Skip to main content

Advertisement

Log in

Identification of a disease complex involving a novel monopartite begomovirus with beta- and alphasatellites associated with okra leaf curl disease in Oman

  • Brief Report
  • Published:
Archives of Virology Aims and scope Submit manuscript

Abstract

Okra leaf curl disease (OLCD) is an important viral disease of okra in tropical and subtropical areas. The disease is caused by begomovirus-satellite complexes. A begomovirus and associated betasatellite and alphasatellite were identified in symptomatic okra plants from Barka, in the Al-Batinah region of Oman. Analysis of the begomovirus sequences showed them to represent a new begomovirus most closely related to cotton leaf curl Gezira virus (CLCuGeV), a begomovirus of African origin. The sequences showed less than 85 % nucleotide sequence identity to CLCuGeV isolates. The name okra leaf curl Oman virus (OLCOMV) is proposed for the new virus. Further analysis revealed that the OLCOMV is a recombinant begomovirus that evolved by the recombination of CLCuGeV isolates with tomato yellow leaf curl virus-Oman (TYLCV-OM). An alpha- and a betasatellite were also identified from the same plant sample, which were also unique when compared to sequences available in the databases. However, although the betasatellite appeared to be of African origin, the alphasatellite was most closely related to alphasatellites originating from South Asia. This is the first report of a begomovirus-satellite complex infecting okra in Oman.

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.

Fig. 1
Fig. 2

References

  1. Adams MJ, King AMQ, Carstens EB (2013) Ratification vote on taxonomic proposals to the International Committee on Taxonomy of Viruses (2013). Arch Virol. doi:10.1007/s00705-013-1688-5

    Google Scholar 

  2. Briddon RW, Bull SE, Amin I, Mansoor S, Bedford ID, Rishi N, Siwatch SS, Zafar Y, Abdel-Salam AM, Markham PG (2004) Diversity of DNA 1: a satellite-like molecule associated with monopartite begomovirus-DNA β complexes. Virology 324:462–474

    Article  CAS  PubMed  Google Scholar 

  3. Briddon RW, Stanley J (2006) Sub-viral agents associated with plant-infecting single-stranded DNA viruses. Virology 344:198–210

    Article  CAS  PubMed  Google Scholar 

  4. Briddon RW, Brown JK, Moriones E, Stanley J, Zerbini M, Zhou X, Fauquet CM (2008) Recommendations for the classification and nomenclature of the DNA-β satellites of begomoviruses. Arch Virol 153:763–781

    Article  CAS  PubMed  Google Scholar 

  5. Brown JK, Fauquet CM, Briddon RW, Zerbini M, Moriones E, Navas-Castillo J (2012) Geminiviridae. In: King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ (eds) Virus taxonomy. Ninth Report of the International Committee on Taxonomy of Viruses. Elsevier Publication, London, pp 351–373

    Google Scholar 

  6. Fauquet CM, Briddon RW, Brown JK, Moriones E, Stanley J, Zerbini M, Zhou X (2008) Geminivirus strain demarcation and nomenclature. Arch Virol 153:783–821

    Article  CAS  PubMed  Google Scholar 

  7. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  8. Ghanem GAM (2003) Okra leaf curl virus: a monopartite begomovirus infecting okra crop in Saudi Arabia. Arab J Biotechnol 6:139–152

    Google Scholar 

  9. Hanley-Bowdoin L, Settlage SB, Orozco BM, Nagar S, Robertson D (1999) Geminviruses: models for plant DNA replication, transcription, and cell cycle regulation. Crit Rev Plant Sci 18:71–106

    Article  CAS  Google Scholar 

  10. Idris AM, Hussein MH, Abdel-Salam AM, Brown JK (2002) Phylogenetic relationships for okra leaf curl- and hollyhock leaf crumple-associated begomoviruses and first report of associated satellite DNAs. Arab J Biotech 5:67–82

    Google Scholar 

  11. Idris AM, Shahid MS, Briddon RW, Khan AJ, Zhu JK, Brown JK (2011) An unusual alphasatellite associated with monopartite begomoviruses attenuates symptoms and reduces betasatellite accumulation. J Gen Virol 92:706–717

    Article  CAS  PubMed  Google Scholar 

  12. Inoue-Nagata AK, Albuquerque LC, Rocha WB, Nagata T (2004) A simple method for cloning the complete begomovirus genome using the bacteriophage phi29 DNA polymerase. J Virol Methods 116:209–211

