Skip to main content
Log in

Recombination patterns in dicot-infecting mastreviruses mirror those found in monocot-infecting mastreviruses

Archives of Virology Aims and scope Submit manuscript

Abstract

Recombination has profoundly shaped the evolution of viruses in the family Geminiviridae and has been studied extensively in the two best characterised geminivirus lineages: the dicotyledonous plant infecting begomoviruses and the monocotyledonous plant infecting mastreviruses. Here, we demonstrate that the sizes and distributions of recombination events detectable within the members of a third major geminivirus lineage—the dicotyledonous plant infecting mastreviruses—are very similar to those of the monocot-infecting mastreviruses. This suggests that, despite host range differences, very similar biochemical, ecological and evolutionary factors must underlie recombination patterns in the dicot- and monocot-infecting mastreviruses.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

References

  1. Beiko RG, Hamilton N (2006) Phylogenetic identification of lateral genetic transfer events. BMC Evol Biol 6:15

    Article  PubMed  Google Scholar 

  2. Boni MF, Posada D, Feldman MW (2007) An exact nonparametric method for inferring mosaic structure in sequence triplets. Genetics 176:1035–1047

    Article  PubMed  CAS  Google Scholar 

  3. Boulton MI, Pallaghy CK, Chatani M, Macfarlane S, Davies JW (1993) Replication of maize streak virus mutants in maize protoplasts—evidence for a movement protein. Virology 192:85–93

    Article  PubMed  CAS  Google Scholar 

  4. Boulton MI (2002) Functions and interactions of mastrevirus gene products. Physiol Mol Plant Pathol 60:243–255

    Article  CAS  Google Scholar 

  5. Bredell H, Martin DP, Van Harmelen J, Varsani A, Sheppard HW, Donovan R, Gray CM, Williamson C, Team HS (2007) HIV type 1 subtype C gag and nef diversity in southern Africa. Aids Res Hum Retrovir 23:477–481

    Article  PubMed  CAS  Google Scholar 

  6. Briddon RW, Heydarnejad J, Khosrowfar F, Massumi H, Martin DP, Varsani A (2010) Turnip curly top virus, a highly divergent geminivirus infecting turnip in Iran. Virus Res 152:169–175

    Article  PubMed  CAS  Google Scholar 

  7. Briddon RW, Martin DP, Owor BE, Donaldson L, Markham PG, Greber RS, Varsani A (2010) A novel species of mastrevirus (family Geminiviridae) isolated from Digitaria didactyla grass from Australia. Arch Virol 155:1529–1534

    Article  PubMed  CAS  Google Scholar 

  8. Collin S, FernandezLobato M, Gooding PS, Mullineaux PM, Fenoll C (1996) The two nonstructural proteins from wheat dwarf virus involved in viral gene expression and replication are retinoblastoma-binding proteins. Virology 219:324–329

    Article  PubMed  CAS  Google Scholar 

  9. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    Article  PubMed  CAS  Google Scholar 

  10. Farzadfar SH, Pourrahim R, Golnaraghi AR, Ahoonmanesh A (2008) PCR detection and partial molecular characterization of Chickpea chlorotic dwarf virus in naturally infected sugar beet plants in Iran. J Plant Pathol 90:247–251

    CAS  Google Scholar 

  11. Gibbs MJ, Armstrong JS, Gibbs AJ (2000) Sister-Scanning: a Monte Carlo procedure for assessing signals in recombinant sequences. Bioinformatics 16:573–582

    Article  PubMed  CAS  Google Scholar 

  12. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704

    Article  PubMed  Google Scholar 

  13. Hadfield J, Martin DP, Stainton D, Kraberger S, Owor BE, Shepherd DN, Lakay F, Markham PG, Greber RS, Briddon RW, Varsani A (2011) Bromus catharticus striate mosaic virus: a new mastrevirus infecting Bromus catharticus from Australia. Arch Virol

  14. Halley-Stott RP, Tanzer F, Martin DP, Rybicki EP (2007) The complete nucleotide sequence of a mild strain of Bean yellow dwarf virus. Arch Virol 152:1237–1240

