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First Evidence of the Occurrence of Turnip Mosaic Virus in Ukraine and Molecular Characterization of Its Isolate

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First Evidence of the Occurrence of Turnip Mosaic Virus in Ukraine and Molecular Characterization of Its Isolate Received: 7 September 2017 | Accepted: 1 March 2018 DOI: 10.1111/jph.12703 ORIGINAL ARTICLE First evidence of the occurrence of Turnip mosaic virus in Ukraine and molecular characterization of its isolate Oleksiy Shevchenko1 | Ryosuke Yasaka2,3 | Olha Tymchyshyn1 | Tetiana Shevchenko1 | Kazusato Ohshima2,3 1Virology Department, ESC “Institute of Biology and Medicine”, Taras Shevchenko Abstract National University of Kyiv, Kyiv, Ukraine A total of 54 samples of Brassicaceae crops showing symptoms of mosaic, mottling, 2 Laboratory of Plant Virology, Department vein banding and/or leaf deformation were collected in Kyiv region (northern central of Applied Biological Sciences, Faculty of Agriculture, Saga University, Saga, Japan part of Ukraine) in 2014–2015. A half of collected samples was found to be infected 3The United Graduate School of Agricultural with Turnip mosaic virus (TuMV), and TuMV was detected in samples from Brassica Sciences, Kagoshima University, Kagoshima, oleracea var. capitata (cabbage), Raphanus sativus, Brassica juncea, Raphanus sp., Japan Sinapis alba, Camelina sativa and Bunias orientalis (weed). The full- length sequence of Correspondence the genomic RNA of a Ukrainian isolate (UKR9), which was isolated from cabbage, O. Shevchenko, Virology Department, ESC “Institute of Biology and Medicine”, Taras was determined. Recombination analysis of UKR9 isolate showed that this isolate Shevchenko National University of Kyiv, was an interlineage recombinant of world- Brassica and Asian- Brassica/Raphanus phy- Kyiv, Ukraine. Email: [email protected] logenetic groups. This study shows for the first time the occurrence of TuMV in Ukraine. Funding information Japan Society for the Promotion of Science KEYWORDS Brassicaceae, evolution, recombination, Turnip mosaic virus, Ukraine 1 | INTRODUCTION TuMV probably occurs worldwide and has been found in both temperate and subtropical regions of Africa, Asia, Europe, Oceania Turnip mosaic virus (TuMV) is a member of Potyvirus genus belong- and North and South America (Ohshima et al., 2002; Provvidenti, ing to the Potyviridae family of plant viruses. TuMV has flexible fil- 1996; Schwinghamer et al., 2014). In Europe, TuMV was reported amentous particles 700–750 nm long containing a single- stranded from the United Kingdom (Pallett et al., 2008), Spain (Segundo et al., positive- sense genomic RNA of about 10,000 nucleotides (King, 2003), Italy (Guglielmone et al., 2000; Ohshima et al., 2002), Greece Adams, Carstens, & Lefkowitz, 2012). TuMV genome has a single (Jenner & Walsh, 1996; Tomimura et al., 2004), Germany (Tomimura, open reading frame (ORF) translated into a large polyprotein which Gibbs, Jenner, Walsh, & Ohshima, 2003), the Netherlands (Ohshima is subsequently cleaved into 10 functional proteins by virus- encoded et al., 2002), Czech Republic (Petrzik & Lehmann, 1996), Hungary enzymes (Gibbs & Ohshima, 2010; Urcuqui- Inchima, Haenni, & (Horvath, Juretic, Besada, & Mamula, 1975), Bulgaria (Kovachevsky, Bernardi, 2001). Furthermore, an overlapping “pretty interesting 1975), Poland (Kozubek, Irzykowski, & Lehmann, 2007) and Russia Potyviridae ORF” (PIPO) exists in the +2 reading frame within the (Ohshima et al., 2002). region encoding protein 3 (P3) (Chung, Miller, Atkins, & Firth, 2008). Ukraine is one of the largest European countries between TuMV has an extremely wide host range but infects mostly plant the eastern EU states and Middle East region, where TuMV was species from the Brassicaceae family and induces persistent symp- detected in Turkey and Iran (Farzadfar et al., 2009; Korkmaz, toms (mosaic, mottling and chlorotic local lesions). TuMV is consid- Tomitaka, Onder, & Ohshima, 2008; Yasaka et al., 2017). Despite ered one of the most damaging and economically important viruses Ukraine’s geographical location and wide cultivation of differ- for domesticated Brassica plants. TuMV is transmitted by many aphid ent Brassica crops for centuries, TuMV has never been found on species non- persistently as well as mechanically from plant to plant field crops in this country. The only published record of TuMV but not by seed (Walsh & Jenner, 2002). occurrence in Ukraine describes a single virus- infected sample Journal of Phytopathology. 2018;166:429–437. wileyonlinelibrary.com/journal/jph © 2018 Blackwell Verlag GmbH | 429 430 | SHEVCHENKO ET AL. of wild orchid Orchis purpurea from the Crimea peninsula back in 2 | MATERIALS AND METHODS 2004. However, the virus was not recovered from the host plant (Korotieieva & Polishchuk, 2004). 