Rapid host adaptation by extensive recombination

Journal of General Virology

Volumn 90, Issue 3, 2009, Pages 734-746

  van der Walt, Eric ^a   Rybicki, Edward P ^a   Varsani, Arvind ^a   Polston, J E ^b   Billharz, Rosalind ^c   Donaldson, Lara ^a   Monjane, Adérito L ^a   Martin, Darren P ^a  

^a UNIVERSITY OF CAPE TOWN   (South Africa)

^b UNIVERSITY OF FLORIDA   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTATION; ARTICLE; CONTROLLED STUDY; GENOME ANALYSIS; MAIZE STREAK VIRUS; MOLECULAR EVOLUTION; NONHUMAN; PRIORITY JOURNAL; PROGENY; VIRUS CELL INTERACTION; VIRUS RECOMBINATION; VIRUS REPLICATION; VIRUS VIRULENCE; WILD TYPE; GEMINIVIRUS; GENETIC RECOMBINATION; GENETIC SELECTION; GENETICS; ISOLATION AND PURIFICATION; MAIZE; MOLECULAR GENETICS; MUTATION; NUCLEOTIDE SEQUENCE; PATHOGENICITY; PHYSIOLOGY; PLANT DISEASE; PLANT LEAF; VIROLOGY; VIRUS GENOME;

CHIMAERIFORMES; GEMINIVIRIDAE; MAIZE STREAK VIRUS;

VIRUS DNA;

BASE SEQUENCE; DNA, VIRAL; GEMINIVIRIDAE; GENOME, VIRAL; MAIZE STREAK VIRUS; MOLECULAR SEQUENCE DATA; MUTATION; PLANT DISEASES; PLANT LEAVES; RECOMBINATION, GENETIC; SELECTION (GENETICS); ZEA MAYS;

EID: 63449133264     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.007724-0     Document Type: Article

References (65)

