1887

Abstract

The recent identification of a new nanovirus, pea necrotic yellow dwarf virus, from pea in Germany prompted us to survey wild and cultivated legumes for nanovirus infections in several European countries. This led to the identification of two new nanoviruses: black medic leaf roll virus (BMLRV) and pea yellow stunt virus (PYSV), each considered a putative new species. The complete genomes of a PYSV isolate from Austria and three BMLRV isolates from Austria, Azerbaijan and Sweden were sequenced. In addition, the genomes of five isolates of faba bean necrotic yellows virus (FBNYV) from Azerbaijan and Spain and those of four faba bean necrotic stunt virus (FBNSV) isolates from Azerbaijan were completely sequenced, leading to the first identification of FBNSV occurring in Europe. Sequence analyses uncovered evolutionary relationships, extensive reassortment and potential remnants of mixed nanovirus infections, as well as intra- and intercomponent recombination events within the nanovirus genomes. In some virus isolates, diverse types of the same genome component (paralogues) were observed, a type of genome complexity not described previously for any member of the family . Moreover, infectious and aphid-transmissible nanoviruses from cloned genomic DNAs of FBNYV and BMLRV were reconstituted that, for the first time, allow experimental reassortments for studying the genome functions and evolution of these nanoviruses.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.063115-0
2014-05-01
2021-08-06
Loading full text...

Full text loading...

/deliver/fulltext/jgv/95/5/1178.html?itemId=/content/journal/jgv/10.1099/vir.0.063115-0&mimeType=html&fmt=ahah

