1887

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Volume 95, Issue 11

Contrasting genetic structure between two begomoviruses infecting the same leguminous hosts Free

Abstract

Begomoviruses are whitefly-transmitted, ssDNA plant viruses and are among the most damaging pathogens causing epidemics in economically important crops worldwide. Wild/non-cultivated plants play a crucial epidemiological role, acting as begomovirus reservoirs and as ‘mixing vessels' where recombination can occur. Previous work suggests a higher degree of genetic variability in begomovirus populations from non-cultivated hosts compared with cultivated hosts. To assess this supposed host effect on the genetic variability of begomovirus populations, cultivated (common bean, , and lima bean, ) and non-cultivated () legume hosts were sampled from two regions of Brazil. A total of 212 full-length DNA-A genome segments were sequenced from samples collected between 2005 and 2012, and populations of the begomoviruses (BGMV) and (MaYSV) were obtained. We found, for each begomovirus species, similar genetic variation between populations infecting cultivated and non-cultivated hosts, indicating that the presumed genetic variability of the host did not a priori affect viral variability. We observed a higher degree of genetic variation in isolates from MaYSV populations than BGMV populations, which was explained by numerous recombination events in MaYSV. MaYSV and BGMV showed distinct distributions of genetic variation, with the BGMV population (but not MaYSV) being structured by both host and geography.

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© 2014 The Authors
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2014-11-01
2024-04-19
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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 [View Article]
     [Google Scholar]
  2. Alabi O. J., Ogbe F. O., Bandyopadhyay R., Lava Kumar P., Dixon A. G. O., Hughes Jd., 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 [View Article][PubMed]
     [Google Scholar]
  3. Albuquerque L. C., Inoue-Nagata A. K., Pinheiro B., Resende R. O., Moriones E., Navas-Castillo J. 2012; Genetic diversity and recombination analysis of sweepoviruses from Brazil. Virol J 9:241 [View Article][PubMed]
     [Google Scholar]
  4. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. 1990; Basic local alignment search tool. J Mol Biol 215:403–410 [View Article][PubMed]
     [Google Scholar]
  5. 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 [View Article]
     [Google Scholar]
  6. Bonfim K., Faria J. C., Nogueira E. O., Mendes E. A., Aragão F. J. 2007; RNAi-mediated resistance to Bean golden mosaic virus in genetically engineered common bean (Phaseolus vulgaris). Mol Plant Microbe Interact 20:717–726 [View Article][PubMed]
     [Google Scholar]
  7. 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]
  8. Bryant D., Moulton V. 2004; Neighbor-net: an agglomerative method for the construction of phylogenetic networks. Mol Biol Evol 21:255–265 [View Article][PubMed]
     [Google Scholar]
  9. 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 [View Article][PubMed]
     [Google Scholar]
  10. Caciagli P., Medina Piles V., Marian D., Vecchiati M., Masenga V., Mason G., Falcioni T., Noris E. 2009; Virion stability is important for the circulative transmission of tomato yellow leaf curl Sardinia virus by Bemisia tabaci, but virion access to salivary glands does not guarantee transmissibility. J Virol 83:5784–5795 [View Article][PubMed]
     [Google Scholar]
  11. Castillo-Urquiza G. P., Beserra J. E. A. Jr, Bruckner F. P., Lima A. T. M., Varsani A., Alfenas-Zerbini P., Murilo Zerbini F. 2008; Six novel begomoviruses infecting tomato and associated weeds in southeastern Brazil. Arch Virol 153:1985–1989 [View Article][PubMed]
     [Google Scholar]
  12. Costa A. S. 1976; Whitefly-transmitted plant diseases. Annu Rev Phytopathol 14:429–449 [View Article]
     [Google Scholar]
  13. da 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 [View Article][PubMed]
     [Google Scholar]
  14. 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]
