1887

Abstract

The emergence of begomoviruses (whitefly-transmitted viruses classified in the genus Begomovirus, family Geminiviridae) in Brazil probably occurred by horizontal transfer from non-cultivated plants after the introduction of Bemisia tabaci MEAM1. The centre of diversity of Euphorbia heterophylla (Euphorbiaceae) is located in Brazil and Paraguay, where it is an invasive species in soybean and other crops. Reports of possible begomovirus infection of E. heterophylla in Brazil date back to the 1950s. In 2011, Euphorbia yellow mosaic virus (EuYMV) was described in symptomatic plants collected in the Brazilian state of Goiás. Here we assess the genetic variability and population structure of begomoviruses infecting E. heterophylla in samples collected throughout nine Brazilian states from 2009 to 2014. A total of 158 and 57 haplotypes were compared in DNA-A and DNA-B datasets, respectively. Analysis comparing population structure in a large sampled area enabled us to differentiate two subpopulations. Further, the application of discriminant analysis of principal components allowed the differentiation of six subpopulations according to sampling locations and in agreement with phylogenetic analysis. In general, negative selection was predominant in all six subpopulations. Interestingly, we were able to reconstruct the phylogeny based on the information from the 23 sites that contributed most to the geographical structure proposed, demonstrating that these polymorphisms hold supporting information to discriminate between subpopulations. These sites were mapped in the genome and compared at the level of amino acid changes, providing insights into how genetic drift and selection contribute to maintain the patterns of begomovirus population variability from a geographical structuring point of view.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.000784
2017-06-13
2019-10-14
Loading full text...

Full text loading...

/deliver/fulltext/jgv/98/6/1537.html?itemId=/content/journal/jgv/10.1099/jgv.0.000784&mimeType=html&fmt=ahah

