Skip to main content
Log in

A phylogenetic survey of recombination frequency in plant RNA viruses

  • Published:
Archives of Virology Aims and scope Submit manuscript

Summary.

The severe economic consequences of emerging plant viruses highlights the importance of studies of plant virus evolution. One question of particular relevance is the extent to which the genomes of plant viruses are shaped by recombination. To this end we conducted a phylogenetic survey of recombination frequency in a wide range of positive-sense RNA plant viruses, utilizing 975 capsid gene sequences and 157 complete genome sequences. In total, 12 of the 36 RNA virus species analyzed showed evidence for recombination, comprising 17% of the capsid gene sequence alignments and 44% of the genome sequence alignments. Given the conservative nature of our analysis, we propose that recombination is a relatively common process in some plant RNA viruses, most notably the potyviruses.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • R Aaziz M Tepfer (1999) ArticleTitleRecombination in RNA viruses and in virus-resistant transgenic plants J Gen Virol 80 1339–1346 Occurrence Handle1:CAS:528:DyaK1MXjs1OmtL0%3D Occurrence Handle10374949

    CAS  PubMed  Google Scholar 

  • RF Allison WL Schneider AE Greene (1996) ArticleTitleRecombination in plants expressing viral transgenes Semin Virol 7 417–422 Occurrence Handle10.1006/smvy.1996.0050 Occurrence Handle1:CAS:528:DyaK2sXisVeitbc%3D

    Article  CAS  Google Scholar 

  • Blok J, Gibbs AJ (1995) Molecular systematics of the flaviviruses and their relatives. In: Gibbs AJ, Calisher CH, Garcia-Arenal F (eds), Molecular basis of virus evolution. Cambridge University Press, Cambridge, pp 270–289

  • J Bonnet A Fraile S Sacristan JM Malpica F Garcia-Arenal (2005) ArticleTitleRole of recombination in the evolution of natural populations of Cucumber mosaic virus, a tripartite RNA plant virus Virology 332 359–368 Occurrence Handle10.1016/j.virol.2004.11.017 Occurrence Handle1:CAS:528:DC%2BD2MXmslGjtA%3D%3D Occurrence Handle15661167

    Article  CAS  PubMed  Google Scholar 

  • M Bousalem S Dallot S Fuji KT Natsuaki (2003) ArticleTitleOrigin, world-wide dispersion, bio-geographical diversification, radiation and recombination: an evolutionary history of the Yam mild mosaic virus (YMMV) Infect Genet Evol 3 189–206 Occurrence Handle10.1016/S1567-1348(03)00085-6 Occurrence Handle1:CAS:528:DC%2BD3sXns1KlsLw%3D Occurrence Handle14522183

    Article  CAS  PubMed  Google Scholar 

  • M Bousalem EJP Douzery D Fargette (2000) ArticleTitleHigh genetic diversity, distant phylogenetic relationships and intraspecies recombination events among natural populations of Yam mosaic virus: a contribution to understanding potyvirus evolution J Gen Virol 81 243–255 Occurrence Handle1:CAS:528:DC%2BD3cXjvVOjsw%3D%3D Occurrence Handle10640564

    CAS  PubMed  Google Scholar 

  • JJ Bujarski P Kaesberg (1986) ArticleTitleGenetic recombination between RNA components of a multipartite plant virus Nature 321 528–531 Occurrence Handle10.1038/321528a0 Occurrence Handle1:CAS:528:DyaL28XktlKmtrc%3D Occurrence Handle2423879

    Article  CAS  PubMed  Google Scholar 

  • ER Chare EA Gould EC Holmes (2003) ArticleTitlePhylogenetic analysis reveals a low rate of homologous recombination in negative-sense RNA viruses J Gen Virol 84 2691–2703 Occurrence Handle10.1099/vir.0.19277-0 Occurrence Handle1:CAS:528:DC%2BD3sXotF2gtLg%3D Occurrence Handle13679603

    Article  CAS  PubMed  Google Scholar 

  • S Crochu S Cook H Attoui RN Charrel RN De Chesse M Belhouchet JJ Lemasson P de Micco X de Lamballerie (2004) ArticleTitleSequences of flavivirus-related RNA viruses persist in DNA form integrated in the genome of Aedes spp. mosquitoes J Gen Virol 85 1971–1980 Occurrence Handle10.1099/vir.0.79850-0 Occurrence Handle1:CAS:528:DC%2BD2cXlvFKhtbw%3D Occurrence Handle15218182

    Article  CAS  PubMed  Google Scholar 

  • E Domingo JJ Holland (1997) ArticleTitleRNA virus mutations for fitness and survival Annu Rev Microbiol 51 151–178 Occurrence Handle10.1146/annurev.micro.51.1.151 Occurrence Handle1:CAS:528:DyaK2sXms1Shsbo%3D Occurrence Handle9343347

    Article  CAS  PubMed  Google Scholar 

  • JW Drake JJ Holland (1999) ArticleTitleMutation rates among RNA viruses Proc Natl Acad Sci USA 96 13910–13913 Occurrence Handle10.1073/pnas.96.24.13910 Occurrence Handle1:CAS:528:DyaK1MXns1Oqtb0%3D Occurrence Handle10570172

    Article  CAS  PubMed  Google Scholar 

  • SF Elena A Moya (1999) ArticleTitleRate of deleterious mutation and the distribution of its effects on fitness in Vesicular stomatitis virus J Evol Biol 12 1078–1088 Occurrence Handle10.1046/j.1420-9101.1999.00110.x

    Article  Google Scholar 

  • A Fraile JL Alonso-Prados MA Aranda JJ Bernal JM Malpica F Garcia-Arenal (1997) ArticleTitleGenetic exchange by recombination or reassortment is infrequent in natural populations of a tripartite RNA plant virus J Virol 71 934–940 Occurrence Handle1:CAS:528:DyaK2sXls1ejtA%3D%3D Occurrence Handle8995610

    CAS  PubMed  Google Scholar 

  • R Froissart D Rose M Uzest L Galibert S Blanc Y Michalakis (2005) ArticleTitleRecombination every day: Abundant recombination in a virus during a single multi-cellular host infection PloS Biol 3 e89 Occurrence Handle10.1371/journal.pbio.0030089 Occurrence Handle15737066

    Article  PubMed  Google Scholar 

  • S Gal B Pisan T Hohn N Grimsley B Hohn (1992) ArticleTitleAgroinfection of transgenic plants leads to viable Cauliflower mosaic virus by intermolecular recombination Virology 187 525–533 Occurrence Handle10.1016/0042-6822(92)90455-X Occurrence Handle1:CAS:528:DyaK38XhvVyrsLY%3D Occurrence Handle1546451

    Article  CAS  PubMed  Google Scholar 

  • Gibbs M (1995) The luteovirus supergroup: rampant recombination and persistent partnerships. In: Gibbs AJ, Calisher CH, Garcia-Arenal F (eds), Molecular basis of virus evolution. Cambridge University Press, Cambridge, pp 351–368

  • AE Greene RF Allison (1994) ArticleTitleRecombination between viral RNA and transgenic plant transcripts Science 263 1423–1425 Occurrence Handle1:CAS:528:DyaK2cXjtFOju7c%3D Occurrence Handle8128222

    CAS  PubMed  Google Scholar 

  • AE Greene RF Allison (1996) ArticleTitleDeletions in the 3′ untranslated region of Cowpea chlorotic mottle virus transgene reduce recovery of recombinant viruses in transgenic plants Virology 225 231–234 Occurrence Handle1:CAS:528:DyaK28XmvFGjsb4%3D Occurrence Handle8918552

    CAS  PubMed  Google Scholar 

  • T Hayakawa Y Zhu K Itoh Y Kimura T Izawa K Shimamoto S Toriyama (1992) ArticleTitleGenetically engineered rice resistant to Rice stripe virus, an insect-transmitted virus Proc Natl Acad Sci USA 89 9865–9869 Occurrence Handle1:CAS:528:DyaK3sXjvFOr Occurrence Handle1409714

    CAS  PubMed  Google Scholar 

  • WS Hu HM Temin (1990) ArticleTitleRetroviral recombination and reverse transcription Science 250 1227–1233 Occurrence Handle1:CAS:528:DyaK3MXjs1OrsA%3D%3D Occurrence Handle1700865

    CAS  PubMed  Google Scholar 

  • A Jung R Maier JP Vartanian G Bocharov V Jung U Fischer E Meese S Wain-Hobson A Meyerhans (2002) ArticleTitleMultiply infected spleen cells in HIV patients Nature 418 144 Occurrence Handle10.1038/418144a Occurrence Handle1:CAS:528:DC%2BD38XltFGmu7w%3D Occurrence Handle12110879

    Article  CAS  PubMed  Google Scholar 

  • MMC Lai (1992) ArticleTitleRNA recombination in animal and plant viruses Microbiol Rev 56 61–79 Occurrence Handle1:CAS:528:DyaK38XitlWgt7Y%3D Occurrence Handle1579113

    CAS  PubMed  Google Scholar 

  • S Lain JL Riechmann MT Martin JA Garcia (1989) ArticleTitleHomologous potyvirus and flavivirus proteins belonging to a superfamily of helicase-like proteins Gene 82 357–362 Occurrence Handle1:CAS:528:DyaK3cXjtlSlsw%3D%3D Occurrence Handle2555266

    CAS  PubMed  Google Scholar 

  • OL Le Gall M Lanneau T Candresse J Dunez (1995) ArticleTitleThe nucleotide sequence of the RNA-2 of an isolate of the English serotype of Tomato black ring virus: RNA recombination in the history of nepoviruses J Gen Virol 76 1279–1283 Occurrence Handle1:CAS:528:DyaK2MXltlWgs7Y%3D Occurrence Handle7730814

    CAS  PubMed  Google Scholar 

  • HX Lin L Rubio A Smythe M Jiminez BW Falk (2003) ArticleTitleGenetic diversity and biological variation among California isolates of Cucumber mosaic virus J Gen Virol 84 249–258 Occurrence Handle10.1099/vir.0.18673-0 Occurrence Handle1:CAS:528:DC%2BD3sXksl2gsg%3D%3D Occurrence Handle12533721

    Article  CAS  PubMed  Google Scholar 

  • S MacFarlane (1997) ArticleTitleNatural recombination among plant virus genomes: evidence from tobraviruses Semin Virol 8 25–31 Occurrence Handle10.1006/smvy.1997.0103 Occurrence Handle1:CAS:528:DyaK1cXhtVGhtro%3D

    Article  CAS  Google Scholar 

  • IM Moreno JM Malpica JA Diaz-Pendon E Moriones A Fraile F Garcia-Arenal (2004) ArticleTitleVariability and genetic structure of the population of Watermelon mosaic virus infecting melon in Spain Virology 318 451–460 Occurrence Handle10.1016/j.virol.2003.10.002 Occurrence Handle1:CAS:528:DC%2BD2cXht1Kgtr0%3D Occurrence Handle14972570

    Article  CAS  PubMed  Google Scholar 

  • PD Nagy JJ Bujarski (1997) ArticleTitleEngineering of homologous recombination hotspots with AU-rich sequences in Brome mosaic virus J Virol 71 3799–3810 Occurrence Handle1:CAS:528:DyaK2sXisFWiurk%3D Occurrence Handle9094655

    CAS  PubMed  Google Scholar 

  • K Ohshima Y Yamaguchi R Hirota T Hamamoto K Tomimura Z Tan T Sano F Azuhata JA Walsh J Fletcher J Chen A Gera A Gibbs (2002) ArticleTitleMolecular evolution of Turnip mosaic virus: evidence of host adaptation, genetic recombination and geographical spread J Gen Virol 83 1511–1521 Occurrence Handle1:CAS:528:DC%2BD38XktlGitb0%3D Occurrence Handle12029167

    CAS  PubMed  Google Scholar 

  • M Padidam S Sawyer CM Fauquet (1999) ArticleTitlePossible emergence of new geminiviruses by frequent recombination Virology 265 218–255 Occurrence Handle10.1006/viro.1999.0056 Occurrence Handle1:CAS:528:DyaK1MXnvFertbs%3D Occurrence Handle10600594

    Article  CAS  PubMed  Google Scholar 

  • D Posada KA Crandall EC Holmes (2002) ArticleTitleRecombination in evolutionary genomics Annu Rev Genet 36 75–97 Occurrence Handle10.1146/annurev.genet.36.040202.111115 Occurrence Handle1:CAS:528:DC%2BD3sXjsleluw%3D%3D Occurrence Handle12429687

    Article  CAS  PubMed  Google Scholar 

  • A Poutaraud C Desbiez O Lemaire H Lecoq E Herrbach (2004) ArticleTitleCharacterisation of a new potyvirus species infecting meadow saffron (Colchicum autumnale) Arch Virol 149 1267–1277 Occurrence Handle10.1007/s00705-004-0307-x Occurrence Handle1:CAS:528:DC%2BD2cXltVKmsLo%3D Occurrence Handle15221530

    Article  CAS  PubMed  Google Scholar 

  • MJ Roossinck (1997) ArticleTitleMechanisms of plant virus evolution Annu Rev Phytopathol 35 191–209 Occurrence Handle10.1146/annurev.phyto.35.1.191 Occurrence Handle1:CAS:528:DyaK2sXmtVGhsro%3D Occurrence Handle15012521

    Article  CAS  PubMed  Google Scholar 

  • L Rubio MA Ayllon P Kong A Fernandez M Polek J Guerri P Moreno BW Falk (2001) ArticleTitleGenetic variation of Citrus tristeza virus isolates from California and Spain: Evidence for mixed infections and recombination J Virol 75 8054–8062 Occurrence Handle1:CAS:528:DC%2BD3MXmtFejtb4%3D Occurrence Handle11483750

    CAS  PubMed  Google Scholar 

  • S Sawyer (1989) ArticleTitleStatistical tests for detecting gene conversion Mol Biol Evol 6 526–538 Occurrence Handle1:CAS:528:DyaL1MXlvFWhtb4%3D Occurrence Handle2677599

