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Wisteria Vein Mosaic Virus Detected for the First Time in Iran from an Unknown Host by Analysis of Aphid Vectors

  • Valouzi, Hajar (Department of Plant Protection, Faculty of Agricultural Sciences and Food Industries, Science and Research Branch, Islamic Azad University) ;
  • Hashemi, Seyedeh-Shahrzad (Department of Plant Protection, Faculty of Agricultural Sciences and Food Industries, Science and Research Branch, Islamic Azad University) ;
  • Wylie, Stephen J. (Plant Biotechnology Research Group - Virology, State Agricultural Biotechnology Centre, Murdoch University) ;
  • Ahadiyat, Ali (Department of Plant Protection, Faculty of Agricultural Sciences and Food Industries, Science and Research Branch, Islamic Azad University) ;
  • Golnaraghi, Alireza (Department of Plant Protection, Faculty of Agricultural Sciences and Food Industries, Science and Research Branch, Islamic Azad University)
  • Received : 2019.10.29
  • Accepted : 2019.12.23
  • Published : 2020.02.01

Abstract

The development of reverse transcription-polymerase chain reaction using degenerate primers against conserved regions of most potyviral genomes enabled sampling of the potyvirome. However, these assays usually involve sampling potential host plants, but identifying infected plants when they are asymptomatic is challenging, and many plants, especially wild ones, contain inhibitors to DNA amplification. We used an alternative approach which utilized aphid vectors and indicator plants to identify potyviruses capable of infecting common bean (Phaseolus vulgaris). Aphids were collected from a range of asymptomatic leguminous weeds and trees in Iran, and transferred to bean seedlings under controlled conditions. Bean plants were tested serologically for potyvirus infections four-weeks postinoculation. The serological assay and symptomatology together indicated the presence of one potyvirus, and symptomology alone implied the presence of an unidentified virus. The partial genome of the potyvirus, encompassing the complete coat protein gene, was amplified using generic potyvirus primers. Sequence analysis of the amplicon confirmed the presence of an isolate of Wisteria vein mosaic virus (WVMV), a virus species not previously identified from Western Asia. Phylogenetic analyses of available WVMV sequences categorized them into five groups: East Asian-1 to 3, North American and World. The Iranian isolate clustered with those in the World group. Multiple sequence alignment indicated the presence of some genogroup-specific amino acid substitutions among the isolates studied. Chinese isolates were sister groups of other isolates and showed higher nucleotide distances as compared with the others, suggesting a possible Eastern-Asian origin of WVMV, the main region where Wisteria might have originated.

Keywords

References

  1. Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W. and Lipman, D. J. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402. https://doi.org/10.1093/nar/25.17.3389
  2. Atoni, E., Wang, Y., Karungu, S., Waruhiu, C., Zohaib, A., Obanda, V., Agwanda, B., Mutua, M., Xia, H. and Yuan, Z. 2018. Metagenomic virome analysis of Culex mosquitoes from Kenya and China. Viruses 10:30. https://doi.org/10.3390/v10010030
  3. Bos, L. 1996. Wisteria vein mosaic potyvirus. In: Viruses of plants: descriptions and lists from the VIDE Database, eds. by A. A. Brunt, K. Crabtree, M. J. Dallwitz, A. J. Gibbs and L. Watson, pp. 1407-1409. CAB International, Wallingford, UK.
  4. Brunt, A. A., Crabtree, K., Dallwitz, M. J., Gibbs, A. J. and Watson, L. 1996. Viruses of plants: descriptions and lists from the VIDE Database. CAB International, Wallingford, UK. 1504 pp.
