Skip to main content
SpringerLink
Log in

Structure and function of viroids

  • Review
  • Published:
Biophysics of structure and mechanism Aims and scope Submit manuscript

Abstract

Viroids are an independent class of plant pathogens which are distinguished from viruses by the absence of a protein coat and by their unusually small size. They are single-stranded circular RNAs composed of about 360 nucleotide residues. Sequence analysis and physicochemical studies of the potato spindle tuber viroid (PSTV) have shown that, as a result of intra-molecular base pairing, viroids form a unique rod-like secondary structure which is characterized by a serial arrangement of double-helical sections and internal loops. There is no indication for an additional tertiary structure because all parts of the molecule are freely accessible to ligand interaction. During the denaturation all of the native base pairs of viroids are dissociated in one highly cooperative transition, and in the same process very stable hairpins which are not present in the native structure are newly formed. Most of the properties of the structure and structural transitions of PSTV have been found also in citrus exocortis viroid, chrysanthemum stunt viroid and four different viroid-like RNAs associated with the cadang-cadang disease. The close similarity between these viroids is more expressed in the overall structure and in thermodynamic and functional domains than in the primary sequence. The stiffness of all viroids can be described by an unique persistence length of 300 å. Characteristically, regions of premelting, regions of stable hairpins, and the sequence UACUACCCGGUGG which is opposite to one of the stable hairpins, are the most conservative sequences in the molecules. Current hypotheses about the function of viroids are discussed on the basis of their structural and thermodynamic features. The suggestion that viroid RNA has features similar to DNA has been supported by the finding that they are replicated in vitro by the DNA-dependent RNA polymerase II of the host plant. The highly conserved sequence in viroids mentioned above corresponds very closely to a segment at the 5′-end of the small nuclear RNA U1 of eukaryotes. Because this segment is discussed in recent models, to be involved in the splicing process, a hypothesis is proposed in which viroids interfere with the splicing process leading to a pathogenic misregulation of mRNA processing.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Arnberg AC, van Ommen GJB, Grivell LA, van Bruggen EFJ, Borst P (1980) Some yeast mitochondrial RNAs are circular. Cell 19: 313–319

    Google Scholar 

  • Borer PN, Dengler B, Tinoco J Jr, Uhlenbeck OC (1974) Stability of ribonucleic acid double stranded helices. J Mol Biol 86: 843–853

    Google Scholar 

  • Branch AD, Robertson HD, Dickson E (1981) Longer-than-unit-length viroid minus strands are present in RNA from infected plants. Proc Natl Acad Sci USA 78: 6381–6385

    Google Scholar 

  • Colpan M, Schumacher J, Brüggemann W, SÄnger HL, Riesner D Large scale purification of viroid RNA using Cs2SO4-gradient centrifugation and HPLC. Submitted

  • De la Torre JG, Bloomfield VA (1981) Hydrodynamic properties of complex, rigid biological macromolecules: Theory and applications. Q. Rev Biophys 14: 81–139

    Google Scholar 

  • Dickson E (1981) A model for the involvement of viroids in RNA splicing. Virology 115: 216–221

    Google Scholar 

  • Diener TO (1971) Potato spindle tuber ‘virus’. IV. A replicating low molecular weight RNA. Virology 45: 411–428

    Google Scholar 

  • Diener TO (1979) Viroids: Structure and function. Science 205: 859–866

    Google Scholar 

  • Diener TO (1981) Are viroids escaped introns? Proc Natl Acad Sci USA 78: 5014–5015

    Google Scholar 

  • Diener TO, Lawson RH (1973) Chrysanthemum stunt: A viroid disease. Virology 51: 94–101

    Google Scholar 

  • Gralla J, Crothers DM (1973a) Free energy of imperfect nucleic acid helices II. Small hairpin loops. J Mol Biol 73: 497–511

    Google Scholar 

  • Gralla J, Crothers DM (1973b) Free energy of imperfect nucleic acid helices III. Small internal loops resulting from mismatches. J Mol Biol 78: 301–319

    Google Scholar 

  • Grill LK, Semancik JS (1978) RNA sequences complementary to citrus exocortis viroid in nucleic acid preparations from infected Gynura aurantiaca. Proc Natl Acad Sci USA 75: 896–900

    Google Scholar 

  • Gross HJ, Riesner D (1980) Viroids: A class of subviral pathogens. Angew Chem Int Ed Eng 19: 231–243; Angew Chem 92: 233–245

    Google Scholar 

  • Gross HJ, Domdey H, Lossow Ch, Jank P, Raba M, Alberty H, SÄnger HL (1978) Nucleotide sequence and secondary structure of potato spindle tuber viroid. Nature 273: 203–208

