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Identification of a Nanovirus-Alphasatellite Complex in Sophora Alopecuroides

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Identification of a Nanovirus-Alphasatellite Complex in Sophora Alopecuroides Accepted Manuscript Title: Identification of a nanovirus-alphasatellite complex in Sophora alopecuroides Author: Jahangir Heydarnejad Mehdi Kamali Hossain Massumi Anders Kvarnheden Maketalena F. Male Simona Kraberger Daisy Stainton Darren P. Martin Arvind Varsani PII: S0168-1702(17)30009-6 DOI: http://dx.doi.org/doi:10.1016/j.virusres.2017.03.023 Reference: VIRUS 97113 To appear in: Virus Research Received date: 5-1-2017 Revised date: 15-3-2017 Accepted date: 18-3-2017 Please cite this article as: Heydarnejad, J., Kamali, M., Massumi, H., Kvarnheden, A., Male, M.F., Kraberger, S., Stainton, D., Martin, D.P., Varsani, A.,Identification of a nanovirus-alphasatellite complex in Sophora alopecuroides, Virus Research (2017), http://dx.doi.org/10.1016/j.virusres.2017.03.023 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. 1 Identification of a nanovirus-alphasatellite complex in Sophora alopecuroides 2 Jahangir Heydarnejad 1* , Mehdi Kamali 1, Hossain Massumi 1, Anders Kvarnheden 2, Maketalena 3 F. Male 3, Simona Kraberger 3,4 , Daisy Stainton 3,5 , Darren P. Martin 6 and Arvind Varsani 3,7,8* 4 5 1Department of Plant Protection, College of Agriculture, Shahid Bahonar University of Kerman, 6 Kerman, Iran 7 2Department of Plant Biology, Uppsala BioCenter, Linnean Center of Plant Biology in Uppsala, 8 Swedish University of Agricultural Sciences, Box 7080, SE-750 07 Uppsala, Sweden 9 3School of Biological Sciences, University of Canterbury, Private Bag 4800, Christchurch, 8140, 10 New Zealand 11 4Department of Microbiology, Immunology and Pathology, Colorado State University, Fort 12 Collins, CO 80523, USA 13 5School of Biological Sciences, The University of Queensland, Brisbane, Queensland 4072, 14 Australia 15 6Computational Biology Group, Institute of Infectious Disease and Molecular Medicine, 16 University of Cape Town Faculty of Health Sciences, Observatory 7925. South Africa 17 7Structural Biology Research Unit, Department of Clinical Laboratory Sciences, University of 18 Cape Town, Rondebosch, 7701, Cape Town, South Africa 19 8The Biodesign Center for Fundamental and Applied Microbiomics, Center for Evolution and 20 Medicine, School of Life Sciences, Arizona State University, Tempe, AZ 85287-5001, USA 21 22 *Corresponding authors 23 Dr Jahangir Heydarnejad, Department of Plant Protection, College of Agriculture, Shahid 24 Bahonar University of Kerman, Kerman, Iran, Fax: 0098 341 3222043, E-mail: 25 [email protected] Manuscript 26 Assoc Prof. Arvind Varsani, The Biodesign Center for Fundamental and Applied Microbiomics, 27 Center for Evolution and Medicine, School of Life Sciences, Arizona State University, Tempe, 28 AZ 85287-5001, USA, Tel: +1 480 410 9366. E-mail: [email protected] 29 1 Page 1 of 23 30 Key words: Nanovirus; Sophora alopecuroides ; Iran; alphasatellite; high throughput sequencing 31 Accepted Manuscript 2 Page 2 of 23 31 Abstract 32 Viruses in the genus Nanovirus of the family Nanoviridae generally have eight individually 33 encapsidated circular genome components and have been predominantly found infecting 34 Fabaceae plants in Europe, Australia, Africa and Asia. For over a decade Sophora alopecuroides 35 L. (Fabaceae) plants have been observed across Iran displaying dwarfing, yellowing, stunted 36 leaves and yellow vein banding. Using a high-throughput sequencing approach, sequences were 37 identified within one such plant that had similarities to nanovirus genome components. From this 38 plant, the nanovirus-like molecules DNA-R (n=4), DNA-C (n=2), DNA-S (n=1), DNA-M (n=1), 39 DNA-N (n=1), DNA-U1 (n=1), DNA-U2 (n=1) and DNA-U4 (n=1) were amplified, cloned and 40 sequenced. Other than for the DNA-R, these components share less than 71% identity with those 41 of other known nanoviruses. The four DNA-R molecules were highly diverse, sharing only 65- 42 71% identity with each other and 64-86% identity with those of other nanoviruses. In the S. 43 alopecuroides plant 14 molecules sharing 57.7-84.6% identity with previously determined 44 sequences of nanovirus-associated alphasatellites were also identified. Given the research 45 activity in the nanovirus field during the last five years coupled with high-throughput sequence 46 technologies, many more diverse nanoviruses and nanovirus-associated satellites are likely to be 47 identified. 48 Accepted Manuscript 3 Page 3 of 23 48 1. Introduction 49 The family Nanoviridae contains plant-infecting viruses with multi-component single-stranded 50 DNA (ssDNA) genomes that are individually encapsidated within isometric 17-20 nm virions. 