Synonymous site variation due to recombination explains higher genetic variability in begomovirus populations infecting non-cultivated hosts

Journal of General Virology

Volumn 94, Issue PART2, 2013, Pages 418-431

  Lima, Alison T M ^a   Sobrinho, Roberto R ^a   González Aguilera, Jorge ^a,c   Rocha, Carolina S ^a,d   Silva, Sarah J C ^a,e   Xavier, César A D ^a   Silva, Fábio N ^a   Duffy, Siobain ^b   Zerbini, Francisco Murilo ^a  

^a FEDERAL UNIVERSITY OF VIÇOSA   (Brazil)

^b RUTGERS UNIVERSITY   (United States)

^c EMBRAPA CERRADOS   (Brazil)

^d FuturaGene Brasil   (Brazil)

^e FEDERAL UNIVERSITY OF ALAGOAS   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BEGOMOVIRUS; EVOLUTION; GENE MUTATION; GENETIC RECOMBINATION; GENETIC VARIABILITY; GEOGRAPHIC DISTRIBUTION; HOST; MACROPTILIUM YELLOW SPOT VIRUS; NONHUMAN; PHYLOGENY; PLANT VIRUS; POPULATION GENETICS; PRIORITY JOURNAL; TILLAGE; TOMATO SEVERE RUGOSE VIRUS;

BEGOMOVIRUS; BRAZIL; CLUSTER ANALYSIS; DNA, VIRAL; GENETIC VARIATION; MOLECULAR SEQUENCE DATA; PHYLOGENY; PLANT DISEASES; PLANTS; RECOMBINATION, GENETIC; SEQUENCE ANALYSIS, DNA;

ALEYRODIDAE; BEGOMOVIRUS; LYCOPERSICON ESCULENTUM; MACROPTILIUM; RNA VIRUSES; TOMATO SEVERE RUGOSE VIRUS;

EID: 84872472866     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.047241-0     Document Type: Article

References (86)