References

  1. Abraham A. D., Menzel W., Lesemann D. E., Varrelmann M., Vetten H. J. 2006; Chickpea chlorotic stunt virus: a new polerovirus infecting cool-season food legumes in Ethiopia. Phytopathology 96:437–446 [View Article][PubMed]
    [Google Scholar]
  2. Abraham A. D., Bencharki B., Torok V., Katul L., Varrelmann M., Josef Vetten H. 2010; Two distinct nanovirus species infecting faba bean in Morocco. Arch Virol 155:37–46 [View Article][PubMed]
    [Google Scholar]
  3. Abraham A. D., Varrelmann M., Vetten H. J. 2012; Three distinct nanoviruses, one of which represents a new species, infect faba bean in Ethiopia. Plant Dis 96:1045–1053 [View Article]
    [Google Scholar]
  4. Alberter B., Ali Rezaian M., Jeske H. 2005; Replicative intermediates of Tomato leaf curl virus and its satellite DNAs. Virology 331:441–448 [View Article][PubMed]
    [Google Scholar]
  5. Babín M., Ortiz V., Castro S., Romero J. 2000; First detection of faba bean necrotic yellows virus in Spain. Plant Dis 84:707 [View Article]
    [Google Scholar]
  6. Briddon R. W., Patil B. L., Bagewadi B., Nawaz-ul-Rehman M. S., Fauquet C. M. 2010; Distinct evolutionary histories of the DNA-A and DNA-B components of bipartite begomoviruses. BMC Evol Biol 10:97 [View Article][PubMed]
    [Google Scholar]
  7. Briddon R. W., Ghabrial S., Lin N.-S., Palukaitis P., Scholthof K.-B. G., Vetten H. J. 2012; Satellites and other virus-dependent nucleic acids. In Virus Taxonomy. Ninth Report of the International Committee on Taxonomy of Viruses pp. 1211–1219 Edited by King A. M. Q., Adams M. J., Carstens E. C., Lefkowitz E. J. London: Elsevier/Academic Press;
    [Google Scholar]
  8. Chakraborty S., Vanitharani R., Chattopadhyay B., Fauquet C. M. 2008; Supervirulent pseudorecombination and asymmetric synergism between genomic components of two distinct species of begomovirus associated with severe tomato leaf curl disease in India. J Gen Virol 89:818–828 [View Article][PubMed]
    [Google Scholar]
  9. Chen L. F., Rojas M., Kon T., Gamby K., Xoconostle-Cazares B., Gilbertson R. L. 2009; A severe symptom phenotype in tomato in Mali is caused by a reassortant between a novel recombinant begomovirus (Tomato yellow leaf curl Mali virus) and a betasatellite. Mol Plant Pathol 10:415–430 [View Article][PubMed]
    [Google Scholar]
  10. Chu P. W., Helms K. 1988; Novel virus-like particles containing circular single-stranded DNAs associated with subterranean clover stunt disease. Virology 167:38–49 [View Article][PubMed]
    [Google Scholar]
  11. Codoñer F. M., Elena S. F. 2008; The promiscuous evolutionary history of the family Bromoviridae. . J Gen Virol 89:1739–1747 [View Article][PubMed]
    [Google Scholar]
  12. Franz A., Makkouk K. M., Katul L., Vetten H. J. 1996; Monoclonal antibodies for the detection and differentiation of faba bean necrotic yellows virus isolates. Ann Appl Biol 128:255–268 [View Article]
    [Google Scholar]
  13. Grigoras I., Timchenko T., Katul L., Grande-Pérez A., Vetten H. J., Gronenborn B. 2009; Reconstitution of authentic nanovirus from multiple cloned DNAs. J Virol 83:10778–10787 [View Article][PubMed]
    [Google Scholar]
  14. Grigoras I., Gronenborn B., Vetten H. J. 2010a; First report of a nanovirus disease of pea in Germany. Plant Dis 94:642 [View Article]
    [Google Scholar]
  15. Grigoras I., Timchenko T., Grande-Pérez A., Katul L., Vetten H. J., Gronenborn B. 2010b; High variability and rapid evolution of a nanovirus. J Virol 84:9105–9117 [View Article][PubMed]
    [Google Scholar]
  16. Gu H., Zhang C., Ghabrial S. A. 2007; Novel naturally occurring bean pod mottle virus reassortants with mixed heterologous RNA1 genomes. Phytopathology 97:79–86 [View Article][PubMed]
    [Google Scholar]
  17. Guindon S., Dufayard J. F., Lefort V., Anisimova M., Hordijk W., Gascuel O. 2010; New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321 [View Article][PubMed]
    [Google Scholar]
  18. Horser C., Harding R., Dale J. 2001; Banana bunchy top nanovirus DNA-1 encodes the ‘master’ replication initiation protein. J Gen Virol 82:459–464[PubMed]
    [Google Scholar]
  19. Hu J. M., Fu H. C., Lin C. H., Su H. J., Yeh H. H. 2007; Reassortment and concerted evolution in banana bunchy top virus genomes. J Virol 81:1746–1761 [View Article][PubMed]
    [Google Scholar]
  20. Hughes A. L. 2004; Birth-and-death evolution of protein-coding regions and concerted evolution of non-coding regions in the multi-component genomes of nanoviruses. Mol Phylogenet Evol 30:287–294 [View Article][PubMed]
    [Google Scholar]
  21. Hyder M. Z., Shah S. H., Hameed S., Naqvi S. M. 2011; Evidence of recombination in the Banana bunchy top virus genome. Infect Genet Evol 11:1293–1300 [View Article][PubMed]
    [Google Scholar]
  22. Ince W. L., Gueye-Mbaye A., Bennink J. R., Yewdell J. W. 2013; Reassortment complements spontaneous mutation in influenza A virus NP and M1 genes to accelerate adaptation to a new host. J Virol 87:4330–4338 [View Article][PubMed]
    [Google Scholar]
  23. 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 Methods 116:209–211 [View Article][PubMed]
    [Google Scholar]
  24. Katul L., Maiss E., Morozov S. Y., Vetten H. J. 1997; Analysis of six DNA components of the faba bean necrotic yellows virus genome and their structural affinity to related plant virus genomes. Virology 233:247–259 [View Article][PubMed]
    [Google Scholar]
  25. Katul L., Timchenko T., Gronenborn B., Vetten H. J. 1998; Ten distinct circular ssDNA components, four of which encode putative replication-associated proteins, are associated with the faba bean necrotic yellows virus genome. J Gen Virol 79:3101–3109[PubMed]
    [Google Scholar]
  26. Kraberger S., Harkins G. W., Kumari S. G., Thomas J. E., Schwinghamer M. W., Sharman M., Collings D. A., Briddon R. W., Martin D. P., Varsani A. 2013; Evidence that dicot-infecting mastreviruses are particularly prone to inter-species recombination and have likely been circulating in Australia for longer than in Africa and the Middle East. Virology 444:282–291 [View Article][PubMed]
