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Genome characterization of parsley severe stunt-associated virus in Iran

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Abstract

Parsley severe stunt-associated virus (PSSaV) is a recently identified nanovirus first reported in Germany. During a survey for identification of nanoviruses infecting apiaceous plants in south-eastern Iran, PSSaV was identified and characterized using a combination of rolling circle amplification (RCA) and high-throughput sequencing. Parsley plant samples were collected from vegetable production farms in Kerman province. From two symptomatic samples (39Ba and 40Ba), seven PSSaV components (DNA-C, -S, -M, -R, -N, -U1 and -U2) with two phylogenetically distinct variants of DNA-R (R1 and R2) were identified. In common with the German isolate of PSSaV, no DNA-U4 component was identified. In addition, associated alphasatellite molecules were identified in samples 39Ba [n = 6] and 40Ba [n = 5]. Sequence analyses showed that concatenated component sequences of the two Iranian PSSaVs share 97.2% nucleotide identity with each other and 82% to the German isolate. The coat proteins (CPs) of the PSSaV Iranian sequences share 97.2% amino acid identity and ~ 84% identity with that of the German isolate. Sequence and phylogenetic analyses of a total of 11 recovered alphasatellites from the two samples can be classified into the genera Fabenesatellite [n = 2], Milvetsatellite [n = 1], Mivedwarsatellite [n = 2], Subclovsatellite [n = 2], Sophoyesatellite [n = 4] in the family Alphasatellitidae. Identification of PSSaV and other nanoviruses in wild and cultivated plants in Iran reveals that nanoviruses could be causing yield reduction in crops plants in this country.

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References

  1. Abtahi F, Hosseini SA (2020) Incidence and distribution of Tobacco streak virus isolated from parsley Petroselinum sativum. J Crop Prot 9(4):683–997

    Google Scholar 

  2. Alavinejad E, Behjatnia SAA, Izadpanah K, Masoumi M (2011) Molecular detection of Faba bean necrotic yellows virus in legume fields of some North, North West and South provinces of Iran. In Proceedings of the 7th National Biotechnology Congress, Tehran, Iran, p 6

  3. Aronson MN, Meyer AD, Gyorgyey J, Katul L, Vetten HJ, Gronenborn B, Timchenko T (2000) Clink, a nanovirus-encoded protein, binds both pRB and SKP1. J Virol 74(7):2967–2972. https://doi.org/10.1128/jvi.74.7.2967-2972.2000

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215(3):403–410. https://doi.org/10.1016/S0022-2836(05)80360-2

    Article  CAS  PubMed  Google Scholar 

  5. Briddon RW, Martin DP, Roumagnac P, Navas-Castillo J, Fiallo-Olive E, Moriones E, Lett JM, Zerbini FM, Varsani A (2018) Alphasatellitidae: a new family with two subfamilies for the classification of geminivirus- and nanovirus-associated alphasatellites. Arch Virol 163:2587–2600. https://doi.org/10.1007/s00705-018-3854-2

    Article  CAS  PubMed  Google Scholar 

  6. Chu PW, Keese P, Qiu BS, Waterhouse PM, Gerlach WL (1993) Putative full-length clones of the genomic DNA segments of subterranean clover stunt virus and identification of the segment coding for the viral coat protein. Virus Res 27:161–171. https://doi.org/10.1016/0168-1702(93)90079-3

    Article  CAS  PubMed  Google Scholar 

  7. Crooks GE, Hon G, Chandonia JM, Brenner SE (2004) WebLogo: a sequence logo generator. Genome Res 14:1188–1190. https://doi.org/10.1101/gr.849004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772. https://doi.org/10.1038/nmeth.2109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Di Mattia J, Vernerey M-S, Yvon M, Pirolles E, Villegas M, Gaafar Y, Ziebell H, Michalakis Y, Zeddam J-L, Blanc S (2020) Route of a multipartite nanovirus across the body of its aphid vector. J Virol 94:e01998-e2019. https://doi.org/10.1128/JVI.01998-19

    Article  PubMed  PubMed Central  Google Scholar 

  10. Gallet R, Kraberger S, Filloux D, Galzi S, Fontes H, Martin DP, Varsani A, Roumagnac P (2018) Nanovirus-alphasatellite complex identified in Vicia cracca in the Rhone delta region of France. Arch Virol 163:695–700. https://doi.org/10.1007/s00705-017-3634-4