1. Ala-Poikela, M., Svensson, E., Rojas, A., Horko, T., Paulin, L., Valkonen, J. P. T. & Kvarnheden, A. (2005). Genetic diversity and mixed infections of begomoviruses infecting tomato, pepper and cucurbit crops in Nicaragua. Plant Pathol 54, 448-459.
2. Alabi, O. J., Ogbe, F. O., Bandyopadhyay, R., Dixon, A. G., Hughes, J. & Naidu, R. A. (2007). The occurrence of African cassava mosaic virus and East African cassava mosaic Cameroon virus in natural hosts other than cassava in Nigeria. Phytopathology 97, S3.
3. Alabi, O. J., Ogbe, F. O., Bandyopadhyay, R., Lava Kumar, P., Dixon, A. G. O., Hughes, J. D. & Naidu, R. A. (2008). Alternate hosts of African cassava mosaic virus and East African cassava mosaic Cameroon virus in Nigeria. Arch Virol 153, 1743-1747.
4. Barbosa, J. C., Barreto, S. S., Inoue-Nagata, A. K., Reis, M. S., Firmino, A. C., Bergamin Filho, A. & Rezende, J. A. M. (2009). Natural infection of Nicandra physaloides by Tomato severe rugose virus in Brazil. J Gen Plant Pathol 75, 440-443.
5. Bedford, I. D., Kelly, A., Banks, G. K., Briddon, R. W., Cenis, J. L. & Markham, P. G. (1998). Solanum nigrum: an indigenous weed reservoir for a tomato yellow leaf curl geminivirus in southern Spain. Eur J Plant Pathol 104, 221-222.
6. Berrie, L. C., Rybicki, E. P. & Rey, M. E. C. (2001). Complete nucleotide sequence and host range of South African cassava mosaic virus: further evidence for recombination amongst begomoviruses. J Gen Virol 82, 53-58.
7. Bezerra-Agasie, I. C., Ferreira, G. B., Ávila, A. C. & Inoue-Nagata, A. K. (2006). First report of Tomato severe rugose virus in chili pepper in Brazil. Plant Dis 90, 114.
8. Blair, M. W., Basset, M. J., Abouzid, A. M., Hiebert, E., Polston, J. E., McMillan, R. T., Graves, W. & Lamberts, M. (1995). Ocurrence of bean golden mosaic virus in Florida. Plant Dis 79, 529-533.
9. Briddon, R. W., Bedford, I. D., Tsai, J. H. & Markham, P. G. (1996). Analysis of the nucleotide sequence of the treehopper-transmitted geminivirus, tomato pseudo-curly top virus, suggests a recombinant origin. Virology 219, 387-394.
10. Brown, J. K. & Bird, J. (1992). Whitefly-transmitted geminiviruses and associated disorders in the Americas and the Caribbean basin. Plant Dis 76, 220-225.
11. Brown, J. K., Fauquet, C. M., Briddon, R. W., Zerbini, F. M., Moriones, E. & Navas-Castillo, J. (2012). Family Geminiviridae. In Virus Taxonomy 9th Report of the International Committee on Taxonomy of Viruses, pp. 351-373. Edited by A. M. Q. King, M. J. Adams, E. B. Carstens & E. J. Lefkowitz. London, UK: Elsevier Academic Press.
12. Bull, S. E., Briddon, R. W., Sserubombwe, W. S., Ngugi, K., Markham, P. G. & Stanley, J. (2006). Genetic diversity and phylogeography of cassava mosaic viruses in Kenya. J Gen Virol 87, 3053-3065.
13. Chare, E. R. & Holmes, E. C. (2004). Selection pressures in the capsid genes of plant RNA viruses reflect mode of transmission. J Gen Virol 85, 3149-3157.
14. Davino, S., Napoli, C., Dellacroce, C., Miozzi, L., Noris, E., Davino, M. & Accotto, G. P. (2009). Two new natural begomovirus recombinants associated with the tomato yellow leaf curl disease co-exist with parental viruses in tomato epidemics in Italy. Virus Res 143, 15-23.
15. Doyle, J. J. & Doyle, J. L. (1987). A rapid DNA isolation procedure for small amounts of fresh leaf tissue. Phytochem Bull 19, 11-15.
16. Duffy, S. & Holmes, E. C. (2008). Phylogenetic evidence for rapid rates of molecular evolution in the single-stranded DNA begomovirus Tomato yellow leaf curl virus. J Virol 82, 957-965.
17. Duffy, S. & Holmes, E. C. (2009). Validation of high rates of nucleotide substitution in geminiviruses: phylogenetic evidence from East African cassava mosaic viruses. J Gen Virol 90, 1539-1547.
18. Edgar, R. C. (2004). MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5, 113.
19. Fernandes, F. R., de Albuquerque, L. C., de Britto Giordano, L., Boiteux, L. S., de Avila, A. C. & Inoue-Nagata, A. K. (2008). Diversity and prevalence of Brazilian bipartite begomovirus species associated to tomatoes. Virus Genes 36, 251-258.
20. Fiallo-Olivé, E., Navas-Castillo, J., Moriones, E. & Martínez-Zubiaur, Y. (2012). Begomoviruses infecting weeds in Cuba: increased host range and a novel virus infecting Sida rhombifolia. Arch Virol 157, 141-146.