  5. Clover, G. R. G., Denton, J. O. and Denton, G. J. 2015. First report of Wisteria vein mosaic virus on Wisteria spp. in the United Kingdom. New Dis. Rep. 31:1. https://doi.org/10.5197/j.2044-0588.2015.031.001
  6. Clover, G. R. G., Tang, Z., Smales, T. E. and Pearson, M. N. 2003. Taxonomy of Wisteria vein mosaic virus and extensions to its host range and geographical distribution. Plant Pathol. 52:92-96. https://doi.org/10.1046/j.1365-3059.2003.00798.x
  7. de Fatima Rosas-Cardenas, F., Duran-Figueroa, N., Vielle-Calzada, J.-P., Cruz-Hernandez, A., Marsch-Martinez, N. and de Folter, S. 2011. A simple and efficient method for isolating small RNAs from different plant species. Plant Methods 7:4. https://doi.org/10.1186/1746-4811-7-4
  8. Donaldson, E. F., Haskew, A. N., Gates, J. E., Huynh, J., Moore, C. J. and Frieman, M. B. 2010. Metagenomic analysis of the viromes of three North American bat species: viral diversity among different bat species that share a common habitat. J. Virol. 84:13004-13018. https://doi.org/10.1128/JVI.01255-10
  9. Esfandiari, N., Kohi-Habibi, M. and Mosahebi, G. 2006. Occurrence of viruses infecting pea in Iran. Commun. Agric. Appl. Biol. Sci. 71:1281-1287.
  10. Farzadfar, S., Golnaraghi, A. R. and Pourrahim, R. 2002. Plant viruses of Iran. Saman Company, Tehran, Iran. 203 pp.
  11. Farzadfar, S., Tomitaka, Y., Ikematsu, M., Golnaraghi, A. R., Pourrahim, R. and Ohshima, K. 2009. Molecular characterisation of Turnip mosaic virus isolates from Brassicaceae weeds. Eur. J. Plant Pathol. 124:45-55. https://doi.org/10.1007/s10658-008-9390-2
  12. Feng, Y., Krueger, E. N., Liu, S., Dorman, K., Bonning, B. C. and Miller, W. A. 2017. Discovery of known and novel viral genomes in soybean aphid by deep sequencing. Phytobiomes 1:36-45. https://doi.org/10.1094/PBIOMES-11-16-0013-R
  13. Fereres, A. and Raccah, B. 2015. Plant virus transmission by insects. URL https://doi.org/10.1002/9780470015902.a0000760.pub3 [29 October 2019].
  14. Foottit, R. G., Maw, H. E. L., Von Dohlen, C. D. and Hebert, P. D. N. 2008. Species identification of aphids (Insecta: Hemiptera: Aphididae) through DNA barcodes. Mol. Ecol. Resour. 8:1189-1201. https://doi.org/10.1111/j.1755-0998.2008.02297.x
  15. Golnaraghi, A., Shahraeen, N. and Nguyen, H. D. 2018. Characterization and genetic structure of a Tospovirus causing chlorotic ring spots and chlorosis disease on peanut; comparison with Iranian and Polish populations of Tomato yellow fruit ring virus. Plant Dis. 102:1509-1519. https://doi.org/10.1094/PDIS-09-17-1350-RE
  16. Golnaraghi, A. R., Shahraeen, N., Pourrahim, R., Farzadfar, S. and Ghasemi, A. 2004. Occurrence and relative incidence of viruses infecting soybeans in Iran. Plant Dis. 88:1069-1074. https://doi.org/10.1094/PDIS.2004.88.10.1069
  17. Guerrieri, E. and Digilio, M. C. 2008. Aphid-plant interactions: a review. J. Plant Interact. 3:223-232. https://doi.org/10.1080/17429140802567173
  18. Ha, C., Coombs, S., Revill, P. A., Harding, R. M., Vu, M. and Dale, J. L. 2008. Design and application of two novel degenerate primer pairs for the detection and complete genomic characterization of potyviruses. Arch. Virol. 153:25-36. https://doi.org/10.1007/s00705-007-1053-7
  19. Hall, T. A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/ NT. Nucleic Acids Symp. Ser. 41:95-98.
  20. Harrington, R., Katis, N. and Gibson, R. W. 1986. Field assessment of the relative importance of different aphid species in the transmission of potato virus Y. Potato Res. 29:67-76. https://doi.org/10.1007/BF02361982
  21. Hashemi, S. 2015. Distribution model of aphid species as vectors of potyviruses of legumes in climates of Iran with an emphasis on the climates of Markazi province. M.Sc. thesis. Science and Research Branch, Islamic Azad University, Tehran, Iran.
