Skip to main content
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1986 Sep;83(17):6250–6254. doi: 10.1073/pnas.83.17.6250

Viroids and virusoids are related to group I introns.

G Dinter-Gottlieb
PMCID: PMC386480  PMID: 3462692

Abstract

Group I introns are found in nuclear rRNA genes, mitochondrial mRNA and rRNA genes, and chloroplast tRNA genes. The hallmarks of this intron class are a 16-nucleotide consensus sequence and three sets of complementary sequences. The viroids (circular pathogenic plant RNAs) and the virusoids (plant satellite RNAs) also contain the consensus sequence and the three sets of complementary bases. Pairing of the complementary bases would generate a viroid structure resembling a group I intron, which might be stabilized in vivo through interactions with proteins. The Tetrahymena self-splicing rRNA intron further has sequences homologous with regions of potato spindle tuber viroid associated with the severity of viroid symptoms.

Full text

PDF
6250

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Branch A. D., Robertson H. D. A replication cycle for viroids and other small infectious RNA's. Science. 1984 Feb 3;223(4635):450–455. doi: 10.1126/science.6197756. [DOI] [PubMed] [Google Scholar]
  2. 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 U S A. 1981 Oct;78(10):6381–6385. doi: 10.1073/pnas.78.10.6381. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Branch A. D., Robertson H. D., Greer C., Gegenheimer P., Peebles C., Abelson J. Cell-free circularization of viroid progeny RNA by an RNA ligase from wheat germ. Science. 1982 Sep 17;217(4565):1147–1149. doi: 10.1126/science.217.4565.1147. [DOI] [PubMed] [Google Scholar]
  4. Burke J. M., RajBhandary U. L. Intron within the large rRNA gene of N. crassa mitochondria: a long open reading frame and a consensus sequence possibly important in splicing. Cell. 1982 Dec;31(3 Pt 2):509–520. doi: 10.1016/0092-8674(82)90307-5. [DOI] [PubMed] [Google Scholar]
  5. Cech T. R., Tanner N. K., Tinoco I., Jr, Weir B. R., Zuker M., Perlman P. S. Secondary structure of the Tetrahymena ribosomal RNA intervening sequence: structural homology with fungal mitochondrial intervening sequences. Proc Natl Acad Sci U S A. 1983 Jul;80(13):3903–3907. doi: 10.1073/pnas.80.13.3903. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cech T. R., Zaug A. J., Grabowski P. J. In vitro splicing of the ribosomal RNA precursor of Tetrahymena: involvement of a guanosine nucleotide in the excision of the intervening sequence. Cell. 1981 Dec;27(3 Pt 2):487–496. doi: 10.1016/0092-8674(81)90390-1. [DOI] [PubMed] [Google Scholar]
  7. Collmer C. W., Hadidi A., Kaper J. M. Nucleotide sequence of the satellite of peanut stunt virus reveals structural homologies with viroids and certain nuclear and mitochondrial introns. Proc Natl Acad Sci U S A. 1985 May;82(10):3110–3114. doi: 10.1073/pnas.82.10.3110. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cress D. E., Kiefer M. C., Owens R. A. Construction of infectious potato spindle tuber viroid cDNA clones. Nucleic Acids Res. 1983 Oct 11;11(19):6821–6835. doi: 10.1093/nar/11.19.6821. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Cummings D. J., MacNeil I. A., Domenico J., Matsuura E. T. Excision-amplification of mitochondrial DNA during senescence in Podospora anserina. DNA sequence analysis of three unique "plasmids". J Mol Biol. 1985 Oct 20;185(4):659–680. doi: 10.1016/0022-2836(85)90052-x. [DOI] [PubMed] [Google Scholar]
  10. De La Salle H., Jacq C., Slonimski P. P. Critical sequences within mitochondrial introns: pleiotropic mRNA maturase and cis-dominant signals of the box intron controlling reductase and oxidase. Cell. 1982 Apr;28(4):721–732. doi: 10.1016/0092-8674(82)90051-4. [DOI] [PubMed] [Google Scholar]
  11. Dickson E. A model for the involvement of viroids in RNA splicing. Virology. 1981 Nov;115(1):216–221. doi: 10.1016/0042-6822(81)90104-5. [DOI] [PubMed] [Google Scholar]
  12. Diener T. O. Are viroids escaped introns? Proc Natl Acad Sci U S A. 1981 Aug;78(8):5014–5015. doi: 10.1073/pnas.78.8.5014. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Diener T. O. Viroids: structure and function. Science. 1979 Aug 31;205(4409):859–866. doi: 10.1126/science.472709. [DOI] [PubMed] [Google Scholar]
