Recombination in Plant RNA Viruses

  • Peter D. Nagy

Owing to increased global travel of humans carrying plants and viral vectors, introduction of new agricultural practices in combination with climate changes, the emergence of new viruses and novel viral variants is a major, continuing threat to human health and welfare. RNA recombination is one of the major forces in increasing plant virus variability and adaptation to new hosts, often leading to emergence of new variants and resistance-breaking virus strains. RNA recombination can also increase the fitness of plant RNA viruses by repairing defective viral genomes or efficiently removing deleterious mutations that result from error-prone replication. The frequency of RNA recombination is affected by several factors, including the viral replication proteins and various features of the viral RNA templates involved. Host genes also affect viral RNA recombination, suggesting complex interaction between a given virus and its host during viral adaptation and evolution. This chapter summarizes our current knowledge on this evolutionarily important process and its roles in emergence of new viruses or viral variants with altered pathogenecity.


Cucumber Mosaic Virus Tomato Bushy Stunt Virus Brome Mosaic Virus Viral Replicase Defective Interfere 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Aaziz R, Tepfer M (1999) Recombination in RNA viruses and in virus-resistant transgenic plants. J Gen Virol 80(6):1339–1346PubMedGoogle Scholar
  2. Adair TL, Kearney CM (2000) Recombination between a 3-kilobase tobacco mosaic virus transgene and a homologous viral construct in the restoration of viral and nonviral genes. Arch Virol 145(9):1867–1883PubMedCrossRefGoogle Scholar
  3. Alejska M, Kurzyniska-Kokorniak A, Broda M, Kierzek R, Figlerowicz M (2001) How RNA viruses exchange their genetic material. Acta Biochim Pol 48(2):391–407PubMedGoogle Scholar
  4. Aranda MA, Fraile A, Dopazo J, Malpica JM, Garcia-Arenal F (1997) Contribution of mutation and RNA recombination to the evolution of a plant pathogenic RNA. J Mol Evol 44(1):81–88PubMedCrossRefGoogle Scholar
  5. Ayllon MA, Lopez C, Navas-Castillo J, Mawassi M, Dawson WO, Guerri J, Flores R, Moreno P (1999) New defective RNAs from citrus tristeza virus: evidence for a replicase-driven template switching mechanism in their generation. J Gen Virol 80(3):817–821PubMedGoogle Scholar
  6. Barajas D, Tenllado F, Diaz-Ruiz JR (2006) Characterization of the recombinant forms arising from a Potato virus X chimeric virus infection under RNA silencing pressure. Mol Plant Microbe Interact 19(8):904–913PubMedCrossRefGoogle Scholar
  7. Bonnet J, Fraile A, Sacristan S, Malpica JM, Garcia-Arenal F (2005) Role of recombination in the evolution of natural populations of Cucumber mosaic virus, a tripartite RNA plant virus. Virology 332(1):359–368PubMedCrossRefGoogle Scholar
  8. Borja M, Rubio T, Scholthof HB, Jackson AO (1999) Restoration of wild-type virus by double recombination of tombusvirus mutants with a host transgene. Mol Plant Microbe Interact 12(2):153–162PubMedCrossRefGoogle Scholar
  9. Bousalem M, Douzery EJ, Fargette D (2000) High 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(1):243–255PubMedGoogle Scholar
  10. Bujarski JJ, Kaesberg P (1986) Genetic recombination between RNA components of a multipartite plant virus. Nature 321(6069):528–531PubMedCrossRefGoogle Scholar
  11. Bujarski JJ, Nagy PD (1994) Targeting of the site of nonhomologous genetic recombination in brome mosaic virus. Arch Virol Suppl 9:231–238PubMedGoogle Scholar
  12. Bujarski JJ, Nagy PD, Flasinski S (1994) Molecular studies of genetic RNA-RNA recombination in brome mosaic virus. Adv Virus Res 43:275–302PubMedCrossRefGoogle Scholar
