1887

Abstract

Maize streak virus (MSV), which causes maize streak disease (MSD), is one of the most serious biotic threats to African food security. Here, we use whole MSV genomes sampled over 30 years to estimate the dates of key evolutionary events in the 500 year association of MSV and maize. The substitution rates implied by our analyses agree closely with those estimated previously in controlled MSV evolution experiments, and we use them to infer the date when the maize-adapted strain, MSV-A, was generated by recombination between two grass-adapted MSV strains. Our results indicate that this recombination event occurred in the mid-1800s, ∼20 years before the first credible reports of MSD in South Africa and centuries after the introduction of maize to the continent in the early 1500s. This suggests a causal link between MSV recombination and the emergence of MSV-A as a serious pathogen of maize.

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2009-12-01
2024-03-29
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References

  1. Briddon R. W., Lunness P., Chamberlin L. C., Markham P. G. 1994; Analysis of the genetic variability of maize streak virus. Virus Genes 9:93–100 [CrossRef]
    [Google Scholar]
  2. Damsteegt V. D. 1983; Maize streak virus: I. Host range and vulnerability of maize germ plasm. Plant Dis 67:734–737 [CrossRef]
    [Google Scholar]
  3. Drummond A. J., Rambaut A. 2007; beast: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214 [CrossRef]
    [Google Scholar]
  4. Drummond A. J., Ho S. Y., Phillips M. J., Rambaut A. 2006; Relaxed phylogenetics and dating with confidence. PLoS Biol 4:e88 [CrossRef]
    [Google Scholar]
  5. 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 (TYLCV). J Virol 82:957–965 [CrossRef]
    [Google Scholar]
  6. 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]
    [Google Scholar]
  7. Fargette D., Pinel-Galzi A., Sérémé D., Lacombe S., Hébrard E., Traoré O., Konaté G. 2008; Diversification of rice yellow mottle virus and related viruses spans the history of agriculture from the neolithic to the present. PLoS Pathog 4:e1000125 [CrossRef]
    [Google Scholar]
  8. Fondong V. N., Pita J. S., Rey M. E., 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
    [Google Scholar]
  9. Fuller C. 1901 Mealie Variegation. First Report of the Government Entomologist, 1899–1900 Pietermaritzburg, Natal: P. Davis & Sons, Government Printers;
    [Google Scholar]
  10. García-Andrés S., Tomas D. M., Sanchez-Campos S., Navas-Castillo J., Moriones E. 2007a; Frequent occurrence of recombinants in mixed infections of tomato yellow leaf curl disease-associated begomoviruses. Virology 365:210–219 [CrossRef]
    [Google Scholar]
  11. García-Andrés S., Accotto G. P., Navas-Castillo J., Moriones E. 2007b; 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]
    [Google Scholar]
  12. 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 [CrossRef]
    [Google Scholar]
  13. Gibbs A. J., Ohshima K., Phillips M. J., Gibbs M. J. 2008; The prehistory of potyviruses: their initial radiation was during the dawn of agriculture. PLoS One 3:e2523 [CrossRef]
    [Google Scholar]
  14. Grasso C., Lee C. 2004; Combining partial order alignment and progressive multiple sequence alignment increases alignment speed and scalability to very large alignment problems. Bioinformatics 20:1546–1556 [CrossRef]
    [Google Scholar]
  15. Harkins G. W., Delport W., Duffy S., Wood N., Monjane A. L., Owor B. E., Donaldson L., Saumtally S., Triton G. other authors 2009; Experimental evidence indicating that mastreviruses probably did not co-diverge with their hosts. Virol J 6:104 [CrossRef]
    [Google Scholar]
  16. 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 [CrossRef]
    [Google Scholar]
  17. Hughes F. L., Rybicki E. P., von Wechmar M. B. 1992; Genome typing of southern African subgroup 1 geminiviruses. J Gen Virol 73:1031–1040 [CrossRef]
    [Google Scholar]
  18. ICTVdB Management 2006; 00.029.0.01.001. Maize streak virus. In ICTVdB – The Universal Virus Database, version 4Edited by Büchen-Osmond. http://www.ncbi.nlm.nih.gov/ICTVdb/ICTVdB/
    [Google Scholar]
  19. 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
    [Google Scholar]
  20. Kass R. E., Raftery A. E. 1995; Bayes Factors. J Am Stat Assoc 90:773–795 [CrossRef]
    [Google Scholar]
  21. Konate G., Traore O. 1992; Reservoir hosts of maize streak virus (MSV) in the Sudan Sahel zone: identification and spatio temporal distribution. Phytoprotection 73:111–117 [CrossRef]
    [Google Scholar]
  22. Kopp A. 1930; Les maladies des plantes à La Réunion. Rev Bot Appl Agric Trop 105:1–7 (in French
    [Google Scholar]
  23. Kopp A., d'Emmerez de Charmoy D. 1931; Nouvelles constatations sur les maladies à virus de la canne à sucre et du maïs. C R Acad Sciences 193:876–878 (in French
    [Google Scholar]
  24. Kopp A., d'Emmerez de Charmoy D. 1932; Observations nouvelles concernant la mosaïque de la canne à sucre et le streak du maïs à la Réunion. Station Agronomique Réunion. Travaux Techniques 3:1–10 (in French
