Viruses representing two new genomovirus species identified in citrus from Tunisia

Abstract

Using a high-throughput sequencing approach, we identified four genomoviruses (family Genomoviridae) associated with a sweet orange (Citrus sinensis) plant collected in Tunisia. The ssDNA genomes of these genomoviruses, which were amplified, cloned and Sanger sequenced, range in size from 2156 to 2191 nt. Three of these viruses share > 99% full-genome pairwise sequence identity and are referred to as citrus Tunisia genomovirus 1 (CTNGmV-1). The CTNGmV-1 isolates share < 62% genome-wide pairwise nucleotide sequence identity with other genomoviruses and belong to the genus Gemykolovirus. The genome of the fourth virus, which was called CTNGmV-2, shares < 68% nucleotide sequence identity with other genomoviruses and belongs to the genus Gemycircularvirus. Based on the species demarcation criteria for members of the family Genomoviridae, CTNGmV-1 and -2 would each represent a new species. Although found associated with Citrus sp. plants, it is likely that these viruses infect fungi or other organisms associated with the plants.

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References

  1. 1.

    Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    CAS  Google Scholar 

  2. 2.

    Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PA (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455–477

    CAS  Article  Google Scholar 

  3. 3.

    Chiumenti M, Greco C, Antelmi I, Sion V, Altamura G, Nigro F, Saldarelli P (2019) Molecular characterisation of a novel gemycircularvirus associated with olive trees in Italy. Virus Res 263:169–172

    CAS  Article  Google Scholar 

  4. 4.

    Conceicao-Neto N, Zeller M, Heylen E, Lefrere H, Mesquita JR, Matthijnssens J (2015) Fecal virome analysis of three carnivores reveals a novel nodavirus and multiple gemycircularviruses. Virol J 12:79

    Article  Google Scholar 

  5. 5.

    Darriba D, Taboada GL, Doallo R, Posada D (2011) ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 27:1164–1165

    CAS  Article  Google Scholar 

  6. 6.

    Dayaram A, Opong A, Jaschke A, Hadfield J, Baschiera M, Dobson RC, Offei SK, Shepherd DN, Martin DP, Varsani A (2012) Molecular characterisation of a novel cassava associated circular ssDNA virus. Virus Res 166:130–135

    CAS  Article  Google Scholar 

  7. 7.

    FAO (2015) Citrus fruit statistics 2015. http://www.fao.org/3/a-i5558e.pdf

  8. 8.

    Geering ADW, Hull R (2012) Family—Caulimoviridae. In: King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ (eds) Virus taxonomy. Elsevier, San Diego, pp 429–443

    Google Scholar 

  9. 9.

    Guindon S, Dufayard J-F, 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(3):307–321

    CAS  Article  Google Scholar 

  10. 10.

    King AM, Lefkowitz E, Adams MJ, Carstens EB (2011) Virus taxonomy: ninth report of the International Committee on Taxonomy of Viruses. Elsevier, Oxford

    Google Scholar 

  11. 11.

    Kraberger S, Waits K, Ivan J, Newkirk E, VandeWoude S, Varsani A (2018) Identification of circular single-stranded DNA viruses in faecal samples of Canada lynx (Lynx canadensis), moose (Alces alces) and snowshoe hare (Lepus americanus) inhabiting the Colorado San Juan Mountains. Infect Genet Evol 64:1–8

    CAS  Article  Google Scholar 

  12. 12.

    Krupovic M, Ghabrial SA, Jiang D, Varsani A (2016) Genomoviridae: a new family of widespread single-stranded DNA viruses. Arch Virol 161:2633–2643

    CAS  Article  Google Scholar 

  13. 13.

    Lamas NS, Fontenele RS, Melo FL, Costa AF, Varsani A, Ribeiro SG (2016) Complete genome sequence of a genomovirus associated with common bean plant leaves in Brazil. Genome Announc 4:e01247

    Article  Google Scholar 

  14. 14.

    Letunic I, Bork P (2016) Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res 44:W242–W245

    CAS  Article  Google Scholar 

  15. 15.

    Liu S, Xie J, Cheng J, Li B, Chen T, Fu Y, Li G, Wang M, Jin H, Wan H, Jiang D (2016) Fungal DNA virus infects a mycophagous insect and utilizes it as a transmission vector. Proc Natl Acad Sci USA 113:12803–12808

    CAS  Article  Google Scholar 

  16. 16.