    Article  CAS  PubMed  Google Scholar 

  11. Grigoras I, Vetten HJ, Commandeur U, Ziebell H, Gronenborn B, Timchenko T (2018) Nanovirus DNA-N encodes a protein mandatory for aphid transmission. Virology 522:281–291. https://doi.org/10.1016/j.virol.2018.07.001

    Article  CAS  PubMed  Google Scholar 

  12. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321. https://doi.org/10.1093/sysbio/syq010

    Article  CAS  PubMed  Google Scholar 

  13. Hassan-Sheikhi P, Heydarnejad J, Massumi H, Kraberger S, Varsani A (2020) Novel nanovirus and associated alphasatellites identified in milk vetch plants with chlorotic dwarf disease in Iran. Virus Res 276:197830. https://doi.org/10.1016/j.virusres.2019.197830

    Article  CAS  PubMed  Google Scholar 

  14. Heydarnejad J, Kamali M, Massumi H, Kvarnheden A, Male MF, Kraberger S, Stainton D, Martin DP, Varsani A (2017) Identification of a nanovirus-alphasatellite complex in Sophora alopecuroides. Virus Res 235:24–32. https://doi.org/10.1016/j.virusres.2017.03.023

    Article  CAS  PubMed  Google Scholar 

  15. Heydarnejad J, Hassan-Sheikhi P, Bagheri S, Sadeghi-Majd J, Avish-Koohshahi A (2019) Natural hosts and transmission of Sophora yellow stunt-associated virus. Iran J Plant Pathol 54:291–303

    Google Scholar 

  16. Jackman SD, Vandervalk BP, Mohamadi H, Chu J, Yeo S, Hammond SA, Jahesh G, Khan H, Coombe L, Warren RL, Birol I (2017) ABySS 2.0: resource-efficient assembly of large genomes using a Bloom filter. Genome Res 27:768–777. https://doi.org/10.1101/gr.214346.116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Kalendar R, Samuilova O, Ivanov KI (2017) FastPCR: an in silico tool for fast primer and probe design and advanced sequence analysis. Genomics 109:312–319. https://doi.org/10.1016/j.ygeno.2017.05.005

    Article  CAS  PubMed  Google Scholar 

  18. Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780. https://doi.org/10.1093/molbev/mst010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Katul L, Maiss E, Morozov SY, Vetten HJ (1997) Analysis of six DNA components of the faba bean necrotic yellows virus genome and their structural affinity to related plant virus genomes. Virology 233:247–259. https://doi.org/10.1006/viro.1997.8611

    Article  CAS  PubMed  Google Scholar 

  20. Lageix S, Catrice O, Deragon JM, Gronenborn B, Pelissier T, Ramirez BC (2007) The nanovirus-encoded Clink protein affects plant cell cycle regulation through interaction with the retinoblastoma-related protein. J Virol 81:4177–4185. https://doi.org/10.1128/JVI.02103-06

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Lotfipour M, Izadpanah K, Behjatnia SAA (2017) Identification and molecular characterization of Faba bean necrotic stunt virus, a new nanovirus in legume fields in Iran. Iran J Plant Pathol 52:503–517

    Google Scholar 

  22. Makkouk KM, Fazlali Y, Kumari SG, Farzadfar S (2002) First record of Beet western yellows virus, Chickpea chlorotic dwarf virus, Faba bean necrotic yellows virus and Soybean dwarf virus infecting chickpea and lentil crops in Iran. Plant Pathol 51:387–387. https://doi.org/10.1046/j.1365-3059.2002.00700.x

    Article  Google Scholar 

  23. Ministry of Agriculture Jihad (2020) Agricultural statistics. Crops, vol 1. MAJ Publication (Persian), p 89

    Google Scholar 

  24. Muhire BM, Varsani A, Martin DP (2014) SDT: a virus classification tool based on pairwise sequence alignment and identity calculation. PLoS ONE 9:e108277. https://doi.org/10.1371/journal.pone.0108277

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Salehi M, Esmailzadeh Hosseini SA, Salehi E, Bertaccini A (2016) Detection and characterization of phytoplasma strains associated with field bindweed witches’ broom disease in Iran. J Phytopathol 164:996–1002. https://doi.org/10.1111/jph.12520

    Article  CAS  Google Scholar 

  26. Shepherd DN, Martin DP, Lefeuvre P, Monjane AL, Owor BE, Rybicki EP, Varsani A (2008) A protocol for the rapid isolation of full geminivirus genomes from dried plant tissue. J Virol Methods 149:97–102. https://doi.org/10.1016/j.jviromet.2007.12.014