21. Fondong, V. N., Pita, J. S., Rey, M. E. C., de Kochko, A., Beachy, R. N. & Fauquet, C. M. (2000). Evidence of synergism between African cassava mosaic virus and a new double-recombinant geminivirus infecting cassava in Cameroon. J Gen Virol 81, 287-297.
22. Fu, Y. X. & Li, W. H. (1993). Statistical tests of neutrality of mutations. Genetics 133, 693-709.
23. 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.
24. 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.
25. García-Andrés, S., Tomás, D. M., Sánchez-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.
26. García-Arenal, F., Fraile, A. & Malpica, J. M. (2003). Variation and evolution of plant virus populations. Int Microbiol 6, 225-232.
27. Gilbertson, R. L., Faria, J. C., Ahlquist, P. & Maxwell, D. P. (1993). Genetic diversity in geminiviruses causing bean golden mosaic disease: the nucleotide sequence of the infectious cloned DNA components of a Brazilian isolate of bean golden mosaic geminivirus. Phytopathology 83, 709-715.
28. González-Aguilera, A., Tavares, S. S., Ramos-Sobrinho, R., Xavier, C. A. D., Dueñas-Hurtado, F., Lara-Rodrigues, R. M., Silva, D. J. H. & Zerbini, F. M. (2012). Genetic structure of a Brazilian population of the begomovirus Tomato severe rugose virus (ToSRV). Trop Plant Pathol 37, 346-353.
29. Graham, A. P., Martin, D. P. & Roye, M. E. (2010). Molecular characterization and phylogeny of two begomoviruses infecting Malvastrum americanum in Jamaica: evidence of the contribution of inter-species recombination to the evolution of malvaceous weed associated begomoviruses from the northern Caribbean. Virus Genes 40, 256-266.
30. Hanley-Bowdoin, L., Settlage, S. B. & Robertson, D. (2004). Reprogramming plant gene expression: a prerequisite to geminivirus DNA replication. Mol Plant Pathol 5, 149-156.
31. Harrison, B. D. & Robinson, D. J. (1999). Natural genomic and antigenic variation in white-fly transmitted geminiviruses (begomo viruses). Annu Rev Phytopathol 37, 369-398.
32. Harrison, B. D., Zhou, X., Otim Nape, G. W., Liu, Y. & Robinson, D. J. (1997). Role of a novel type of double infection in the geminivirus induced epidemic of severe cassava mosaic in Uganda. Ann Appl Biol 131, 437-448.
33. Ilyina, T. V. & Koonin, E. V. (1992). Conserved sequence motifs in the initiator proteins for rolling circle DNA replication encoded by diverse replicons from eubacteria, eucaryotes and archaebacteria. Nucleic Acids Res 20, 3279-3285.
34. 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 phi 29 DNA polymerase. J Virol Met 116, 209-211.
35. 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.
36. Kosakovsky Pond, S. L. & Frost, S. D. W. (2005). Not so different after all: a comparison of methods for detecting amino acid sites under selection. Mol Biol Evol 22, 1208-1222.
37. Lefeuvre, P., Lett, J. M., Reynaud, B. & Martin, D. P. (2007a). Avoidance of protein fold disruption in natural virus recombinants. PLoS Pathog 3, e181.
38. 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.
39. Lefeuvre, P., Lett, J. M., Varsani, A. & Martin, D. P. (2009). Widely conserved recombination patterns among single-stranded DNA viruses. J Virol 83, 2697-2707.
40. Legg, J. P. & Fauquet, C. M. (2004). Cassava mosaic geminiviruses in Africa. Plant Mol Biol 56, 585-599.
41. Legg, J. P. & Thresh, J. M. (2000). Cassava mosaic virus disease in East Africa: a dynamic disease in a changing environment. Virus Res 71, 135-149.
42. Londoñ o, A., Riego-Ruiz, L. & Arguello-Astorga, G. R. (2010). DNA binding specificity determinants of replication proteins encoded by eukaryotic ssDNA viruses are adjacent to widely separated RCR conserved motifs. Arch Virol 155, 1033-1046.
43. Lozano, G., Trenado, H. P., Valverde, R. A. & Navas-Castillo, J. (2009). Novel begomovirus species of recombinant nature in sweet potato (Ipomoea batatas) and Ipomoea indica: taxonomic and phylogenetic implications. J Gen Virol 90, 2550-2562.
44. Martin, D. P., van der Walt, E., Posada, D. & Rybicki, E. P. (2005). The evolutionary value of recombination is constrained by genome modularity. PLoS Genet 1, e51.