  15. Edgar R. C. 2004; MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5:1–19 [View Article][PubMed]
     [Google Scholar]
  16. Faria J. C., Maxwell D. P. 1999; Variability in geminivirus isolates associated with Phaseolus spp. in Brazil. Phytopathology 89:262–268 [View Article][PubMed]
     [Google Scholar]
  17. Fernandes F. R., Cruz A. R. R., Faria J. C., Zerbini F. M., Aragão F. J. L. 2009; Three distinct begomoviruses associated with soybean in central Brazil. Arch Virol 154:1567–1570 [View Article][PubMed]
     [Google Scholar]
  18. 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 [View Article][PubMed]
     [Google Scholar]
  19. 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 [View Article][PubMed]
     [Google Scholar]
  20. 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 [View Article][PubMed]
     [Google Scholar]
  21. 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 [View Article][PubMed]
     [Google Scholar]
  22. Ge L. M., Zhang J. T., Zhou X. P., Li H. Y. 2007; Genetic structure and population variability of tomato yellow leaf curl China virus. J Virol 81:5902–5907 [View Article][PubMed]
     [Google Scholar]
  23. Gilbertson R. L., Faria J. C., Hanson S. F., Morales F. J., Ahlquist P. G., Maxwell D. P., Russell D. R. 1991a; Cloning of the complete DNA genomes of four bean-infecting geminiviruses and determining their infectivity by electric discharge particle acceleration. Phytopathology 81:980–985 [View Article]
     [Google Scholar]
  24. Gilbertson R. L., Hidayat S. H., Martinez R. T., Leong S. A., Faria J. C., Morales F. J., Maxwell D. P. 1991b; Differentiation of bean-infecting geminiviruses by nucleic acid hybridization probes and aspects of bean golden mosaic in Brazil. Plant Dis 75:336–342 [View Article]
     [Google Scholar]
  25. González-Aguilera J., Tavares S. S., Sobrinho R. 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 [View Article]
     [Google Scholar]
  26. Hanley-Bowdoin L., Bejarano E. R., Robertson D., Mansoor S. 2013; Geminiviruses: masters at redirecting and reprogramming plant processes. Nat Rev Microbiol 11:777–788 [View Article][PubMed]
     [Google Scholar]
  27. Höhnle M., Höfer P., Bedford I. D., Briddon R. W., Markham P. G., Frischmuth T. 2001; Exchange of three amino acids in the coat protein results in efficient whitefly transmission of a nontransmissible Abutilon mosaic virus isolate. Virology 290:164–171 [View Article][PubMed]
     [Google Scholar]
  28. Hou Y. M., Gilbertson R. L. 1996; Increased pathogenicity in a pseudorecombinant bipartite geminivirus correlates with intermolecular recombination. J Virol 70:5430–5436[PubMed]
     [Google Scholar]
  29. Huson D. H., Bryant D. 2006; Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23:254–267 [View Article][PubMed]
     [Google Scholar]
  30. 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 [View Article][PubMed]
     [Google Scholar]
  31. 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 φ29 DNA polymerase. J Virol Met 116:209–211 [View Article][PubMed]
     [Google Scholar]
  32. Kheyr-Pour A., Bananej K., Dafalla G. A., Caciagli P., Noris E., Ahoonmanesh A., Lecoq H., Gronenborn B. 2000; Watermelon chlorotic stunt virus from the Sudan and Iran: sequence comparisons and identification of a whitefly-transmission determinant. Phytopathology 90:629–635 [View Article][PubMed]
     [Google Scholar]
  33. Koonin E. V., Ilyina T. V. 1992; Geminivirus replication proteins are related to prokaryotic plasmid rolling circle DNA replication initiator proteins. J Gen Virol 73:2763–2766 [View Article][PubMed]
     [Google Scholar]
  34. 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 [View Article][PubMed]
     [Google Scholar]
  35. Lefeuvre P., Lett J. M., Reynaud B., Martin D. P. 2007a; Avoidance of protein fold disruption in natural virus recombinants. PLoS Pathog 3:e181 [View Article][PubMed]
     [Google Scholar]
  36. 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 [View Article][PubMed]
     [Google Scholar]
  37. 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 [View Article][PubMed]
     [Google Scholar]