  13. Canto T, Choi SK, Palukaitis P (2001) A subpopulation of RNA 1 of Cucumber mosaic virus contains 3′ termini originating from RNAs 2 or 3. J Gen Virol 82(4):941–945PubMedGoogle Scholar
  14. Carpenter CD, Simon AE (1996) In vivo restoration of biologically active 3′ ends of virus-associated RNAs by nonhomologous RNA recombination and replacement of a terminal motif. J Virol 70(1);478–486PubMedGoogle Scholar
  15. Carpenter CD, Oh JW, Zhang C, Simon AE (1995) Involvement of a stem-loop structure in the location of junction sites in viral RNA recombination. J Mol Biol 245(5):608–622PubMedCrossRefGoogle Scholar
  16. Cascone PJ, Haydar TF, Simon AE (1993) Sequences and structures required for recombination between virus-associated RNAs. Science 260(5109):801–805PubMedCrossRefGoogle Scholar
  17. Chandrika R, Rabindran S, Lewandowski DJ, Manjunath KL, Dawson WO (2000) Full-length tobacco mosaic virus RNAs and defective RNAs have different 3′ replication signals. Virology 273(1):198–209PubMedCrossRefGoogle Scholar
  18. Chare ER, Holmes EC (2006) A phylogenetic survey of recombination frequency in plant RNA viruses. Arch Virol 151(5):933–946PubMedCrossRefGoogle Scholar
  19. Chen YK, Goldbach R, Prins M (2002). Inter- and intramolecular recombinations in the cucumber mosaic virus genome related to adaptation to alstroemeria. J Virol 76(8):4119–4124PubMedCrossRefGoogle Scholar
  20. Cheng CP, Nagy PD (2003) Mechanism of RNA recombination in carmo- and tombusviruses: evidence for template switching by the RNA-dependent RNA polymerase in vitro. J Virol 77(22):12033–12047PubMedCrossRefGoogle Scholar
  21. Cheng CP, Pogany J, Nagy PD (2002) Mechanism of DI RNA formation in tombusviruses: dissecting the requirement for primer extension by the tombusvirus RNA dependent RNA polymerase in vitro. Virology 304(2):460–473PubMedCrossRefGoogle Scholar
  22. Cheng CP, Panavas T, Luo G, Nagy PD (2005) Heterologous RNA replication enhancer stimulates in vitro RNA synthesis and template-switching by the carmovirus, but not by the tombusvirus, RNA-dependent RNA polymerase: implication for modular evolution of RNA viruses. Virology 341(1):107–121PubMedCrossRefGoogle Scholar
  23. Cheng CP, Serviene E, Nagy PD (2006) Suppression of viral RNA recombination by a host exoribonuclease. J Virol 80(6):2631–2640PubMedCrossRefGoogle Scholar
  24. Chetverin AB, Chetverina HV, Demidenko AA, Ugarov VI (1997) Nonhomologous RNA recombination in a cell-free system: evidence for a transesterification mechanism guided by secondary structure. Cell 88(4):503–513PubMedCrossRefGoogle Scholar
  25. Desbiez C, Lecoq H (2004) The nucleotide sequence of Watermelon mosaic virus (WMV, Potyvirus) reveals interspecific recombination between two related potyviruses in the 5′ part of the genome. Arch Virol 149(8):1619–1632PubMedCrossRefGoogle Scholar
  26. DeStefano JJ, Bambara RA, Fay PJ (1994) The mechanism of human immunodeficiency virus reverse transcriptase-catalyzed strand transfer from internal regions of heteropolymeric RNA templates. J Biol Chem 269(1):161–168PubMedGoogle Scholar
  27. Desvoyes B, Scholthof HB (2002) Host-dependent recombination of a Tomato bushy stunt virus coat protein mutant yields truncated capsid subunits that form virus-like complexes which benefit systemic spread. Virology 304(2):434–442PubMedCrossRefGoogle Scholar
  28. Eliasco E, Livieratos IC, Muller G, Guzman M, Salazar LF, Coutts RH (2006) Sequences of defective RNAs associated with potato yellow vein virus. Arch Virol 151(1):201–204PubMedCrossRefGoogle Scholar
  29. Escriu F, Fraile A, Garcia-Arenal F (2003) The evolution of virulence in a plant virus. Evol Int J Org Evol 57(4):755–765Google Scholar