References

  1. Zerbini FM, Briddon RW, Idris A, Martin DP, Moriones E et al. ICTV Virus Taxonomy Profile: Geminiviridae. J Gen Virol 2017;98:131–133 [CrossRef][PubMed]
    [Google Scholar]
  2. Harrison BD, Robinson DJ. Natural genomic and antigenic variation in white-fly transmitted geminiviruses (begomoviruses). Annu Rev Phytopathol 1999;39:369–398[CrossRef]
    [Google Scholar]
  3. Rojas MR, Hagen C, Lucas WJ, Gilbertson RL. Exploiting chinks in the plant's armor: evolution and emergence of geminiviruses. Annu Rev Phytopathol 2005;43:361–394 [CrossRef][PubMed]
    [Google Scholar]
  4. Duffy S, Holmes EC. Phylogenetic evidence for rapid rates of molecular evolution in the single-stranded DNA begomovirus Tomato yellow leaf curl virus. J Virol 2008;82:957–965 [CrossRef][PubMed]
    [Google Scholar]
  5. Duffy S, Holmes EC. Validation of high rates of nucleotide substitution in geminiviruses: phylogenetic evidence from East African cassava mosaic viruses. J Gen Virol 2009;90:1539–1547 [CrossRef][PubMed]
    [Google Scholar]
  6. Padidam M, Sawyer S, Fauquet CM. Possible emergence of new geminiviruses by frequent recombination. Virology 1999;265:218–225 [CrossRef][PubMed]
    [Google Scholar]
  7. Andrade EC, Manhani GG, Alfenas PF, Calegario RF, Fontes EP et al. Tomato yellow spot virus, a tomato-infecting begomovirus from Brazil with a closer relationship to viruses from Sida sp., forms pseudorecombinants with begomoviruses from tomato but not from Sida. J Gen Virol 2006;87:3687–3696 [CrossRef][PubMed]
    [Google Scholar]
  8. Jones DR. Plant viruses transmitted by whiteflies. Eur J Plant Pathol 2003;109:195–219 [CrossRef]
    [Google Scholar]
  9. Dinsdale A, Cook L, Riginos C, Buckley YM, de Barro P. Refined global analysis of Bemisia tabaci (Hemiptera: Sternorrhyncha: Aleyrodoidea: Aleyrodidae) mitochondrial cytochrome oxidase 1 to identify species level genetic boundaries. Ann Entomol Soc Am 2010;103:196–208 [CrossRef]
    [Google Scholar]
  10. Navas-Castillo J, Fiallo-Olivé E, Sánchez-Campos S. Emerging virus diseases transmitted by whiteflies. Annu Rev Phytopathol 2011;49:219–248 [CrossRef][PubMed]
    [Google Scholar]
  11. Castillo-Urquiza GP, Beserra JE Jr, Bruckner FP, Lima AT, Varsani A et al. Six novel begomoviruses infecting tomato and associated weeds in Southeastern Brazil. Arch Virol 2008;153:1985–1989 [CrossRef][PubMed]
    [Google Scholar]
  12. Silva SJC, Castillo-Urquiza GP, Hora-Júnior BT, Assunção IP, Lima GSA et al. Species diversity, phylogeny and genetic variability of begomovirus populations infecting leguminous weeds in northeastern Brazil. Plant Pathol 2012;61:457–467 [CrossRef]
    [Google Scholar]
  13. Silva FN, Lima AT, Rocha CS, Castillo-Urquiza GP, Alves-Júnior M et al. Recombination and pseudorecombination driving the evolution of the begomoviruses Tomato severe rugose virus (ToSRV) and Tomato rugose mosaic virus (ToRMV): two recombinant DNA-A components sharing the same DNA-B. Virol J 2014;11:66 [CrossRef][PubMed]
    [Google Scholar]
  14. Pinto VB, Silva JP, Fiallo-Olivé E, Navas-Castillo J, Zerbini FM. Novel begomoviruses recovered from Pavonia sp. in Brazil. Arch Virol 2016;161:735–739 [CrossRef][PubMed]
    [Google Scholar]
  15. Fiallo-Olivé E, Zerbini FM, Navas-Castillo J. Complete nucleotide sequences of two new begomoviruses infecting the wild malvaceous plant Melochia sp. in Brazil. Arch Virol 2015;160:3161–3164 [CrossRef][PubMed]
    [Google Scholar]
  16. Awadalla P. The evolutionary genomics of pathogen recombination. Nat Rev Genet 2003;4:50–60 [CrossRef][PubMed]
    [Google Scholar]
  17. Sattar MN, Kvarnheden A, Saeed M, Briddon RW. Cotton leaf curl disease – an emerging threat to cotton production worldwide. J Gen Virol 2013;94:695–710 [CrossRef][PubMed]
    [Google Scholar]