45. Martin, D. P., Lemey, P., Lott, M., Moulton, V., Posada, D. & Lefeuvre, P. (2010). RDP3: a flexible and fast computer program for analyzing recombination. Bioinformatics 26, 2462-2463.
46. Martin, D. P., Lefeuvre, P., Varsani, A., Hoareau, M., Semegni, J. Y., Dijoux, B., Vincent, C., Reynaud, B. & Lett, J. M. (2011). Complex recombination patterns arising during geminivirus coinfections preserve and demarcate biologically important intra-genome inter action networks. PLoS Pathog 7, e1002203.
47. Monci, F., Sánchez-Campos, S., Navas-Castillo, J. & Moriones, E. (2002). A natural recombinant between the geminiviruses Tomato yellow leaf curl Sardinia virus and Tomato yellow leaf curl virus exhibits a novel pathogenic phenotype and is becoming prevalent in Spanish populations. Virology 303, 317-326.
48. Monde, G., Walangululu, J., Winter, S. & Bragard, C. (2010). Dual infection by cassava begomoviruses in two leguminous species (Fabaceae) in Yangambi, Northeastern Democratic Republic of Congo. Arch Virol 155, 1865-1869.
49. Morales, F. J. & Anderson, P. K. (2001). The emergence and dissemination of whitefly-transmitted geminiviruses in Latin America. Arch Virol 146, 415-441.
50. Morales, F. J. & Jones, P. G. (2004). The ecology and epidemiology of whitefly-transmitted viruses in Latin America. Virus Res 100, 57-65.
51. Morilla, G., Krenz, B., Jeske, H., Bejarano, E. R. & Wege, C. (2004). Tête à tête of tomato yellow leaf curl virus and tomato yellow leaf curl sardinia virus in single nuclei. J Virol 78, 10715-10723.
52. Moriones, E. & Navas-Castillo, J. (2000). Tomato yellow leaf curl virus, an emerging virus complex causing epidemics worldwide. Virus Res 71, 123-134.
53. Navas-Castillo, J., Sánchez-Campos, S., Noris, E., Louro, D., Accotto, G. P. & Moriones, E. (2000). Natural recombination between Tomato yellow leaf curl virus-is and Tomato leaf curl virus. J Gen Virol 81, 2797-2801.
54. 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.
55. Orozco, B. M., Kong, L. J., Batts, L. A., Elledge, S. & Hanley-Bowdoin, L. (2000). The multifunctional character of a geminivirus replication protein is reflected by its complex oligomerization properties. J Biol Chem 275, 6114-6122.
56. Padidam, M., Sawyer, S. & Fauquet, C. M. (1999). Possible emergence of new geminiviruses by frequent recombination. Virology 265, 218-225.
57. Pita, J. S., Fondong, V. N., Sangaré, A., Otim-Nape, G. W., Ogwal, S. & Fauquet, C. M. (2001). Recombination, pseudorecombination and synergism of geminiviruses are determinant keys to the epidemic of severe cassava mosaic disease in Uganda. J Gen Virol 82, 655-665.
58. Polston, J. E. & Anderson, P. K. (1997). The emergence of whitefly transmitted geminiviruses in tomato in the western hemisphere. Plant Dis 81, 1358-1369.
59. Posada, D. & Crandall, K. A. (1998). MODELTEST: testing the model of DNA substitution. Bioinformatics 14, 817-818.
60. Posada, D. & Crandall, K. A. (2002). The effect of recombination on the accuracy of phylogeny estimation. J Mol Evol 54, 396-402.
61. Power, A. G. (2000). Insect transmission of plant viruses: a constraint on virus variability. Curr Opin Plant Biol 3, 336-340.
62. Prasanna, H. C. & Rai, M. (2007). Detection and frequency of recombination in tomato-infecting begomoviruses of South and Southeast Asia. Virol J 4, 111.
63. Reddy, R. V. C., Colvin, J., Muniyappa, V. & Seal, S. (2005). Diversity and distribution of begomoviruses infecting tomato in India. Arch Virol 150, 845-867.
64. Ribeiro, S. G., Ambrozevícius, L. P., Ávila, A. C., Bezerra, I. C., Calegario, R. F., Fernandes, J. J., Lima, M. F., de Mello, R. N., Rocha, H. & Zerbini, F. M. (2003). Distribution and genetic diversity of tomato-infecting begomoviruses in Brazil. Arch Virol 148, 281-295.
65. Rocha, C. S. (2011). Variability and genetic structure of begomovirus populations infecting tomato and non-cultivated hosts in south western Brazil. DS Thesis, Dep de Fitopatologia, 129 p. Viçosa, MG: Universidade Federal de Viçosa.
66. Rojas, M. R., Hagen, C., Lucas, W. J. & Gilbertson, R. L. (2005). Exploiting chinks in the plant's armor: evolution and emergence of geminiviruses. Annu Rev Phytopathol 43, 361-394.
