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Volume 94, Issue 4

Dahlia latent viroid: a recombinant new species of the family posing intriguing questions about its origin and classification Free

Abstract

A viroid-like RNA has been detected in two asymptomatic dahlia accessions by return and double PAGE. It appeared smaller than and , the two members of the genus , family , reported in this ornamental previously. RT-PCR with primers designed for amplifying all pospiviroids produced no amplicons, but RT-PCR with random primers revealed a 342 nt RNA. The sequence of this RNA was confirmed with specific primers, which additionally revealed its presence in many dahlia cultivars. The RNA was named (DLVd) because it replicates autonomously, but symptomlessly, in dahlia and shares maximum sequence identity with other viroids of less than 56 %. Furthermore, DLVd displays characteristic features of the family : a predicted rod-like secondary structure of minimum free energy with a central conserved region (CCR), and the ability to form the metastable structures hairpins I and II. Its CCR is identical to that of (HSVd, genus ). However, DLVd: (i) has the terminal conserved region present in members of the genus , but absent in HSVd, and (ii) lacks the terminal conserved hairpin present in HSVd. Phylogenetic reconstructions indicate that HSVd and (genus ) are the closest relatives of DLVd, but DLVd differs from these viroids in its host range, restricted to dahlia so far. Therefore, while DLVd fulfils the criteria to be a novel species of the family , its recombinant origin makes assignment to the genera or problematic.

  • Received:
  • Accepted:
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© 2013 SGM
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2013-04-01
2024-04-24
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References

  1. Abraitiene A., Zhao Y., Hammond R. 2008; Nuclear targeting by fragmentation of the potato spindle tuber viroid genome. Biochem Biophys Res Commun 368:470–475 [View Article][PubMed]
     [Google Scholar]
  2. Boonham N., Pérez L. G., Mendez M. S., Peralta E. L., Blockley A., Walsh K., Barker I., Mumford R. A. 2004; Development of a real-time RT-PCR assay for the detection of potato spindle tuber viroid. J Virol Methods 116:139–146 [View Article][PubMed]
     [Google Scholar]
  3. Botermans M., van de Vossenberg B. T. L. H., Verhoeven J. Th. J., Roenhorst J. W., Hooftman M., Dekter R., Meekes E. T. M. 2013; Development and validation of a real-time RT-PCR assay for generic detection of pospiviroids. J Virol Methods 187:43–50 [View Article][PubMed]
     [Google Scholar]
  4. Candresse T., Góra-Sochacka A., Zagórski W. 2001; Restoration of secondary hairpin II is associated with restoration of infectivity of a non-viable recombinant viroid. Virus Res 75:29–34 [View Article][PubMed]
     [Google Scholar]
  5. De Rijk P., Wuyts J., De Wachter R. 2003; RnaViz 2: an improved representation of RNA secondary structure. Bioinformatics 19:299–300 [View Article][PubMed]
     [Google Scholar]
  6. Diener T. O. 2003; Discovering viroids–a personal perspective. Nat Rev Microbiol 1:75–80 [View Article][PubMed]
     [Google Scholar]
  7. Ding B. 2009; The biology of viroid–host interactions. Annu Rev Phytopathol 47:105–131 [View Article][PubMed]
     [Google Scholar]
  8. Felsenstein J. 1985; Confidence limits on phylogenies: an approach using the boot-strap. Evolution 39:783–791 [View Article]
     [Google Scholar]
  9. Flores R., Durán-Vila N., Pallás V., Semancik J. S. 1985; Detection of viroid and viroid-like RNAs from grapevine. J Gen Virol 66:2095–2102 [View Article]
     [Google Scholar]
  10. Flores R., Di Serio F., Hernández C. 1997; Viroids: the non-coding genomes. Semin Virol 8:65–73 [View Article]
     [Google Scholar]
  11. Flores R., Randles J. W., Bar-Joseph M., Diener T. O. 1998; A proposed scheme for viroid classification and nomenclature. Arch Virol 143:623–629 [View Article][PubMed]
     [Google Scholar]
  12. Flores R., Daròs J. A., Hernández C. 2000; Avsunviroidae family: viroids containing hammerhead ribozymes. Adv Virus Res 55:271–323 [View Article][PubMed]
     [Google Scholar]
  13. Flores R., Hernández C., Martínez de Alba A. E., Daròs J. A., Di Serio F. 2005; Viroids and viroid–host interactions. Annu Rev Phytopathol 43:117–139 [View Article][PubMed]
     [Google Scholar]
  14. Flores R., Serra P., Minoia S., Di Serio F., Navarro B. 2012; Viroids: from genotype to phenotype just relying on RNA sequence and structural motifs. Front Microbiol 3: article 217
    [Google Scholar]
  15. Gas M. E., Hernández C., Flores R., Daròs J. A. 2007; Processing of nuclear viroids in vivo: an interplay between RNA conformations. PLoS Pathog 3:e182 [View Article][PubMed]
     [Google Scholar]
  16. Gozmanova M., Denti M. A., Minkov I. N., Tsagris M., Tabler M. 2003; Characterization of the RNA motif responsible for the specific interaction of potato spindle tuber viroid RNA (PSTVd) and the tomato protein Virp1. Nucleic Acids Res 31:5534–5543 [View Article][PubMed]
     [Google Scholar]
  17. Hammond R., Smith D. R., Diener T. O. 1989; Nucleotide sequence and proposed secondary structure of Columnea latent viroid: a natural mosaic of viroid sequences. Nucleic Acids Res 17:10083–10094 [View Article][PubMed]
     [Google Scholar]
  18. Henco K., Sänger H. L., Riesner D. 1979; Fine structure melting of viroids as studied by kinetic methods. Nucleic Acids Res 6:3041–3059 [View Article][PubMed]
     [Google Scholar]
  19. Hu C. C., Hsu Y. H., Lin N. S. 2009; Satellite RNAs and satellite viruses of plants. Viruses 1:1325–1350 [View Article][PubMed]
     [Google Scholar]
  20. Hutchins C. J., Rathjen P. D., Forster A. C., Symons R. H. 1986; Self-cleavage of plus and minus RNA transcripts of avocado sunblotch viroid. Nucleic Acids Res 14:3627–3640 [View Article][PubMed]
     [Google Scholar]
  21. Keese P., Symons R. H. 1985; Domains in viroids: evidence of intermolecular RNA rearrangements and their contribution to viroid evolution. Proc Natl Acad Sci U S A 82:4582–4586 [View Article][PubMed]
     [Google Scholar]
  22. Koltunow A. M., Rezaian M. A. 1988; Grapevine yellow speckle viroid: structural features of a new viroid group. Nucleic Acids Res 16:849–864 [View Article][PubMed]
     [Google Scholar]
  23. Larkin M. A., Blackshields G., Brown N. P., Chenna R., McGettigan P. A., McWilliam H., Valentin F., Wallace I. M., Wilm A. other authors 2007; clustal w and clustal x version 2.0. Bioinformatics 23:2947–2948 [View Article][PubMed]
     [Google Scholar]
  24. Maniataki E., Martinez de Alba A. E., Sägesser R., Tabler M., Tsagris M. 2003; Viroid RNA systemic spread may depend on the interaction of a 71-nucleotide bulged hairpin with the host protein VirP1. RNA 9:346–354 [View Article][PubMed]
     [Google Scholar]
  25. McInnes J. L., Symons R. H. 1991; Comparative structure of viroids and their rapid detection using radioactive and nonradioactive nucleic acid probes. In Viroids and Satellites: Molecular Parasites at the Frontier of Life pp. 21–58 Edited by Maramorosch K. Boca Raton, FL: CRC Press;
     [Google Scholar]
  26. Nakashima A., Hosokawa M., Maeda S., Yazawa S. 2007; Natural infection of chrysanthemum stunt viroid in dahlia plants. J Gen Plant Pathol 73:225–227 [View Article]
     [Google Scholar]
  27. Navarro B., Daròs J. A., Flores R. 1996; A general strategy for cloning viroids and other small circular RNAs that uses minimal amounts of template and does not require prior knowledge of its sequence. J Virol Methods 56:59–66 [View Article][PubMed]
     [Google Scholar]
  28. Ohno T., Takamatsu N., Meshi T., Okada Y. 1983; Hop stunt viroid: molecular cloning and nucleotide sequence of the complete cDNA copy. Nucleic Acids Res 11:6185–6197 [View Article][PubMed]
     [Google Scholar]
  29. Osaki H., Ohtsu Y., Kudo A. 1998; Two rapid extraction methods to detect apple scar skin and hop stunt viroids by RT-PCR. Acta Hortic 472:603–611
     [Google Scholar]
  30. Owens R. A., Flores R., Di Serio F., Li S.-F., Pallás V., Randles J. W., Sano T., Vidalakis G. 2011; Viroids. In Virus Taxonomy. Ninth Report of the International Committee on Taxonomy of Viruses pp. 1221–1234 Edited by King A. M. Q., Adams M. J., Carstens E. B., Lefkowitz E. J. London, UK: Elsevier Academic Press;
     [Google Scholar]
  31. Pallás V., Navarro A., Flores R. 1987; Isolation of a viroid-like RNA from hop different from hop stunt viroid. J Gen Virol 68:3201–3205 [View Article]
     [Google Scholar]
  32. Qu F., Heinrich C., Loss P., Steger G., Tien P., Riesner D. 1993; Multiple pathways of reversion in viroids for conservation of structural elements. EMBO J 12:2129–2139[PubMed]
     [Google Scholar]
  33. Riesner D. 1991; Viroids: from thermodynamics to cellular structure and function. Mol Plant Microbe Interact 4:122–131 [View Article][PubMed]
     [Google Scholar]
  34. Riesner D., Henco K., Rokohl U., Klotz G., Kleinschmidt A. K., Domdey H., Jank P., Gross H. J., Sänger H. L. 1979; Structure and structure formation of viroids. J Mol Biol 133:85–115 [View Article][PubMed]
     [Google Scholar]
  35. Rivera-Bustamante R. F., Gin R., Semancik J. S. 1986; Enhanced resolution of circular and linear molecular forms of viroid and viroid-like RNA by electrophoresis in a discontinuous-pH system. Anal Biochem 156:91–95 [View Article][PubMed]
     [Google Scholar]
  36. Roenhorst J. W., Butôt R. P. T., Van der Heijden K. A., Hooftman M., Van Zaayen A. 2000; Detection of chrysanthemum stunt viroid and potato spindle tuber viroid by return-polyacrylamide gel electrophoresis. EPPO Bull 30:453–456 [CrossRef]
     [Google Scholar]
  37. Saitou N., Nei M. 1987; The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425[PubMed]
     [Google Scholar]
  38. Sambrook J., Russell D. W. 2001 Molecular Cloning: a Laboratory Manual, 3rd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
     [Google Scholar]
  39. Sänger H. L., Klotz G., Riesner D., Gross H. J., Kleinschmidt A. K. 1976; Viroids are single-stranded covalently closed circular RNA molecules existing as highly base-paired rod-like structures. Proc Natl Acad Sci U S A 73:3852–3856 [View Article][PubMed]
     [Google Scholar]
  40. Schumacher J., Meyer N., Riesner D., Weidemann H. L. 1986; Diagnostic procedure for detection of viroids and viruses with circular RNAs by return-gel electrophoresis. J Phytopathol 115:332–343 [View Article]
     [Google Scholar]
  41. Serra P., Barbosa C. J., Daròs J. A., Flores R., Duran-Vila N. 2008; Citrus viroid V: molecular characterization and synergistic interactions with other members of the genus Apscaviroid . Virology 370:102–112 [View Article][PubMed]
     [Google Scholar]
  42. Takeda R., Ding B. 2009; Viroid intercellular trafficking: RNA motifs, cellular factors and broad impacts. Viruses 1:210–221 [View Article][PubMed]
     [Google Scholar]
  43. Tamura K., Nei M., Kumar S. 2004; Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Natl Acad Sci U S A 101:11030–11035 [View Article][PubMed]
     [Google Scholar]
  44. Tamura K., Dudley J., Nei M., Kumar S. 2007; mega4: molecular evolutionary genetics analysis (mega) software version 4.0. Mol Biol Evol 24:1596–1599 [View Article][PubMed]
     [Google Scholar]
  45. Tsagris E. M., Martínez de Alba A. E., Gozmanova M., Kalantidis K. 2008; Viroids. Cell Microbiol 10:2168–2179 [View Article][PubMed]
     [Google Scholar]
  46. Tsushima T., Murakami S., Ito H., He Y.-H., Raj A. P. C., Sano T. 2011; Molecular characterization of potato spindle tuber viroid in dahlia. J Gen Plant Pathol 77:253–256 [View Article]
     [Google Scholar]
  47. Verhoeven J. Th. J., Jansen C. C. C., Willemen T. M., Kox L. F. F., Owens R. A., Roenhorst J. W. 2004; Natural infections of tomato by Citrus exocortis viroid, Columnea latent viroid, Potato spindle tuber viroid and Tomato chlorotic dwarf viroid . Eur J Plant Pathol 110:823–831 [View Article]
     [Google Scholar]
  48. Verhoeven J. Th. J., Jansen C. C. C., Roenhorst J. W., Flores R., de la Peña M. 2009; Pepper chat fruit viroid: biological and molecular properties of a proposed new species of the genus Pospiviroid . Virus Res 144:209–214 [View Article][PubMed]
     [Google Scholar]
  49. Verhoeven J. Th. J., Hüner L., Marn M. V., Plesko I. M., Roenhorst J. W. 2010; Mechanical transmission of potato spindle tuber viroid between plants of Brugmansia suaveoles, Solanum jasminoides and potatoes and tomatoes. Eur J Plant Pathol 128:417–421 [View Article]
     [Google Scholar]
  50. Verhoeven J. Th. J., Botermans M., Meekes E. T. M., Roenhorst J. W. 2012; Tomato apical stunt viroid in the Netherlands: most prevalent pospiviroid in ornamentals and first outbreak in tomatoes. Eur J Plant Pathol 133:803–810 [View Article]
     [Google Scholar]
  51. Zhong X., Archual A. J., Amin A. A., Ding B. 2008; A genomic map of viroid RNA motifs critical for replication and systemic trafficking. Plant Cell 20:35–47 [View Article][PubMed]
     [Google Scholar]
  52. Zuker M. 2003; mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31:3406–3415 [View Article][PubMed]
     [Google Scholar]
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Dahlia latent viroid: a recombinant new species of the family Pospiviroidae posing intriguing questions about its origin and classification
J. Gen. Virol. 94, 711 (2013); https://doi.org/10.1099/vir.0.048751-0
/content/journal/jgv/10.1099/vir.0.048751-0
/content/journal/jgv/10.1099/vir.0.048751-0
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