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.
References
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
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
Briddon RW, Stanley J (2006) Sub-viral agents associated with plant-infecting single-stranded DNA viruses. Virology 344:198–210
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
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
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
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791
Ghanem GAM (2003) Okra leaf curl virus: a monopartite begomovirus infecting okra crop in Saudi Arabia. Arab J Biotechnol 6:139–152
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Martin DP, Rybicki EP (2000) RDP: detection of recombination amongst aligned sequences. Bioinformatics 16:562–563
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
Moffat AS (1999) Geminiviruses emerge as serious crop threat. Science 286:1835
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
Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, New York
Orozco BM, Hanley-Bowdoin L (1996) A DNA structure is required for geminivirus replication origin function. J Virol 7:148–158
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
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
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
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
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
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
Sawyer S (1989) Statistical tests for detecting gene conversion. Mol Biol Evol 6:526–538
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
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
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
Varma A, Malathi VG (2003) Emerging geminivirus problems: a serious threat to crop production. Ann App Biol 142:145–164
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
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
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
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
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.’’
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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
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DOI: https://doi.org/10.1007/s00705-013-1926-x