51 The two genera within the family, Nanovirus and Babuvirus, are differentiated based on their 52 biological and genomic properties. Viruses in both genera are transmitted by aphids with 53 members of the genus Nanovirus infecting dicotyledonous host plants and those of the genus 54 Babuvirus infecting monocotyledonous plants. Also, whereas members of the genus Nanovirus 55 have eight genome components (named DNA-R, DNA-S, DNA-M, DNA-C, DNA-N, DNA-U1, 56 DNA-U2 and DNA-U4) that are between 970 and 1021 nucleotides (nts) in length, members of 57 the genus Babuvirus have six components (DNA-R, DNA-S, DNA-M, DNA-C, DNA-N, and 58 DNA-U3) that are between 1013 and 1116 nts in length (Table 1) (Vetten et al. , 2012). 59 60 There are presently eight recognized species in the genus Nanovirus (Table 1) (Abraham et al. , 61 2012; Boevink et al. , 1995; Chu and Helms, 1988; Grigoras et al. , 2014; Grigoras et al. , 2010; 62 Grigoras et al. , 2009; Katul et al. , 1998; Sano et al. , 1998), which have so far been found 63 infecting various predominantly leguminous species (Table 1). The host symptoms include 64 stunting, necrosis, leaf yellowing or reddening and leaf curling (Vetten et al. , 2012). 65 66 The DNA-R, DNA-S, DNA-M, DNA-C and DNA-N components of nanoviruses and 67 babuviruses are homologous and all encode a protein of known function. DNA-R encodes a 68 replication-associated protein (Rep) (Burns et al. , 1995; Hafner et al. , 1997; Harding et al. , 1993) 69 which is involved in replicating all canonical components. DNA-S encodes the capsid protein 70 (CP); (Wanitchakorn et al. , 1997). DNA-C encodes a cell-cycle link protein (Clink) which is 71 involved in switchingAccepted the plant host into DNA repli Manuscriptcation or S-phase to increase replication of 72 the other components (Aronson et al. , 2000; Lageix et al. , 2007; Wanitchakorn et al. , 2000). 73 DNA-M encodes a movement protein (MP) and based on cellular localisation studies DNA-N 74 encodes a putative nuclear shuttle protein (NSP) (Wanitchakorn et al. , 2000). The DNA-U1, 75 DNA-U2, and DNA-U4 components have unknown functions. 4 Page 4 of 23 76 77 The components of a nanovirus genome share two homologous regions: the common region 78 stem-loop (CR-I) and the common region II (CR-II). In addition to the canonical genome 79 components, nanoviruses have also been found associated with satellite molecules known as 80 alphasatellites. Like the canonical DNA-R component, these molecules contain a rep -like gene, 81 however, unlike DNA-R, they are unable to trans-replicate the canonical genome components 82 with which they are associated (Horser et al. , 2001; Timchenko et al. , 1999; Timchenko et al. , 83 2000). Alphasatellites that are related to those of nanoviruses are also found associated with 84 viruses in the genera Begomovirus and Mastrevirus of the family Geminiviridae (Kumar et al. , 85 2014; Zhou, 2013). 86 87 Sophora alopecuroides L. (Fabaceae) is a wild perennial herb that is widely distributed across 88 the arid and semi-arid regions of Iran and other parts of Asia (Bisby et al. , 1994). It is primarily 89 used as livestock feed but in traditional Chinese medicine it is also used to treat fever and 90 diarrhea (Song et al. , 1999; Zhao et al. , 2013). Over the past decade in Iran S. alopecuroides 91 plants have been observed throughout most parts of the country with apparent disease symptoms 92 including severe yellowing and stunting, shrunken leaves and yellow vein banding (Figure 1). In 93 this report a putative nanovirus in the genus Nanovirus recovered from S. alopecuroides is 94 described. 95 96 2. Materials and methods 97 2.1 DNA isolation, amplification of circular molecules and Illumina sequencing 98 A symptomatic Acceptedsample of Sophora alopecuroides Manuscript L. (Fabaceae; Figure 1) was collected at 99 Shahid Bahonar University of Kerman (Kerman, Iran) in 2014 and total DNA was extracted 100 according to Zhang et al. (1998). Circular DNA sequences were amplified using rolling circle 101 amplification with Phi29 DNA polymerase as previously described (Shepherd et al. , 2008). The 5 Page 5 of 23 102 amplified circular DNA was sequenced on an Illumina HiSeq 2500 sequencer at Noveogene 103 (Hong Kong). 104 105 2.2 De novo assembly of Illumina sequencing reads and analysis of resulting contigs 106 The Illumina sequenced paired-end reads were de novo assembled using ABySS v1.9 (Simpson 107 et al. , 2009) assembler. Contigs of >500 nts were analyzed using BLASTn and BLASTx 108 (Altschul et al. , 1990) against a viral database to identify viral-like contigs. In the 3366 contigs 109 that were > 500 nts viral sequences were identified that shared similarities to nanovirus 110 components and alphasatellite sequences. 111 112 2.3 Recovery and characterization of circular molecules with viral and alphasatellite 113 sequences 114 Abutting primers were designed for all de novo assembled contigs that had similarities to 115 nanovirus and alphasatellite sequences in order to recover, verify and archive the DNA 116 molecules.
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