    Article  PubMed  CAS  Google Scholar 

  15. Harkins GW, Martin DP, Duffy S, Monjane AL, Shepherd DN, Windram OP, Owor BE, Donaldson L, van Antwerpen T, Sayed RA, Flett B, Ramusi M, Rybicki EP, Peterschmitt M, Varsani A (2009) Dating the origins of the maize-adapted strain of maize streak virus, MSV-A. J Gen Virol 90:3066–3074

    Article  PubMed  CAS  Google Scholar 

  16. Heath L, van der Walt E, Varsani A, Martin DP (2006) Recombination patterns in aphthoviruses mirror those found in other picornaviruses. J Virol 80:11827–11832

    Article  PubMed  CAS  Google Scholar 

  17. Heyraud-Nitschke F, Schumacher S, Laufs J, Schaefer S, Schell J, Gronenborn B (1995) Determination of the origin cleavage and joining domain of geminivirus Rep proteins. Nucleic Acids Res 23:910–916

    Article  PubMed  CAS  Google Scholar 

  18. Horn NM, Reddy SV, Reddy DVR (1995) Assessment of Yield Losses Caused by Chickpea Chlorotic Dwarf Geminivirus in Chickpea (Cicer-Arietinum) in India. Eur J Plant Pathol 101:221–224

    Article  Google Scholar 

  19. Horn NM, Reddy SV, van den Heuvel JFM, Reddy DVR (1996) Survey of chickpea (Cicer arietinum L) for chickpea stunt disease and associated viruses in India and Pakistan. Plant Dis 80:286–290

    Article  Google Scholar 

  20. Horvath GV, Pettko-Szandtner A, Nikovics K, Bilgin M, Boulton M, Davies JW, Gutierrez C, Dudits D (1998) Prediction of functional regions of the maize streak virus replication-associated proteins by protein–protein interaction analysis. Plant Mol Biol 38:699–712

    Article  PubMed  CAS  Google Scholar 

  21. 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

    Article  PubMed  CAS  Google Scholar 

  22. Klute KA, Nadler SA, Stenger DC (1996) Horseradish curly top virus is a distinct subgroup II geminivirus species with rep and C4 genes derived from a subgroup III ancestor. J Gen Virol 77:1369–1378

    Article  PubMed  CAS  Google Scholar 

  23. Kreuze JF, Perez A, Untiveros M, Quispe D, Fuentes S, Barker I, Simon R (2009) Complete viral genome sequence and discovery of novel viruses by deep sequencing of small RNAs: A generic method for diagnosis, discovery and sequencing of viruses. Virology 388:1–7

    Article  PubMed  CAS  Google Scholar 

  24. Kumari SG, Makkouk KM, Loh MH, Negassi K, Tsegay S, Kidane R, Kibret A, Tesfatsion Y (2008) Viral diseases affecting chickpea crops in Eritrea. Phytopathol Mediterr 47:42–49

    CAS  Google Scholar 

  25. Lefeuvre P, Lett JM, Reynaud B, Martin DP (2007) Avoidance of protein fold disruption in natural virus recombinants. PLoS Pathog 3:1782–1789

    Article  CAS  Google Scholar 

  26. Lefeuvre P, Lett JM, Varsani A, Martin DP (2009) Widely conserved recombination patterns among single-stranded DNA viruses. J Virol 83:2697–2707

    Article  PubMed  CAS  Google Scholar 

  27. Lefeuvre P, Martin DP, Harkins G, Lemey P, Gray AJA, Meredith S, Lakay F, Monjane A, Lett JM, Varsani A, Heydarnejad J (2010) The spread of tomato yellow leaf curl virus from the Middle East to the World. PLoS Pathog 6:e1001164

    Article  PubMed  Google Scholar 

  28. Lemey P, Lott M, Martin DP, Moulton V (2009) Identifying recombinants in human and primate immunodeficiency virus sequence alignments using quartet scanning. BMC Bioinformatics 10:126

    Article  PubMed  Google Scholar 

  29. Liu L, van Tonder T, Pietersen G, Davies JW, Stanley J (1997) Molecular characterization of a subgroup I geminivirus from a legume in South Africa. J Gen Virol 78:2113–2117