67. Roossinck, M. J. (2003). Plant RNA virus evolution. Curr Opin Microbiol 6, 406-409.
68. Rothenstein, D., Haible, D., Dasgupta, I., Dutt, N., Patil, B. L. & Jeske, H. (2006). Biodiversity and recombination of cassava-infecting begomoviruses from southern India. Arch Virol 151, 55-69.
69. Rozas, J., Sánchez-DelBarrio, J. C., Messeguer, X. & Rozas, R. (2003). DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19, 2496-2497.
70. Sanz, A. I., Fraile, A., Gallego, J. M., Malpica, J. M. & García-Arenal, F. (1999). Genetic variability of natural populations of cotton leaf curl geminivirus, a single-stranded DNA virus. J Mol Evol 49, 672-681.
71. Sanz, A. I., Fraile, A., García-Arenal, F., Zhou, X., Robinson, D. J., Khalid, S., Butt, T. & Harrison, B. D. (2000). Multiple infection, recombination and genome relationships among begomovirus isolates found in cotton and other plants in Pakistan. J Gen Virol 81, 1839-1849.
72. Saunders, K., Bedford, I. D. & Stanley, J. (2001). Pathogenicity of a natural recombinant associated with ageratum yellow vein disease: implications for geminivirus evolution and disease aetiology. Virology 282, 38-47.
73. Scheffler, K., Martin, D. P. & Seoighe, C. (2006). Robust inference of positive selection from recombining coding sequences. Bioinformatics 22, 2493-2499.
74. 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.
75. Seal, S. E., Jeger, M. J. & Van den Bosch, F. (2006). Begomovirus evolution and disease management. Adv Virus Res 67, 297-316.
76. Silva, S. J., Castillo-Urquiza, G. P., Hora Júnior, B. T., Assunção, I. P., Lima, G. S. A., Pio-Ribeiro, G., Mizubuti, E. S. G. & Zerbini, F. M. (2011). High genetic variability and recombination in a begomovirus population infecting the ubiquitous weed Cleome affinis in north eastern Brazil. Arch Virol 156, 2205-2213.
77. Silva, S. J. C., Castillo-Urquiza, G. P., Hora-Junior, B. T., Assunção, I. P., Lima, G. S. A., Pio-Ribeiro, G., Mizubuti, E. S. G. & Zerbini, F. M. (2012). Species diversity, phylogeny and genetic variability of begomovirus populations infecting leguminous weeds in northeastern Brazil. Plant Pathol 61, 457-467.
78. Souza-Dias, J. A. C., Sawazaki, H. E., Pernambuco-Fo, P. C. A., Elias, L. M. & Maluf, H. (2008). Tomato severe rugose virus: another begomovirus causing leaf deformation and mosaic symptoms on potato in Brazil. Plant Dis 92, 487-488.
79. Sserubombwe, W. S., Briddon, R. W., Baguma, Y. K., Ssemakula, G. N., Bull, S. E., Bua, A., Alicai, T., Omongo, C., Otim-Nape, G. W. & Stanley, J. (2008). Diversity of begomoviruses associated with mosaic disease of cultivated cassava (Manihot esculenta Crantz) and its wild relative (Manihot glaziovii Mull. Arg.) in Uganda. J Gen Virol 89, 1759-1769.
80. Swofford, D. L. (2003). PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4. Sunderland, Massachusetts: Sinauer Associates.
81. Tiendrébéogo, F., Lefeuvre, P., Hoareau, M., Harimalala, M. A., De Bruyn, A., Villemot, J., Traoré, V. S., Konaté, G., Traoré, A. S. & other authors (2012). Evolution of African cassava mosaic virus by recombination between bipartite and monopartite begomoviruses. Virol J 9, 67.
82. Torres-Pacheco, I., Garzón-Tiznado, J. A., Brown, J. K., Becerra-Flora, A. & Rivera-Bustamante, R. (1996). Detection and distribution of geminiviruses in Mexico and the Southern United States. Phytopathology 86, 1186-1192.
83. Were, H. K., Winter, S. & Maiss, E. (2004). Viruses infecting cassava in Kenya. Plant Dis 88, 17-22.
84. Wyant, P. S., Gotthardt, D., Schafer, B., Krenz, B. & Jeske, H. (2011). The genomes of four novel begomoviruses and a new Sida micrantha mosaic virus strain from Bolivian weeds. Arch Virol 156, 347-352.
85. Zerbini, F. M., Andrade, E. C., Barros, D. R., Ferreira, S. S., Lima, A. T. M., Alfenas, P. F. & Mello, R. N. (2005). Traditional and novel strategies for geminivirus management in Brazil. Australas Plant Pathol 34, 475-480.
86. Zhou, X., Liu, Y., Calvert, L., Munoz, C., Otim-Nape, G. W., Robinson, D. J. & Harrison, B. D. (1997). Evidence that DNA-A of a geminivirus associated with severe cassava mosaic disease in Uganda has arisen by interspecific recombination. J Gen Virol 78, 2101-2111.