    Google Scholar 

  • Gross HJ, Krupp G, Domdey H, Steger G, Riesner D, SÄnger HL (1981) The structure of three plant viroids. Nucleic Acids Res (Symposium Series) 10: 91–98

    Google Scholar 

  • Gross HJ, Krupp G, Domdey H, Raba M, Jank P, Lossow Ch, Alberty H, Ramm K, SÄnger HL (1982) Nucleotide sequence and secondary structure of citrus exocortis and chrysanthemum stunt viroid. Eur J Biochem 121: 249–257

    Google Scholar 

  • Haseloff J, Symons RH (1981) Chrysanthemum stunt viroid: Primary sequence and secondary structure. Nucleic Acids Res 9: 2741–2752

    Google Scholar 

  • Haseloff J, Symons RH (1982) Comparative sequences and structure of viroid-like RNAs of two plants viruses. Nucleic Acids Res 10: 3681–3691

    Google Scholar 

  • Haseloff J, Mohamed NA, Symons RH (1982) Viroid RNAs of cadang-cadang disease of coconuts. Nature 299: 316–321

    Google Scholar 

  • Henco K, SÄnger HL, Riesner D (1979) Fine structure melting of viroids as studied by kinetic methods. Nucleic Acids Res 6: 3041–3059

    Google Scholar 

  • Henco K, Steger G, Riesner D (1980) Melting curves on less than 1 Μg of nucleic acid. Anal Biochem 101: 225–229

    Google Scholar 

  • Hollings M, Stone OM (1973) Some properties of chrysanthemum stunt, a virus with the characteristics of an uncoated ribonucleic acid. Ann Appl Biol 74: 333–348

    Google Scholar 

  • Imperial JS, Rodriguez MJB, Randies JW (1981) Variation in the viroid-like RNA associated with cadang-cadang disease: Evidence for an increase in molecular weight with disease progress. J Gen Virol 56: 77–85

    Google Scholar 

  • Kleinschmidt AK, Klotz G, Seliger H (1981) Viroid structure. Ann Rev Biophys Bioeng 10: 115–132

    Google Scholar 

  • Kovacic RT, van Holde KE (1977) Sedimentation of homogeneous double-strand DNA molecules. Biochemistry 16: 1490–1498

    Google Scholar 

  • Langowski J, Henco K, Riesner D, SÄnger HL (1978) Common structural features of different viroids: Serial arrangement of double helical sections and internal loops. Nucleic Acids Res 5: 1589–1610

    Google Scholar 

  • Lerner MR, Boyle JA, Mount SM, Wolin SL, Steitz JA (1980) Are snRNPs involved in splicing? Nature 283: 220–224

    Google Scholar 

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

    Google Scholar 

  • Ming-Ta Hsu, Coca-Prados M (1979) Electronmicroscopic evidence for the circular form of RNA in the cytoplasm of eukaryotic cells. Nature 280: 339–340

    Google Scholar 

  • Mohamed NA, Imperial J, Haseloff J, Buenaflor G, Randles JW (1981) Variation in the viroid-like RNA associated with cadang-cadang disease of coconut. V. International Congress of Virology, Strasbourg 1981, abstract P 21/11

  • Owens RA, Smith DR, Diener TO (1978) Measurement of viroid sequence homology by hybridization with complementary DNA prepared in vitro. Virology 89: 388–394

    Google Scholar 

  • Pörschke D, Uhlenbeck OC, Martin FH (1973) Thermodynamics and kinetics of the helix-coil transition of oligomers containing GC basepairs. Biopolymers 12: 1313–1335

    Google Scholar 

  • Rackwitz HR, Rohde W, SÄnger HL (1981) DNA-dependent RNA polymerase II of plant origin transcribes viroid RNA into full-length copies. Nature 291: 297–301

    Google Scholar 

  • Randles JW (1975) Association of two ribonucleic acid species with cadang-cadang disease of coconut palm. Phytopathology 65: 163–167

    Google Scholar 

  • Randles JW, Davies C, Hatta T, Gould AR, Francki RIB (1981) Studies on encapsidated viroid-like RNA I. Characterization of Velvet tobacco mottle virus. Virology 108: 111–122

    Google Scholar 

  • Randles JW, Steger G, Riesner D (1982) Structural transitions in viroid-like RNAs associated with Cadang-cadang disease, Velvet tobacco mottle virus, and Solanum nodiflorum mottle virus. Nucleic Acids Res 10: 5569–5586

    Google Scholar 

  • Riesner D, Römer R (1973) Thermodynamics and kinetics of conformational transitions in oligonucleotides and tRNA. In: Duchesne J (ed) Physico-chemical properties of nucleic acids, vol 2. Academic Press, London New York, pp 237–318

