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Discovering viroids — a personal perspective

Abstract

During 1970 and 1971, I discovered that a devastating disease of potato plants is not caused by a virus, as had been assumed, but by a new type of subviral pathogen, the viroid. Viroids are so small — one fiftieth of the size of the smallest viruses — that many scientists initially doubted their existence. We now know that viroids cause many damaging diseases of crop plants. Fortunately, new methods that are based on the unique properties of viroids now promise effective control.

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Figure 1: Analytical methods used for determining the size of potato spindle tuber viroid.
Figure 2: Recognition of the viroid as a physical entity.
Figure 3: Illustration (to scale) of a typical viroid compared with viruses and the bacterium Escherichia coli.
Figure 4: Secondary structures of viroids.

References

  1. Avery, O. T., MacLeod, C. M. & McCarty, M. Studies of the chemical nature of the substance inducing transformation of pneumococcal types. Induction of transformation by a desoxyribonucleic acid fraction isolated from Pneumococcus type III. J. Exp. Med. 79, 137–158 (1944).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  2. Beijerinck, M. W. Ueber ein Contagium vivum fluidum als Ursache der Fleckenkrankheit der Tabaksblätter. Verh. Kon. Akad. Wetensch. VI, 3–21 (1898).

    Google Scholar 

  3. Brakke, M. K. Density-gradient centrifugation: A new separation technique. J. Am. Chem. Soc. 73, 1847–1848 (1951).

    CAS  Article  Google Scholar 

  4. Diener, T. O. & Raymer, W. B. Potato spindle tuber virus: a plant virus with properties of a free nucleic acid. Science 158, 378–381 (1967).

    CAS  Article  PubMed  Google Scholar 

  5. Brakke, M. K. Systemic infections for the assay of plant viruses. Ann. Rev Phytopathol. 8, 61–84 (1970).

    Article  Google Scholar 

  6. Diener, T. O. Viroids. Adv. Virus Res. 17, 295–313 (1972).

    CAS  Article  PubMed  Google Scholar 

  7. Diener, T. O. Potato spindle tuber “virus”. IV. A replicating, low-molecular weight RNA. Virology 45, 411–428 (1971).

    CAS  Article  PubMed  Google Scholar 

  8. Lawson, R. H. Some properties of chrysanthemum stunt virus. Phytopathology 58, 885 (1968).

    Google Scholar 

  9. Semancik, J. S. & Weathers, L. G. Exocortis virus of Citrus: association of infectivity with nucleic acid preparations. Virology 36, 326–328 (1968).

    CAS  Article  PubMed  Google Scholar 

  10. Sänger, H. L. An infectious and replicating RNA of low molecular weight: The agent of the exocortis disease of Citrus. Adv. Biosc. 8, 103–116 (1972).

    Google Scholar 

  11. Diener, T. O. Potato spindle tuber viroid. VIII. Correlation of infectivity with a UV-absorbing component and thermal denaturation properties of the RNA. Virology 50, 606–609 (1972).

    CAS  Article  PubMed  Google Scholar 

  12. Flores, R., Randles, J. W., Bar-Joseph, M. & Diener, T. O. Viroids. in Virus Taxonomy, Seventh Report of the International Committee on Taxonomy of Viruses (eds van Regenmortel, M. H. V. et al.) 1009–1024 (Academic Press, San Diego, 2000).

    Google Scholar 

  13. Flores, R., Daròs, J. A. & Hernández, C. Avsunviroidae family: viroids containing hammerhead ribozymes. Adv. Virus Res. 55, 271–323 (2000).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  14. Keese, P. & Symons, R. H. Domains in viroids: Evidence of intermolecular RNA rearrangements and their contribution to viroid evolution. Proc. Natl Acad. Sci. USA 82, 4582–4586 (1985).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  15. Branch, A. D., Robertson, H. D. & Dickson, E. Longer-than unit length viroid minus strands are present in RNA from infected plants. Proc. Natl Acad. Sci. USA 78, 6381–6385 (1981).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  16. Owens, R. A. & Diener, T. O. RNA intermediates in potato spindle tuber viroid replication. Proc. Natl Acad. Sci. USA 79, 113–117 (1982).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  17. Tsagris, M., Tabler, M., Mühlbach, H. P. & Sänger, H. L. Linear oligomeric potato spindle tuber viroid (PSTV) RNAs are accurately processed in vitro to the monomeric circular viroid proper when incubated with a nuclear extract from healthy potato cells. EMBO J. 6, 2173–2183 (1987).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  18. Gross, H. J. et al. A severe and a mild potato spindle tuber viroid isolate differ in three nucleotide exchanges only. Biosci. Rep. 1, 235–241 (1981).

    CAS  Article  PubMed  Google Scholar 

  19. Sano, T., Candresse, T., Hammond, R. W., Diener, T. O. & Owens, R. A. Identification of multiple structural domains regulating viroid pathogenicity. Proc. Natl Acad. Sci. USA 89, 10104–10108 (1992).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  20. Qi, Y. & Ding, B. Inhibition of cell growth and shoot development by a specific nucleotide sequence in a noncoding viroid RNA. The Plant Cell 15, 1360–1374 (2003).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  21. Diener, T. O. The viroid: Biological oddity or evolutionary fossil? Adv. Virus Res. 57, 137–184 (2001).