  18. Lefeuvre P, Moriones E. Recombination as a motor of host switches and virus emergence: geminiviruses as case studies. Curr Opin Virol 2015;10:14–19 [CrossRef][PubMed]
    [Google Scholar]
  19. Wilson AK. Euphorbia heterophylla: a review of distribution, importance and control. Trop Pest Manag 1981;27:32–38 [CrossRef]
    [Google Scholar]
  20. Cronquist A. An Integrated System of Classification of Flowering Plants New York: Columbia University Press; 1981; p.1262
    [Google Scholar]
  21. Vidal RA, Winkler LM. Euphorbia heterophylla L. resistant to herbicide inhibitors of acetolactate synthase: II - Geographic distribution and genetic characterization of biotypes from Rio Grande do Sul plains. Rev Bras Agroc 2004;10:461–465
    [Google Scholar]
  22. Christoffoleti PJ. Aspectos Da Resistência De Plantas Daninhas a Herbicidas, 3rd ed. Piracicaba: HRAC-BR; 2008; p.120
    [Google Scholar]
  23. Costa AS, Bennett CW. Whitefly transmitted mosaic of Euphorbia prunifolia. Phytopathology 1950;40:266–283
    [Google Scholar]
  24. Fernandes FR, Albuquerque LC, de Oliveira CL, Cruz AR, da Rocha WB et al. Molecular and biological characterization of a new Brazilian begomovirus, euphorbia yellow mosaic virus (EuYMV), infecting Euphorbia heterophylla plants. Arch Virol 2011;156:2063–2069 [CrossRef][PubMed]
    [Google Scholar]
  25. Tavares SS, Ramos-Sobrinho R, González-Aguilera J, Lima GSA, Assunção IP et al. Further molecular characterization of weed-associated begomoviruses in Brazil with an emphasis on Sida spp. Planta Daninha 2012;30:305–315 [CrossRef]
    [Google Scholar]
  26. Barreto SS, Hallwass M, Aquino OM, Inoue-Nagata AK. A study of weeds as potential inoculum sources for a tomato-infecting begomovirus in central Brazil. Phytopathology 2013;103:436–444 [CrossRef][PubMed]
    [Google Scholar]
  27. Richter KS, Ende L, Jeske H. Rad54 is not essential for any geminiviral replication mode in planta. Plant Mol Biol 2015;87:193–202 [CrossRef][PubMed]
    [Google Scholar]
  28. Sottoriva LD, Lourenção AL, Colombo CA. Performance of Bemisia tabaci (Genn.) biotype B (Hemiptera: Aleyrodidae) on weeds. Neotrop Entomol 2014;43:574–581 [CrossRef][PubMed]
    [Google Scholar]
  29. Rocha CS, Castillo-Urquiza GP, Lima AT, Silva FN, Xavier CA et al. Brazilian begomovirus populations are highly recombinant, rapidly evolving, and segregated based on geographical location. J Virol 2013;87:5784–5799 [CrossRef][PubMed]
    [Google Scholar]
  30. Briddon RW, Patil BL, Bagewadi B, Nawaz-Ul-Rehman MS, Fauquet CM. Distinct evolutionary histories of the DNA-A and DNA-B components of bipartite begomoviruses. BMC Evol Biol 2010;10:97 [CrossRef][PubMed]
    [Google Scholar]
  31. Lima AT, Sobrinho RR, González-Aguilera J, Rocha CS, Silva SJ et al. Synonymous site variation due to recombination explains higher genetic variability in begomovirus populations infecting non-cultivated hosts. J Gen Virol 2013;94:418–431 [CrossRef][PubMed]
    [Google Scholar]
  32. Prasanna HC, Sinha DP, Verma A, Singh M, Singh B et al. The population genomics of begomoviruses: global scale population structure and gene flow. Virol J 2010;7:220 [CrossRef][PubMed]
    [Google Scholar]
  33. Jombart T, Devillard S, Balloux F. Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet 2010;11:94 [CrossRef][PubMed]
    [Google Scholar]
  34. Albuquerque LC, Varsani A, Fernandes FR, Pinheiro B, Martin DP et al. Further characterization of tomato-infecting begomoviruses in Brazil. Arch Virol 2012;157:747–752 [CrossRef][PubMed]
    [Google Scholar]
  35. Fernandes FR, Cruz AR, Faria JC, Zerbini FM, Aragão FJ. Three distinct begomoviruses associated with soybean in central Brazil. Arch Virol 2009;154:1567–1570 [CrossRef][PubMed]
    [Google Scholar]
  36. Sobrinho RR, Xavier CA, Pereira HM, Lima GS, Assunção IP et al. Contrasting genetic structure between two begomoviruses infecting the same leguminous hosts. J Gen Virol 2014;95:2540–2552 [CrossRef][PubMed]
