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Coleus blumei viroid 7: a novel viroid resulting from genome recombination between Coleus blumei viroids 1 and 5

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Abstract

The genus Coleviroid, family Pospiviroidae, comprises six known viroids, all infecting Plectranthus scutellarioides (Coleus blumei; coleus). In 2017, a novel viroid-like RNA sequence that shares ca. 65% identity with Coleus blumei viroid 1 (CbVd-1) was identified in a coleus cultivar infected by multiple coleviroids. Further sequence and secondary structure analyses are consistent with the discovery of a seventh viroid in the genus Coleviroid: tentatively named "Coleus blumei viroid 7" (CbVd-7). The viroid appears to be the product of a natural recombination event between CbVd-1 and Coleus blumei viroid 5. We prove CbVd-7 to be infectious and in turn demonstrate the ability of all known coleviroid left- and right-arm segments to recombine. With a length of 234 nucleotides, this is the smallest viroid described to date.

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References

  1. Škorić D (2017) Viroid Biology. Chapter 5. In: Hadidi A, Flores R, Randles JW, Palukaitis P (eds) Viroids and satellites. Academic Press, Elsevier, Amsterdam, pp 53–61

    Chapter  Google Scholar 

  2. Hadidi A, Flores R, Randles JW, Semancik JS (2003) Viroids. CSIRO Publishing, Collingwood

    Book  Google Scholar 

  3. Flores R, Hernández C, Martínez de Alba AE, Daròs J-A, Di Serio F (2005) Viroids and viroid-host interactions. Annu Rev Phytopathol 43:117–139

    Article  CAS  Google Scholar 

  4. Nie X, Singh RP (2017) Coleus blumei viroids. Chapter 27. In: Hadidi A, Flores R, Randles JW, Palukaitis P (eds) Viroids and satellites. Academic Press, Elsevier, Amsterdam, pp 289–295

    Chapter  Google Scholar 

  5. Spieker RL (1996) In vitro-generated “inverse” chimeric Coleus blumei viroids evolve in vivo into infectious RNA replicons. J Gen Virol 77:2839–2846

    Article  CAS  Google Scholar 

  6. Hou WY, Sano T, Li F, Wu ZJ, Li L, Li SF (2009) Identification and characterization of a new coleviroid (CbVd-5). Arch Virol 154:315–320

    Article  CAS  Google Scholar 

  7. Hou WY, Li SF, Wu ZJ, Jiang DM, Sano T (2009) Coleus blumei viroid 6: a new tentative member of the genus Coleviroid derived from natural genome shuffling. Arch Virol 154:993–997

    Article  CAS  Google Scholar 

  8. Jiang DM, Li SF, Fu FH, Wu ZJ, Xie LH (2013) First report of Coleus blumei viroid 5 from Coleus blumei in India and Indonesia. Plant Dis 97:561

    Article  CAS  Google Scholar 

  9. Roslan NNC, Thanarajoo SS, Kadir J, Kong LL, Vadamalai G (2017) First report of Coleus blumei viroid in Malaysia. J Plant Pathol 99:800

    Google Scholar 

  10. Škorić D, Černi S, Jezernik K, Butković A (2019) Molecular characterization of Coleus blumei viroids 1 and 3 in Plectranthus scutellarioides in Croatia. Eur J Plant Pathol 155:731–742

    Article  Google Scholar 

  11. Jiang D, Gao R, Qin L, Wu Z, Xie L, Hou W, Li S (2014) Infectious cDNA clones of four viroids in Coleus blumei and molecular characterization of their progeny. Virus Res 180:97–101

    Article  CAS  Google Scholar 

  12. Spieker RL, Marinkovic S, Sanger HL (1996) A new sequence variant of Coleus blumei viroid 3 from the Coleus blumei cultivar “Fairway Ruby.” Arch Virol 141:1377

    Article  CAS  Google Scholar 

  13. Chung BN, Choi GS (2008) Incidence of Coleus blumei viroid 1 in seeds of commercial coleus in Korea. Plant Pathol J 24:305–308

    Article  CAS  Google Scholar 

  14. Smith RL, Lawrence J, Shukla M, Singh M, Li X, Xu H, Gardner K, Nie X (2018) First report of Coleus blumei viroid 5 and molecular confirmation of Coleus blumei viroid 1 in commercial Coleus blumei in Canada. Plant Dis 102:1862

    Article  CAS  Google Scholar 

  15. Nie X, Singh RP (2001) Differential accumulation of Potato virus A and expression of pathogenesis-related genes in resistant potato cv. Shepody upon graft inoculation. Phytopathology 91:197–203

    Article  CAS  Google Scholar 

  16. Singh RP (1991) Return-polyacrylamide gel electrophoresis for the detection of viroids. In: Maramorosch K (ed) Viroids and Satellites: molecular parasites at the frontier of life. CRC Press, Boca Raton, pp 89–107

    Google Scholar 

  17. Nilsen TW (2013) Gel purification of RNA. Cold Spring Harb Protoc 2013:180–183

    PubMed  Google Scholar 

  18. Jiang D, Wu Z, Xie L, Sano T, Li S (2011) Sap-direct RT-PCR for the rapid detection of Coleus blumei viroids of the genus Coleviroid from natural host plants. J Virol Methods 174:123–127

    Article  CAS  Google Scholar 

  19. Owens RA, Flores R, Di Serio F, Li SF, Pallás V, Randles JW, Sano T, Vidalakis G (2012) Viroids. In: King AMQ, Adams MJ, Carstens EB, Lefkowits EJ (eds) Virus taxonomy: classification and nomenclature of viruses. Ninth Report of the International Committee on Taxonomy of Viruses. Academic Press, Elsevier, London, pp 1221–1234

  20. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Söding J, Thompson JD, Higgins DG (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7:539

    Article  Google Scholar 

  21. Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    Article  CAS  Google Scholar 

  22. Zuker M (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31:3406–3415

    Article  CAS  Google Scholar 

  23. Sano T, Candresse T, Hammond RW, Diener TO, Owens RA (1992) Identification of multiple structural domains regulating viroid pathogenicity. Proc Natl Acad Sci USA 89:10104–10108

    Article  CAS  Google Scholar 

  24. Sano T, Ishiguro A (1998) Viability and pathogenicity of inter subgroup viroid chimeras suggest possible involvement of the terminal right region in replication. Virology 240:238–244

    Article  CAS  Google Scholar 

  25. Smith RL, Lawrence J, Shukla M, Singh M, Li SX, Xu H, Chen D, Gardner K, Nie X (2019) Occurrence of Coleus blumei viroid 6 in commercial Coleus blumei in Canada—the first report outside of China. Plant Dis 103:782

    Article  Google Scholar 

  26. Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754–1760

    Article  CAS  Google Scholar 

  27. Chiumenti M, Navarro B, Chandresse T, Flores R, Di Serio F (2021) Reassessing species demarcation criteria in viroid taxonomy by pairwise identity matrices. Virus Evol 7(1):veab001

    Article  Google Scholar 

  28. Kofalvi S, Marcos JF, Canizares MC, Pallas V, Candresse T (1997) Hop stunt viroid (HSVd) sequence variants from Prunus species: evidence for recombination between HSVd isolates. J Gen Virol 78:3177–3186

    Article  CAS  Google Scholar 

  29. Rezaian MA (1990) Australian grapevine viroid - evidence for extensive recombination between viroids. Nucl Acids Res 18:1813–1818

    Article  CAS  Google Scholar 

  30. Sano T, Isono S, Matsuki K, Kawaguchi-Ito Y, Tanaka K, Kondo K, Iijima A, Bar-Joseph M (2009) Vegetative propagation and its possible role as a genetic bottleneck in the shaping of the apple fruit crinkle viroid populations in apple and hop plants. Virus Genes 37:298–303

    Article  Google Scholar 

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

    Article  Google Scholar 

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Acknowledgements

This work was supported in part by the Canadian Food Inspection Agency (Project no. CHA-P-1601) and Agriculture and Agri-Food Canada (Project no. J-001508). The authors thank Jingbai Nie, Yasmine Soqrat, and Cassandra Gilchrist for technical assistance; the greenhouse staff of Agriculture and Agri-Food Canada’s Fredericton Research and Development Centre for maintenance of plants; and the anonymous nursery for cooperation in sample collection.

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Author notes

  1. Ryan L. Smith, Manisha Shukla, and Alexa Creelman have contributed equally to this work.

Authors and Affiliations

  1. Fredericton Research and Development Centre, Agriculture and Agri-Food Canada, 850 Lincoln Road, Fredericton, NB, E3B 4Z7, Canada

    Ryan L. Smith, Manisha Shukla, Alexa Creelman, Kyle Gardner & Xianzhou Nie

  2. Department of Biology, University of New Brunswick, P.O. Box 4400, Fredericton, NB, E3B 5A3, Canada

    Ryan L. Smith & Janice Lawrence

  3. Agricultural Certification Services, 1030 Lincoln Road, Fredericton, NB, E3B 8B7, Canada

    Mathuresh Singh

  4. Canadian Food Inspection Agency, Charlottetown Laboratory, 93 Mount Edward Road, Charlottetown, PE, C1A 5T1, Canada

    Huimin Xu & Xiang Li

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  1. Ryan L. Smith
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Correspondence to Xianzhou Nie.

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Supplementary Information

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705_2021_5201_MOESM1_ESM.jpg

Supplementary file1 Supplementary Fig. S1 Return-polyacrylamide gel electrophoresis (R-PAGE) detection of viroids in different plant species. R-PAGE was performed as described by Singh (1991) [16]. Lane 1, tomato; lane 2, Vinca major; lanes 3 and 4, Coleus blumei. Viroid-suspect fragments are indicated by arrows (JPG 198 KB)

705_2021_5201_MOESM2_ESM.jpg

Supplementary file2 Supplementary Fig. S2 Reverse transcription polymerase chain reaction (RT-PCR) detection of Coleus blumei viroid 7 (CbVd-7) in coleus plants inoculated with CbVd-7 transcripts. Left panel, RT-PCR assays with different primer combinations on representative samples. Lane M, 1-kb Plus DNA Ladder (Invitrogen); lanes 1-6, coleus plants (cv. Pinto) inoculated with CbVd-7 monomer (lanes 1-3) and dimer (lane 4-6) transcripts; lanes 7-9, coleus plants infected with CbVd-1, -5, and -7, respectively; lane 10, CbVd-free plant; lane 11, no-template control. Plants sampled in lanes 2 and 3 were confirmed via amplicon sequencing to be successfully inoculated with CbVd-7. The PCR products at the anticipated sizes are indicated by arrows. Right panel, diagram of the viroids and the primer locations and orientations. The numbers in the diagram indicate the starting and the ending nucleotide positions of the primers corresponding to the respective viroids. The orientations of the primers are indicated by arrows. Plants sampled in lanes 2 and 3 were confirmed via amplicon sequencing to be successfully inoculated with CbVd-7. Primer sequences, which are described in the main text, are also shown at the bottom of this figure (JPG 554 KB)

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Smith, R.L., Shukla, M., Creelman, A. et al. Coleus blumei viroid 7: a novel viroid resulting from genome recombination between Coleus blumei viroids 1 and 5. Arch Virol 166, 3157–3163 (2021). https://doi.org/10.1007/s00705-021-05201-z

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