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Molecular and Biological Characterization of Chilli Leaf Curl Virus and Associated Tomato Leaf Curl Betasatellite Infecting Toba

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Molecular and Biological Characterization of Chilli Leaf Curl Virus and Associated Tomato Leaf Curl Betasatellite Infecting Toba Shahid et al. Virology Journal (2019) 16:131 https://doi.org/10.1186/s12985-019-1235-4 RESEARCH Open Access Molecular and biological characterization of Chilli leaf curl virus and associated Tomato leaf curl betasatellite infecting tobacco in Oman Muhammad Shafiq Shahid1*† , Muhammad Shafiq1†, Amir Raza1, Abdullah M. Al-Sadi1 and Rob W. Briddon2 Abstract Background: In Oman tobacco (Nicotiana tabacum; family Solanaceae) is a minor crop, which is produced only for local consumption. In 2015, tobacco plants exhibiting severe downward leaf curling, leaf thickening, vein swelling, yellowing and stunting were identified in fields of tobacco in Suhar Al-Batina region, Oman. These symptoms are suggestive of begomovirus (genus Begomovirus, family Geminiviridae) infection. Methods: Circular DNA molecules were amplified from total DNA extracted from tobacco plants by rolling circle amplification (RCA). Viral genomes were cloned from RCA products by restriction digestion and betasatellites were cloned by PCR amplification from RCA product, using universal primers. The sequences of full-length clones were obtained by Sanger sequencing and primer walking. Constructs for the infectivity of virus and betasatellite were produced and introduced into plants by Agrobacterium-mediated inoculation. Results: The full-length sequences of 3 begomovirus and 3 betasatellite clones, isolated from 3 plants, were obtained. Analysis of the full-length sequences determined showed the virus to be a variant of Chilli leaf curl virus (ChiLCV) and the betasatellite to be a variant of Tomato leaf curl betasatellite (ToLCB). Both the virus and the betasatellite isolated from tobacco show the greatest levels of sequence identity to isolates of ChiLCV and ToLCB identified in other hosts in Oman. Additionally clones of ChiLCV and ToLCB were shown, by Agrobacterium-mediated inoculation, to be infectious to 3 Nicotiana species, including N. tabacum.InN. benthamiana the betasatellite was shown to change the upward leaf rolling symptoms to a severe downward leaf curl, as is typical for many monopartite begomoviruses with betasatellites. Conclusions: The leaf curl disease of tobacco in Oman was shown to be caused by ChiLCV and ToLCB. This is the first identification of ChiLCV with ToLCB infecting tobacco. The study shows that, despite the low diversity of begomoviruses and betasatellites in Oman, the extant viruses/betasatellites are able to fill the niches that present themselves. Keywords: Geminivirus, Begomovirus, Betasatellite, Chilli leaf curl virus, Tomato leaf curl betasatellite, Nicotiana tabacum * Correspondence: [email protected] †Muhammad Shafiq Shahid and Muhammad Shafiq contributed equally to this work. 1Department of Crop Sciences, College of Agricultural and Marine Sciences, Sultan Qaboos University, Al-Khod, 123 Muscat, Oman Full list of author information is available at the end of the article © The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Shahid et al. Virology Journal (2019) 16:131 Page 2 of 9 Background The study described here has analysed the etiology of Viruses of the genus Begomovirus (family Geminiviridae) a leaf curl disease of tobacco recently identified for the cause economically important diseases of many crops first time in Oman. The results show that the disease is throughout tropical and subtropical regions. Begomo- associated with ChiLCV and ToLCB. Additionally Agro- viruses have circular single-stranded (ss) DNA genomes, bacterium-mediated inoculation of the cloned virus and that are encapsidated in distinctive twinned icosahedral betasatellite were used to satisfy Koch’s postulates. The (geminate) particles and are transmitted exclusively by the significance of the findings is discussed. whitefly Bemisia tabaci [1]. The genomes of begomo- viruses are either bipartite, consisting of two ~ 2.6–2.8 kb Methods genomic components known as DNA A and DNA B, or DNA extraction and initial detection of a begomovirus monopartite, consisting of a single ~ 2.6–2.8 kb compo- and satellite by polymerase chain reaction nent that is a homolog of the DNA A of bipartite viruses. Total nucleic acid was extracted from leaf samples using a The majority of begomoviruses native to the New World cetyltrimethylammonium bromide-based method [12]and are bipartite, whereas the majority of begomoviruses kept at − 20 °C. Extracted DNA was used as a template in native to the Old World (OW) are monopartite [1]. The polymerase chain reaction (PCR) with primer pairs for the genomes (or DNA A components) of begomoviruses detection of begomoviruses (TYLCD-356 (5′-ATCATT originating from the OW encode six genes. In the TCCACKCCCGYCTCGA-3′/TYLCD-1044 5′-GCRTGM complementary-sense the genes encode the replication- GTACABGCCATATACA-3′), amplifying an ~ 800 nt associated protein, the transcriptional-activator protein, product, betasatellites (Sat101/Sat102), amplifying an ~ the replication-enhancer protein and the (A) C4 protein. 