  38. Legg J. P., Fauquet C. M. 2004; Cassava mosaic geminiviruses in Africa. Plant Mol Biol 56:585–599 [View Article][PubMed]
     [Google Scholar]
  39. Lima A. T. M., Sobrinho R. R., González-Aguilera J., Rocha C. S., Silva S. J. C., Xavier C. A. D., Silva F. N., Duffy S., Zerbini F. M. 2013; Synonymous site variation due to recombination explains higher genetic variability in begomovirus populations infecting non-cultivated hosts. J Gen Virol 94:418–431 [View Article][PubMed]
     [Google Scholar]
  40. Liu L., Pinner M. S., Davies J. W., Stanley J. 1999; Adaptation of the geminivirus bean yellow dwarf virus to dicotyledonous hosts involves both virion-sense and complementary-sense genes. J Gen Virol 80:501–506[PubMed]
     [Google Scholar]
  41. 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 [View Article][PubMed]
     [Google Scholar]
  42. 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 [View Article][PubMed]
     [Google Scholar]
  43. 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 [View Article][PubMed]
     [Google Scholar]
  44. 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 [View Article][PubMed]
     [Google Scholar]
  45. 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 [View Article][PubMed]
     [Google Scholar]
  46. 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 [View Article][PubMed]
     [Google Scholar]
  47. Morales F. J. 2006; History and current distribution of begomoviruses in Latin America. Adv Virus Res 67:127–162 [View Article][PubMed]
     [Google Scholar]
  48. Morales F. J., Anderson P. K. 2001; The emergence and dissemination of whitefly-transmitted geminiviruses in Latin America. Arch Virol 146:415–441 [View Article][PubMed]
     [Google Scholar]
  49. Muhire B., Martin D. P., Brown J. K., Navas-Castillo J., Moriones E., Zerbini F. M., Rivera-Bustamante R., Malathi V. G., Briddon R. W., Varsani A. 2013; A genome-wide pairwise-identity-based proposal for the classification of viruses in the genus Mastrevirus (family Geminiviridae). Arch Virol 158:1411–1424 [View Article][PubMed]
     [Google Scholar]
  50. Nash T. E., Dallas M. B., Reyes M. I., Buhrman G. K., Ascencio-Ibañez J. T., Hanley-Bowdoin L. 2011; Functional analysis of a novel motif conserved across geminivirus Rep proteins. J Virol 85:1182–1192 [View Article][PubMed]
     [Google Scholar]
  51. Navas-Castillo J., Fiallo-Olivé E., Sánchez-Campos S. 2011; Emerging virus diseases transmitted by whiteflies. Annu Rev Phytopathol 49:219–248 [View Article][PubMed]
     [Google Scholar]
  52. 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 [View Article][PubMed]
     [Google Scholar]
  53. Ng J. C., Falk B. W. 2006; Virus–vector interactions mediating nonpersistent and semipersistent transmission of plant viruses. Annu Rev Phytopathol 44:183–212 [View Article][PubMed]
     [Google Scholar]
  54. Noris E., Vaira A. M., Caciagli P., Masenga V., Gronenborn B., Accotto G. P. 1998; Amino acids in the capsid protein of tomato yellow leaf curl virus that are crucial for systemic infection, particle formation, and insect transmission. J Virol 72:10050–10057[PubMed]
     [Google Scholar]
  55. Padidam M., Sawyer S., Fauquet C. M. 1999; Possible emergence of new geminiviruses by frequent recombination. Virology 265:218–225 [View Article][PubMed]
     [Google Scholar]
  56. 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]
  57. Power A. G. 2000; Insect transmission of plant viruses: a constraint on virus variability. Curr Opin Plant Biol 3:336–340 [View Article][PubMed]
     [Google Scholar]
  58. Raja P., Wolf J. N., Bisaro D. M. 2010; RNA silencing directed against geminiviruses: post-transcriptional and epigenetic components. Biochim Biophys Acta 1799:337–351 [View Article][PubMed]
     [Google Scholar]
  59. 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 [View Article][PubMed]
     [Google Scholar]
  60. 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 [View Article][PubMed]
     [Google Scholar]
