• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of microrevMicrobiol Mol Biol Rev ArchivePermissionsJournals.ASM.orgMMBR ArticleJournal InfoAuthorsReviewers
Microbiol Rev. Mar 1992; 56(1): 61–79.
PMCID: PMC372854

RNA recombination in animal and plant viruses.

Abstract

An increasing number of animal and plant viruses have been shown to undergo RNA-RNA recombination, which is defined as the exchange of genetic information between nonsegmented RNAs. Only some of these viruses have been shown to undergo recombination in experimental infection of tissue culture, animals, and plants. However, a survey of viral RNA structure and sequences suggests that many RNA viruses were derived form homologous or nonhomologous recombination between viruses or between viruses and cellular genes during natural viral evolution. The high frequency and widespread nature of RNA recombination indicate that this phenomenon plays a more significant role in the biology of RNA viruses than was previously recognized. Three types of RNA recombination are defined: homologous recombination; aberrant homologous recombination, which results in sequence duplication, insertion, or deletion during recombination; and nonhomologous (illegitimate) recombination, which does not involve sequence homology. RNA recombination has been shown to occur by a copy choice mechanism in some viruses. A model for this recombination mechanism is presented.

Full text

Full text is available as a scanned copy of the original print version. Get a printable copy (PDF file) of the complete article (3.9M), or click on a page image below to browse page by page. Links to PubMed are also available for Selected References.