    Google Scholar 

  • Riesner D, Henco K, Rokohl U, Klotz G, Kleinschmidt AK, Domdey H, Jank P, Gross HJ, SÄnger HL (1979) Structure and structure formation of viroids. J Mol Biol 133: 85–115

    Google Scholar 

  • Riesner D, Colpan M, Randies JW (1982a) A microcell for the temperature-jump technique. Anal Biochem 121: 186–189

    Google Scholar 

  • Riesner D, Kaper JM, Randles JW (1982b) Stiffness of viroids and viroid-like RNA in solution. Nucleic Acids Res 10: 5587–5598

    Google Scholar 

  • Romaine CP, Horst RK (1975) Suggested viroid etiology for chrysanthemum chlorotic mottle disease. Virology 64: 86–95

    Google Scholar 

  • Rubin H, Kallenbach NR (1975) Conformational statistics of short RNA chains. J Chem Phys 62: 2766–2776

    Google Scholar 

  • SÄnger HL (1972) An infectious and replicating RNA of low molecular weight: The agent of the exocortis disease of citrus. Adv. Biosci 8: 103–116

    Google Scholar 

  • SÄnger HL (1980) Structure and possible functions of viroids. Ann NY Acad Sci 354: 251–278

    Google Scholar 

  • SÄnger HL, Klotz G, Riesner D, Gross HJ, Kleinschmidt AK (1976) 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

    Google Scholar 

  • Sasaki M, Shikata E (1977) On some properties of hop stunt disease agent, a viroid. Proc Jpn Acad Ser B 53: 109–112

    Google Scholar 

  • Scheffler JE, Elson EL, Baldwin RL (1970) Helix formation by d(TA)-Oligomers II. Analysis of the helix-coil transitions of linear and circular oligomers. J Mol Biol 48: 145–171

    Google Scholar 

  • Semancik JS, Weathers LG (1972) Exocortis disease: Evidence for a new species of ‘infectious’ low molecular weight RNA in plants. Nature (New Biol) 237: 242–244

    Google Scholar 

  • Singh RP, Clark MC (1971) Infectious low molecular weight ribonucleic acid from tomato. Biochem Biophys Res Commun 44: 1077–1083

    Google Scholar 

  • Steger G, Gross HJ, Randies JW, SÄnger HL, Riesner D (1983) Thermodynamic calculations on the stability and conformational transitions of viroids. (manuscript in preparation)

  • Symons RH (1981) Avocado sunblotch viroid: Primary sequence and proposed secondary structure. Nucleic Acids Res 9: 6527–6537

    Google Scholar 

  • Thomas W, Mohamed NA (1979) Avocado sunblotch — A viroid disease? Aust Plant Pathol Soc Newslett 8: 1–3

    Google Scholar 

  • Van Dorst HJM, Peters D (1974) Some biological observation on pale fruit, a viroid-incited disease of cucumber. Neth J Plant Pathol 870: 85–95

    Google Scholar 

  • Visvader JE, Bould AR, Bruening GE, Symons RH (1982) Citrus exocortis viroid: Nucleotide sequence and secondary structure of an Australian isolate. FEES Lett 137: 288–292

    Google Scholar 

  • Wild U, Ramm K, SÄnger HL, Riesner D (1980) Loops in viroids. Eur J Biochem 103: 227–235

    Google Scholar 

  • Yamakawa H, Fujii M (1973) Translation friction coefficient of worm-like chains. Macromolecules 6: 407–415

    Google Scholar 

  • Zelazny B, Randies JW, Boccardo G, Imperial JS (1982) The cadang-cadang disease of coconut palm. Scientia Filipinas (in press)

Download references

Author information

Authors and Affiliations

  1. Institut für Physikalische Biologie, UniversitÄt Düsseldorf, D-4000, Düsseldorf, Germany

    G. Steger

  2. Institut für Biochemie, UniversitÄt Würzburg, D-8700, Würzburg, Germany

    H. J. Gross

  3. Department of Plant Pathology, University of Adelaide, Waite Agricultural Research Institute, 5064, Glen Osmond, South Australia

    J. W. Randles

  4. Max-Planck-Institut für Biochemie, D-8033, Martinsried bei München, Germany

    H. L. SÄnger

Authors
  1. D. Riesner
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. G. Steger
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J. Schumacher
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. H. J. Gross
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. J. W. Randles
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. H. L. SÄnger
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Riesner, D., Steger, G., Schumacher, J. et al. Structure and function of viroids. Biophys. Struct. Mechanism 9, 145–170 (1983). https://doi.org/10.1007/BF00537813

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00537813

Key words

Search

Navigation