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Molecular characterization of faba bean necrotic yellows viruses in Tunisia

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Abstract

Faba bean necrotic yellows virus (FBNYV) (genus Nanovirus; family Nanoviridae) has a genome comprising eight individually encapsidated circular single-stranded DNA components. It has frequently been found infecting faba bean (Vicia faba L.) and chickpea (Cicer arietinum L.) in association with satellite molecules (alphasatellites). Genome sequences of FBNYV from Azerbaijan, Egypt, Iran, Morocco, Spain and Syria have been determined previously and we now report the first five genome sequences of FBNYV and associated alphasatellites from faba bean sampled in Tunisia. In addition, we have determined the genome sequences of two additional FBNYV isolates from chickpea plants sampled in Syria and Iran. All individual FBNYV genome component sequences that were determined here share > 84% nucleotide sequence identity with FBNYV sequences available in public databases, with the DNA-M component displaying the highest degree of diversity. As with other studied nanoviruses, recombination and genome component reassortment occurs frequently both between FBNYV genomes and between genomes of nanoviruses belonging to other species.

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References

  1. Abraham A, Varrelmann M, Vetten H (2008) Molecular evidence for the occurrence of two new luteoviruses in cool season food legumes in Northeast Africa. Afr J Biotechnol 7:414–420

    CAS  Google Scholar 

  2. Abraham AD, 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

    Article  CAS  PubMed  Google Scholar 

  3. Abraham AD, Varrelmann M, Josef Vetten H (2012) Three distinct nanoviruses, one of which represents a new species, infect faba bean in Ethiopia. Plant Dis 96:1045–1053

    Article  CAS  Google Scholar 

  4. Al-Nsour A, Mansour A, Al-Musa A, Salem N (1998) Distribution and incidence of faba bean necrotic yellows virus in Jordan. Plant Pathol 47:510–515

    Article  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Franz A, Makkouk KM, Vetten HJ (1995) Faba bean necrotic yellows virus naturally infects phaseolus bean and cowpea in the coastal area of Syria. J Phytopathol 143:319–320

    Article  Google Scholar 

  7. Franz A, Makkouk K, Katul L, Vetten H (1996) Monoclonal antibodies for the detection and differentiation of faba bean necrotic yellows virus isolates. Ann Appl Biol 128:255–268

    Article  Google Scholar 

  8. Franz A, Makkouk KM, Vetten HJ (1997) Host range of faba bean necrotic yellows virus and potential yield loss in infected faba bean. Phytopathol Mediterr 36:94–103

    Google Scholar 

  9. Franz AW, van der Wilk F, Verbeek M, Dullemans AM, van den Heuvel JF (1999) Faba bean necrotic yellows virus (genus Nanovirus) requires a helper factor for its aphid transmission. Virology 262:210–219

    Article  CAS  PubMed  Google Scholar 

  10. Gallet R, Kraberger S, Filloux D, Galzi S, Fontes H, Martin DP, Varsani A, Roumagnac P (2017) Nanovirus-alphasatellite complex identified in Vicia cracca in the Rhône delta river region of France. Arch Virol. https://doi.org/10.1007/s00705-017-3634-4

  11. Grigoras I, Timchenko T, Grande-Pérez A, Katul L, Vetten H-J, Gronenborn B (2010) High variability and rapid evolution of a nanovirus. J Virol 84:9105–9117

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Grigoras I, Ginzo AIdC, Martin DP, Varsani A, Romero J, Mammadov AC, Huseynova IM, Aliyev JA, Kheyr-Pour A, Huss H, Ziebell H, Timchenko T, Vetten H-J, Gronenborn B (2014) Genome diversity and evidence of recombination and reassortment in nanoviruses from Europe. J Gen Virol 95:1178–1191

    Article  CAS  PubMed  Google Scholar 

  13. 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

    Article  CAS  PubMed  Google Scholar 

  14. Heydarnejad J, Kamali M, Massumi H, Kvarnheden A, Male MF, Kraberger S, Stainton D, Martin DP, Varsani A (2017) Identification of a nanovirus-alphasatellite complex in sophora alopecuroides. Virus Res 235:24–32

    Article  CAS  PubMed  Google Scholar 

  15. Horser CL, Karan M, Harding RM, Dale JL (2001) Additional Rep-encoding DNAs associated with banana bunchy top virus. Arch Virol 146:71–86

    Article  CAS  PubMed  Google Scholar 

  16. Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Meth 14:587–589

    Article  CAS  Google Scholar 

  17. Katul L, Maiss E, Vetten HJ (1995) Sequence analysis of a faba bean necrotic yellows virus DNA component containing a putative replicase gene. J Gen Virol 76:475–479