    PubMed  CAS  Google Scholar 

  30. Liu L, Davies JW, Stanley J (1998) Mutational analysis of bean yellow dwarf virus, a geminivirus of the genus Mastrevirus that is adapted to dicotyledonous plants. J Gen Virol 79:2265–2274

    PubMed  CAS  Google Scholar 

  31. Liu L, Pinner MS, Davies JW, 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  CAS  Google Scholar 

  32. Makkouk KM, Dafalla G, Hussein M, Kumari SG (1995) The natural occurrence of chickpea chlorotic dwarf geminivirus in chickpea and Faba bean in the Sudan. J Phytopathol Phytopathologische Zeitschrift 143:465–466

    Article  Google Scholar 

  33. Makkouk KM, Bashir M, Jones RAC, Kumari SG (2001) Survey for viruses in lentil and chickpea crops in Pakistan. Zeitschrift Fur Pflanzenkrankheiten Und Pflanzenschutz J Plant Dis Protect 108:258–268

    CAS  Google Scholar 

  34. Makkouk KM, Kumari SG, Shahraeen N, Fazlali Y, Farzadfar S, Ghotbi T, Mansouri AR (2003) Identification and seasonal variation of viral diseases of chickpea and lentil in Iran. Zeitschrift Fur Pflanzenkrankheiten Und Pflanzenschutz J Plant Dis Protect 110:157–169

    Google Scholar 

  35. Martin D, Rybicki E (2000) RDP: detection of recombination amongst aligned sequences. Bioinformatics 16:562–563

    Article  PubMed  CAS  Google Scholar 

  36. Martin DP, Rybicki EP (2002) Investigation of Maize streak virus pathogenicity determinants using chimaeric genomes. Virology 300:180–188

    Article  PubMed  CAS  Google Scholar 

  37. Martin DP, Posada D, Crandall KA, Williamson C (2005) A modified bootscan algorithm for automated identification of recombinant sequences and recombination breakpoints. Aids Res Hum Retrovir 21:98–102

    Article  PubMed  CAS  Google Scholar 

  38. Martin DP, Williamson C, Posada D (2005) RDP2: recombination detection and analysis from sequence alignments. Bioinformatics 21:260–262

    Article  PubMed  CAS  Google Scholar 

  39. Martin DP, 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

    Article  PubMed  CAS  Google Scholar 

  40. Morris BAM, Richardson KA, Haley A, Zhan XC, Thomas JE (1992) The nucleotide-sequence of the infectious cloned DNA component of tobacco yellow dwarf virus reveals features of geminiviruses infecting monocotyledonous plants. Virology 187:633–642

    Article  PubMed  CAS  Google Scholar 

  41. Nahid N, Amin I, Mansoor S, Rybicki EP, van der Walt E, Briddon RW (2008) Two dicot-infecting mastreviruses (family Geminiviridae) occur in Pakistan. Arch Virol 153:1441–1451

    Article  PubMed  CAS  Google Scholar 

  42. Owor BE, Martin DP, Shepherd DN, Edema R, Monjane AL, Rybicki EP, Thomson JA, Varsani A (2007) Genetic analysis of maize streak virus isolates from Uganda reveals widespread distribution of a recombinant variant. J Gen Virol 88:3154–3165

    Article  PubMed  CAS  Google Scholar 

  43. Padidam M, Sawyer S, Fauquet CM (1999) Possible emergence of new geminiviruses by frequent recombination. Virology 265:218–225

    Article  PubMed  CAS  Google Scholar 

  44. Pita JS, Fondong VN, Sangare A, Otim-Nape GW, Ogwal S, Fauquet CM (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  CAS  Google Scholar 

  45. Posada D, Crandall KA (2001) Evaluation of methods for detecting recombination from DNA sequences: computer simulations. Proc Natil Acad Sci USA 98:13757–13762

    Article  CAS  Google Scholar 

  46. Ramsell JNE, Lemmetty A, Jonasson J, Andersson A, Sigvald R, Kvarnheden A (2008) Sequence analyses of Wheat dwarf virus isolates from different hosts reveal low genetic diversity within the wheat strain. Plant Pathol 57:834–841

