1887

Abstract

Begomoviruses are ssDNA plant viruses that cause serious epidemics in economically important crops worldwide. Non-cultivated plants also harbour many begomoviruses, and it is believed that these hosts may act as reservoirs and as mixing vessels where recombination may occur. Begomoviruses are notoriously recombination-prone, and also display nucleotide substitution rates equivalent to those of RNA viruses. In Brazil, several indigenous begomoviruses have been described infecting tomatoes following the introduction of a novel biotype of the whitefly vector in the mid-1990s. More recently, a number of viruses from non-cultivated hosts have also been described. Previous work has suggested that viruses infecting non-cultivated hosts have a higher degree of genetic variability compared with crop-infecting viruses. We intensively sampled cultivated and non-cultivated plants in similarly sized geographical areas known to harbour either the weed-infecting (MaYSV) or the crop-infecting (ToSRV), and compared the molecular evolution and population genetics of these two distantly related begomoviruses. The results reinforce the assertion that infection of non-cultivated plant species leads to higher levels of standing genetic variability, and indicate that recombination, not adaptive selection, explains the higher begomovirus variability in non-cultivated hosts.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.047241-0
2013-02-01
2020-07-08
Loading full text...

Full text loading...

/deliver/fulltext/jgv/94/2/418.html?itemId=/content/journal/jgv/10.1099/vir.0.047241-0&mimeType=html&fmt=ahah

References

  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 [CrossRef]
    [Google Scholar]
  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
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  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 [CrossRef]
    [Google Scholar]
  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 [CrossRef]
    [Google Scholar]
  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[PubMed]
    [Google Scholar]
  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 [CrossRef]
    [Google Scholar]
  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 [CrossRef]
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  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 [CrossRef]
    [Google Scholar]
  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 King A. M. Q., Adams M. J., Carstens E. B., Lefkowitz E. J. London, UK: Elsevier Academic Press;
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  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
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  18. Edgar R. C. 2004; muscle: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5:113 [CrossRef][PubMed]
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  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[PubMed]
    [Google Scholar]
  22. Fu Y. X., Li W. H. 1993; Statistical tests of neutrality of mutations. Genetics 133:693–709[PubMed]
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  26. García-Arenal F., Fraile A., Malpica J. M. 2003; Variation and evolution of plant virus populations. Int Microbiol 6:225–232 [CrossRef][PubMed]
    [Google Scholar]
  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 [CrossRef]
    [Google Scholar]
  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 [CrossRef]
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  31. Harrison B. D., Robinson D. J. 1999; Natural genomic and antigenic variation in white-fly transmitted geminiviruses (begomoviruses). Annu Rev Phytopathol 37:369–398 [CrossRef]
    [Google Scholar]
  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 [CrossRef]
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  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 [CrossRef]
    [Google Scholar]
  35. Jeske H., Lütgemeier M., Preiss W. 2001; DNA forms indicate rolling circle and recombination-dependent replication of Abutilon mosaic virus. EMBO J 20:6158–6167 [CrossRef][PubMed]
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  40. Legg J. P., Fauquet C. M. 2004; Cassava mosaic geminiviruses in Africa. Plant Mol Biol 56:585–599 [CrossRef][PubMed]
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  42. Londoño A., Riego-Ruiz L., Argüello-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 [CrossRef][PubMed]
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  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 interaction networks. PLoS Pathog 7:e1002203 [CrossRef][PubMed]
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  49. Morales F. J., Anderson P. K. 2001; The emergence and dissemination of whitefly-transmitted geminiviruses in Latin America. Arch Virol 146:415–441 [CrossRef][PubMed]
    [Google Scholar]
  50. Morales F. J., Jones P. G. 2004; The ecology and epidemiology of whitefly-transmitted viruses in Latin America. Virus Res 100:57–65 [CrossRef][PubMed]
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  52. Moriones E., Navas-Castillo J. 2000; Tomato yellow leaf curl virus, an emerging virus complex causing epidemics worldwide. Virus Res 71:123–134 [CrossRef][PubMed]
    [Google Scholar]
  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[PubMed]
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  56. Padidam M., Sawyer S., Fauquet C. M. 1999; Possible emergence of new geminiviruses by frequent recombination. Virology 265:218–225 [CrossRef][PubMed]
    [Google Scholar]
  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[PubMed]
    [Google Scholar]
  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 [CrossRef]
    [Google Scholar]
  59. Posada D., Crandall K. A. 1998; modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818 [CrossRef][PubMed]
    [Google Scholar]
  60. Posada D., Crandall K. A. 2002; The effect of recombination on the accuracy of phylogeny estimation. J Mol Evol 54:396–402[PubMed] [CrossRef]
    [Google Scholar]
  61. Power A. G. 2000; Insect transmission of plant viruses: a constraint on virus variability. Curr Opin Plant Biol 3:336–340 [CrossRef][PubMed]
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  65. Rocha C. S. 2011 Variability and genetic structure of begomovirus populations infecting tomato and non-cultivated hosts in southwestern 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 [CrossRef][PubMed]
    [Google Scholar]
  67. Roossinck M. J. 2003; Plant RNA virus evolution. Curr Opin Microbiol 6:406–409 [CrossRef][PubMed]
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  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[PubMed]
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  73. Scheffler K., Martin D. P., Seoighe C. 2006; Robust inference of positive selection from recombining coding sequences. Bioinformatics 22:2493–2499 [CrossRef][PubMed]
    [Google Scholar]
  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[PubMed]
    [Google Scholar]
  75. Seal S. E., Jeger M. J., Van den Bosch F. 2006; Begomovirus evolution and disease management. Adv Virus Res 67:297–316 [CrossRef][PubMed]
    [Google Scholar]
  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 northeastern Brazil. Arch Virol 156:2205–2213 [CrossRef][PubMed]
    [Google Scholar]
  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 [CrossRef]
    [Google Scholar]
  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 [CrossRef]
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  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 [CrossRef][PubMed]
    [Google Scholar]
  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 [CrossRef]
    [Google Scholar]
  83. Were H. K., Winter S., Maiss E. 2004; Viruses infecting cassava in Kenya. Plant Dis 88:17–22 [CrossRef]
    [Google Scholar]
  84. Wyant P. S., Gotthardt D., Schäfer 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 [CrossRef][PubMed]
    [Google Scholar]
  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 [CrossRef]
    [Google Scholar]
  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[PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.047241-0
Loading
/content/journal/jgv/10.1099/vir.0.047241-0
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error