1350 nt product [13], and alphasatellites (DNA101/ The two genes in the virion-sense encode the (A) V2 pro- DNA102), amplifying an ~ 1380 nt product [14]. Addition- tein and the coat protein [2]. ally the primer pair βC1F (5′-AGACCCGGGATGAC Most monopartite begomoviruses are associated with a GATCAGATATAATAACA-3′)/βC1R (5′-ACGTCGAC group of ssDNA satellites collectively known as betasa- TCACACACACACTTTCGTACA-3′), amplifying a ~ tellites [3, 4]. Betasatellites are approximately half the 350 nt product, was used in PCR for the detection of size of their helper begomoviruses (~ 1.4 kb) and depend betasatellites. on the helper virus for their replication, movement in plants and transmission between plants [4]. The struc- Rolling circle amplification, cloning and sequencing ture of betasatellites is highly conserved comprising of a Circular DNA molecules in nucleic acid samples were sequence rich in adenine (A-rich), a sequence conserved enriched using rolling circle amplification (RCA) as between all betasatellites, known as the satellite con- described earlier [15]. Restriction of the high molecular served region (SCR), that contains a predicted hairpin weight concatameric RCA products with BamHI resulted structure with the nonanucleotide sequence TAATAT- in ~ 2.7 kb fragments, which were eluted from agarose gels TAC forming part of the loop, and a single conserved using a GeneJet Gel Extraction Kit (Thermo Fisher (between all betasatellites) gene with a capacity to en- Scientific) and cloned in BamHI restricted pGEM-3zf (+) code an ≥118 amino acid product known as βC1 [5]. (Promega Madison, USA). Potentially full-length clones The first disease caused by a begomovirus in Oman resulting from RCA (for begomovirus) and PCR (for beta- was identified in 1993, although the causative viruses satellite) were sequenced commercially using the primer- and satellites were not characterized until much later walking approach (Macrogen Inc., South Korea). [6]. Despite this the identified diversity of begomoviruses and betasatellites in Oman remains low relative to the Sequence assembly and analysis known diversity on the Indian sub-continent. The ma- Sequences were assembled using SeqMan, part of the jority of these viruses and satellites appear to have been Lasergene package of sequence analysis software (DNA introduced to the country or have evolved from intro- Star Inc., Madison, WI, USA). Related sequences available duced species. In this respect Oman holds an unusual in the GenBank database were identified using the Basic position, being at the front of a meeting of begomo- Local Alignment Search Tool nucleotide (BLASTn) [16] viruses introduced from Africa, such as Tomato leaf curl run on-line (http://blast.ncbi.nlm.nih.gov/Blast.cgi). Open Sudan virus and African cassava mosaic Zanzibar virus reading frames (ORFs) in sequences were identified using [7, 8], begomoviruses and satellites introduced from the the ORF Finder program run on-line (https://www.ncbi. Indian sub-continent, such as Chilli leaf curl virus nlm.nih.gov/orffinder/). The Species Demarcation Tool (ChiLCV) and Tomato leaf curl betasatellite (ToLCB [9]; (SDT), with the MUSCLE option, was used to calculate ), and viruses native to the Middle East region, such as sequence identity values [17]. Pairwise multiple sequence Tomato yellow leaf curl virus (TYLCV) and Watermelon alignments were produced using the MUSCLE algo- chlorotic stunt virus [10, 11]. rithm implemented in MEGA6 [18]. The evolutionary Shahid et al. Virology Journal (2019) 16:131 Page 3 of 9 relationships between sequences were determined by con- yellowing and stunting (Fig. 1). In the fields between 60 structing phylogenetic trees using Clustal X (neighbor- and 70% of plants were exhibiting symptoms. joining method) and displayed using Treeview [19]. Leaves from four symptomatic N. tabacum plants, originating from two independent but neighbouring Production of constructs for Agrobacterium-mediated fields (500 m apart), were collected, as well as a non- inoculation of plants symptomatic
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