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Yellow Tailflower Mild Mottle Virus and Pelargonium Zonate Spot Virusco-Infect a Wild Plant of Red-Striped Tailflower in Australia

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Yellow Tailflower Mild Mottle Virus and Pelargonium Zonate Spot Virusco-Infect a Wild Plant of Red-Striped Tailflower in Australia MURDOCH RESEARCH REPOSITORY This is the author’s final version of the work, as accepted for publication following peer review but without the publisher’s layout or pagination. The definitive version is available at : http://dx.doi.org/10.1111/ppa.12416 Li, H., Zhang, C., Luo, H., Jones, M.G.K., Sivasithamparam, K., Koh, S-H, Ong, J.W.L. and Wylie, S.J. (2016) Yellow tailflower mild mottle virus and Pelargonium zonate spot virusco-infect a wild plant of red-striped tailflower in Australia. Plant Pathology, 65 (3). pp. 503-509. http://researchrepository.murdoch.edu.a/27335/ Copyright: © 2015 British Society for Plant Pathology It is posted here for your personal use. No further distribution is permitted. Article Type: Original Article Yellow tailflower mild mottle virus and Pelargonium zonate spot virus co-infect a wild plant of red-striped tailflower in Australia Hua Li, C. Zhang, H. Luo, M.G.K. Jones, K. Sivasithamparam, S-H Koh, J.W.L. Ong, S.J. Wylie* Plant Biotechnology Group –Plant Virology, Western Australian State Agricultural Biotechnology Centre, School of Veterinary and Life Sciences, Murdoch University, Perth, Western Australia 6150, Australia. Article *Corresponding author. Email: [email protected] Running head: YTMMV, PZSV infect Anthocercis ilicifolia Key words: Plant virus ecology; Solanaceae; tobamovirus; anulavirus, indigenous plant virus, virus invasion, virus emergenc Abstract Isolates of an Australian indigenous virus Yellow tailflower mild mottle virus (YTMMV- Kalbarri) and an exotic virus Pelargonium zonate spot virus (PZSV-SW13) are described from Anthocercis ilicifolia Hook. subspecies ilicifolia (red striped tailflower, family Solanaceae), a species endemic to Western Australia. This is the first report of either virus from this plant species. The complete genome sequences of YTMMV-Kalbarri and of PZSV- This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. Please cite this article as doi: 10.1111/ppa.12416 Accepted This article is protected by copyright. All rights reserved. SW13 were obtained. YTMMV-Kalbarri shared 97% nucleotide pairwise identity with the sequence of the type isolate YTMMV-Cervantes. The sequence PZSV-SW13 shared greatest sequence identity with the partial sequence of an Australian isolate of PZSV also from a wild plant, and with a sunflower-derived isolate of PZSV from Argentina. An experimental host range study was done of YTMMV-Kalbarri using cultivated and wild solanaceous and non- solanaceous plants. Most solanaceous plants became systemically infected, with symptoms of systemic infection ranging from asymptomatic to whole plant necrosis. Based on these studies, we suggest that YTMMV has the potential to become a pathogen of commercial species of Solanaceae. This study provides further evidence that PZSV is present in wild plants in Australia, in this case an indigenous host species, and possible routes by which it Article invaded Australia are discussed. Introduction Anthocercis (family Solanaceae, subfamily Nicotianoideae) is a genus of 15 plant species endemic to southern Australia (Haegi, 1986). Previously, we isolated a tobamovirus (Genus Tobamovirus, family Virgaviridae) from A. littoria (yellow tailflower), a spindly shrub 3 m in height that grows along the coastline in calcareous sand, limestone ridges and sand dunes on south-western Australia, but the virus was not detected from A. viscosa (sticky tailflower) plants growing in Albany, 400 km to the south. The new tobamovirus was named Yellow tailflower mild mottle virus (YTMMV) (Wylie et al 2014). Pelargonium zonate spot virus (PZSV) (genus Anulavirus, family Bromoviridae) was first isolated from Pelargonium zonale (Geraniaceae) in Italy (Quacquarelli and Gallitelli, 1979), but has since been shown to have a broader host range, notably capsicum and tomato (Solanaceae), in which it is vertically transmitted, sunflower and globe artichoke This article is protected by copyright. All rights reserved. Accepted (Asteraceae), kiwifruit (Actinidiaceae), and several weeds from the families Brassicaceae, some of which it has been shown to be vertically transmitted in, and Asteraceae (Gallitelli, 1982; Luis-Arteaga et al. 2000; Gebre-Selassie et al. 2002; Finetti-Sialer and Gallitelli, 2003; Liu and Sears, 2007; Escriu et al. 2009; Gulati-Sakhuja et al. 2009; Lapidot et al. 2010; Biccheri et al. 2012; Giolitti et al. 2014). Its geographical range includes much of Europe and the Americas. In Australia, PZSV was recently described for the first time in Cakile maritima (Brassicaceae), a self-introduced exotic weed species (Luo et al. 2010). Here, we describe the complete genome sequences of new isolates of YTMMV and PZSV that co-infected a wild plant of Anthocercis ilicifolia subsp. ilicifolia (red-striped tailflower), Article a new host species for both viruses. Although details of the host range of PZSV have been published, the potential host range of YTMMV is not known. The natural hosts of YTMMV live at the interface between wild and managed systems, and consequently the opportunity exists for the virus to expand its host range into cultivated plant species. Thus, we undertook an experimental host range study of the new YTMMV isolate and the type YTMMV isolate, and we discuss the potential of YTMMV to emerge as a pathogen of commercial importance. Further, we speculate as to how PZSV may have entered Australia, given that it has not yet been detected there in commercial plantings. Materials and Methods Virus identification In October 2013 leaves were collected from a red striped tailflower plant exhibiting leaf chlorosis and a number of dead or dying branches (Fig. 1a). The plant was in visibly poor health amongst a group of more healthy-looking plants scattered along a limestone ridge overlooking the Indian Ocean near the coastal town of Kalbarri. Total nucleic acids were This article is protected by copyright. All rights reserved. Accepted extracted from 1 g of leaves and enriched for dsRNA using a cellulose-based method (Morris and Dodds, 1979) modified by replacing Whatman CF11 cellulose powder with Machery- Nagel MN100 cellulose powder. cDNA was synthesized from 1 μg heat denatured RNA using adaptor-tailed random primers and GoScript™ reverse transcription system (Promega). PCR amplification was carried out using tagged primers that annealed to the adaptor sequences at the ends of cDNA strands. Amplicons were purified using Mag PCR clean-up beads (Axygen Biosciences). Library construction and paired-end sequencing of cDNA over 150 cycles using Illumina HiSeq2000 technology (Illumina Inc, San Diego, CA) were done by Macrogen Inc, Seoul. Article Analysis of sequences and assembly of contigs were done after trimming off 20 nucleotides (nt) from each end of each sequence read. The ‘De Novo Assembly’ function in CLC Genomics Workbench v7 (Qiagen) was used with default (automatic) word size and bubble size. Contigs sequences were used to interrogate NCBI GenBank using BlastN and BlastX, and sequences representing genomes of YTMMV-Kalbarri and PZSV-SW13 RNAs 1-3 were identified. Editing and alignment of contigs to generate consensus nucleotide (nt) and amino acid (aa) sequences were done in CLC Genomics Workbench using a Gap open cost of 10 and Gap extension cost of 1.0. Experimental host range of YTMMV Macerated leaf material from the original host plants of YTMMV-Kalbarri and YTMMV- Cervantes was inoculated to plants of N. benthamiana (accession RA-4). Virus-specific primers (below) were used to confirm that severely symptomatic N. benthamiana plants were infected with YTMMV, but not with PZSV. Macerated leaf material from symptomatic N. benthamiana plants was used to inoculate 1-12 plants each of 12 solanaceous species in five This article is protected by copyright. All rights reserved. Accepted genera, comprising commercial species, weeds, and two indigenous species. Additionally, 3- 6 plants of 16 non-solanaceous species were inoculated with the same inoculum (Table 1). Inoculum consisted of macerated new leaves of YTMMV-infected N. benthamiana mixed with chilled 100 mM phosphate buffer (pH 7.0). This was gently applied to leaves of test plants using diatomaceous earth (Sigma-Alrich) as an abrasive. In each case, an equal number of mock-inoculated plants were tested. Plants were grown in a rotted bark and sand mix to which 5 g each of lime and dolomite and 40 g of slow release NPK fertiliser were added per 40 L of potting mix. Plants were grown in a temperature-controlled and insect-proof glasshouse under natural light at 22°C and scored for symptoms there 35 days post- inoculation (dpi). The presence of YTMMV was tested for using virus-specific primers Article (below). Symptom development indices. Symptom development was monitored on inoculated plants every day until 35 dpi when they were scored using a simple qualitative assessment of symptom severity: 1. No infection as determined by RT-PCR using YTMMV-specific primers 2. Local lesions or asymptomatic presence in inoculated leaves only. No systemic infection detected. 3. No symptoms of infection observed. Systemic spread confirmed by RT-PCR. 4. Mild symptoms of chlorosis, mosaic and/or leaf deformation evident. Slight stunting may be evident. Ring patterns or small necrotic lesions sometimes visible. 5. Moderate symptoms of chlorosis, mosaic and/or leaf deformation. Moderate
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