1887

Abstract

Maize streak virus (MSV; family , genus ), the causal agent of maize streak disease, ranks amongst the most serious biological threats to food security in subSaharan Africa. Although five distinct MSV strains have been currently described, only one of these – MSV-A – causes severe disease in maize. Due primarily to their not being an obvious threat to agriculture, very little is known about the ‘grass-adapted’ MSV strains, MSV-B, -C, -D and -E. Since comparing the genetic diversities, geographical distributions and natural host ranges of MSV-A with the other MSV strains could provide valuable information on the epidemiology, evolution and emergence of MSV-A, we carried out a phylogeographical analysis of MSVs found in uncultivated indigenous African grasses. Amongst the 83 new MSV genomes presented here, we report the discovery of six new MSV strains (MSV-F to -K). The non-random recombination breakpoint distributions detectable with these and other available mastrevirus sequences partially mirror those seen in begomoviruses, implying that the forces shaping these breakpoint patterns have been largely conserved since the earliest geminivirus ancestors. We present evidence that the ancestor of all MSV-A variants was the recombinant progeny of ancestral MSV-B and MSV-G/-F variants. While it remains unknown whether recombination influenced the emergence of MSV-A in maize, our discovery that MSV-A variants may both move between and become established in different regions of Africa with greater ease, and infect more grass species than other MSV strains, goes some way towards explaining why MSV-A is such a successful maize pathogen.

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2008-09-01
2024-03-28
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References

  1. Awadalla P. 2003; The evolutionary genomics of pathogen recombination. Nat Rev Genet 4:50–60 [CrossRef]
    [Google Scholar]
  2. Bigarré L., Salah M., Granier M., Frutos R., Thouvenel J. C., Peterschmitt M. 1999; Nucleotide sequence evidence for three distinct sugarcane streak mastreviruses. Arch Virol 144:2331–2344 [CrossRef]
    [Google Scholar]
  3. Boni M. F., Posada D., Feldman M. W. 2007; An exact nonparametric method for inferring mosaic structure in sequence triplets. Genetics 176:1035–1047
    [Google Scholar]
  4. Bosque-Perez N. A. 2000; Eight decades of maize streak virus research. Virus Res 71:107–121 [CrossRef]
    [Google Scholar]
  5. Briddon R. W., Lunness P., Chamberlin L. C., Pinner M. S., Brundish H., Markham P. G. 1992; The nucleotide sequence of an infectious insect-transmissible clone of the geminivirus Panicum streak virus . J Gen Virol 73:1041–1047 [CrossRef]
    [Google Scholar]
  6. 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]
  7. 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]
    [Google Scholar]
  8. Clarke B. A., Rybicki E. P., Hughes F. L., Kirby R., von Wechmar M. B. 1989; Characterization of southern African isolates of Maize streak virus – typing of 3 isolates by restriction mapping. Intervirology 30:86–95
    [Google Scholar]
  9. Dekker E. L., Pinner M. S., Markham P. G., van Regenmortel M. H. V. 1988; Characterization of maize streak virus isolates from different plant species by polyclonal and monoclonal antibodies. J Gen Virol 69:983–990 [CrossRef]
    [Google Scholar]
  10. Delatte H., Martin D. P., Naze F., Goldbach R., Reynaud B., Peterschmitt M., Lett J. M. 2005; South West Indian Ocean islands tomato begomovirus populations represent a new major monopartite begomovirus group. J Gen Virol 86:1533–1542 [CrossRef]
    [Google Scholar]
  11. 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]
  12. 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]
  13. 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]
  14. Gibbs M. J., Armstrong J. S., Gibbs A. J. 2000; Sister-Scanning: a Monte Carlo procedure for assessing signals in recombinant sequences. Bioinformatics 16:573–582 [CrossRef]
    [Google Scholar]