    Article  CAS  PubMed  Google Scholar 

  18. Katul L, Maiss E, Morozov SY, Vetten HJ (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

    Article  CAS  PubMed  Google Scholar 

  19. Katul L, Timchenko T, Gronenborn B, Vetten HJ (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(Pt 12):3101–3109

    Article  CAS  PubMed  Google Scholar 

  20. Katul U, Vetten H, Maiss E, Makkouk K, Lesemann DE, Casper R (1993) Characterisation and serology of virus-like particles associated with faba bean necrotic yellows. Ann Appl Biol 123:629–647

    Article  Google Scholar 

  21. Kraberger S, Harkins GW, Kumari SG, Thomas JE, Schwinghamer MW, Sharman M, Collings DA, Briddon RW, Martin DP, 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

    Article  CAS  PubMed  Google Scholar 

  22. Kumari SG (2002) A study on Luteoviruses affecting cool-season food legumes. Department of Plant Protection, Faculty of Agriculture. Aleppo University, Aleppo, Syria

  23. Kumari SG, Makkouk KM (2007) Virus diseases of faba bean (Vicia faba L.) in Asia and Africa. Plant Viruses 1:93–105

    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. Makkouk K, Comeau A (1994) Evaluation of various methods for the detection of barley yellow dwarf virus by the tissue-blot immunoassay and its use for virus detection in cereals inoculated at different growth stages. Eur J Plant Pathol 100:71–80

    Article  Google Scholar 

  26. Makkouk K, Rizkallah L, Madkour M, El-Sherbeeny M, Kumari S, Amriti A, Solh M (1994) Survey of faba bean (Vicia faba L.) for viruses in Egypt. Phytopathol Mediterr 33:207–211

    Google Scholar 

  27. Makkouk K, Kumari S (1996) Detection of ten viruses by the tissue-blot immunoassay (TBIA). Arab J Plant Prot 14:3–9

    Google Scholar 

  28. Makkouk K, Kumari S, Hughes JdA, Muniyappa V, Kulkarni N (2003) Other legumes. Virus and virus-like diseases of major crops in developing countries. Springer, pp 447–476

  29. Makkouk KM, Fazlali Y, Kumari SG, Farzadfar S (2002) First record of Beet western yellows virus, Chickpea chlorotic dwarf virus, Faba bean necrotic yellows virus and Soybean dwarf virus infecting chickpea and lentil crops in Iran. Plant Pathol 51:387

    Article  Google Scholar 

  30. Makkouk KM, Hamed AA, Hussein M, Kumari SG (2003) First report of Faba bean necrotic yellows virus (FBNYV) infecting chickpea (Cicer arietinum) and faba bean (Vicia faba) crops in Sudan. Plant Pathol 52:412

    Article  Google Scholar 

  31. Makkouk KM, Rizkallah L, Kumari SG, Zaki M, Enein RA (2003) First record of Chickpea chlorotic dwarf virus (CpCDV) affecting faba bean (Vicia faba) crops in Egypt. Plant Pathol 52:413

    Article  Google Scholar 

  32. Makkouk KM, Kumari SG (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

    Article  CAS  PubMed  Google Scholar 

  33. Martin DP, Murrell B, Golden M, Khoosal A, Muhire B (2015) RDP4: Detection and analysis of recombination patterns in virus genomes. Virus Evol 1:vev003

    Article  PubMed  PubMed Central  Google Scholar 

  34. Muhire BM, Varsani A, Martin DP (2014) SDT: a virus classification tool based on pairwise sequence alignment and identity calculation. PLoS One 9:e108277

    Article  PubMed  PubMed Central  Google Scholar 

  35. Najar A, Makkouk KM, Kumari SG (2000) First record of Faba bean necrotic yellows virus and Beet western yellows virus infecting Faba bean in Tunisia. Plant Dis 84:1046

    Article  Google Scholar 

  36. Nguyen L-T, Schmidt HA, von Haeseler A, Minh BQ (2015) IQ-TREE: a fast and effective Stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 32:268–274

    Article  CAS  PubMed  Google Scholar 

  37. 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

    Article  Google Scholar 

  38. Rosario K, Padilla-Rodriguez M, Kraberger S, Stainton D, Martin DP, Breitbart M, Varsani A (2013) Discovery of a novel mastrevirus and alphasatellite-like circular DNA in dragonflies (Epiprocta) from Puerto Rico. Virus Res 171:231–237

    Article  CAS  PubMed  Google Scholar 

  39. 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

    Article  CAS  PubMed  Google Scholar 

  40. Savory FR, Ramakrishnan U (2014) Asymmetric patterns of reassortment and concerted evolution in Cardamom bushy dwarf virus. Infect Genet Evol 24:15–24