    [Google Scholar]
  27. Kumari S. G., Attar N., Mustafayev E., Akparov Z. 2009; First report of faba bean necrotic yellows virus affecting legume crops in Azerbaijan. Plant Dis 93:1220 [View Article]
    [Google Scholar]
  28. 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]
  29. Makkouk K. M., Kumari S. G. 2009; Epidemiology and integrated management of persistently transmitted aphid-borne viruses of legume and cereal crops in West Asia and North Africa. Virus Res 141:209–218 [View Article][PubMed]
    [Google Scholar]
  30. 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]
  31. Martin D. P., Biagini P., Lefeuvre P., Golden M., Roumagnac P., Varsani A. 2011; Recombination in eukaryotic single stranded DNA viruses. Viruses 3:1699–1738 [View Article][PubMed]
    [Google Scholar]
  32. Medina R. A., García-Sastre A. 2011; Influenza A viruses: new research developments. Nat Rev Microbiol 9:590–603 [View Article][PubMed]
    [Google Scholar]
  33. 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]
  34. Mustafayev E., Kumari S. G., Attar N., Zeynal A. 2011; Viruses infecting chickpea and lentil crops in Azerbaijan. Australas Plant Pathol 40:612–620 [View Article]
    [Google Scholar]
  35. Nahid N., Amin I., Mansoor S., Rybicki E. P., van der Walt E., Briddon R. W. 2008; Two dicot-infecting mastreviruses (family Geminiviridae) occur in Pakistan. Arch Virol 153:1441–1451 [View Article][PubMed]
    [Google Scholar]
  36. Ortiz V., Navarro E., Castro S., Carazo G., Romero J. 2006; Incidence and transmission of faba bean necrotic yellows virus (FBNYV) in Spain. Span J Agric Res 4:255–260 [CrossRef]
    [Google Scholar]
  37. Palukaitis P., García-Arenal F. 2003; Cucumoviruses. Adv Virus Res 62:241–323 [View Article][PubMed]
    [Google Scholar]
  38. 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]
  39. Posada D. 2008; jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256 [View Article][PubMed]
    [Google Scholar]
  40. Rosario K., Breitbart M. 2011; Exploring the viral world through metagenomics. Curr Opin Virol 1:289–297 [View Article][PubMed]
    [Google Scholar]
  41. Rosario K., Duffy S., Breitbart M. 2012; A field guide to eukaryotic circular single-stranded DNA viruses: insights gained from metagenomics. Arch Virol 157:1851–1871 [View Article][PubMed]
    [Google Scholar]
  42. Sano Y., Wada M., Hashimoto Y., Matsumoto T., Kojima M. 1998; Sequences of ten circular ssDNA components associated with the milk vetch dwarf virus genome. J Gen Virol 79:3111–3118[PubMed]
    [Google Scholar]
  43. Sicard A., Yvon M., Timchenko T., Gronenborn B., Michalakis Y., Gutierrez S., Blanc S. 2013; Gene copy number is differentially regulated in a multipartite virus. Nat Commun 4:2248 [View Article][PubMed]
    [Google Scholar]
  44. Sikorski A., Kearvell J., Elkington S., Dayaram A., Argüello-Astorga G. R., Varsani A. 2013; Novel ssDNA viruses discovered in yellow-crowned parakeet (Cyanoramphus auriceps) nesting material. Arch Virol 158:1603–1607 [View Article][PubMed]
    [Google Scholar]
  45. Stainton D., Kraberger S., Walters M., Wiltshire E. J., Rosario K., Halafihi M., Lolohea S., Katoa I., Faitua T. H. other authors 2012; Evidence of inter-component recombination, intra-component recombination and reassortment in banana bunchy top virus. J Gen Virol 93:1103–1119 [View Article][PubMed]
    [Google Scholar]
  46. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. 2011; mega5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739 [View Article][PubMed]
    [Google Scholar]
  47. Thomas J. E. 2008; Banana bunchy top virus. In Encyclopedia of Virology, 3rd edn. pp. 272–279 Edited by Mahy B. W. J., Van Regenmortel M. Oxford: Elsevier; [View Article]
    [Google Scholar]
  48. Timchenko T., de Kouchkovsky F., Katul L., David C., Vetten H. J., Gronenborn B. 1999; A single rep protein initiates replication of multiple genome components of faba bean necrotic yellows virus, a single-stranded DNA virus of plants. J Virol 73:10173–10182[PubMed]
    [Google Scholar]
  49. Timchenko T., Katul L., Sano Y., de Kouchkovsky F., Vetten H. J., Gronenborn B. 2000; The master rep concept in nanovirus replication: identification of missing genome components and potential for natural genetic reassortment. Virology 274:189–195 [View Article][PubMed]
    [Google Scholar]
  50. Timchenko T., Katul L., Aronson M., Vega-Arreguín J. C., Ramirez B. C., Vetten H. J., Gronenborn B. 2006; Infectivity of nanovirus DNAs: induction of disease by cloned genome components of Faba bean necrotic yellows virus. J Gen Virol 87:1735–1743 [View Article][PubMed]
    [Google Scholar]
  51. Varsani A., van der Walt E., Heath L., Rybicki E. P., Williamson A. L., Martin D. P. 2006; Evidence of ancient papillomavirus recombination. J Gen Virol 87:2527–2531 [View Article][PubMed]
    [Google Scholar]
  52. Vetten H. J. 2008; Nanoviruses. In Encyclopedia of Virology, 3rd edn. pp. 385–391 Edited by Mahy B. W. J., Van Regenmortel M. Oxford: Elsevier; [View Article]
    [Google Scholar]
  53. Vetten H. J., Dale J. L., Grigoras I., Gronenborn B., Harding R., Randles J. W., Sano Y., Thomas J. E., Timchenko T., Yeh H.-H. 2012; Family Nanoviridae . In Virus Taxonomy. Ninth Report of the International Committee on Taxonomy of Viruses pp. 395–404 Edited by King A. M. Q., Adams M. J., Carstens E. C., Lefkowitz E. J. London: Elsevier/Academic Press;
    [Google Scholar]
  54. Yoon H. S., Price D. C., Stepanauskas R., Rajah V. D., Sieracki M. E., Wilson W. H., Yang E. C., Duffy S., Bhattacharya D. 2011; Single-cell genomics reveals organismal interactions in uncultivated marine protists. Science 332:714–717 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.063115-0
Loading
/content/journal/jgv/10.1099/vir.0.063115-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited this month Most Cited RSS feed

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