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Agut H, Kean KM, Bellocq C, Fichot O, Girard M. Intratypic recombination of polioviruses: evidence for multiple crossing-over sites on the viral genome. J Virol. 1987 May;61(5):1722–1725. [PMC free article] [PubMed]
  • Allison RF, Janda M, Ahlquist P. Sequence of cowpea chlorotic mottle virus RNAs 2 and 3 and evidence of a recombination event during bromovirus evolution. Virology. 1989 Sep;172(1):321–330. [PubMed]
  • Allison R, Thompson C, Ahlquist P. Regeneration of a functional RNA virus genome by recombination between deletion mutants and requirement for cowpea chlorotic mottle virus 3a and coat genes for systemic infection. Proc Natl Acad Sci U S A. 1990 Mar;87(5):1820–1824. [PMC free article] [PubMed]
  • Angenent GC, Posthumus E, Brederode FT, Bol JF. Genome structure of tobacco rattle virus strain PLB: further evidence on the occurrence of RNA recombination among tobraviruses. Virology. 1989 Jul;171(1):271–274. [PubMed]
  • Baker SC, Lai MM. An in vitro system for the leader-primed transcription of coronavirus mRNAs. EMBO J. 1990 Dec;9(12):4173–4179. [PMC free article] [PubMed]
  • Banner LR, Keck JG, Lai MM. A clustering of RNA recombination sites adjacent to a hypervariable region of the peplomer gene of murine coronavirus. Virology. 1990 Apr;175(2):548–555. [PubMed]
  • Baric RS, Fu K, Schaad MC, Stohlman SA. Establishing a genetic recombination map for murine coronavirus strain A59 complementation groups. Virology. 1990 Aug;177(2):646–656. [PubMed]
  • Baric RS, Nelson GW, Fleming JO, Deans RJ, Keck JG, Casteel N, Stohlman SA. Interactions between coronavirus nucleocapsid protein and viral RNAs: implications for viral transcription. J Virol. 1988 Nov;62(11):4280–4287. [PMC free article] [PubMed]
  • Baric RS, Shieh CK, Stohlman SA, Lai MM. Analysis of intracellular small RNAs of mouse hepatitis virus: evidence for discontinuous transcription. Virology. 1987 Feb;156(2):342–354. [PubMed]
  • Brayton PR, Stohlman SA, Lai MM. Further characterization of mouse hepatitis virus RNA-dependent RNA polymerases. Virology. 1984 Feb;133(1):197–201. [PubMed]
  • Brownlie J, Clarke MC, Howard CJ. Experimental production of fatal mucosal disease in cattle. Vet Rec. 1984 Jun 2;114(22):535–536. [PubMed]
  • Brunier D, Michel B, Ehrlich SD. Copy choice illegitimate DNA recombination. Cell. 1988 Mar 25;52(6):883–892. [PubMed]
  • Bujarski JJ, Dzianott AM. Generation and analysis of nonhomologous RNA-RNA recombinants in brome mosaic virus: sequence complementarities at crossover sites. J Virol. 1991 Aug;65(8):4153–4159. [PMC free article] [PubMed]
  • Bujarski JJ, Kaesberg P. Genetic recombination between RNA components of a multipartite plant virus. Nature. 321(6069):528–531. [PubMed]
  • Butterworth BE, Shimshick EJ, Yin FH. Association of the polioviral RNA polymerase complex with phospholipid membranes. J Virol. 1976 Aug;19(2):457–466. [PMC free article] [PubMed]
  • Cascone PJ, Carpenter CD, Li XH, Simon AE. Recombination between satellite RNAs of turnip crinkle virus. EMBO J. 1990 Jun;9(6):1709–1715. [PMC free article] [PubMed]
  • Cavanagh D, Davis PJ. Evolution of avian coronavirus IBV: sequence of the matrix glycoprotein gene and intergenic region of several serotypes. J Gen Virol. 1988 Mar;69(Pt 3):621–629. [PubMed]
  • Coffin JM. Structure, replication, and recombination of retrovirus genomes: some unifying hypotheses. J Gen Virol. 1979 Jan;42(1):1–26. [PubMed]
  • Collett MS, Moennig V, Horzinek MC. Recent advances in pestivirus research. J Gen Virol. 1989 Feb;70(Pt 2):253–266. [PubMed]
  • Cooper PD. A genetic map of poliovirus temperature-sensitive mutants. Virology. 1968 Aug;35(4):584–596. [PubMed]
  • Copper PD, Steiner-Pryor A, Scotti PD, Delong D. On the nature of poliovirus genetic recombinants. J Gen Virol. 1974 Apr;23(1):41–49. [PubMed]
  • Dennis DE, Brian DA. RNA-dependent RNA polymerase activity in coronavirus- infected cells. J Virol. 1982 Apr;42(1):153–164. [PMC free article] [PubMed]
  • Dominguez G, Wang CY, Frey TK. Sequence of the genome RNA of rubella virus: evidence for genetic rearrangement during togavirus evolution. Virology. 1990 Jul;177(1):225–238. [PubMed]
  • Dreher TW, Rao AL, Hall TC. Replication in vivo of mutant brome mosaic virus RNAs defective in aminoacylation. J Mol Biol. 1989 Apr 5;206(3):425–438. [PubMed]
  • Fields BN. Genetics of Reovirus. Curr Top Microbiol Immunol. 1981;91:1–24. [PubMed]
  • Fields S, Winter G. Nucleotide sequences of influenza virus segments 1 and 3 reveal mosaic structure of a small viral RNA segment. Cell. 1982 Feb;28(2):303–313. [PubMed]
  • Geigenmüller-Gnirke U, Weiss B, Wright R, Schlesinger S. Complementation between Sindbis viral RNAs produces infectious particles with a bipartite genome. Proc Natl Acad Sci U S A. 1991 Apr 15;88(8):3253–3257. [PMC free article] [PubMed]
  • Goldbach R. Genome similarities between plant and animal RNA viruses. Microbiol Sci. 1987 Jul;4(7):197–202. [PubMed]
  • Hahn CS, Lustig S, Strauss EG, Strauss JH. Western equine encephalitis virus is a recombinant virus. Proc Natl Acad Sci U S A. 1988 Aug;85(16):5997–6001. [PMC free article] [PubMed]
  • Haseloff J, Goelet P, Zimmern D, Ahlquist P, Dasgupta R, Kaesberg P. Striking similarities in amino acid sequence among nonstructural proteins encoded by RNA viruses that have dissimilar genomic organization. Proc Natl Acad Sci U S A. 1984 Jul;81(14):4358–4362. [PMC free article] [PubMed]
  • Haseltine WA, Kleid DG, Panet A, Rothenberg E, Baltimore D. Ordered transcription of RNA tumor virus genomes. J Mol Biol. 1976 Sep 5;106(1):109–131. [PubMed]
  • HIRST GK. Genetic recombination with Newcastle disease virus, polioviruses, and influenza. Cold Spring Harb Symp Quant Biol. 1962;27:303–309. [PubMed]
  • Holland J, Spindler K, Horodyski F, Grabau E, Nichol S, VandePol S. Rapid evolution of RNA genomes. Science. 1982 Mar 26;215(4540):1577–1585. [PubMed]
  • Hu WS, Temin HM. 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. [PMC free article] [PubMed]
  • Huisman MJ, Cornelissen BJ, Groenendijk CF, Bol JF, van Vloten-Doting L. Alfalfa mosaic virus temperature-sensitive mutants. V. The nucleotide sequence of TBTS 7 RNA 3 shows limited nucleotide changes and evidence for heterologous recombination. Virology. 1989 Aug;171(2):409–416. [PubMed]
  • Javier RT, Sedarati F, Stevens JG. Two avirulent herpes simplex viruses generate lethal recombinants in vivo. Science. 1986 Nov 7;234(4777):746–748. [PubMed]
  • Junghans RP, Boone LR, Skalka AM. Retroviral DNA H structures: displacement-assimilation model of recombination. Cell. 1982 Aug;30(1):53–62. [PubMed]
  • Kassavetis GA, Chamberlin MJ. Pausing and termination of transcription within the early region of bacteriophage T7 DNA in vitro. J Biol Chem. 1981 Mar 25;256(6):2777–2786. [PubMed]
  • Katz JB, Henderson LM, Erickson GA. Recombination in vivo of pseudorabies vaccine strains to produce new virus strains. Vaccine. 1990 Jun;8(3):286–288. [PubMed]
  • Keck JG, Matsushima GK, Makino S, Fleming JO, Vannier DM, Stohlman SA, Lai MM. In vivo RNA-RNA recombination of coronavirus in mouse brain. J Virol. 1988 May;62(5):1810–1813. [PMC free article] [PubMed]
  • Keck JG, Stohlman SA, Soe LH, Makino S, Lai MM. Multiple recombination sites at the 5'-end of murine coronavirus RNA. Virology. 1987 Feb;156(2):331–341. [PubMed]
  • Keese P, Symons RH. Domains in viroids: evidence of intermolecular RNA rearrangements and their contribution to viroid evolution. Proc Natl Acad Sci U S A. 1985 Jul;82(14):4582–4586. [PMC free article] [PubMed]
  • Khatchikian D, Orlich M, Rott R. Increased viral pathogenicity after insertion of a 28S ribosomal RNA sequence into the haemagglutinin gene of an influenza virus. Nature. 1989 Jul 13;340(6229):156–157. [PubMed]
  • King AM, McCahon D, Saunders K, Newman JW, Slade WR. Multiple sites of recombination within the RNA genome of foot-and-mouth disease virus. Virus Res. 1985 Nov;3(4):373–384. [PubMed]
  • King AM, McCahon D, Slade WR, Newman JW. Recombination in RNA. Cell. 1982 Jul;29(3):921–928. [PubMed]
  • King B, Potts BJ, Brian DA. Bovine coronavirus hemagglutinin protein. Virus Res. 1985 Feb;2(1):53–59. [PubMed]
  • Kirkegaard K, Baltimore D. The mechanism of RNA recombination in poliovirus. Cell. 1986 Nov 7;47(3):433–443. [PubMed]
  • Kuge S, Saito I, Nomoto A. Primary structure of poliovirus defective-interfering particle genomes and possible generation mechanisms of the particles. J Mol Biol. 1986 Dec 5;192(3):473–487. [PubMed]
  • Kusters JG, Niesters HG, Lenstra JA, Horzinek MC, van der Zeijst BA. Phylogeny of antigenic variants of avian coronavirus IBV. Virology. 1989 Mar;169(1):217–221. [PubMed]
  • Lai MM. Coronavirus: organization, replication and expression of genome. Annu Rev Microbiol. 1990;44:303–333. [PubMed]
  • Lai MM, Baric RS, Makino S, Keck JG, Egbert J, Leibowitz JL, Stohlman SA. Recombination between nonsegmented RNA genomes of murine coronaviruses. J Virol. 1985 Nov;56(2):449–456. [PMC free article] [PubMed]
  • Lake JR, Priston AJ, Slade WR. A genetic recombination map of foot-and-mouth disease virus. J Gen Virol. 1975 Jun;27(3):355–367. [PubMed]
  • Landick R, Carey J, Yanofsky C. Detection of transcription-pausing in vivo in the trp operon leader region. Proc Natl Acad Sci U S A. 1987 Mar;84(6):1507–1511. [PMC free article] [PubMed]
  • Lazarus LH, Barzilai R. Association of foot-and-mouth disease virus replicase with RNA template and cytoplasmic membranes. J Gen Virol. 1974 May;23(2):213–218. [PubMed]
  • Lazzarini RA, Keene JD, Schubert M. The origins of defective interfering particles of the negative-strand RNA viruses. Cell. 1981 Oct;26(2 Pt 2):145–154. [PubMed]
  • LEDINKO N. Genetic recombination with poliovirus type 1. Studies of crosses between a normal horse serum-resistant mutant and several guanidine-resistant mutants of the same strain. Virology. 1963 May;20:107–119. [PubMed]
  • Lee HJ, Shieh CK, Gorbalenya AE, Koonin EV, La Monica N, Tuler J, Bagdzhadzhyan A, Lai MM. The complete sequence (22 kilobases) of murine coronavirus gene 1 encoding the putative proteases and RNA polymerase. Virology. 1991 Feb;180(2):567–582. [PubMed]
  • Lin FL, Sperle K, Sternberg N. Model for homologous recombination during transfer of DNA into mouse L cells: role for DNA ends in the recombination process. Mol Cell Biol. 1984 Jun;4(6):1020–1034. [PMC free article] [PubMed]
  • Luytjes W, Bredenbeek PJ, Noten AF, Horzinek MC, Spaan WJ. Sequence of mouse hepatitis virus A59 mRNA 2: indications for RNA recombination between coronaviruses and influenza C virus. Virology. 1988 Oct;166(2):415–422. [PubMed]
  • Makino S, Fleming JO, Keck JG, Stohlman SA, Lai MM. RNA recombination of coronaviruses: localization of neutralizing epitopes and neuropathogenic determinants on the carboxyl terminus of peplomers. Proc Natl Acad Sci U S A. 1987 Sep;84(18):6567–6571. [PMC free article] [PubMed]
  • Makino S, Keck JG, Stohlman SA, Lai MM. High-frequency RNA recombination of murine coronaviruses. J Virol. 1986 Mar;57(3):729–737. [PMC free article] [PubMed]
  • McCahon D. The genetics of aphthovirus. Brief review. Arch Virol. 1981;69(1):1–23. [PubMed]
  • McCahon D, King AM, Roe DS, Slade WR, Newman JW, Cleary AM. Isolation and biochemical characterization of intertypic recombinants of foot-and-mouth disease virus. Virus Res. 1985 Jul;3(1):87–100. [PubMed]
  • McCahon D, Slade WR, Priston RA, Lake JR. An extended genetic recombination map for foot-and-mouth diseases virus. J Gen Virol. 1977 Jun;35(3):555–565. [PubMed]
  • MESELSON M, WEIGLE JJ. Chromosome brekage accompanying genetic recombination in bacteriophage. Proc Natl Acad Sci U S A. 1961 Jun 15;47:857–868. [PMC free article] [PubMed]
  • Meyers G, Tautz N, Dubovi EJ, Thiel HJ. Viral cytopathogenicity correlated with integration of ubiquitin-coding sequences. Virology. 1991 Feb;180(2):602–616. [PubMed]
  • Mills DR, Dobkin C, Kramer FR. Template-determined, variable rate of RNA chain elongation. Cell. 1978 Oct;15(2):541–550. [PubMed]
  • Minor PD, John A, Ferguson M, Icenogle JP. Antigenic and molecular evolution of the vaccine strain of type 3 poliovirus during the period of excretion by a primary vaccinee. J Gen Virol. 1986 Apr;67(Pt 4):693–706. [PubMed]
  • Monroe SS, Schlesinger S. RNAs from two independently isolated defective interfering particles of Sindbis virus contain a cellular tRNA sequence at their 5' ends. Proc Natl Acad Sci U S A. 1983 Jun;80(11):3279–3283. [PMC free article] [PubMed]
  • Munishkin AV, Voronin LA, Chetverin AB. An in vivo recombinant RNA capable of autocatalytic synthesis by Q beta replicase. Nature. 1988 Jun 2;333(6172):473–475. [PubMed]
  • Palese P. The genes of influenza virus. Cell. 1977 Jan;10(1):1–10. [PubMed]
  • Pincus SE, Diamond DC, Emini EA, Wimmer E. Guanidine-selected mutants of poliovirus: mapping of point mutations to polypeptide 2C. J Virol. 1986 Feb;57(2):638–646. [PMC free article] [PubMed]
  • PRINGLE CR. EVIDENCE OF GENETIC RECOMBINATION IN FOOT-AND-MOUTH DISEASE VIRUS. Virology. 1965 Jan;25:48–54. [PubMed]
  • Rao AL, Hall TC. Requirement for a viral trans-acting factor encoded by brome mosaic virus RNA-2 provides strong selection in vivo for functional recombinants. J Virol. 1990 May;64(5):2437–2441. [PMC free article] [PubMed]
  • Rao AL, Sullivan BP, Hall TC. Use of Chenopodium hybridum facilitates isolation of brome mosaic virus RNA recombinants. J Gen Virol. 1990 Jun;71(Pt 6):1403–1407. [PubMed]
  • Romanova LI, Blinov VM, Tolskaya EA, Viktorova EG, Kolesnikova MS, Guseva EA, Agol VI. The primary structure of crossover regions of intertypic poliovirus recombinants: a model of recombination between RNA genomes. Virology. 1986 Nov;155(1):202–213. [PubMed]
  • Simon AE, Howell SH. The virulent satellite RNA of turnip crinkle virus has a major domain homologous to the 3' end of the helper virus genome. EMBO J. 1986 Dec 20;5(13):3423–3428. [PMC free article] [PubMed]
  • Snijder EJ, den Boon JA, Horzinek MC, Spaan WJ. Comparison of the genome organization of toro- and coronaviruses: evidence for two nonhomologous RNA recombination events during Berne virus evolution. Virology. 1991 Jan;180(1):448–452. [PubMed]
  • Steinhauer DA, de la Torre JC, Holland JJ. High nucleotide substitution error frequencies in clonal pools of vesicular stomatitis virus. J Virol. 1989 May;63(5):2063–2071. [PMC free article] [PubMed]
  • Steinhauer DA, de la Torre JC, Meier E, Holland JJ. Extreme heterogeneity in populations of vesicular stomatitis virus. J Virol. 1989 May;63(5):2072–2080. [PMC free article] [PubMed]
  • Steinhauer DA, Holland JJ. Direct method for quantitation of extreme polymerase error frequencies at selected single base sites in viral RNA. J Virol. 1986 Jan;57(1):219–228. [PMC free article] [PubMed]
  • Strauss JH, Strauss EG. Evolution of RNA viruses. Annu Rev Microbiol. 1988;42:657–683. [PubMed]
  • Surratt CK, Milan SC, Chamberlin MJ. Spontaneous cleavage of RNA in ternary complexes of Escherichia coli RNA polymerase and its significance for the mechanism of transcription. Proc Natl Acad Sci U S A. 1991 Sep 15;88(18):7983–7987. [PMC free article] [PubMed]
  • Sutton RE, Boothroyd JC. Evidence for trans splicing in trypanosomes. Cell. 1986 Nov 21;47(4):527–535. [PubMed]
  • Tolskaya EA, Romanova LI, Blinov VM, Viktorova EG, Sinyakov AN, Kolesnikova MS, Agol VI. Studies on the recombination between RNA genomes of poliovirus: the primary structure and nonrandom distribution of crossover regions in the genomes of intertypic poliovirus recombinants. Virology. 1987 Nov;161(1):54–61. [PubMed]
  • Tsiang M, Monroe SS, Schlesinger S. Studies of defective interfering RNAs of Sindbis virus with and without tRNAAsp sequences at their 5' termini. J Virol. 1985 Apr;54(1):38–44. [PMC free article] [PubMed]
  • van der Kuyl AC, Neeleman L, Bol JF. Complementation and recombination between alfalfa mosaic virus RNA3 mutants in tobacco plants. Virology. 1991 Aug;183(2):731–738. [PubMed]
  • Vlasak R, Luytjes W, Leider J, Spaan W, Palese P. The E3 protein of bovine coronavirus is a receptor-destroying enzyme with acetylesterase activity. J Virol. 1988 Dec;62(12):4686–4690. [PMC free article] [PubMed]
  • Weiss BG, Schlesinger S. Recombination between Sindbis virus RNAs. J Virol. 1991 Aug;65(8):4017–4025. [PMC free article] [PubMed]
  • Wilson V, Taylor P, Desselberger U. Crossover regions in foot-and-mouth disease virus (FMDV) recombinants correspond to regions of high local secondary structure. Arch Virol. 1988;102(1-2):131–139. [PubMed]
  • Yokomori K, La Monica N, Makino S, Shieh CK, Lai MM. Biosynthesis, structure, and biological activities of envelope protein gp65 of murine coronavirus. Virology. 1989 Dec;173(2):683–691. [PubMed]
  • Zhang CX, Cascone PJ, Simon AE. Recombination between satellite and genomic RNAs of turnip crinkle virus. Virology. 1991 Oct;184(2):791–794. [PubMed]

Articles from Microbiological Reviews are provided here courtesy of American Society for Microbiology (ASM)

Formats:

Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...

Links

  • MedGen
    MedGen
    Related information in MedGen
  • PubMed
    PubMed
    PubMed citations for these articles

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...