1. Casado, C. G., Javier, O. G., Padron, E., Bean, S. J., McKenna, R., Agbandje-McKenna, M. & Boulton, M. I. (2004). Isolation and characterization of subgenomic DNAs encapsidated in "single" T = 1 isometric particles of Maize streak virus. Virology 323, 164-171.
2. Chao, L. (1990). Fitness of RNA virus decreased by Muller's ratchet. Nature 348, 454-455.
3. Chare, E. R. & Holmes, E. C. (2006). A phylogenetic survey of recombination frequency in plant RNA viruses. Arch Virol 151, 933-946.
4. Chenault, K. D. & Melcher, U. (1994). Phylogenetic relationships reveal recombination among isolates of cauliflower mosaic virus. J Mol Evol 39, 496-505.
5. Delatte, H., Martin, D. P., Naze, F., Goldbach, R., Reynaud, B., Peterschmitt, M. & Lett, J. M. (2005). South West Indian Ocean islands tomato begomovirus populations represent a new major monopartite begomovirus group. J Gen Virol 86, 1533-1542.
6. de Visser, J. A. & Elena, S. F. (2007). The evolution of sex: empirical insights into the roles of epistasis and drift. Nat Rev Genet 8, 139-149.
7. Donson, J., Morris-Krsinich, B. A., Mullineaux, P. M., Boulton, M. I. & Davies, J. W. (1984). A putative primer for second-strand DNA synthesis of maize streak virus is virion-associated. EMBO J 3, 3069-3073.
8. Drummond, D. A., Silberg, J. J., Meyer, M. M., Wilke, C. O. & Arnold, F. H. (2005). On the conservative nature of intragenic recombination. Proc Natl Acad Sci U S A 102, 5380-5385.
9. Felsenstein, J. (1974). The evolutionary advantage of recombination. Genetics 78, 737-756.
10. García-Andrés, S., Monci, F., Navas-Castillo, J. & Moriones, E. (2006). Begomovirus genetic diversity in the native plant reservoir Solanum nigrum: evidence for the presence of a new virus species of recombinant nature. Virology 350, 433-442.
11. García-Andrés, S., Accotto, G. P., Navas-Castillo, J. & Moriones, E. (2007a). Founder effect, plant host, and recombination shape the emergent population of begomoviruses that cause the tomato yellow leaf curl disease in the Mediterranean basin. Virology 359, 302-312.
12. García-Andrés, S., Tomas, D. M., Sanchez-Campos, S., Navas-Castillo, J. & Moriones, E. (2007b). Frequent occurrence of recombinants in mixed infections of tomato yellow leaf curl disease-associated begomoviruses. Virology 365, 210-219.
13. Ge, L., Zhang, J., Zhou, X. & Li, H. (2007). Genetic structure and population variability of tomato yellow leaf curl China virus. J Virol 81, 5902-5907.
14. Gerrish, P. J. & Lenski, R. E. (1998). The fate of competing beneficial mutations in an asexual population. Genetica 102-103, 127-144.
15. Gussow, D. & Clackson, T. (1989). Direct clone characterization from plaques and colonies by the polymerase chain reaction. Nucleic Acids Res 17, 4000.
16. Heath, L., Martin, D. P., Warburton, L., Perrin, M., Horsfield, W., Kingsley, C., Rybicki, E. P. & Williamson, A. L. (2004). Evidence of unique genotypes of beak and feather disease virus in southern Africa. J Virol 78, 9277-9284.
17. Heath, L., van der Walt, E., Varsani, A. & Martin, D. P. (2006). Recombination patterns in aphthoviruses mirror those found in other picornaviruses. J Virol 80, 11827-11832.
18. Huertas, P. & Aguilera, A. (2003). Cotranscriptionally formed DNA:RNA hybrids mediate transcription elongation impairment and transcription-associated recombination. Mol Cell 12, 711-721.
19. Inoue-Nagata, A. K., Albuquerque, L. C., Rocha, W. B. & Nagata, T. (2004). A simple method for cloning the complete begomovirus genome using the bacteriophage Q29 DNA polymerase. J Virol Methods 116, 209-211.
20. Isnard, M., Granier, M., Frutos, R., Reynaud, B. & Peterschmitt, M. (1998). Quasispecies nature of three maize streak virus isolates obtained through different modes of selection from a population used to assess response to infection of maize cultivars. J Gen Virol 79, 3091-3099.
21. Jeske, H., Lutgemeier, M. & Preiss, W. (2001). DNA forms indicate rolling circle and recombination-dependent replication of Abutilon mosaic virus. EMBO J 20, 6158-6167.
22. Katz, R. A. & Skalka, A. M. (1990). Generation of diversity in retroviruses. Annu Rev Genet 24, 409-445.