  15. Giussani L. M., Cota-Sanchez J. H., Zuloaga F. O., Kellogg E. A. 2001; A molecular phylogeny of the grass subfamily Panicoideae ( Poaceae ) shows multiple origins of C4 photosynthesis. Am J Bot 88:1993–2012 [CrossRef]
    [Google Scholar]
  16. 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]
  17. Guindon S., Gascuel O. 2003; A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704 [CrossRef]
    [Google Scholar]
  18. 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]
  19. Hughes F. L., Rybicki E. P., Kirby R. 1993; Complete nucleotide sequence of sugarcane streak Monogeminivirus . Arch Virol 132:171–182 [CrossRef]
    [Google Scholar]
  20. 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 [CrossRef]
    [Google Scholar]
  21. Lefeuvre P., Martin D. P., Hoareau M., Naze F., Delatte H., Thierry M., Varsani A., Becker N., Reynaud B., Lett J. M. 2007a; Begomovirus ‘melting pot’ in the south-west Indian Ocean islands: molecular diversity and evolution through recombination. J Gen Virol 88:3458–3468 [CrossRef]
    [Google Scholar]
  22. Lefeuvre P., Lett J. M., Reynaud B., Martin D. P. 2007b; Avoidance of protein fold disruption in natural virus recombinants. PLoS Pathog 3:e181 [CrossRef]
    [Google Scholar]
  23. Martin D., Rybicki E. 2000; RDP: detection of recombination amongst aligned sequences. Bioinformatics 16:562–563 [CrossRef]
    [Google Scholar]
  24. Martin D. P., Rybicki E. P. 2002; Investigation of Maize streak virus pathogenicity determinants using chimaeric genomes. Virology 300:180–188 [CrossRef]
    [Google Scholar]
  25. 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]
  26. 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]
  27. Martin D. P., Posada D., Crandall K. A., Williamson C. 2005a; A modified bootscan algorithm for automated identification of recombinant sequences and recombination breakpoints. AIDS Res Hum Retroviruses 21:98–102 [CrossRef]
    [Google Scholar]
  28. Martin D. P., Williamson C., Posada D. 2005b; RDP2: recombination detection and analysis from sequence alignments. Bioinformatics 21:260–262 [CrossRef]
    [Google Scholar]
  29. Martin D. P., van der Walt E., Posada D., Rybicki E. P. 2005c; The evolutionary value of recombination is constrained by genome modularity. PLoS Genet 1:e51 [CrossRef]
    [Google Scholar]
  30. McClean A. P. D. 1947 Some Forms of Streak Virus Occurring in Maize, Sugar-Cane and Wild Grasses Pretoria: South Africa Government Printers;
    [Google Scholar]
  31. Mesfin T., den Hollander J., Markham P. G. 1991; Cicadulina species and maize streak virus in Ethiopia. Trop Pest Manage 37:240–244 [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. 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]
    [Google Scholar]
  34. Olmstead R. G., Sweere J. A. 1994; Combining data in phylogenetic systematics: an empirical approach using three molecular data sets in the Solanaceae . Syst Biol 43:467–481 [CrossRef]
    [Google Scholar]
  35. Oluwafemi S., Varsani A., Monjane A. L., Shepherd D. N., Owor B. E., Rybicki E. P., Martin D. P. 2008; A new African streak virus species from Nigeria. Arch Virol 153:1407–1410 [CrossRef]
    [Google Scholar]
  36. Owor B. E., Shepherd D. N., Taylor N. J., Edema R., Monjane A. L., Thomson J. A., Martin D. P., Varsani A. 2007a; Successful application of FTA classic card technology and use of bacteriophage phi29 DNA polymerase for large-scale field sampling and cloning of complete maize streak virus genomes. J Virol Methods 140:100–105 [CrossRef]
    [Google Scholar]
  37. Owor B. E., Martin D. P., Shepherd D. N., Edema R., Monjane A. L., Rybicki E. P., Thomson J. A., Varsani A. 2007b; 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]
  38. Padidam M., Sawyer S., Fauquet C. M. 1999; Possible emergence of new geminiviruses by frequent recombination. Virology 265:218–225 [CrossRef]
    [Google Scholar]
  39. Penny D., White W. T., Hendy M. D., Phillips M. J. 2007; A bias in ML estimates of branch lengths in the presence of multiple signals. Mol Biol Evol 25:239–242
    [Google Scholar]
  40. Peterschmitt M., Reynaud B., Sommermeyer G., Baudin P. 1991; Characterization of maize streak virus isolates using monoclonal and polyclonal antibodies and by transmission to a few hosts. Plant Dis 75:27–32 [CrossRef]
    [Google Scholar]
  41. Peterschmitt M., Granier M., Frutos R., Reynaud B. 1996; Infectivity and complete nucleotide sequence of the genome of a genetically distinct strain of maize streak virus from Réunion Island. Arch Virol 141:1637–1650 [CrossRef]
    [Google Scholar]
  42. Pinner M. S., Markham P. G. 1990; Serotyping and strain identification of maize streak virus isolates. J Gen Virol 71:1635–1640 [CrossRef]
    [Google Scholar]
  43. Pinner M. S., Markham P. G., Markham R. H., Dekker E. L. 1988; Characterisation of maize streak virus – description of strains – symptoms. Plant Pathol 37:74–87 [CrossRef]
    [Google Scholar]
  44. 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]
  45. Posada D. 2006; ModelTest Server: a web-based tool for the statistical selection of models of nucleotide substitution online. Nucleic Acids Res 34:W700–W703
    [Google Scholar]
  46. Posada D., Crandall K. A. 2001; Evaluation of methods for detecting recombination from DNA sequences: computer simulations. Proc Natl Acad Sci U S A 98:13757–13762 [CrossRef]
    [Google Scholar]
  47. Posada D., Crandall K. A. 2002; The effect of recombination on the accuracy of phylogeny estimation. J Mol Evol 54:396–402 [CrossRef]
    [Google Scholar]
  48. 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]
    [Google Scholar]
  49. 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]
  50. Shepherd D. N., Martin D. P., Lefeuvre P., Monjane A. L., Owor B. E., Rybicki E. P., Varsani A. 2008a; A protocol for the rapid isolation of full geminivirus genomes from dried plant tissue. J Virol Methods
    [Google Scholar]
  51. Shepherd D. N., Varsani A., Windram O., Lefeuvre P., Monjane A. L., Owor B., Martin D. P. 2008b; Novel sugarcane streak and sugarcane streak Réunion mastrevirus from southern Africa and La Réunion. Arch Virol 153:605–609 [CrossRef]
    [Google Scholar]
  52. Shung C. Y., Sunter J., Sirasanagandla S. S., Sunter G. 2006; Distinct viral sequence elements are necessary for expression of Tomato golden mosaic virus complementary sense transcripts that direct AL2 and AL3 gene expression. Mol Plant Microbe Interact 19:1394–1405 [CrossRef]
    [Google Scholar]
  53. Smith J. M. 1992; Analyzing the mosaic structure of genes. J Mol Evol 34:126–129
    [Google Scholar]
  54. Stanley J., Bisaro D. M., Briddon R. W., Brown J. K., Fauquet C. M., Harrison B. D., Rybicki E. P., Stenger D. C. 2005; Geminiviridae . In Virus Taxonomy, Eighth Report of the International Committee on the Taxonomy of Viruses pp 301–306Edited by Fauquet C. M., Mayo M. A., Maniloff J., Desselberger U., Ball L. A. London: Elsevier;
    [Google Scholar]
  55. Storey H. H., McClean A. P. D. 1930; The transmission of streak disease between maize, sugarcane and wild grasses. Ann Appl Biol 17:691–719 [CrossRef]
    [Google Scholar]
  56. 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]
  57. Thompson J. D., Higgins D. G., Gibson T. J. 1994; clustal w: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680 [CrossRef]
    [Google Scholar]
  58. van Antwerpen T., McFarlane S. S., Buchanan G. F., Shepherd D. N., Martin D. P., Rybicki E. P., Varsani A. 2008; First report of Maize streak virus field infection of sugarcane in South Africa. Plant Dis 92:982
    [Google Scholar]
  59. Varsani A., Oluwafemi S., Shepherd D. N., Monjane A. L., Owor B., Windram O., Rybicki E. P., Lefeuvre P., Martin D. P. 2008; Panicum streak virus diversity is similar to that observed for Maize streak virus . Arch Virol 153:601–604 [CrossRef]
    [Google Scholar]
  60. 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]
  61. 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]
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