  30. Falk BW, Bruening G (1994). Will transgenic crops generate new viruses and new diseases? Science 263(5152):1395–1396PubMedCrossRefGoogle Scholar
  31. Fernandez-Cuartero B, Burgyan J, Aranda MA, Salanki K, Moriones E, Garcia-Arenal F (1994) Increase in the relative fitness of a plant virus RNA associated with its recombinant nature. Virology 203(2):373–377PubMedCrossRefGoogle Scholar
  32. Figlerowicz M, Nagy PD, Bujarski JJ (1997) A mutation in the putative RNA polymerase gene inhibits nonhomologous, but not homologous, genetic recombination in an RNA virus. Proc Natl Acad Sci USA 94(5):2073–2078PubMedCrossRefGoogle Scholar
  33. Figlerowicz M, Nagy PD, Tang N, Kao CC, Bujarski JJ (1998) Mutations in the N terminus of the brome mosaic virus polymerase affect genetic RNA-RNA recombination. J Virol 72(11):9192–9200PubMedGoogle Scholar
  34. Flint SJ, Enquist LW, Racaniello VR, Skalka AM (2004) Principles of virology. American Society for Microbiology, WashingtonGoogle Scholar
  35. Froissart R, Roze D, Uzest M, Galibert L, Blanc S, Michalakis Y (2005) Recombination every day: abundant recombination in a virus during a single multi-cellular host infection. PLoS Biol 3(3):e89PubMedCrossRefGoogle Scholar
  36. Garcia-Arenal F, Fraile A, Malpica JM (2003) Variation and evolution of plant virus populations. Int Microbiol 6(4):225–232PubMedCrossRefGoogle Scholar
  37. Garcia-Ruiz H, Ahlquist P (2006) Inducible yeast system for Viral RNA recombination reveals requirement for an RNA replication signal on both parental RNAs. J Virol 80(17):8316–8328PubMedCrossRefGoogle Scholar
  38. Ge X, Scott SW, Zimmerman MT (1997) The complete sequence of the genomic RNAs of spinach latent virus. Arch Virol 142(6):1213–1226PubMedCrossRefGoogle Scholar
  39. Glasa M, Candresse T (2005) Partial sequence analysis of an atypical Turkish isolate provides further information on the evolutionary history of Plum pox virus (PPV). Virus Res 108(1–2):199–206PubMedCrossRefGoogle Scholar
  40. Greene AE, Allison RF (1994) Recombination between viral RNA and transgenic plant transcripts. Science 263(5152):1423–1425PubMedCrossRefGoogle Scholar
  41. Guan H, Simon AE (2000) Polymerization of nontemplate bases before transcription initiation at the 3′ ends of templates by an RNA-dependent RNA polymerase: an activity involved in 3′ end repair of viral RNAs. Proc Natl Acad Sci USA 97(23):12451–12456PubMedCrossRefGoogle Scholar
  42. Guo LH, Cao YH, Li DW, Niu SN, Cai ZN, Han CG, Zhai YF, Yu JL (2005) Analysis of nucleotide sequences and multimeric forms of a novel satellite RNA associated with beet black scorch virus. J Virol 79(6):3664–3674PubMedCrossRefGoogle Scholar
  43. Guyader S, Ducray DG (2002) Sequence analysis of Potato leafroll virus isolates reveals genetic stability, major evolutionary events and differential selection pressure between overlapping reading frame products. J Gen Virol 83(7):1799–1807PubMedGoogle Scholar
  44. Hauser S, Stevens M, Beuve M, Lemaire O (2002) Biological properties and molecular characterization of beet chlorosis virus (BChV). Arch Virol 147(4):745–762PubMedCrossRefGoogle Scholar
  45. Havelda Z, Dalmay T, Burgyan J (1997) Secondary structure-dependent evolution of Cymbidium ringspot virus defective interfering RNA. J Gen Virol 78(6):1227–1234PubMedGoogle Scholar
  46. Hema M, Gopinath K, Kao C (2005) Repair of the tRNA-like CCA sequence in a multipartite positive-strand RNA virus. J Virol 79(3):1417–1427PubMedCrossRefGoogle Scholar
  47. Hernandez C, Carette JE, Brown DJ, Bol JF (1996) Serial passage of tobacco rattle virus under different selection conditions results in deletion of structural and nonstructural genes in RNA 2. J Virol 70(8):4933–4940PubMedGoogle Scholar