23. Keightley, P. D. & Otto, S. P. (2006). Interference among deleterious mutations favours sex and recombination in finite populations. Nature 443, 89-92.
24. Lefeuvre, P., Lett, J. M., Reynaud, B. & Martin, D. P. (2007a). Avoidance of protein fold disruption in natural virus recombinants. PLoS Pathog 3, e181.
25. Lefeuvre, P., Martin, D. P., Hoareau, M., Naze, F., Delatte, H., Thierry, M., Varsani, A., Becker, N., Reynaud, B. & Lett, J. M. (2007b). Begomovirus 'melting pot' in the south-west Indian Ocean islands: molecular diversity and evolution through recombination. J Gen Virol 88, 3458-3468.
26. Martin, D. P. & Rybicki, E. P. (1998). Microcomputer-based quantification of maize streak virus symptoms in Zea mays. Phytopathology 88, 422-427.
27. Martin, D. P. & Rybicki, E. P. (2000). Improved efficiency of Zea mays agroinoculation with Maize streak virus. Plant Dis 84, 1096-1098.
28. Martin, D. P. & Rybicki, E. P. (2002). Investigation of Maize streak virus pathogenicity determinants using chimaeric genomes. Virology 300, 180-188.
29. Martin, D. P., Willment, J. A. & Rybicki, E. P. (1999). Evaluation of Maize streak virus pathogenicity in differentially resistant Zea mays genotypes. Phytopathology 89, 695-700.
30. Martin, D. P., Willment, J. A., Billharz, R., Velders, R., Odhiambo, B., Njuguna, J., James, D. & Rybicki, E. P. (2001). Sequence diversity and virulence in Zea mays of Maize streak virus isolates. Virology 288, 247-255.
31. Martin, D. P., van der Walt, E., Posada, D. & Rybicki, E. P. (2005a). The evolutionary value of recombination is constrained by genome modularity. PLoS Genet 1, e51.
32. Martin, D. P., Williamson, C. & Posada, D. (2005b). RDP2: recombination detection and analysis from sequence alignments. Bioinformatics 21, 260-262.
33. Meinschad, C. & Winnacker, E. L. (1980). Recombination in adenovirus. I. Analysis of recombinant viruses under non-selective conditions. J Gen Virol 48, 219-224.
34. Muller, H. J. (1964). The relation of recombination to mutational advance. Mutat Res 106, 2-9.
35. Ndunguru, J., Legg, J. P., Aveling, T. A., Thompson, G. & Fauquet, C. M. (2005). Molecular biodiversity of cassava begomoviruses in Tanzania: evolution of cassava geminiviruses in Africa and evidence for East Africa being a center of diversity of cassava geminiviruses. Virol J 2, 21.
36. Odelberg, S. J., Weiss, R. B., Hata, A. & White, R. (1995). Template-switching during DNA synthesis by Thermus aquaticus DNA polymerase I. Nucleic Acids Res 23, 2049-2057.
37. Owor, B. E., Martin, D. P., Shepherd, D. N., Edema, R., Monjane, A. L., Rybicki, E. P., Thomson, J. A. & Varsani, A. (2007a). Genetic analysis of maize streak virus isolates from Uganda reveals widespread distribution of a recombinant variant. J Gen Virol 88, 3154-3165.
38. Owor, B. E., Shepherd, D. N., Taylor, N. J., Edema, R., Monjane, A. L., Thomson, J. A., Martin, D. P. & Varsani, A. (2007b). Successful application of FTA Classic Card technology and use of bacteriophage φ29 DNA polymerase for large-scale field sampling and cloning of complete maize streak virus genomes. J Virol Methods 140, 100-105.
39. Padidam, M., Sawyer, S. & Fauquet, C. M. (1999). Possible emergence of new geminiviruses by frequent recombination. Virology 265, 218-225.
40. Palmer, K. E., Schnippenkoetter, W. H. & Rybicki, E. P. (1998). Geminivirus isolation and DNA extraction. Methods Mol Biol 81, 41-52.
41. Posada, D. & Crandall, K. A. (2002). The effect of recombination on the accuracy of phylogeny estimation. J Mol Evol 54, 396-402.
42. Prasanna, H. C. & Rai, M. (2007). Detection and frequency of recombination in tomato-infecting begomoviruses of south and southeast Asia. Virol J 4, 111.
43. Preiss, W. & Jeske, H. (2003). Multitasking in replication is common among geminiviruses. J Virol 77, 2972-2980.
44. Sambrook, J., Fritsch, E. F. & Maniatis, T. (1989). Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
45. Saunders, K., Lucy, A. & Stanley, J. (1991). DNA forms of the geminivirus African cassava mosaic virus consistent with a rolling circle mechanism of replication. Nucleic Acids Res 19, 2325-2330.