  61. Ribeiro S. G., Martin D. P., Lacorte C., Simões I. C., Orlandini D. R. S., Inoue-Nagata A. K. 2007; Molecular and biological characterization of Tomato chlorotic mottle virus suggests that recombination underlies the evolution and diversity of Brazilian tomato begomoviruses. Phytopathology 97:702–711 [View Article][PubMed]
     [Google Scholar]
  62. Rocha C. S., Castillo-Urquiza G. P., Lima A. T. M., Silva F. N., Xavier C. A. D., Hora-Júnior B. T., Beserra-Júnior J. E. A., Malta A. W. O., Martin D. P. other authors 2013; Brazilian begomovirus populations are highly recombinant, rapidly evolving, and segregated based on geographical location. J Virol 87:5784–5799 [View Article][PubMed]
     [Google Scholar]
  63. 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 [View Article][PubMed]
     [Google Scholar]
  64. Rokyta D. R., Wichman H. A. 2009; Genic incompatibilities in two hybrid bacteriophages. Mol Biol Evol 26:2831–2839 [View Article][PubMed]
     [Google Scholar]
  65. 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 [View Article][PubMed]
     [Google Scholar]
  66. 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 [View Article][PubMed]
     [Google Scholar]
  67. 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 [View Article][PubMed]
     [Google Scholar]
  68. Scheffler K., Martin D. P., Seoighe C. 2006; Robust inference of positive selection from recombining coding sequences. Bioinformatics 22:2493–2499 [View Article][PubMed]
     [Google Scholar]
  69. 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]
  70. Silva S. J. C., 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. 2012; Species diversity, phylogeny and genetic variability of begomovirus populations infecting leguminous weeds in northeastern Brazil. Plant Pathol 61:457–467 [View Article]
     [Google Scholar]
  71. Simon-Loriere E., Galetto R., Hamoudi M., Archer J., Lefeuvre P., Martin D. P., Robertson D. L., Negroni M. 2009; Molecular mechanisms of recombination restriction in the envelope gene of the Human immunodeficiency virus . PLoS Pathog 5:e1000418 [View Article]
     [Google Scholar]
  72. 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 [View Article][PubMed]
     [Google Scholar]
  73. Stamatakis A. 2006; RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690 [CrossRef]
     [Google Scholar]
  74. Tavares S. S., Ramos-Sobrinho R., Gonzalez-Aguilera J., Lima G. S. A., Assunção I. P., Zerbini F. M. 2012; Further molecular characterization of weed-associated begomoviruses in Brazil with an emphasis on Sida spp. Planta Daninha 30:305–315 [View Article]
     [Google Scholar]
  75. 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 [View Article][PubMed]
     [Google Scholar]
  76. Umaharan P., Padidam M., Phelps R. H., Beachy R. N., Fauquet C. M. 1998; Distribution and diversity of geminiviruses in Trinidad and Tobago. Phytopathology 88:1262–1268 [View Article][PubMed]
     [Google Scholar]
  77. Varma A., Malathi V. G. 2003; Emerging geminivirus problems: a serious threat to crop production. Ann Appl Biol 142:145–164 [View Article]
     [Google Scholar]
  78. Varsani A., Navas-Castillo J., Moriones E., Hernández-Zepeda C., Idris A., Brown J. K., Zerbini F. M., Martin D. P. 2014; Establishment of three new genera in the family Geminiviridae: Becurtovirus, Eragrovirus and Turncurtovirus. . Arch Virol 159: [Epub ahead of print] [View Article][PubMed]
     [Google Scholar]
  79. Wright S. 1949; The genetical structure of populations. Ann Eugen 15:323–354 [View Article][PubMed]
     [Google Scholar]
  80. 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 [View Article][PubMed]
     [Google Scholar]
  81. Wyant P. S., Strohmeier S., Schäfer B., Krenz B., Assunção I. P., Lima G. S. D., Jeske H. 2012; Circular DNA genomics (circomics) exemplified for geminiviruses in bean crops and weeds of northeastern Brazil. Virology 427:151–157 [View Article][PubMed]
     [Google Scholar]
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Contrasting genetic structure between two begomoviruses infecting the same leguminous hosts
J. Gen. Virol. 95, 2540 (2014); https://doi.org/10.1099/vir.0.067009-0
/content/journal/jgv/10.1099/vir.0.067009-0
/content/journal/jgv/10.1099/vir.0.067009-0
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