    [Google Scholar]
  37. Idris AM, Mills-Lujan K, Martin K, Brown JK. Melon chlorotic leaf curl virus: characterization and differential reassortment with closest relatives reveal adaptive virulence in the squash leaf curl virus clade and host shifting by the host-restricted bean calico mosaic virus. J Virol 2008;82:1959–1967 [CrossRef][PubMed]
    [Google Scholar]
  38. Lefeuvre P, Lett JM, Varsani A, Martin DP. Widely conserved recombination patterns among single-stranded DNA viruses. J Virol 2009;83:2697–2707 [CrossRef][PubMed]
    [Google Scholar]
  39. Nouri S, Arevalo R, Falk BW, Groves RL. Genetic structure and molecular variability of Cucumber mosaic virus isolates in the United States. PLoS One 2014;9:e96582 [CrossRef][PubMed]
    [Google Scholar]
  40. García-Arenal F, Fraile A, Malpica JM. Variability and genetic structure of plant virus populations. Annu Rev Phytopathol 2001;39:157–186 [CrossRef][PubMed]
    [Google Scholar]
  41. González-Aguilera J, Tavares SS, Sobrinho RR, Xavier CAD, Dueñas-Hurtado F et al. Genetic structure of a brazilian population of the begomovirus Tomato severe rugose virus (ToSRV). Tropical Plant Pathology 2012;37:346–353 [CrossRef]
    [Google Scholar]
  42. Yang XL, Zhou MN, Qian YJ, Xie Y, Zhou XP. Molecular variability and evolution of a natural population of tomato yellow leaf curl virus in Shanghai, China. J Zhejiang Univ Sci B 2014;15:133–142 [CrossRef][PubMed]
    [Google Scholar]
  43. Acosta-Leal R, Duffy S, Xiong Z, Hammond RW, Elena SF. Advances in plant virus evolution: translating evolutionary insights into better disease management. Phytopathology 2011;101:1136–1148 [CrossRef][PubMed]
    [Google Scholar]
  44. Jombart T. adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 2008;24:1403–1405 [CrossRef][PubMed]
    [Google Scholar]
  45. Hadjistylli M, Roderick GK, Brown JK. Global population structure of a worldwide pest and virus vector: genetic diversity and population history of the Bemisia tabaci sibling species group. PLoS One 2016;11:e0165105 [CrossRef][PubMed]
    [Google Scholar]
  46. Dalmon A, Halkett F, Granier M, Delatte H, Peterschmitt M. Genetic structure of the invasive pest Bemisia tabaci: evidence of limited but persistent genetic differentiation in glasshouse populations. Heredity (Edinb) 2008;100:316–325 [CrossRef][PubMed]
    [Google Scholar]
  47. Tahiri A, Halkett F, Granier M, Gueguen G, Peterschmitt M. Evidence of gene flow between sympatric populations of the Middle East-Asia Minor 1 and Mediterranean putative species of Bemisia tabaci. Ecol Evol 2013;3:2619–2633 [CrossRef]
    [Google Scholar]
  48. De Barro PJ. Genetic structure of the whitefly Bemisia tabaci in the Asia–Pacific region revealed using microsatellite markers. Mol Ecol 2005;14:3695–3718 [CrossRef][PubMed]
    [Google Scholar]
  49. Marubayashi JM, Yuki VA, Rocha KCG, Mituti T, Pelegrinotti FM et al. At least two indigenous species of the Bemisia tabaci complex are present in Brazil. J Appl Entomol 2013;137:113–121 [CrossRef]
    [Google Scholar]
  50. da Fonseca Barbosa L, Yuki VA, Marubayashi JM, de Marchi BR, Perini FL et al. First report of Bemisia tabaci Mediterranean (Q biotype) species in Brazil. Pest Manag Sci 2015;71:501–504 [CrossRef][PubMed]
    [Google Scholar]
  51. Rodelo-Urrego M, Pagán I, González-Jara P, Betancourt M, Moreno-Letelier A et al. Landscape heterogeneity shapes host-parasite interactions and results in apparent plant-virus codivergence. Mol Ecol 2013;22:2325–2340 [CrossRef][PubMed]
    [Google Scholar]
  52. Rodelo-Urrego M, García-Arenal F, Pagán I. The effect of ecosystem biodiversity on virus genetic diversity depends on virus species: a study of chiltepin-infecting begomoviruses in Mexico. Virus Evol 2015;1:vev004 [CrossRef][PubMed]
    [Google Scholar]