    [Google Scholar]
  25. 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]
    [Google Scholar]
  26. Martin D. P., Rybicki E. P. 2002; Investigation of maize streak virus pathogenicity determinants using chimaeric genomes. Virology 300:180–188 [CrossRef]
    [Google Scholar]
  27. Martin D. P., Shepherd D. N. 2009; The epidemiology, economic impact and control of maize streak disease. Food Security 1:305–315 [CrossRef]
    [Google Scholar]
  28. 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 [CrossRef]
    [Google Scholar]
  29. 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 [CrossRef]
    [Google Scholar]
  30. 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]
    [Google Scholar]
  31. McCann J. 2001; Maize and grace: history, corn, and Africa's new landscapes, 1500–1999. Comp Stud Soc Hist 43:246–272 [CrossRef]
    [Google Scholar]
  32. 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]
    [Google Scholar]
  33. 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 [CrossRef]
    [Google Scholar]
  34. 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 φ 29 DNA polymerase for large-scale field sampling and cloning of complete maize streak virus genomes. J Virol Methods 140:100–105 [CrossRef]
    [Google Scholar]
  35. 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
    [Google Scholar]
  36. Rybicki E. P., Dennis S., Napier G., Hughes F. L. 1998; Novel grass and wheat strains of maize streak virus detected by DNA amplification and sequencing. Mol Plant Pathol On-Line. http://www.bspp.org.uk/mppol/1998/0929rybicki/
  37. Schierup M. H., Hein J. 2000; Recombination and the molecular clock. Mol Biol Evol 17:1578–1579 [CrossRef]
    [Google Scholar]
  38. Schnippenkoetter W. H., Martin D. P., Hughes F., Fyvie M., Willment J. A., James D., von Wechmar B., Rybicki E. P. 2001; The biological and genomic characterisation of three mastreviruses. Arch Virol 146:1075–1088 [CrossRef]
    [Google Scholar]
  39. Shepherd D. N., Martin D. P., McGivern D. R., Boulton M. I., Thomson J. A., Rybicki E. P. 2005; A three-nucleotide mutation altering the maize streak virus Rep pRBR-interaction motif reduces symptom severity in maize and partially reverts at high frequency without restoring pRBR-Rep binding. J Gen Virol 86:803–813 [CrossRef]
    [Google Scholar]
  40. Shepherd D. N., Martin D. P., Varsani A., Thomson J. A., Rybicki E. P., Klump H. H. 2006; Restoration of native folding of single-stranded DNA sequences through reverse mutations: an indication of a new epigenetic mechanism. Arch Biochem Biophys 453:108–122 [CrossRef]
    [Google Scholar]
  41. Shepherd D. N., Martin D. P., Lefeuvre P., Monjane A. L., Owor B. E., Rybicki E. P., Varsani A. 2008; A protocol for the rapid isolation of full geminivirus genomes from dried plant tissue. J Virol Methods 149:97–102 [CrossRef]
    [Google Scholar]
  42. Suchard M. A., Weiss R. E., Sinsheimer J. S. 2001; Bayesian selection of continuous-time Markov chain evolutionary models. Mol Biol Evol 18:1001–1013 [CrossRef]
    [Google Scholar]
  43. Tamura K., Dudley J., Nei M., Kumar S. 2007; mega4: Molecular Evolutionary Genetics Analysis (mega) software version 4.0. Mol Biol Evol 24:1596–1599 [CrossRef]
    [Google Scholar]
  44. Tee K. K., Pybus O. G., Parker J., Ng K. P., Kamarulzaman A., Takebe Y. 2009; Estimating the date of origin of an HIV-1 circulating recombinant form. Virology 387:229–234 [CrossRef]
    [Google Scholar]
  45. Urbino C., Thébaud G., Granier M., Blanc S., Peterschmitt M. 2008; A novel cloning strategy for isolating, genotyping and phenotyping genetic variants of geminiviruses. Virol J 5:135 [CrossRef]
    [Google Scholar]
  46. van der Walt E., Palmer K. E., Martin D. P., Rybicki E. P. 2008a; Viable chimaeric viruses confirm the biological importance of sequence specific maize streak virus movement protein and coat protein interactions. Virol J 5:61 [CrossRef]
    [Google Scholar]
  47. van der Walt E., Martin D. P., Varsani A., Polston J. E., Rybicki E. P. 2008b; Experimental observations of rapid maize streak virus evolution reveal a strand-specific nucleotide substitution bias. Virol J 5:104 [CrossRef]
    [Google Scholar]
  48. van der Walt E., Rybicki E. P., Varsani A., Polston J. E., Billharz R., Donaldson L., Monjane A. L., Martin D. P. 2009; Rapid host adaptation by extensive recombination. J Gen Virol 90:734–746 [CrossRef]
    [Google Scholar]
  49. 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 2008; 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 [CrossRef]
    [Google Scholar]
  50. Willment 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 [CrossRef]
    [Google Scholar]
  51. Willment 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 [CrossRef]
    [Google Scholar]
  52. Wu B., Melcher U., Guo X., Wang X., Fan L., Zhou G. 2008; Assessment of codivergence of Mastreviruses with their plant hosts. BMC Evol Biol 8:335 [CrossRef]
    [Google Scholar]
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