    Loconsole G, Saldarelli P, Doddapaneni H, Savino V, Martelli GP, Saponari M (2012) Identification of a single-stranded DNA virus associated with citrus chlorotic dwarf disease, a new member in the family Geminiviridae. Virology 432:162–172

    CAS  Article  Google Scholar 

  17. 17.

    Marzano SL, Domier LL (2016) Novel mycoviruses discovered from metatranscriptomics survey of soybean phyllosphere phytobiomes. Virus Res 213:332–342

    CAS  Article  Google Scholar 

  18. 18.

    Muhire BM, Varsani A, Martin DP (2014) SDT: a virus classification tool based on pairwise sequence alignment and identity calculation. PLoS One 9:e108277

    Article  Google Scholar 

  19. 19.

    Nakasu EYT, Melo FL, Michereff M, Nagata T, Ribeiro BM, Ribeiro SG, Lacorte C, Inoue-Nagata AK (2017) Discovery of two small circular ssDNA viruses associated with the whitefly Bemisia tabaci (vol 162, pg 2835, 2017). Arch Virol 162:3563–3566

    CAS  Article  Google Scholar 

  20. 20.

    Navarro B, Minutolo M, De Stradis A, Palmisano F, Alioto D, Di Serio F (2018) The first phlebo-like virus infecting plants: a case study on the adaptation of negative-stranded RNA viruses to new hosts. Mol Plant Pathol 19:1075–1089

    CAS  Article  Google Scholar 

  21. 21.

    Navarro B, Zicca S, Minutolo M, Saponari M, Alioto D, Di Serio F (2018) A negative-stranded rna virus infecting citrus trees: the second member of a new genus within the order bunyavirales. Front Microbiol 9:2340

    Article  Google Scholar 

  22. 22.

    Umer M, Liu JW, You HF, Xu C, Dong KL, Luo N, Kong LH, Li XP, Hong N, Wang GP, Fan XD, Kotta-Loizou I, Xu W (2019) Genomic, morphological and biological traits of the viruses infecting major fruit trees. Virus Basel 11:515

    CAS  Article  Google Scholar 

  23. 23.

    Varsani A, Krupovic M (2017) Sequence-based taxonomic framework for the classification of uncultured single-stranded DNA viruses of the family Genomoviridae. Virus Evol 3:vew037

    Article  Google Scholar 

  24. 24.

    Xu L, Li G, Jiang D, Chen W (2018) Sclerotinia sclerotiorum: an evaluation of virulence theories. Annu Rev Phytopathol 56:311–338

    CAS  Article  Google Scholar 

  25. 25.

    Yu X, Li B, Fu Y, Jiang D, Ghabrial SA, Li G, Peng Y, Xie J, Cheng J, Huang J, Yi X (2010) A geminivirus-related DNA mycovirus that confers hypovirulence to a plant pathogenic fungus. Proc Natl Acad Sci USA 107:8387–8392

    CAS  Article  Google Scholar 

  26. 26.

    Zerbini FM, Briddon RW, Idris A, Martin DP, Moriones E, Navas-Castillo J, Rivera-Bustamante R, Roumagnac P, Varsani A, Ictv Report C (2017) ICTV virus taxonomy profile: geminiviridae. J Gen Virol 98:131–133

    CAS  Article  Google Scholar 

  27. 27.

    Zhang W, Yang SX, Shan TL, Hou R, Liu ZJ, Li W, Guo LH, Wang Y, Chen P, Wang XC, Feng FF, Wang H, Chen C, Shen Q, Zhou CL, Hua XG, Cui L, Deng XT, Zhang ZH, Qi DW, Delwart E (2017) Virome comparisons in wild-diseased and healthy captive giant pandas. Microbiome 5:90

    Article  Google Scholar 

  28. 28.

    Zhao L, Rosario K, Breitbart M, Duffy S (2019) Eukaryotic circular rep-encoding single-stranded DNA (CRESS DNA) viruses: ubiquitous viruses with small genomes and a diverse host range. Adv Virus Res 103:71–133

    CAS  Article  Google Scholar 

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Acknowledgements

C.C-J was supported by a Research Internship Scholarships Abroad (BEPE) project (number 2019/08186-2) funded by São Paulo Research Foundation (FAPESP).

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Correspondence to Asma Najar or Arvind Varsani.

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GenBank accession nos. MN708482–MN708485.

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Chabi-Jesus, C., Najar, A., Fontenele, R.S. et al. Viruses representing two new genomovirus species identified in citrus from Tunisia. Arch Virol 165, 1225–1229 (2020). https://doi.org/10.1007/s00705-020-04569-8

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