  22. Hull, R. 2014. Plant virology. 5th ed. Academic Press, Amsterdam, Netherlands. 1104 pp.
  23. Islam, W., Lin, W., Islam, S. U., Arif, M., Li, X., Yang, Y., Ding, X., Du, Z. and Wu, Z. 2018. Genetic diversity of begomoviruses in Pakistan captured through a vector based survey. Microb. Pathogen. 118:91-97. https://doi.org/10.1016/j.micpath.2018.03.019
  24. Ji, Z.-L., Zhu, P.-X., Ji, Y.-H., Xu, F. and Zhu, F. 2019. First report of wisteria vein mosaic virus in Chinese wisteria in Jiangxi Province in China. J. Plant Pathol. 101:1259-1260. https://doi.org/10.1007/s42161-019-00318-2
  25. Jo, Y., Lian, S., Chu, H., Cho, J. K., Yoo, S.-H., Choi, H., Yoon, J.-Y., Choi, S.-K., Lee, B. C. and Cho, W. K. 2018. Peach RNA viromes in six different peach cultivars. Sci. Rep. 8:1844. https://doi.org/10.1038/s41598-018-20256-w
  26. Jones, D. R. 2005. Plant viruses transmitted by thrips. Eur. J. Plant Pathol. 113:119-157. https://doi.org/10.1007/s10658-005-2334-1
  27. Jones, S., Baizan-Edge, A., MacFarlane, S. and Torrance, L. 2017. Viral diagnostics in plants using next generation sequencing: computational analysis in practice. Front. Plant Sci. 8:1770. https://doi.org/10.3389/fpls.2017.01770
  28. Kaiser, W. J., Danesh, D., Okhovat, M. and Mossahebi, H. 1968. Diseases of pulse crops (edible legumes) in Iran. Plant Dis. Rep. 52:687-689.
  29. Kaminska, M., Malinowski, T., Rudzinska-Langwald, A. and Diaz, L. C. 2006. The occurrence of Wisteria vein mosaic virus in Wisteria floribunda DC plants in Poland. J. Phytopathol. 154:414-417. https://doi.org/10.1111/j.1439-0434.2006.01118.x
  30. Letunic, I. and Bork, P. 2019. Interactive tree of life (iTOL) v4: recent updates and new developments. Nucleic Acids Res. 47:W256-W259. https://doi.org/10.1093/nar/gkz239
  31. Li., J., Jiang, J.-H., Fu, C.-X. and Tang, S.-Q. 2014. Molecular systematics and biogeography of Wisteria inferred from nucleotide sequences of nuclear and plastid genes. J. Syst. Evol. 52:40-50. https://doi.org/10.1111/jse.12061
  32. Li, L., Victoria, J. G., Wang, C., Jones, M., Fellers, G. M., Kunz, T. H. and Delwart, E. 2010. Bat guano virome: predominance of dietary viruses from insects and plants plus novel mammalian viruses. J. Virol. 84:6955-6965. https://doi.org/10.1128/JVI.00501-10
  33. Liang, W. X., Song, L. M., Li, Y., Tian, G. Z., Li, H. F. and Fan, Z. F. 2004. First report of Wisteria vein mosaic virus in China. Plant Pathol. 53:516. https://doi.org/10.1111/j.1365-3059.2004.01035.x
  34. Liang, W. X., Song, L. M., Tian, G. Z., Li, H. F. and Fan, Z. F. 2006. The genomic sequence of Wisteria vein mosaic virus and its similarities with other potyviruses. Arch. Virol. 151:2311-2319. https://doi.org/10.1007/s00705-006-0780-5
  35. Liu, S., Vijayendran, D., Chen, Y. and Bonning, B. 2016. Aphis glycines virus 2, a novel insect virus with a unique genome structure. Viruses 8:315. https://doi.org/10.3390/v8110315
  36. MacDiarmid, R., Rodoni, B., Melcher, U., Ochoa-Corona, F. and Roossinck, M. 2013. Biosecurity implications of new technology and discovery in plant virus research. PLoS Pathog. 9:e1003337. https://doi.org/10.1371/journal.ppat.1003337
  37. Martin, D. P., Murrell, B., Golden, M., Khoosal, A. and Muhire, B. 2015. RDP4: detection and analysis of recombination patterns in virus genomes. Virus Evol. 1:vev003.
