, editors. Vol. 35. Academic Press; Boca Raton: 1988. pp. 137–176. (Advances in Virus Research). [DOI] [PubMed] [Google Scholar]
  • 27.Olkkonen VM, Gottlieb P, Strassman J, Qiao X, Bamford DH, Mindich L. Vol. 87. 1990. In vitro assembly of infectious nucleocapsids of bacteriophage Φ6: Formation of a recombinant double-stranded RNA virus; pp. 9173–9177. (Proc Natl Acad Sci USA). [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 28.Johnson MD, Mindich L. Isolation and characterization of nonsense mutants in gene 10 of bacteriophage Φ6. J Virol. 1994;68:2331–2338. doi: 10.1128/jvi.68.4.2331-2338.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 29.Onodera S, Qiao X, Gottlieb P, Strassman J, Frilander M, Mindich L. RNA structure and heterologous recombination in the dsRNA bacteriophage Φ6. J Virol. 1993;67:4914–4922. doi: 10.1128/jvi.67.8.4914-4922.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 30.Gottlieb P, Strassman J, Qiao X, Frilander M, Frucht A, Mindich L. In vitro packaging and replication of individual genomic segments of bacteriophage Φ6 RNA. J Virol. 1992;66:2611–2616. doi: 10.1128/jvi.66.5.2611-2616.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 31.Frilander M, Gottlieb P, Strassman J, Bamford DH, Mindich L. Dependence of minus strand synthesis upon complete genomic packaging in the dsRNA bacteriophage Φ6. J Virol. 1992;66:5013–5017. doi: 10.1128/jvi.66.8.5013-5017.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 32.Zhang J, Temin HM. Retrovirus recombination depends on the length of sequence identity and is not error prone. J Virol. 1994;68:2409–2414. doi: 10.1128/jvi.68.4.2409-2414.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 33.Chamberlin MJ. Wiley-Liss; New York: 1993. New models for the mechanism of transcription elongation and its regulation. [PubMed] [Google Scholar]
  • 34.Mindich L, Qiao X, Onodera S, Gottlieb P, Frilander M. RNA structural requirements for stability and minus strand synthesis in the dsRNA bacteriophage Φ6. Virology. 1994;202:258–263. doi: 10.1006/viro.1994.1341. [DOI] [PubMed] [Google Scholar]
  • 35.Nagy PD, Bujarski JJ. Vol. 90. 1993. Targeting the site of RNA-RNA recombination in brome mosaic virus with antisense sequences; pp. 6390–6394. (Proc Natl Acad Sci USA). [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 36.Bujarski JJ, Dzianott AM. Generation and analysis of nonhomologous RNA-RNA recombinants in brome mosaic virus: sequence complementarities at crossover sites. J Virol. 1991;65:4153–4159. doi: 10.1128/jvi.65.8.4153-4159.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 37.Romanova LI, Blinov VM, Tolskaya EA, Viktorova EG, Kolesnikowa MS, Guseva EA, Agol VI. The primary structure of crossover regions of intertypic poliovirus recombinants: a model of recombination between RNA genomes. Virology. 1986;155:202–213. doi: 10.1016/0042-6822(86)90180-7. [DOI] [PubMed] [Google Scholar]
  • 38.Cascone PJ, Haydar TF, Simon AE. Sequences and structures required for recombination between virus-associated RNAs. Science. 1993;260:801–805. doi: 10.1126/science.8484119. [DOI] [PubMed] [Google Scholar]
  • 39.McIntyre M, Rosenbaum V, Rappold W, Desselberger M, Wood D, Desselberg U. Biophysical characterization of rotavirus particles containing rearranged genomes. J Gen Virol. 1987;68:2961–2966. doi: 10.1099/0022-1317-68-11-2961. [DOI] [PubMed] [Google Scholar]
  • 40.Ballard A, McCrae MA, Desselberg U. Nucleotide sequences of normal and rearranged RNA segments 10 of human rotaviruses. J Gen Virol. 1992;73:633–638. doi: 10.1099/0022-1317-73-3-633. [DOI] [PubMed] [Google Scholar]
  • 41.Casini G, Revel HR. A new small low-abundant nonstructural protein encoded by the L segment of the dsRNA bacteriophage Φ6. Virology. 1994;203:221–228. doi: 10.1006/viro.1994.1479. [DOI] [PubMed] [Google Scholar]
  • 42.Gottlieb P, Strassman J, Qiao X, Frucht A, Mindich L. In vitro replication, packaging and transcription of the segmented dsRNA genome of bacteriophage Φ6: studies with procapsids assembled from plasmid encoded proteins. J Bacteriol. 1990;172:5774–5782. doi: 10.1128/jb.172.10.5774-5782.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]

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