2.1 | Sample collection TuMV isolates are biologically classified into five host infect- Samples were collected in the crop- producing areas of Kyiv ing types. [OM] host infecting type isolates infect some plants (northern central part of Ukraine) where Brassicaceae plants were of Brassicaceae but not Brassica plants. (B) host infecting type cultivated during the growing seasons of 2014–2015. Sampling lo- isolates infect Brassica plants latently and occasionally and do cations included two botanical gardens (Botanical garden of Taras not infect Raphanus plants. B host infecting type isolates infect Shevchenko National University of Kyiv and Botanical garden of many species of Brassica plants systemically with mosaic on un- the National Academy of Sciences of Ukraine), the city centre, inoculated leaves but do not infect Raphanus plants. B(R) host Museum of Folk Architecture and Life of Ukraine (open- air loca- infecting type isolates infect many species of Brassica plants sys- tion w/o agricultural activity), and private gardens where differ- temically with mosaic symptoms but occasionally infect Raphanus ent brassica plants were regularly cultivated. Several large fields plants, and BR host infecting type isolates infect both Brassica in Luka and Gorenychi villages used for commercial cabbage cul- and Raphanus plants systemically with mosaic symptoms (Nguyen tivation were chosen for sampling in Kyiv region. Brassica plants et al., 2013). (cabbage, red radish, mustard, gold of pleasure, hill mustard), Phylogenetic relationships using the genomic sequences of dif- showing TuMV- like symptoms of mosaic, mottling, vein banding ferent TuMV isolates collected from around the world showed that and/or leaf deformation, were collected. Some symptomatic non- TuMV isolates fall into six major TuMV phylogenetic groups called Brassicaceae species were also collected (Ohshima et al., 2002). Orchis, basal- Brassica (basal- B), Iranian, basal- Brassica/Raphanus Several leaves were collected from each plant, placed in airtight (basal- BR), Asian- Brassica/Raphanus (Asian- BR) and world- Brassica plastic bags filled with silica gel with colour indicator (Wako Pure (world- B) (Nguyen et al., 2013; Ohshima et al., 2002; Yasaka et al., Chemical Industries, Ltd., Osaka, Japan). 2017). The basal- B group of (B) or B host infecting type isolates is most variable, not monophyletic and originating from both non- brassicas and brassicas from Eurasia. Closest to it is the monophy- 2.2 | Enzyme- linked immunosorbent assay letic basal- BR group of BR host infecting type Eurasian isolates. The least variable group is the Asian- BR group formed by BR host Collected samples were tested for TuMV infection by direct infecting type isolates, mostly from Raphanus plants from East double- antibody sandwich enzyme- linked immunosorbent assay Asia. The world- B group is composed of isolates from all conti- (DAS- ELISA), as described by Clark and Adams (1977), using nents, mostly from brassicas, and consists of the B host infecting TuMV- specific polyclonal antibodies (Ohshima et al., 2002). type isolates from Europe and BR host infecting type isolates from Briefly, 0.5 g leaf tissue was ground to a powder with a mortar Asia. and pestle in 10 ml phosphate- buffered saline, pH 7.4, contain- The studies indicate that recombination plays an important role ing 0.05% Tween 20, 2.0% polyvinylpyrrolidone (MW 40 000) and in TuMV evolution. The phylogeographic analyses showed that 0.2% bovine serum albumin. Nunc MaxiSorp™ microtitre plates TuMV probably originated from a virus of wild orchids in Germany (Thermo Fisher Scientific K.K., Yokohama, Japan) were coated and, while adapting to wild and domestic brassicas, spread via with TuMV- specific polyclonal antibodies (1:200) in carbonate Southern Europe to Asia Minor no more than 850 years ago. The buffer. Leaf extracts were then added to the plates in duplicate populations of Orchis and basal- B group in Europe and Asia Minor wells and incubated for overnight at 4°C. The presence of TuMV in are older than other populations of this virus (Nguyen et al., 2013; the samples was detected in 200 μl homogenate by TuMV- specific Yasaka et al., 2017). antibodies conjugated to alkaline phosphatase using p- nitrophenyl Ukraine is also one of the possible candidates for the emergence phosphate substrate (Wako Pure Chemical Industries, Ltd.). of TuMV, as there are many different orchid species growing natu- Absorbance values at 405 nm were measured using a ImmunoMini rally, especially in the west of the country (Carpathian region) and in NJ- 2300 microtitre plate reader (BioTec Co. Ltd., Tokyo, Japan). its southern part (Crimea peninsula), but not exclusively. The exten- Absorbance values, measured 60 min after adding the substrate, sive list of Ukrainian orchid species includes Orchis militaris—one of greater than three times those of the negative controls were con- the tentative “hotbeds” of TuMV emergence. The discovery of TuMV sidered positive.
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