    Article  CAS  PubMed  Google Scholar 

  27. Sokhansanj Y, Bananej K, Rakhshandehroo F, Ahoonmanesh A (2018) Molecular characterization of three Faba bean necrotic yellows virus (FBNYV) isolates, originated from chickpea in Iran. J Appl Entomol Phytopathol 86:75–90

    Google Scholar 

  28. Stover BC, Muller KF (2010) TreeGraph 2: combining and visualizing evidence from different phylogenetic analyses. BMC Bioinform 11:7. https://doi.org/10.1186/1471-2105-11-7

    Article  Google Scholar 

  29. Thomas JE, Gronenborn G, Harding RM, Mandal B, Grigoras I, Randles JW, Sano Y, Timchenko T, Vetten HJ, Yeh HH, Ziebell H (2021) ICTV virus taxonomy profile: Nanoviridae. J Gen Virol. https://doi.org/10.1099/jgv.0.001544

    Article  PubMed  PubMed Central  Google Scholar 

  30. Timchenko T, de Kouchkovsky F, Katul L, David C, Vetten HJ, Gronenborn B (1999) A single rep protein initiates replication of multiple genome components of faba bean necrotic yellows virus, a single-stranded DNA virus of plants. J Virol 73:10173–10182. https://doi.org/10.1128/JVI.73.12.10173-10182.1999

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Timchenko T, Katul L, Sano Y, de Kouchkovsky F, Vetten HJ, Gronenborn B (2000) The master rep concept in nanovirus replication: identification of missing genome components and potential for natural genetic reassortment. Virology 274:189–195. https://doi.org/10.1006/viro.2000.0439

    Article  CAS  PubMed  Google Scholar 

  32. Vetten HJ, Dale JL, Grigoras I, Gronenborn B, Harding R, Randles JW, Sano Y, Thomas JE, Timchenko T, Yeh H-H (2012) Family Nanoviridae. In: King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ (eds) Virus taxonomy. Ninth Report of the International Committee on taxonomy of viruses. Elsevier, London, pp 395–404

    Google Scholar 

  33. Vetten HJ, Knierim D, Rakoski MS, Menzel W, Maiss E, Gronenborn B, Winter S, Krenz B (2019) Identification of a novel nanovirus in parsley. Arch Virol 164:1883–1887. https://doi.org/10.1007/s00705-019-04280-3

    Article  CAS  PubMed  Google Scholar 

  34. Wanitchakorn R, Hafner GJ, Harding RM, Dale JL (2000) Functional analysis of proteins encoded by banana bunchy top virus DNA-4 to -6. J Gen Virol 81:299–306. https://doi.org/10.1099/0022-1317-81-1-299

    Article  CAS  PubMed  Google Scholar 

  35. Wyant PS, Strohmeier S, Schäfer B, Krenz B, Assunção IP, de Andrade Lima GS, Jeske H (2012) Circular DNA genomics (circomics) exemplified for geminiviruses in bean crops and weeds of northeastern Brazil. Virology 427(2):151–157. https://doi.org/10.1016/j.virol.2012.02.007

    Article  CAS  PubMed  Google Scholar 

  36. Zhang YP, Uyemoto JK, Kirkpatrick BC (1998) A small-scale procedure for extracting nucleic acids from woody plants infected with various phytopathogens for PCR assay. J Virol Methods 71:45–50. https://doi.org/10.1016/s0166-0934(97)00190-0

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This research work was supported by Research and Technology Institute of Plant Production (RTIPP), Shahid Bahonar University of Kerman, Iran (Grant No. P/900/106).

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VH, HJ and JH designed the study; TK, HJ, HM and JH prepared and provided laboratory support; VH and HJ amplified and sequenced viral genome components; VH, HJ, JH, RSF, SK and AV analysed the sequence data; JH and AV drafted the manuscript, and all authors read and approved the final version.

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Correspondence to Jahangir Heydanejad.

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Edited by Karel Petrzik.

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11262_2021_1835_MOESM1_ESM.xlsx

Supplementary Data 1. Pairwise identity matrices of the genome, individual components and those of the associated alphasatellites. Sequence of the DNA-U4 component of approved and proposed nanovirus species was removed to compare with the concatenated sequences of PSSaV. (XLSX 142 kb)

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Hasanvand, V., Heydanejad, J., Massumi, H. et al. Genome characterization of parsley severe stunt-associated virus in Iran. Virus Genes 57, 293–301 (2021). https://doi.org/10.1007/s11262-021-01835-y

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