  53. Doyle JJ, Doyle JL. A rapid DNA isolation procedure for small amounts of fresh leaf tissue. Phytochem Bull 1987;19:11–15
    [Google Scholar]
  54. Inoue-Nagata AK, Albuquerque LC, Rocha WB, Nagata T. A simple method for cloning the complete begomovirus genome using the bacteriophage phi29 DNA polymerase. J Virol Methods 2004;116:209–211 [CrossRef][PubMed]
    [Google Scholar]
  55. Brown JK, Zerbini FM, Navas-Castillo J, Moriones E, Ramos-Sobrinho R et al. Revision of Begomovirus taxonomy based on pairwise sequence comparisons. Arch Virol 2015;160:1593–1619 [CrossRef][PubMed]
    [Google Scholar]
  56. Muhire BM, Varsani A, Martin DP. SDT: a virus classification tool based on pairwise sequence alignment and identity calculation. PLoS One 2014;9:e108277 [CrossRef][PubMed]
    [Google Scholar]
  57. Edgar RC. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 2004;5:113 [CrossRef][PubMed]
    [Google Scholar]
  58. Martin DP, Murrell B, Golden M, Khoosal A, Muhire B. RDP4: detection and analysis of recombination patterns in virus genomes. Virus Evol 2015;1:vev003 [CrossRef][PubMed]
    [Google Scholar]
  59. Ronquist F, Huelsenbeck JP. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003;19:1572–1574 [CrossRef][PubMed]
    [Google Scholar]
  60. Nylander JAA. MrModeltest v2. Program distributed by the author Evolutionary Biology Centre Uppsala University: 2004
    [Google Scholar]
  61. Rozas J, Sánchez-Delbarrio JC, Messeguer X, Rozas R. DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 2003;19:2496–2497 [CrossRef][PubMed]
    [Google Scholar]
  62. Lima ATM, Silva JCF, Silva FN, Castillo-Urquiza GP, Silva FF et al. The diversification of begomovirus populations is predominantly driven by mutational dynamics. Virus Evol 2017;3:vex005 [CrossRef][PubMed]
    [Google Scholar]
  63. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR et al. 2013; Vegan: community Ecology Package. R package version 2.0-7. http://CRANR-projectorg/package=vegan [Accessed on May 22, 2017]
  64. Haubold B, Hudson RR. LIAN 3.0: detecting linkage disequilibrium in multilocus data. Linkage analysis. Bioinformatics 2000;16:847–849 [CrossRef][PubMed]
    [Google Scholar]
  65. Hubisz MJ, Falush D, Stephens M, Pritchard JK. Inferring weak population structure with the assistance of sample group information. Mol Ecol Resour 2009;9:1322–1332 [CrossRef][PubMed]
    [Google Scholar]
  66. Earl DA, Vonholdt BM. STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the evanno method. Conserv Genet Resour 2012;4:359–361 [CrossRef]
    [Google Scholar]
  67. Waniez P. Philcarto: histoire de vie d’un logiciel de cartographie. Eur J Geo 2010;497 [CrossRef]
    [Google Scholar]
  68. Weir BS. Genetic Data Analysis II: Methods for Discrete Population Genetic Data Sunderland, Massachusetts: Sinauer Associated Inc; 1996; p.445
    [Google Scholar]
  69. Excoffier L, Lischer HE. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 2010;10:564–567 [CrossRef][PubMed]
    [Google Scholar]
  70. Dupanloup I, Schneider S, Excoffier L. A simulated annealing approach to define the genetic structure of populations. Mol Ecol 2002;11:2571–2581 [CrossRef][PubMed]
    [Google Scholar]
  71. Delport W, Poon AF, Frost SD, Kosakovsky Pond SL. Datamonkey 2010: a suite of phylogenetic analysis tools for evolutionary biology. Bioinformatics 2010;26:2455–2457 [CrossRef][PubMed]
    [Google Scholar]
  72. Martin DP, Posada D, Crandall KA, Williamson C. A modified bootscan algorithm for automated identification of recombinant sequences and recombination breakpoints. AIDS Res Hum Retroviruses 2005;21:98–102 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.000784
Loading
/content/journal/jgv/10.1099/jgv.0.000784
Loading

Data & Media loading...

Supplementary File 1

PDF

Most Cited This Month

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