    Article  CAS  PubMed  Google Scholar 

  41. Stainton D, Martin DP, Muhire BM, Lolohea S, Halafihi M, Lepoint P, Blomme G, Crew KS, Sharman M, Kraberger S, Dayaram A, Walters M, Collings DA, Mabvakure B, Lemey P, Harkins GW, Thomas JE, Varsani A (2015) The global distribution of Banana bunchy top virus reveals little evidence for frequent recent, human-mediated long distance dispersal events. Virus Evol 1:vev009

    Article  PubMed  PubMed Central  Google Scholar 

  42. Stöver BC, Müller KF (2010) TreeGraph 2: combining and visualizing evidence from different phylogenetic analyses. BMC Bioinform 11:7

    Article  Google Scholar 

  43. Timchenko T, De Kouchkovsky F, Katul L, David C, Vetten HJ, 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

    CAS  PubMed  PubMed Central  Google Scholar 

  44. Timchenko T, Katul L, Sano Y, de Kouchkovsky F, Vetten HJ, 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

    Article  CAS  PubMed  Google Scholar 

  45. Vetten HJ, Dale JL, Grigoras I, Gronenborn B, Harding R, Randles JW, Sano Y, Thomas JE, Timchenko T, Yeh HH (2012) Nanoviridae. In: King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ (eds) Virus taxonomy: ninth report of the international committee on taxonomy of viruse. Elsevier, Academic Press, Amsterdam, pp 395–404

    Google Scholar 

  46. Zhou X (2013) Advances in understanding begomovirus satellites. Ann Rev Phytopathol 51:357–381

    Article  CAS  Google Scholar 

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Acknowledgements

This work was supported by funds from ICARDA awarded to SGK. AV and DPM are supported by the National Research Foundation of South Africa.

GenBank accession numbers

KX431380-KX431435, MF510471-MF510474.

Author information

Authors and Affiliations

  1. The Biodesign Center for Fundamental and Applied Microbiomics, Center for Evolution and Medicine, School of Life sciences, Arizona State University, Tempe, AZ, 85287-5001, USA

    Simona Kraberger & Arvind Varsani

  2. Virology Laboratory, International Centre for Agricultural Research in the Dry Areas (ICARDA), Tunis, Tunisia

    Safaa G. Kumari

  3. International Centre for Agricultural Research in the Dry Areas (ICARDA), Dalia Building, 2nd Floor, Bashir El-Kassar St., Verdun, P.O. Box 114/5055, Beirut, 1108-2010, Lebanon

    Safaa G. Kumari

  4. Laboratory of Plant Protection, National Institute of Agronomic Research of Tunisia, Rue Hédi Karray, 1004, El Menzah, Tunisia

    Asma Najar

  5. School of Biological Sciences, The University of Queensland, Brisbane, QLD, 4072, Australia

    Daisy Stainton

  6. Computational Biology Group, Institute of Infectious Diseases and Molecular Medicine, University of Cape Town, Cape Town, 7925, South Africa

    Darren P. Martin

  7. Structural Biology Research Unit, Department of Clinical Laboratory Sciences, University of Cape Town, Observatory, Cape Town, South Africa

    Arvind Varsani

Authors
  1. Simona Kraberger
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  2. Safaa G. Kumari
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  4. Daisy Stainton
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  5. Darren P. Martin
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  6. Arvind Varsani
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Corresponding authors

Correspondence to Safaa G. Kumari or Arvind Varsani.

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The authors declare there are no conflicts of interest.

Research involving human participants and/or animals

The research did not involve human participants or animals.

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The research did not involve human participants or animals.

Additional information

Handling Editor: F. Murilo Zerbini.

Electronic supplementary material

Below is the link to the electronic supplementary material.

705_2017_3651_MOESM1_ESM.docx

Supplementary Table 1 List of abutting forward and reverse primers used to isolate full FBNYV genome components and FBNY- associated satellites (DOCX 13 kb)

705_2017_3651_MOESM2_ESM.docx

Supplementary Table 2 List of FBNYV genomes, country of origin, and accession number for each component. Those in bold indicate isolates recovered in this study (DOCX 21 kb)

705_2017_3651_MOESM3_ESM.docx

Supplementary Table 3 List of FBNYV-associated alphasatellites, country of origin, and accession number for each isolate. Those in bold indicate isolates recovered in this study (DOCX 19 kb)

705_2017_3651_MOESM4_ESM.xls

Supplementary Data 1 Pairwise nucleotide sequence identity comparisons of FBNYV component sequences and nanovirus-associated alphasatellite sequences. Names highlighted in red indicate isolates recovered in this study (XLS 92 kb)

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Kraberger, S., Kumari, S.G., Najar, A. et al. Molecular characterization of faba bean necrotic yellows viruses in Tunisia. Arch Virol 163, 687–694 (2018). https://doi.org/10.1007/s00705-017-3651-3

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