    CAS  Article  PubMed  Google Scholar 

  22. Diener, T. O. Circular RNAs: Relics of precellular evolution? Proc. Natl Acad. Sci. USA. 86, 9370–9374 (1989).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  23. Sharp, P. A. On the origin of RNA splicing and introns. Cell 42, 397–400 (1985).

    CAS  Article  PubMed  Google Scholar 

  24. Paul, N. & Joyce, G. F. A self-replicating ligase ribozyme. Proc. Natl Acad. Sci. USA 99, 12733–12740 (2000).

    Article  Google Scholar 

  25. Owens, R. A. & Diener, T. O. Sensitive and rapid diagnosis of potato spindle tuber viroid disease by nucleic acid hybridization. Science 213, 670–672 (1981).

    CAS  Article  PubMed  Google Scholar 

  26. Yang, X. et al. Ribozyme-mediated high resistance against potato spindle tuber viroid in transgenic potatoes. Proc. Natl Acad. Sci. USA 94, 4861–4865 (1997).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  27. Sano, T., Nagayama, A., Ogawa, T., Ishida, I. & Okada, Y. Transgenic potato expressing a double-stranded RNA-specific ribonuclease is resistant to potato spindle tuber viroid. Nature Biotechol. 15, 1290–1294 (1997).

    CAS  Article  Google Scholar 

  28. Sänger, H. L. & Brandenburg, E. Ueber die Gewinnung von infektiösem Presssaft aus “Wintertyp”-Pflanzen des Tabak-Rattle–Virus durch Phenolextraktion. Naturwiss. 48, 391 (1961).

    Article  Google Scholar 

  29. Siegel, A., Zaitlin, M. & Sehgal, O. P. The isolation of defective tobacco mosaic virus strains. Proc. Natl Acad. Sci. USA 48, 1845–1851 (1962).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  30. Diener, T. O. Isolation of an infectious, ribonuclease-sensitive fraction from tobacco leaves recently inoculated with tobacco mosaic virus. Virology 16, 140–146 (1962).

    CAS  Article  PubMed  Google Scholar 

  31. Schneider, I. R. Characteristics of a satellite-like virus of tobacco ringspot virus. Virology 45, 108–122 (1971).

    CAS  Article  PubMed  Google Scholar 

  32. Diener, T. O. Potato spindle tuber virus: A plant virus with properties of a free nucleic acid. III. Subcellular location of PSTV-RNA and the question of whether virions exist in extracts or in situ. Virology 43, 75–89 (1971).

    CAS  Article  PubMed  Google Scholar 

  33. Sogo, J. M., Koller, T. & Diener, T. O. Potato spindle tuber viroid. X. Visualization and size determination by electron microscopy. Virology 55, 70–80 (1973).

    CAS  Article  PubMed  Google Scholar 

  34. Davies, J. W., Kaesberg, P. & Diener, T. O. Potato spindle tuber viroid. XII. An investigation of viroid RNA as a messenger for protein synthesis. Virology 61, 281–286 (1974).

    CAS  Article  PubMed  Google Scholar 

  35. Hall, T. C., Wepprich, R. K., Davies, J. W., Weathers, L. G. & Semancik, J. S. Functional distinctions between the ribonucleic acids from citrus exocortis viroid and plant viruses: Cell-free translation and aminoacylation reactions. Virology 61, 486–492 (1974).

    CAS  Article  PubMed  Google Scholar 

  36. Sänger, H L., Klotz, G., Riesner, D., Gross, H. J. & Kleinschmidt, A. K. Viroids are single-stranded covalently closed circular RNA molecules existing as highly base-paired rod-like structures. Proc. Natl Acad. Sci. USA 73, 3852–3856 (1976).

    Article  PubMed  PubMed Central  Google Scholar 

  37. McClements, W. L. & Kaesberg, P. Size and secondary structure of potato spindle tuber viroid. Virology 76, 477–484 (1977).

    CAS  Article  PubMed  Google Scholar 

  38. Gross, H. J. et al. Nucleotide sequence and secondary structure of potato spindle tuber viroid. Nature 273, 203–208 (1978).

    CAS  Article  PubMed  Google Scholar 

  39. Diener, T. O. The viroid — a subviral pathogen. Am. Sci. 71, 481–489 (1983).

    Google Scholar 

  40. Malfitano, M. et al. Peach latent mosaic viroid variants inducing peach calico (extreme chlorosis) contain a characteristic insertion that is responsible for this symptomatology. Virology (in the press).

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FURTHER INFORMATION

Subviral RNA Database

Glossary

LOCAL LESION ASSAY

A technique to estimate the relative virus or viroid concentration, which involves rubbing variously diluted aliquots of a preparation onto leaves of a hypersensitive host plant that reacts to infection with the production of visible chlorotic or necrotic spots, the number of which is directly related to the virus or viroid concentration.

VIROID

A pathogen that exists in vivo as an unencapsidated nucleic acid. The nucleic acid is a single molecular species RNA.

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Diener, T. Discovering viroids — a personal perspective. Nat Rev Microbiol 1, 75–80 (2003). https://doi.org/10.1038/nrmicro736

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