  38. Moury, B., Fabre, F. and Senoussi, R. 2007. Estimation of the number of virus particles transmitted by an insect vector. Proc. Natl. Acad. Sci. U. S. A. 104:17891-17896. https://doi.org/10.1073/pnas.0702739104
  39. Mowat, W. P. and Dawson, S. 1987. Detection and identification of plant viruses by ELISA using crude sap extracts and unfractionated antisera. J. Virol. Methods 15:233-247. https://doi.org/10.1016/0166-0934(87)90101-7
  40. Mozaffarian, V. 2013. Identification of medicinal and aromatic plants of Iran. Farhang Moaser Publishers, Tehran, Iran. 1350 pp.
  41. Mumford, R., Boonham, N., Tomlinson, J. and Barker, I. 2006. Advances in molecular phytodiagnostics: new solutions for old problems. Eur. J. Plant Pathol. 116:1-19. https://doi.org/10.1007/s10658-006-9037-0
  42. Naidu, R. A. and Karthikeyan, G. 2008. First report of Wisteria vein mosaic virus in Wisteria sinensis in the United States of America. Plant Health Prog. 9:42. https://doi.org/10.1094/PHP-2008-0818-01-BR
  43. Ong, J. W. L., Li, H., Sivasithamparam, K., Dixon, K. W., Jones, M. G. K. and Wylie, S. J. 2017. The challenges of using highthroughput sequencing to track multiple bipartite mycoviruses of wild orchid-fungus partnerships over consecutive years. Virology 510:297-304. https://doi.org/10.1016/j.virol.2017.07.031
  44. Paez-Espino, D., Eloe-Fadrosh, E. A., Pavlopoulos, G. A., Thomas, A. D., Huntemann, M., Mikhailova, N., Rubin, E., Ivanova, N. N. and Kyrpides, N. C. 2016. Uncovering Earth's virome. Nature 536:425-430. https://doi.org/10.1038/nature19094
  45. Pappu, S. S., Brand, R., Pappu, H. R., Rybicki, E. P., Gough, K. H., Frenkel, M. J. and Niblett, C. L. 1993. A polymerase chain reaction method adapted for selective amplification and cloning of 3' sequences of potyviral genomes: application to dasheen mosaic virus. J. Virol. Methods 41:9-20. https://doi.org/10.1016/0166-0934(93)90158-N
  46. Pettersson, J. H.-O., Shi, M., Bohlin, J., Eldholm, V., Brynildsrud, O. B., Paulsen, K. M., Andreassen, A. and Holmes, E. C. 2017. Characterizing the virome of Ixodes ricinus ticks from northern Europe. Sci. Rep. 7:10870. https://doi.org/10.1038/s41598-017-11439-y
  47. Posada, D. 2002. Evaluation of methods for detecting recombination from DNA sequences: empirical data. Mol. Biol. Evol. 19:708-717. https://doi.org/10.1093/oxfordjournals.molbev.a004129
  48. Roossinck, M. J. 2012. Plant virus metagenomics: biodiversity and ecology. Annu. Rev. Genet. 46:359-369. https://doi.org/10.1146/annurev-genet-110711-155600
  49. Schrader, C., Schielke, A., Ellerbroek, L. and Johne, R. 2012. PCR inhibitors - occurrence, properties and removal. J. Appl. Microbiol. 113:1014-1026. https://doi.org/10.1111/j.1365-2672.2012.05384.x
  50. Shahraeen, N., Ghotbi, T., Elkhache, A. D. and Sahandi, A. 2005. A survey of viruses affecting French bean (Phaseolus vulgaris) in Iran includes a first report of Southern bean mosaic virus and Bean pod mottle virus. Plant Dis. 89:1012.