  14. Garriga G., Lambowitz A. M. RNA splicing in neurospora mitochondria: self-splicing of a mitochondrial intron in vitro. Cell. 1984 Dec;39(3 Pt 2):631–641. doi: 10.1016/0092-8674(84)90470-7. [DOI] [PubMed] [Google Scholar]
  15. Grabowski P. J., Zaug A. J., Cech T. R. The intervening sequence of the ribosomal RNA precursor is converted to a circular RNA in isolated nuclei of Tetrahymena. Cell. 1981 Feb;23(2):467–476. doi: 10.1016/0092-8674(81)90142-2. [DOI] [PubMed] [Google Scholar]
  16. Gross H. J., Domdey H., Lossow C., Jank P., Raba M., Alberty H., Sänger H. L. Nucleotide sequence and secondary structure of potato spindle tuber viroid. Nature. 1978 May 18;273(5659):203–208. doi: 10.1038/273203a0. [DOI] [PubMed] [Google Scholar]
  17. Gross H. J., Krupp G., Domdey H., Raba M., Jank P., Lossow C., Alberty H., Ramm K., Sänger H. L. Nucleotide sequence and secondary structure of citrus exocortis and chrysanthemum stunt viroid. Eur J Biochem. 1982 Jan;121(2):249–257. doi: 10.1111/j.1432-1033.1982.tb05779.x. [DOI] [PubMed] [Google Scholar]
  18. Halbreich A., Pajot P., Foucher M., Grandchamp C., Slonimski P. A pathway of cytochrome b mRNA processing in yeast mitochondria: specific splicing steps and an intron-derived circular DNA. Cell. 1980 Feb;19(2):321–329. doi: 10.1016/0092-8674(80)90506-1. [DOI] [PubMed] [Google Scholar]
  19. Haseloff J., Symons R. H. Comparative sequence and structure of viroid-like RNAs of two plant viruses. Nucleic Acids Res. 1982 Jun 25;10(12):3681–3691. doi: 10.1093/nar/10.12.3681. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Henco K., Sänger H. L., Riesner D. Fine structure melting of viroids as studied by kinetic methods. Nucleic Acids Res. 1979 Jul 11;6(9):3041–3059. doi: 10.1093/nar/6.9.3041. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Keese P., Symons R. H. Domains in viroids: evidence of intermolecular RNA rearrangements and their contribution to viroid evolution. Proc Natl Acad Sci U S A. 1985 Jul;82(14):4582–4586. doi: 10.1073/pnas.82.14.4582. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Kiefer M. C., Owens R. A., Diener T. O. Structural similarities between viroids and transposable genetic elements. Proc Natl Acad Sci U S A. 1983 Oct;80(20):6234–6238. doi: 10.1073/pnas.80.20.6234. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Kikuchi Y., Tyc K., Filipowicz W., Sänger H. L., Gross H. J. Circularization of linear viroid RNA via 2'-phosphomonoester, 3', 5'-phosphodiester bonds by a novel type of RNA ligase from wheat germ and Chlamydomonas. Nucleic Acids Res. 1982 Dec 11;10(23):7521–7529. doi: 10.1093/nar/10.23.7521. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Kruger K., Grabowski P. J., Zaug A. J., Sands J., Gottschling D. E., Cech T. R. Self-splicing RNA: autoexcision and autocyclization of the ribosomal RNA intervening sequence of Tetrahymena. Cell. 1982 Nov;31(1):147–157. doi: 10.1016/0092-8674(82)90414-7. [DOI] [PubMed] [Google Scholar]
  25. Michel F., Cummings D. J. Analysis of class I introns in a mitochondrial plasmid associated with senescence of Podospora anserina reveals extraordinary resemblance to the Tetrahymena ribosomal intron. Curr Genet. 1985;10(1):69–79. doi: 10.1007/BF00418495. [DOI] [PubMed] [Google Scholar]
  26. Michel F., Dujon B. Conservation of RNA secondary structures in two intron families including mitochondrial-, chloroplast- and nuclear-encoded members. EMBO J. 1983;2(1):33–38. doi: 10.1002/j.1460-2075.1983.tb01376.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Netter P., Jacq C., Carignani G., Slonimski P. P. Critical sequences within mitochondrial introns: cis-dominant mutations of the "cytochrome-b-like" intron of the oxidase gene. Cell. 1982 Apr;28(4):733–738. doi: 10.1016/0092-8674(82)90052-6. [DOI] [PubMed] [Google Scholar]
  28. Noller H. F., Woese C. R. Secondary structure of 16S ribosomal RNA. Science. 1981 Apr 24;212(4493):403–411. doi: 10.1126/science.6163215. [DOI] [PubMed] [Google Scholar]
  29. Owens R. A., Diener T. O. RNA intermediates in potato spindle tuber viroid replication. Proc Natl Acad Sci U S A. 1982 Jan;79(1):113–117. doi: 10.1073/pnas.79.1.113. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Padgett R. A., Konarska M. M., Grabowski P. J., Hardy S. F., Sharp P. A. Lariat RNA's as intermediates and products in the splicing of messenger RNA precursors. Science. 1984 Aug 31;225(4665):898–903. doi: 10.1126/science.6206566. [DOI] [PubMed] [Google Scholar]