    CAS  PubMed  Google Scholar 

  • JE Schoelz WM Wintermantel (1993) ArticleTitleExpansion of viral host range through comple- mentation and recombination in transgenic plants Plant Cell 5 1669–1679 Occurrence Handle10.1105/tpc.5.11.1669 Occurrence Handle1:CAS:528:DyaK2cXisVSgt74%3D Occurrence Handle12271051

    Article  CAS  PubMed  Google Scholar 

  • K Scholthof HB Scholthof AO Jackson (1993) ArticleTitleControl of plant virus diseases by pathogen-derived resistance in transgenic plants Plant Physiol 102 7–12 Occurrence Handle1:CAS:528:DyaK3sXkvFWit7s%3D Occurrence Handle12231793

    CAS  PubMed  Google Scholar 

  • N Shapka PD Nagy (2004) ArticleTitleThe AU-rich RNA recombination hot spot sequence of Brome mosaic virus is functional in tombusviruses: Implications for the mechanism of RNA recombination J Virol 78 2288–2300 Occurrence Handle10.1128/JVI.78.5.2288-2300.2004 Occurrence Handle1:CAS:528:DC%2BD2cXhs1Sltrg%3D Occurrence Handle14963125

    Article  CAS  PubMed  Google Scholar 

  • Shukla DD, Ward WW, Brunt AA (1994) The potyviridae. CAB International, Wallingford

  • K Strimmer A von Haesler (1996) ArticleTitleQuartet puzzling: a quartet maximum likelihood method for reconstructing tree topologies Mol Biol Evol 13 964–969 Occurrence Handle1:CAS:528:DyaK28XltlSmsLk%3D

    CAS  Google Scholar 

  • M Suzuki T Hibi C Masuta (2003) ArticleTitleRNA recombination between cucumoviruses: possible role of predicted stem-loop structures and an internal subgenomic promoter-like motif Virology 306 77–86 Occurrence Handle10.1016/S0042-6822(02)00050-8 Occurrence Handle1:CAS:528:DC%2BD3sXhs1Knt7o%3D Occurrence Handle12620800

    Article  CAS  PubMed  Google Scholar 

  • Swofford DL (2002) PAUP*: Phylogenetics analysis using parsimony (*and other methods). Version 4 Sinauer Associates, Sunderland, Mass

  • Z Tan Y Wada J Chen K Ohshima (2004) ArticleTitleInter- and intralineage recombinants are common in natural populations of Turnip mosaic virus J Gen Virol 85 2683–2696 Occurrence Handle1:CAS:528:DC%2BD2cXnsVegs7c%3D Occurrence Handle15302962

    CAS  PubMed  Google Scholar 

  • JD Thompson TJ Gibson F Plewniak F Jeanmougin DG Higgins (1997) ArticleTitleThe CLUSTAL_X windows interface: flexible strategies for multiple sequence alignments aided by quality analysis tools Nucleic Acids Res 25 4876–4882 Occurrence Handle10.1093/nar/25.24.4876 Occurrence Handle1:CAS:528:DyaK1cXntFyntQ%3D%3D Occurrence Handle9396791

    Article  CAS  PubMed  Google Scholar 

  • MC Vives L Rubio A Sambade TE Mirkov P Moreno J Guerri (2005) ArticleTitleEvidence of multiple recombination events between two RNA sequence variants within a Citrus tristeza virus isolate Virology 331 232–237 Occurrence Handle10.1016/j.virol.2004.10.037 Occurrence Handle1:CAS:528:DC%2BD2MXjvF2r Occurrence Handle15629767

    Article  CAS  PubMed  Google Scholar 

  • KA White TJ Morris (1999) ArticleTitleDefective and defective interfering RNAs of monopartite plus-strand RNA plant viruses Curr Top Microbiol Immunol 239 1–17 Occurrence Handle1:CAS:528:DyaK1MXls1akug%3D%3D Occurrence Handle9893366

    CAS  PubMed  Google Scholar 

  • WM Wintermantel JE Schoelz (1996) ArticleTitleIsolation of recombinant virus between Cauliflower mosaic virus and a viral gene in transgenic plants under conditions of moderate selection pressure Virology 223 156–164 Occurrence Handle10.1006/viro.1996.0464 Occurrence Handle1:CAS:528:DyaK28XlsVemtrc%3D Occurrence Handle8806549

    Article  CAS  PubMed  Google Scholar 

  • M Worobey EC Holmes (1999) ArticleTitleEvolutionary aspects of recombination in RNA viruses J Gen Virol 80 2535–2543 Occurrence Handle1:CAS:528:DyaK1MXmsVygsLg%3D Occurrence Handle10573145

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chare, E., Holmes, E. A phylogenetic survey of recombination frequency in plant RNA viruses. Arch Virol 151, 933–946 (2006). https://doi.org/10.1007/s00705-005-0675-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00705-005-0675-x

Keywords

Navigation