    Article  CAS  PubMed  Google Scholar 

  13. Khan AJ, Idris AM, Al-Saady NA, Al-Mahruki MS, Al-Subhi AM, Brown JK (2008) A divergent isolate of tomato yellow leaf curl virus from Oman with an associated DNAβ satellite: an evolutionary link between Asian and the Middle Eastern virus-satellite complexes. Virus Genes 36:169–176

    Article  CAS  PubMed  Google Scholar 

  14. Khan AJ, Akhtar S, Al-Shihi AA, Al-Hinai FM, Briddon RW (2012) Identification of Cotton leaf curl Gezira virus in papaya in Oman. Plant Dis 96:1704

    Article  Google Scholar 

  15. Khan AJ, Akhtar S, Al-Zaidi AM, Singh AK, Briddon RW (2013) Genetic diversity and distribution of a distinct strain of Chili leaf curl virus and associated betasatellite infecting tomato and pepper in Oman. Virus Res. doi:10.1016/j.virusres.2013.07.018

    Google Scholar 

  16. Khan AJ, Akhtar S, Briddon RW, Ammara U, Al-Matrushi AM, Mansoor S (2012) Complete nucleotide sequence of Watermelon chlorotic stunt virus originating from Oman. Viruses 4:1169–1181

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  17. Khan AJ, Akhtar S, Singh AK, Briddon RW (2013) A distinct strain of Tomato leaf curl Sudan virus causes tomato leaf curl disease in Oman. Plant Dis. doi:10.1094/PDIS-02-43313-0210-RE

    Google Scholar 

  18. Khan AJ, Akhtar S, Singh AK, Al-Shehi AA, Al-Matrushi AM, Ammara U, Briddon RW (2012) Recent evolution of a novel begomovirus species causing tomato leaf curl disease in the Al-Batinah region of Oman. Arch Virol in press

  19. Kon T, Rojas MR, Abdourhamane IK, Gilbertson RL (2009) Roles and interactions of begomoviruses and satellite DNAs associated with okra leaf curl disease in Mali, West Africa. J Gen Virol 90:1001–1013

    Article  CAS  PubMed  Google Scholar 

  20. Leke WN, Sattar MN, Ngane EB, Ngeve JM, Kvarnheden A, Brown JK (2013) Molecular characterization of begomoviruses and DNA satellites associated with okra leaf curl disease in Cameroon. Virus Res 174:116–125

    Article  CAS  PubMed  Google Scholar 

  21. Lole KS, Bollinger RC, Paranjape RS, Gadkari D, Kulkarni SS, Novak NG, Ingersoll R, Sheppard HW, Ray SC (1999) Full-length human immunodeficiency virus type1 genomes from subtype C-infected seroconverters in India, with evidence of intersubtype recombination. J Virol 73:152–160

    CAS  PubMed Central  PubMed  Google Scholar 

  22. Mansoor S, Amin I, Hussain M, Zafar Y, Bull S, Briddon RW, Markham PG (2001) Association of a disease complex involving a begomovirus, DNA 1 and a distinct DNA beta with leaf curl disease of okra in Pakistan. Plant Dis 85:922

    Article  Google Scholar 

  23. Martin DP, Rybicki EP (2000) RDP: detection of recombination amongst aligned sequences. Bioinformatics 16:562–563

    Article  CAS  PubMed  Google Scholar 

  24. Melgarejo TA, Kon T, Rojas MR, Paz-Carrasco L, Zerbini FM, Gilbertson RL (2013) Characterization of a New World monopartite begomovirus causing leaf curl disease of tomato in Ecuador and Peru reveals a new direction in geminivirus evolution. J Virol 87:5397–5413

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  25. Moffat AS (1999) Geminiviruses emerge as serious crop threat. Science 286:1835

    Article  CAS  Google Scholar 

  26. Mubin M, Briddon RW, Mansoor S (2009) Complete nucleotide sequence of chili leaf curl virus and its associated satellites naturally infecting potato in Pakistan. Arch Virol 154:365–368

    Article  CAS  PubMed  Google Scholar 

  27. Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, New York

    Google Scholar 

  28. Orozco BM, Hanley-Bowdoin L (1996) A DNA structure is required for geminivirus replication origin function. J Virol 7:148–158

    Google Scholar 

  29. Porebski S, Bailey LG, Baum BR (1997) Modification of a CTAB DNA extraction protocol for plants containing high polysaccharide and polyphenol components. Plant Mol Biol Rep 15:8–15

    Article  CAS  Google Scholar 

  30. Rojas MR, Hagen C, Lucas WJ, Gilbertson RL (2005) Exploiting chinks in the plant’s armor: evolution and emergence of geminiviruses. Ann Rev Phytopathol 43:361–394

    Article  CAS  Google Scholar 

  31. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  32. Sánchez-Campos S, Martínez-Ayala A, Márquez-Martín B, Aragón-Caballero L, Navas-Castillo J, Moriones E (2013) Fulfilling Koch’s postulates confirms the monopartite nature of tomato leaf deformation virus, a begomovirus native to the New World. Virus Res 173:286–293

    Article  PubMed  Google Scholar 

  33. Sattar MN, Kvarnheden A, Saeed M, Briddon RW (2013) Cotton leaf curl disease: an emerging threat to cotton production worldwide. J Gen Virol 94:695–710

    Article  CAS  PubMed  Google Scholar 

  34. Saunders K, Bedford ID, Stanley J (2002) Adaptation from whitefly to leafhopper transmission of an autonomously-replicating nanovirus-like DNA component associated with ageratum yellow vein disease. J Gen Virol 83:909–915

    Google Scholar 

  35. Sawyer S (1989) Statistical tests for detecting gene conversion. Mol Biol Evol 6:526–538

    CAS  PubMed  Google Scholar 

  36. Sohrab SS, Mirza Z, Karim S, Rana D, Abuzenadah AM, Chaudhary AG, Bhattacharya PS (2013) Detection of begomovirus associated with okra leaf curl disease. Arch Phytopath Plant Prot 46:1047–1053

    Article  Google Scholar 

  37. 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  38. Tiendrébéogo F, Lefeuvre P, Hoareau M, Villemot J, Konaté G, Traoré AS, Barro N, Traoré VS, Reynaud B, Traoré O (2010) Molecular diversity of Cotton leaf curl Gezira virus isolates and their satellite DNAs associated with okra leaf curl disease in Burkina Faso. Virol J 7:48

    Article  PubMed Central  PubMed  Google Scholar 

  39. Varma A, Malathi VG (2003) Emerging geminivirus problems: a serious threat to crop production. Ann App Biol 142:145–164

    Article  CAS  Google Scholar 

  40. Venkataravanappa V, Lakshminarayana Reddy C, Jalali S, Krishna Reddy M (2012) Molecular characterization of distinct bipartite begomovirus infecting bhendi (Abelmoschus esculentus L.) in India. Virus Genes 44:522–535

    Article  CAS  PubMed  Google Scholar 

  41. Venkataravanappa V, Lakshminarayana Reddy CN, Swarnalatha P, Devaraju Jalali S, Reddy MK (2012) Molecular evidence for association of cotton leaf curl Allahabad virus with yellow vein mosaic disease of okra in North India. Arch Phytopath Plant Prot 45:2095–2113

    Article  Google Scholar 

  42. Venkataravanappa V, Reddy CNL, Jalali S, Reddy MK (2013) Molecular characterization of a new species of begomovirus associated with yellow vein mosaic of bhendi (Okra) in Bhubhaneswar, India. Eur J Plant Pathol 136:811–822

    Article  CAS  Google Scholar 

  43. Zaffalon V, Mukherjee S, Reddy V, Thompson J, Tepfer M (2011) A survey of geminiviruses and associated satellite DNAs in the cotton-growing areas of northwestern India. Arch Virol 157:483–495

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

This study was supported by research grant number ORG/EBR/09/03, funded by The Research Council, Oman to AJK. RWB is supported by the Higher Education Commission, Government of Pakistan, under the ‘‘Foreign Faculty Hiring Program.’’

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Akhtar J. Khan.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 10425 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Akhtar, S., Khan, A.J., Singh, A.S. et al. Identification of a disease complex involving a novel monopartite begomovirus with beta- and alphasatellites associated with okra leaf curl disease in Oman. Arch Virol 159, 1199–1205 (2014). https://doi.org/10.1007/s00705-013-1926-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00705-013-1926-x

Keywords

Navigation