    Article  CAS  Google Scholar 

  47. Schalk HJ, Matzeit V, Schiller B, Schell J, Gronenborn B (1989) Wheat dwarf virus, a geminivirus of graminaceous plants needs splicing for replication. EMBO J 8:359–364

    PubMed  CAS  Google Scholar 

  48. Schwinghamer MW, Thomas JE, Schilg MA, Parry JN, Dann EK, Moore KJ, Kumari SG (2010) Mastreviruses in chickpea (Cicer arietinum) and other dicotyledonous crops and weeds in Queensland and northern New South Wales, Australia. Australas Plant Pathol 39:551–561

    Article  Google Scholar 

  49. Shepherd DN, Martin DP, McGivern DR, Boulton MI, Thomson JA, Rybicki EP (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

    Article  PubMed  CAS  Google Scholar 

  50. Smith JM (1992) Analyzing the mosaic structure of genes. J Mol Evol 34:126–129

    PubMed  CAS  Google Scholar 

  51. Thomas JE, Parry JN, Schwinghamer MW, Dann EK (2010) Two novel mastreviruses from chickpea (Cicer arietinum) in Australia. Arch Virol 155:1777–1788

    Article  PubMed  CAS  Google Scholar 

  52. van der Walt E, Rybicki EP, Varsani A, Polston JE, Billharz R, Donaldson L, Monjane AL, Martin DP (2009) Rapid host adaptation by extensive recombination. J Gen Virol 90:734–746

    Article  PubMed  Google Scholar 

  53. Varsani A, Oluwafemi S, Windram OP, Shepherd DN, Monjane AL, Owor BE, Rybicki EP, Lefeuvre P, Martin DP (2008) Panicum streak virus diversity is similar to that observed for maize streak virus. Arch Virol 153:601–604

    Article  PubMed  CAS  Google Scholar 

  54. Varsani A, Shepherd DN, Monjane AL, Owor BE, Erdmann JB, Rybicki EP, Peterschmitt M, Briddon RW, Markham PG, Oluwafemi S, Windram OP, Lefeuvre P, Lett JM, Martin DP (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

    Article  PubMed  CAS  Google Scholar 

  55. Varsani A, Monjane AL, Donaldson L, Oluwafemi S, Zinga I, Komba EK, Plakoutene D, Mandakombo N, Mboukoulida J, Semballa S, Briddon RW, Markham PG, Lett JM, Lefeuvre P, Rybicki EP, Martin DP (2009) Comparative analysis of Panicum streak virus and Maize streak virus diversity, recombination patterns and phylogeography. Virol J 6:194

    Article  PubMed  Google Scholar 

  56. Varsani A, Shepherd DN, Dent K, Monjane AL, Rybicki EP, Martin DP (2009) A highly divergent South African geminivirus species illuminates the ancient evolutionary history of this family. Virol J 6:36

    Article  PubMed  Google Scholar 

  57. Weiller GF (1998) Phylogenetic profiles: a graphical method for detecting genetic recombinations in homologous sequences. Mol Biol Evol 15:326–335

    PubMed  CAS  Google Scholar 

  58. Xie Q, Suarezlopez P, Gutierrez C (1995) Identification and analysis of a retinoblastoma binding motif in the replication protein of a plant DNA virus—requirement for efficient viral-DNA replication. EMBO J 14:4073–4082

    PubMed  CAS  Google Scholar 

  59. Zhou XP, Liu YL, Calvert L, Munoz C, OtimNape GW, Robinson DJ, Harrison BD (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  CAS  Google Scholar 

Download references

Acknowledgments

AV is funded by the Marsden fund of New Zealand. R.W.B. is supported by the Higher Education Commission (HEC), Government of Pakistan, under the “Foreign Faculty Hiring Program”.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Arvind Varsani.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Martin, D.P., Briddon, R.W. & Varsani, A. Recombination patterns in dicot-infecting mastreviruses mirror those found in monocot-infecting mastreviruses. Arch Virol 156, 1463–1469 (2011). https://doi.org/10.1007/s00705-011-0994-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00705-011-0994-z

Keywords

Navigation