  48. Hillman BI, Carrington JC, Morris J (1987) A defective interfering RNA that contains a mosaic of a plant virus genome. Cell 51(3):427–433PubMedCrossRefGoogle Scholar
  49. Keese P, Gibbs A (1993) Plant viruses: master explorers of evolutionary space. Curr Opin Genet Dev 3(6):873–877PubMedCrossRefGoogle Scholar
  50. Kim MJ, Kao C (2001) Factors regulating template switch in vitro by viral RNA-dependent RNA polymerases: implications for RNA-RNA recombination. Proc Natl Acad Sci USA 98(9):4972–4977PubMedCrossRefGoogle Scholar
  51. Lai MM (1992) RNA recombination in animal and plant viruses. Microbiol Rev 56(1):61–79PubMedGoogle Scholar
  52. Lartey RT, Voss TC, Melcher U (1996) Tobamovirus evolution: gene overlaps, recombination, and taxonomic implications. Mol Biol Evol 13(10):1327–1338PubMedGoogle Scholar
  53. Le Gall O, Candresse T, Dunez J (1995a) Transfer of the 3′ non-translated region of grapevine chrome mosaic virus RNA-1 by recombination to tomato black ring virus RNA-2 in pseudorecombinant isolates. J Gen Virol 76(5):1285–1289PubMedCrossRefGoogle Scholar
  54. Le Gall OL, Lanneau M, Candresse T, Dunez J (1995b) The 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(5):1279–1283PubMedCrossRefGoogle Scholar
  55. Li XH, Heaton LA, Morris TJ, Simon AE (1989) Turnip crinkle virus defective interfering RNAs intensify viral symptoms and are generated de novo. Proc Natl Acad Sci USA 86(23):9173–9177PubMedCrossRefGoogle Scholar
  56. Lorenzen JH, Meacham T, Berger PH, Shiel PJ, Crosslin JM, Hamm PB, Kopp H (2006) Whole genome characterization of Potato virus Y isolates collected in the western USA and their comparison to isolates from Europe and Canada. Arch Virol 151(6):1055–1074PubMedCrossRefGoogle Scholar
  57. 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. Proc Natl Acad Sci USA 95(18):10487–10492PubMedCrossRefGoogle Scholar
  58. Miller WA, Dinesh-Kumar SP, Paul CP (1995) Luteovirus gene expression. Crit Rev Plant Sci 14:179–211CrossRefGoogle Scholar
  59. Monkewich S, Lin HX, Fabian MR, Xu W, Na H, Ray D, Chernysheva OA, Nagy PD, White KA (2005) The p92 polymerase coding region contains an internal RNA element required at an early step in Tombusvirus genome replication. J Virol 79(8):4848–4858PubMedCrossRefGoogle Scholar
  60. Moreno IM, Malpica JM, Diaz-Pendon JA, Moriones E, Fraile A, Garcia-Arenal F (2004) Variability and genetic structure of the population of watermelon mosaic virus infecting melon in Spain. Virology 318(1):451–460PubMedCrossRefGoogle Scholar
  61. Nagy PD, Bujarski JJ (1992) Genetic recombination in brome mosaic virus: effect of sequence and replication of RNA on accumulation of recombinants. J Virol 66(11):6824–6828PubMedGoogle Scholar
  62. Nagy PD, Bujarski JJ (1993) Targeting the site of RNA-RNA recombination in brome mosaic virus with antisense sequences. Proc Natl Acad Sci USA 90(14):6390–6394PubMedCrossRefGoogle Scholar
  63. Nagy PD, Bujarski JJ (1995) Efficient system of homologous RNA recombination in brome mosaic virus: sequence and structure requirements and accuracy of crossovers. J Virol 69(1):131–140PubMedGoogle Scholar
  64. Nagy PD, Bujarski JJ (1996) Homologous RNA recombination in brome mosaic virus: AU-rich sequences decrease the accuracy of crossovers. J Virol 70(1):415–426PubMedGoogle Scholar
  65. Nagy PD, Bujarski JJ (1997) Engineering of homologous recombination hotspots with AU-rich sequences in brome mosaic virus. J Virol 71(5):3799–3810PubMedGoogle Scholar
  66. Nagy PD, Bujarski JJ (1998) Silencing homologous RNA recombination hot spots with GC-rich sequences in brome mosaic virus. J Virol 72(2):1122–1130PubMedGoogle Scholar
  67. Nagy PD, Pogany J (2006) Yeast as a model host to dissect functions of viral and host factors in tombusvirus replication. Virology 344(1):211–220PubMedCrossRefGoogle Scholar
  68. Nagy PD, Simon AE (1997) New insights into the mechanisms of RNA recombination. Virology 235(1):1–9PubMedCrossRefGoogle Scholar
  69. Nagy PD, Simon AE (1998a) In vitro characterization of late steps of RNA recombination in turnip crinkle virus. I. Role of motif1-hairpin structure. Virology 249(2):379–392PubMedCrossRefGoogle Scholar
  70. Nagy PD, Simon AE (1998b) In vitro characterization of late steps of RNA recombination in turnip crinkle virus. II. The role of the priming stem and flanking sequences. Virology 249(2):393–405PubMedCrossRefGoogle Scholar
  71. Nagy PD, Dzianott A, Ahlquist P, Bujarski JJ (1995) Mutations in the helicase-like domain of protein 1a alter the sites of RNA-RNA recombination in brome mosaic virus. J Virol 69(4):2547–2556PubMedGoogle Scholar
  72. Nagy PD, Carpenter CD, Simon AE (1997) A novel 3′-end repair mechanism in an RNA virus. Proc Natl Acad Sci USA 94(4):1113–1118PubMedCrossRefGoogle Scholar
  73. Nagy PD, Zhang C, Simon AE (1998) Dissecting RNA recombination in vitro: role of RNA sequences and the viral replicase. EMBO J 17(8):2392–2403PubMedCrossRefGoogle Scholar
  74. Nagy PD, Ogiela C, Bujarski JJ (1999a) Mapping sequences active in homologous RNA recombination in brome mosaic virus: prediction of recombination hot spots. Virology 254(1):92–104PubMedCrossRefGoogle Scholar
  75. Nagy PD, Pogany J, Simon AE (1999b) RNA elements required for RNA recombination function as replication enhancers in vitro and in vivo in a plus-strand RNA virus. EMBO J 18(20):5653–5665PubMedCrossRefGoogle Scholar
  76. Ohshima K, Yamaguchi Y, Hirota R, Hamamoto T, Tomimura K, Tan Z, Sano T, Azuhata F, Walsh JA, Fletcher J, Chen J, Gera A, Gibbs A (2002) Molecular evolution of Turnip mosaic virus: evidence of host adaptation, genetic recombination and geographical spread. J Gen Virol 83(6):1511–1521PubMedGoogle Scholar
  77. Panavas T, Nagy PD (2003) Yeast as a model host to study replication and recombination of defective interfering RNA of Tomato bushy stunt virus. Virology 314(1):315–325PubMedCrossRefGoogle Scholar
  78. Panavas T, Nagy PD (2005) Mechanism of stimulation of plus-strand synthesis by an RNA replication enhancer in a tombusvirus. J Virol 79(15):9777–9785PubMedCrossRefGoogle Scholar
  79. Panavas T, Pogany J, Nagy PD (2002) Internal initiation by the cucumber necrosis virus RNA-dependent RNA polymerase is facilitated by promoter-like sequences. Virology 296(2):275–287PubMedCrossRefGoogle Scholar
  80. Panavas T, Panaviene Z, Pogany J, Nagy PD (2003) Enhancement of RNA synthesis by promoter duplication in tombusviruses. Virology 310(1):118–129PubMedCrossRefGoogle Scholar
  81. Panaviene Z, Nagy PD (2003) Mutations in the RNA-binding domains of tombusvirus replicase proteins affect RNA recombination in vivo. Virology 317(2):359–372PubMedCrossRefGoogle Scholar
  82. Pogany J, Romero J, Huang Q, Sgro JY, Shang H, Bujarski JJ (1995) De novo generation of defective interfering-like RNAs in broad bean mottle bromovirus. Virology 212(2):574–586PubMedCrossRefGoogle Scholar
  83. Pogany J, White KA, Nagy PD (2005) Specific binding of tombusvirus replication protein p33 to an internal replication element in the viral RNA is essential for replication. J Virol 79(8):4859–4869PubMedCrossRefGoogle Scholar
  84. Rabindran S, Dawson WO (2001) Assessment of recombinants that arise from the use of a TMV-based transient expression vector. Virology 284(2):182–189PubMedCrossRefGoogle Scholar
  85. Rao AL, Grantham GL (1994) Amplification in vivo of brome mosaic virus RNAs bearing 3′ noncoding region from cucumber mosaic virus. Virology 204(1):478–481PubMedCrossRefGoogle Scholar
  86. Rao AL, Hall TC (1993) Recombination and polymerase error facilitate restoration of infectivity in brome mosaic virus. J Virol 67(2):969–979PubMedGoogle Scholar
  87. Revers F, Le Gall O, Candresse T, Le Romancer M, Dunez J (1996) Frequent occurrence of recombinant potyvirus isolates. J Gen Virol 77(8):1953–1965PubMedCrossRefGoogle Scholar
  88. Robinson DJ (1994) Sequences at the ends of RNA-2 of I6, a recombinant tobravirus Arch Virol Suppl 9:245–51PubMedGoogle Scholar
  89. Rochon DM (1991) Rapid de novo generation of defective interfering RNA by cucumber necrosis virus mutants that do not express the 20-kDa nonstructural protein. Proc Natl Acad Sci USA 88(24):11153–11157PubMedCrossRefGoogle Scholar
  90. Roossinck MJ (1997) Mechanisms of plant virus evolution. Annu Rev Phytopathol 35:191–209PubMedCrossRefGoogle Scholar
  91. Roossinck MJ (2003) Plant RNA virus evolution. Curr Opin Microbiol 6(4):406–409PubMedCrossRefGoogle Scholar
  92. Rubino L, Burgyan J, Grieco F, Russo M (1990) Sequence analysis of cymbidium ringspot virus satellite and defective interfering RNAs. J Gen Virol 71(8):1655–1660PubMedCrossRefGoogle Scholar
  93. Rubio L, Ayllon MA, Kong P, Fernandez A, Polek M, Guerri J, Moreno P, Falk BW (2001) Genetic variation of Citrus tristeza virus isolates from California and Spain: evidence for mixed infections and recombination. J Virol 75(17):8054–8062PubMedCrossRefGoogle Scholar
  94. Schwartz M, Chen J, Janda M, Sullivan M, den Boon J, Ahlquist P (2002) A positive-strand RNA virus replication complex parallels form and function of retrovirus capsids. Mol Cell 9(3):505–514PubMedCrossRefGoogle Scholar
  95. Serva S, Nagy PD (2006) Proteomics analysis of the tombusvirus replicase: Hsp70 molecular chaperone is associated with the replicase and enhances viral RNA replication. J Virol 80(5):2162–2169PubMedCrossRefGoogle Scholar
  96. Serviene E, Shapka N, Cheng CP, Panavas T, Phuangrat B, Baker J, Nagy PD (2005) Genome-wide screen identifies host genes affecting viral RNA recombination. Proc Natl Acad Sci USA 102(30):10545–10550PubMedCrossRefGoogle Scholar
  97. Serviene E, Jiang Y, Cheng CP, Baker J, Nagy PD (2006) Screening of the yeast yTHC collection identifies essential host factors affecting tombusvirus RNA recombination. J Virol 80(3):1231–1241PubMedCrossRefGoogle Scholar
  98. Shapka N, Nagy PD (2004) The 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(5):2288–2300PubMedCrossRefGoogle Scholar
  99. Simon AE (1999) Replication, recombination, and symptom-modulation properties of the satellite RNAs of turnip crinkle virus. Curr Top Microbiol Immunol 239:19–36PubMedGoogle Scholar
  100. Simon AE, Roossinck MJ, Havelda Z (2004) Plant virus satellite and defective interfering RNAs: new paradigms for a new century. Annu Rev Phytopathol 42:415–437PubMedCrossRefGoogle Scholar
  101. Suzuki M, Hibi T, Masuta C (2003) RNA recombination between cucumoviruses: possible role of predicted stem-loop structures and an internal subgenomic promoter-like motif. Virology 306(1):77–86PubMedCrossRefGoogle Scholar
  102. Swanson MM, MacFarlane SA (1999) The E116 isolate of Dutch pea early-browning virus is a recombinant virus. Virus Res 60(1):87–94PubMedCrossRefGoogle Scholar
  103. Tan Z, Wada Y, Chen J, Ohshima K (2004) Inter- and intralineage recombinants are common in natural populations of Turnip mosaic virus. J Gen Virol 85(9):2683–2696PubMedCrossRefGoogle Scholar
  104. Teycheney PY, Marais A, Svanella-Dumas L, Dulucq MJ, Candresse T (2005) Molecular characterization of banana virus X (BVX), a novel member of the Flexiviridae family. Arch Virol 150(9):1715–1727PubMedCrossRefGoogle Scholar
  105. Urbanowicz A, Alejska M, Formanowicz P, Blazewicz J, Figlerowicz M, Bujarski JJ (2005) Homologous crossovers among molecules of brome mosaic bromovirus RNA1 or RNA2 segments in vivo. J Virol 79(9):5732–5742PubMedCrossRefGoogle Scholar
  106. Vigne E, Bergdoll M, Guyader S, Fuchs M (2004) Population structure and genetic variability within isolates of Grapevine fanleaf virus from a naturally infected vineyard in France: evidence for mixed infection and recombination. J Gen Virol 85(8):2435–2445PubMedCrossRefGoogle Scholar
  107. Vigne E, Demangeat G, Komar V, Fuchs M (2005) Characterization of a naturally occurring recombinant isolate of Grapevine fanleaf virus. Arch Virol 150(11):2241–2255PubMedCrossRefGoogle Scholar
  108. Vives MC, Rubio L, Lopez C, Navas-Castillo J, Albiach-Marti MR, Dawson WO, Guerri J, Flores R, Moreno P (1999) The complete genome sequence of the major component of a mild citrus tristeza virus isolate. J Gen Virol 80(3):811–816PubMedGoogle Scholar
  109. Vives MC, Rubio L, Sambade A, Mirkov TE, Moreno P, Guerri J (2005) Evidence of multiple recombination events between two RNA sequence variants within a Citrus tristeza virus isolate. Virology 331(2):232–237PubMedCrossRefGoogle Scholar
  110. White KA, Morris TJ (1994a) Nonhomologous RNA recombination in tombusviruses: generation and evolution of defective interfering RNAs by stepwise deletions. J Virol 68(1):14–24PubMedGoogle Scholar
  111. White KA, Morris TJ (1994b). Recombination between defective tombusvirus RNAs generates functional hybrid genomes. Proc Natl Acad Sci USA 91(9):3642–3646PubMedCrossRefGoogle Scholar
  112. White KA, Morris TJ (1995) RNA determinants of junction site selection in RNA virus recombinants and defective interfering RNAs. RNA 1(10):1029–1040PubMedGoogle Scholar
  113. White KA, Morris TJ (1999) Defective and defective interfering RNAs of monopartite plus-strand RNA plant viruses. Curr Top Microbiol Immunol 239:1–17PubMedGoogle Scholar
  114. White KA, Nagy PD (2004) Advances in the molecular biology of tombusviruses: gene expression, genome replication, and recombination. Prog Nucleic Acid Res Mol Biol 78:187–226PubMedCrossRefGoogle Scholar
  115. Wierzchoslawski R, Bujarski JJ (2006) Efficient in vitro system of homologous recombination in brome mosaic bromovirus. J Virol 80(12):6182–6187PubMedCrossRefGoogle Scholar
  116. Wierzchoslawski R, Dzianott A, Kunimalayan S, Bujarski JJ (2003) A transcriptionally active subgenomic promoter supports homologous crossovers in a plus-strand RNA virus. J Virol 77(12):6769–6776PubMedCrossRefGoogle Scholar
  117. Worobey M, Holmes EC (1999) Evolutionary aspects of recombination in RNA viruses. J Gen Virol 80(10:2535–2543PubMedGoogle Scholar
  118. Wu W, Blumberg BM, Fay PJ, Bambara RA (1995) Strand transfer mediated by human immunodeficiency virus reverse transcriptase in vitro is promoted by pausing and results in misincorporation. J Biol Chem 270(1):325–332PubMedCrossRefGoogle Scholar
  119. Yeh TY, Lin BY, Chang YC, Hsu YH, Lin NS (1999) A defective RNA associated with bamboo mosaic virus and the possible common mechanisms for RNA recombination in potexviruses. Virus Genes 18(2):121–128PubMedCrossRefGoogle Scholar
  120. Zhong Y, Guo A, Li C, Zhuang B, Lai M, Wei C, Luo J, Li Y (2005) Identification of a naturally occurring recombinant isolate of Sugarcane mosaic virus causing maize dwarf mosaic disease. Virus Genes 30(1):75–83PubMedCrossRefGoogle Scholar
  121. Zimmern (1988) Evolution of RNA viruses. In: Domingo JJHE, Ahlquist P (eds) RNA genetics, vol. II. CRC, Boca Raton, pp 211–240Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2008

Authors and Affiliations

  • Peter D. Nagy
    • 1
  1. 1.Department of Plant PathologyUniversity of KentuckyLexingtonUSA

Personalised recommendations