  31. Prody G. A., Bakos J. T., Buzayan J. M., Schneider I. R., Bruening G. Autolytic processing of dimeric plant virus satellite RNA. Science. 1986 Mar 28;231(4745):1577–1580. doi: 10.1126/science.231.4745.1577. [DOI] [PubMed] [Google Scholar]
  32. Riesner D., Henco K., Rokohl U., Klotz G., Kleinschmidt A. K., Domdey H., Jank P., Gross H. J., Sänger H. L. Structure and structure formation of viroids. J Mol Biol. 1979 Sep 5;133(1):85–115. doi: 10.1016/0022-2836(79)90252-3. [DOI] [PubMed] [Google Scholar]
  33. Ruskin B., Krainer A. R., Maniatis T., Green M. R. Excision of an intact intron as a novel lariat structure during pre-mRNA splicing in vitro. Cell. 1984 Aug;38(1):317–331. doi: 10.1016/0092-8674(84)90553-1. [DOI] [PubMed] [Google Scholar]
  34. Schnölzer M., Haas B., Raam K., Hofmann H., Sänger H. L. Correlation between structure and pathogenicity of potato spindle tuber viroid (PSTV). EMBO J. 1985 Sep;4(9):2181–2190. doi: 10.1002/j.1460-2075.1985.tb03913.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Schumacher J., Sänger H. L., Riesner D. Subcellular localization of viroids in highly purified nuclei from tomato leaf tissue. EMBO J. 1983;2(9):1549–1555. doi: 10.1002/j.1460-2075.1983.tb01622.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Steinmetz A., Gubbins E. J., Bogorad L. The anticodon of the maize chloroplast gene for tRNA Leu UAA is split by a large intron. Nucleic Acids Res. 1982 May 25;10(10):3027–3037. doi: 10.1093/nar/10.10.3027. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Tabak H. F., Van der Horst G., Osinga K. A., Arnberg A. C. Splicing of large ribosomal precursor RNA and processing of intron RNA in yeast mitochondria. Cell. 1984 Dec;39(3 Pt 2):623–629. doi: 10.1016/0092-8674(84)90469-0. [DOI] [PubMed] [Google Scholar]
  38. Visvader J. E., Forster A. C., Symons R. H. Infectivity and in vitro mutagenesis of monomeric cDNA clones of citrus exocortis viroid indicates the site of processing of viroid precursors. Nucleic Acids Res. 1985 Aug 26;13(16):5843–5856. doi: 10.1093/nar/13.16.5843. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Waring R. B., Ray J. A., Edwards S. W., Scazzocchio C., Davies R. W. The Tetrahymena rRNA intron self-splices in E. coli: in vivo evidence for the importance of key base-paired regions of RNA for RNA enzyme function. Cell. 1985 Feb;40(2):371–380. doi: 10.1016/0092-8674(85)90151-5. [DOI] [PubMed] [Google Scholar]
  40. Weiss-Brummer B., Holl J., Schweyen R. J., Rödel G., Kaudewitz F. Processing of yeast mitochondrial RNA: involvement of intramolecular hybrids in splicing of cob intron 4 RNA by mutation and reversion. Cell. 1983 May;33(1):195–202. doi: 10.1016/0092-8674(83)90348-3. [DOI] [PubMed] [Google Scholar]
  41. Weiss-Brummer B., Rödel G., Schweyen R. J., Kaudewitz F. Expression of the split gene cob in yeast: evidence for a precursor of a "maturase" protein translated from intron 4 and preceding exons. Cell. 1982 Jun;29(2):527–536. doi: 10.1016/0092-8674(82)90169-6. [DOI] [PubMed] [Google Scholar]
  42. Wolff P., Gilz R., Schumacher J., Riesner D. Complexes of viroids with histones and other proteins. Nucleic Acids Res. 1985 Jan 25;13(2):355–367. doi: 10.1093/nar/13.2.355. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Wollenzien P. L., Cantor C. R., Grant D. M., Lambowitz A. M. RNA splicing in neurospora mitochondria: structure of the unspliced 35S precursor ribosomal RNA detected by psoralen cross-linking. Cell. 1983 Feb;32(2):397–407. doi: 10.1016/0092-8674(83)90459-2. [DOI] [PubMed] [Google Scholar]
  44. Zaug A. J., Cech T. R. Oligomerization of intervening sequence RNA molecules in the absence of proteins. Science. 1985 Sep 13;229(4718):1060–1064. doi: 10.1126/science.2412290. [DOI] [PubMed] [Google Scholar]
  45. Zaug A. J., Grabowski P. J., Cech T. R. Autocatalytic cyclization of an excised intervening sequence RNA is a cleavage-ligation reaction. Nature. 1983 Feb 17;301(5901):578–583. doi: 10.1038/301578a0. [DOI] [PubMed] [Google Scholar]
  46. van der Horst G., Tabak H. F. Self-splicing of yeast mitochondrial ribosomal and messenger RNA precursors. Cell. 1985 Apr;40(4):759–766. doi: 10.1016/0092-8674(85)90335-6. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES