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Recent evolution of a novel begomovirus causing tomato leaf curl disease in the Al-Batinah region of Oman

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Abstract

For last two decades, begomoviruses (family Geminiviridae) have been a major constraint for tomato production in Oman, particularly in the Al-Batinah region, the major agricultural area of Oman. Farms in the Al-Batinah region were surveyed during January-March and November-December in 2012 and January-February in 2013. Leaf samples of tomato plants showing typical leaf curl disease symptoms were collected and analyzed for begomoviruses. Out of fifteen begomovirus clones sequenced, seven were shown to be tomato yellow leaf curl virus strain Oman (TYLCV-OM); three, chili leaf curl virus strain Oman (ChLCV-OM); and one, tomato leaf curl Oman virus (ToLCOMV) – viruses that have previously been shown to occur in Oman. Four sequences were shown to have relatively low percent identity values to known begomoviruses, with the highest (86 %) to isolates of pepper leaf curl Lahore virus, indicating that these should be included in a new species, for which the name “Tomato leaf curl Al Batinah virus” (ToLCABV) is proposed. Although the betasatellite tomato leaf curl betasatellite (ToLCB; 7 full-length sequences isolated) was identified with some isolates of ChLCV-OM, TYLCV-OM and ToLCOMV, it was not identified in association with any of the ToLCABV isolates. Analysis of the sequences of the TYLCV-OM and ToLCOMV isolates characterized here did not show them to differ significantly from previously characterized isolates of these viruses. The three isolates of ChLCV-OM characterized were shown to have a recombination pattern distinct from earlier characterized isolates. ToLCABV was shown to have resulted from recombination between ChLCV-OM and ToLCOMV. A clone of ToLCABV was infectious by Agrobacterium-mediated inoculation to Nicotiana benthamiana and tomato, inducing symptoms typical of those seen in tomato in the field. Additionally, ToLCABV was shown to be able to interact in planta with ToLCB, resulting in a change in symptom phenotype, although the betasatellite did not appear to affect viral DNA levels.

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Acknowledgments

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’’.

Conflict of interest

The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Department of Crop Sciences, College of Agricultural and Marine Sciences, Sultan Qaboos University, Al-Khod 123, Muscat, Sultanate of Oman

    Akhtar J. Khan, Sohail Akhtar, Adel A. Al-Shehi, Abdulrahman M. Al-Matrushi & Ume Ammara

  2. School of Life Sciences, Central University of Gujrat, Gandhinagar, India

    Achuit K. Singh

  3. National Institute for Biotechnology and Genetic Engineering, Jhang Road, Faisalabad, Pakistan

    Rob W. Briddon

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  1. Akhtar J. Khan
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Correspondence to Akhtar J. Khan.

Electronic supplementary material

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Supplementary Fig. 1. Neighbor-joining phylogenetic dendrogram based upon alignment of the sequences of Tomato leaf curl betasatellite (ToLCB) obtained in the study described here with all ToLCB isolates available in the databases and other selected betasatellites. In each case, the database accession number is given. The numbers at nodes represent percent bootstrap confidence scores (1000 iterations). The phylogenetic tree was arbitrarily rooted on the sequence of ageratum yellow vein Singapore alphasatellite (AYVSGV), an unrelated sequence of a similar size, as outgroup. The betasatellite acronyms used are as follows: ageratum yellow leaf curl betasatellite, AYLCB; chili leaf curl betasatellite, ChLCB; cotton leaf curl Gezira betasatellite, CLCuGeB; tomato leaf curl Bangladesh betasatellite, ToLCBDB. The betasatellite isolates produced as part of the study described here are highlighted in grey.

Supplementary Fig. 2. Analysis of chili leaf curl virus (ChLCV) isolates for recombination. Schematic representation of the linearized genomes of the three ChLCV isolates determined here (accession nos. KF229718-KF229720) and three ChLCV isolates characterized previously by Khan et al. [17] showing the origin of recombinant fragments. The p-values for detection of the recombinant fragment by the RDP method are shown. The viruses used were ChLCV strains “Pakistan” (PK) and “Guntur” (Gun), pepper leaf curl Lahore virus (PepLCLV) and tomato leaf curl Oman virus (ToLCOMV). The database accession numbers are given in each case. At the top of the figure, a linearized version of the virus genome shows the approximate positions of genes (the V2 and coat protein [CP] genes in the virion sense and replication-associated protein [Rep], transcriptional-activator protein [TrAP], replication enhancer protein [REn], and C4 genes in the complementary sense) and the non-coding intergenic region (IR).

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Khan, A.J., Akhtar, S., Singh, A.K. et al. Recent evolution of a novel begomovirus causing tomato leaf curl disease in the Al-Batinah region of Oman. Arch Virol 159, 445–455 (2014). https://doi.org/10.1007/s00705-013-1853-x

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