  51. Tamura, K., Stecher, G., Peterson, D., Filipski, A. and Kumar, S. 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30:2725-2729. https://doi.org/10.1093/molbev/mst197
  52. Valouzi, H., Golnaraghi, A., Abedini-Aminabad, L. and Diyanat, M. 2017. Serological and molecular identification of Turnip mosaic virus in some wild plants in Iran. Australas. Plant Dis. Notes 12:3. https://doi.org/10.1007/s13314-016-0225-2
  53. Virgin, H. W. 2014. The virome in mammalian physiology and disease. Cell 157:142-150. https://doi.org/10.1016/j.cell.2014.02.032
  54. Wamonje, F. O., Michuki, G. N., Braidwood, L. A., Njuguna, J. N., Musembi Mutuku, J., Djikeng, A., Harvey, J. J. W. and Carr, J. P. 2017. Viral metagenomics of aphids present in bean and maize plots on mixed-use farms in Kenya reveals the presence of three dicistroviruses including a novel Big Sioux River virus-like dicistrovirus. Virol. J. 14:188. https://doi.org/10.1186/s12985-017-0854-x
  55. Ward, L. I., Tang, J. Z. and Clover, G. R. G. 2008. First report of Wisteria vein mosaic virus on Wisteria sinensis in New Zealand. Plant Dis. 92:1134.
  56. Wegley, L., Edwards, R., Rodriguez-Brito, B., Liu, H. and Rohwer, F. 2007. Metagenomic analysis of the microbial community associated with the coral Porites astreoides. Environ. Microbiol. 9:2707-2719. https://doi.org/10.1111/j.1462-2920.2007.01383.x
  57. Whitfield, A. E., Falk, B. W. and Rotenberg, D. 2015. Insect vector-mediated transmission of plant viruses. Virology 479- 480:278-289. https://doi.org/10.1016/j.virol.2015.03.026
  58. Wylie, S. J., Adams, M., Chalam, C., Kreuze, J., Lopez-Moya, J. J., Ohshima, K., Praveen, S., Rabenstein, F., Stenger, D., Wang, A., Zerbini, F. M. and ICTV Report Consortium. 2017. ICTV Virus Taxonomy Profile: Potyviridae. J. Gen. Virol. 98:352-354. https://doi.org/10.1099/jgv.0.000740
  59. Wylie, S. J. and Jones, M. G. K. 2012. Complete genome sequences of seven carlavirus and potyvirus isolates from Narcissus and Hippeastrum plants in Australia, and proposals to clarify their naming. Arch. Virol. 157:1471-1480. https://doi.org/10.1007/s00705-012-1319-6
  60. Wylie, S. J., Li, H., Dixon, K. W., Richards, H. and Jones, M. G. K. 2013. Exotic and indigenous viruses infect wild populations and captive collections of temperate terrestrial orchids (Diuris species) in Australia. Virus Res. 171:22-32. https://doi.org/10.1016/j.virusres.2012.10.003
  61. Wylie, S. J., Li, H., Saqib, M. and Jones, M. G. K. 2014. The global trade in fresh produce and the vagility of plant viruses: a case study in garlic. PLoS ONE 9:e105044. https://doi.org/10.1371/journal.pone.0105044
  62. Wylie, S. J., Luo, H., Li, H. and Jones, M. G. K. 2012. Multiple polyadenylated RNA viruses detected in pooled cultivated and wild plant samples. Arch. Virol. 157:271-284. https://doi.org/10.1007/s00705-011-1166-x
  63. Yasaka, R., Fukagawa, H., Ikematsu, M., Soda, H., Korkmaz, S., Golnaraghi, A., Katis, N., Ho, S. Y. W., Gibbs, A. J. and Ohshima, K. 2017. The timescale of emergence and spread of Turnip mosaic Potyvirus. Sci. Rep. 7:4240. https://doi.org/10.1038/s41598-017-01934-7
  64. Zheng, L., Rodoni, B. C., Gibbs, M. J. and Gibbs, A. J. 2010. A novel pair of universal primers for the detection of potyviruses. Plant Pathol. 59:211-220. https://doi.org/10.1111/j.1365-3059.2009.02201.x