46. Scheffler, K., Martin, D. P. & Seoighe, C. (2006). Robust inference of positive selection from recombining coding sequences. Bioinformatics 22, 2493-2499.
47. Schierup, M. H. & Hein, J. (2000). Recombination and the molecular clock. Mol Biol Evol 17, 1578-1579.
48. Schnippenkoetter, W. H., Martin, D. P., Willment, J. A. & Rybicki, E. P. (2001). Forced recombination between distinct strains of Maize streak virus. J Gen Virol 82, 3081-3090.
49. Shackelton, L. A., Hoelzer, K., Parrish, C. R. & Holmes, E. C. (2007). Comparative analysis reveals frequent recombination in the parvo-viruses. J Gen Virol 88, 3294-3301.
50. Sharp, P. M., Robertson, D. L. & Hahn, B. H. (1995). Cross-species transmission and recombination of 'AIDS' viruses. Philos Trans R Soc Lond B Biol Sci 349, 41-47.
51. Shepherd, D. N., Mangwende, T., Martin, D. P., Bezuidenhout, M., Thomson, J. A. & Rybicki, E. P. (2007). Inhibition of maize streak virus (MSV) replication by transient and transgenic expression of MSV replication-associated protein mutants. J Gen Virol 88, 325-336.
52. Shepherd, D. N., Varsani, A., Windram, O. P., Lefeuvre, P., Monjane, A. L., Owor, B. E. & Martin, D. P. (2008a). Novel Sugarcane streak and Sugarcane streak Réunion mastreviruses from southern Africa and La Réunion. Arch Virol 153, 605-609.
53. Shepherd, D. N., Martin, D. P., Lefeuvre, P., Monjane, A. L., Owor, B. E., Rybicki, E. P. & Varsani, A. (2008b). A protocol for the rapid isolation of full geminivirus genomes from dried plant tissue. J Virol Methods 149, 97-102.
54. Stenger, D. C., Revington, G. N., Stevenson, M. C. & Bisaro, D. M. (1991). Replicational release of geminivirus genomes from tandemly repeated copies: evidence for rolling-circle replication of a plant viral DNA. Proc Natl Acad Sci U S A 88, 8029-8033.
55. Suzuki, Y., Gojobod, T. & Nakagomi, O. (1998). Intragenic recombinations in rotaviruses. FEBS Lett 427, 183-187.
56. Takeuchi, Y., Horluchi, T. & Kobayashi, T. (2003). Transcription-dependent recombination and the role of fork collision in yeast rDNA. Genes Dev 17, 1497-1506.
57. van der Wait E., Martin, D. P., Varsani, A,, Polston, J. E. & Rybicki, E. P. (2008). Experimental observations of rapid Maize streak virus evolution reveal a strand-specific nucleotide substitution bias. Virol J 5, 104.
58. Varsani, A., van der Walt, E., Heath, L., Rybicki, E. P., Williamson, A. L. & Martin, D. P. (2006). Evidence of ancient papillomavirus recombination. J Gen Virol 87, 2527-2531.
59. Varsani, A., Oluwafemi, S., Windram, O. P., Shepherd, D. N., Monjane, A. L., Owor, B. E., Rybicki, E. P., Lefeuvre, P. & Martin, D. P. (2008a). Panicum streak virus diversity is similar to that observed for maize streak virus. Arch Virol 153, 601-604.
60. Varsani, A., Shepherd, D. N., Monjane, A. L., Owor, B. E., Erdmann, J. B., Rybicki, E. P., Peterschmitt, M., Briddon, R. W., Markham, P. G. & other authors (2008b). Recombination, decreased host specificity and increased mobility may have driven the emergence of maize streak virus as an agricultural pathogen. J Gen Virol 89, 2063-2074.
61. Wiliment J. A., Martin, D. P. & Rybicki, E. P. (2001). Analysis of the diversity of African streak mastreviruses using PCR-generated RFLPs and partial sequence data. J Virol Methods 93, 75-87.
62. Wiliment J. A., Martin, D. P., van der Walt, E. & Rybicki, E. P. (2002). Biological and genomic sequence characterization of Maize streak virus isolates from wheat. Phytopathology 92, 81-86.
63. Willment, J. A. Martin, D. P., Palmer, K. E., Schippenkoetter, W. H., Shepherd, D. N. & Rybicki, E. P. (2007). Identification of long intergenic region sequences involved in maize streak virus replication. J Gen Virol 88, 1831-1841.
64. Worobey, M. (2000). Extensive homologous recombination among widely divergent TT viruses. J Virol 74, 7666-7670.
65. Zhou, X., Liu, Y., Robinson, D. J. & Harrison, B. D. (1998). Four DNA-A variants among Pakistani isolates of cotton leaf curl virus and their affinities to DNA-A of geminivirus isolates firom okra. J Gen Virol 79, 915-923.