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
. 1989 Dec;86(23):9370–9374. doi: 10.1073/pnas.86.23.9370

Circular RNAs: relics of precellular evolution?

T O Diener 1
PMCID: PMC298497  PMID: 2480600

Abstract

The demonstration of enzymatic capabilities of certain RNAs, in addition to their well-known template properties, has led to the recognition that RNAs are the only biological macromolecules that can function both as genotype and phenotype, hence raising the possibility of Darwinian selection and precellular evolution at the RNA level in the absence of DNA or protein. Recent models of such precellular RNA systems are patterned after the properties of intron-derived ribozymes. On the basis of a phylogenetic analysis and known properties of certain small plant pathogenic RNAs (viroids and viroid-like satellite RNAs), I suggest that these plant RNAs are more plausible candidates than introns as "living fossils" of a precellular RNA world. Their small size and circularity would have enhanced probability of their survival in error-prone, primitive self-replicating RNA systems and assured complete replication without the need for initiation or termination signals. All of these RNAs possess efficient mechanisms for the precise cleavage of monomers from oligomeric replication intermediates. Some (most viroids) require a host factor, but others (viroid-like satellite RNAs and one viroid) function as self-cleaving RNA enzymes far smaller and simpler than those derived from introns. The question is raised whether introns could have evolved from viroids or viroid-like satellite RNAs rather than vice versa, as has been widely speculated.

Full text

PDF
9370

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. Buzayan J. M., Gerlach W. L., Bruening G. Satellite tobacco ringspot virus RNA: A subset of the RNA sequence is sufficient for autolytic processing. Proc Natl Acad Sci U S A. 1986 Dec;83(23):8859–8862. doi: 10.1073/pnas.83.23.8859. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Cavalier-Smith T. Selfish DNA and the origin of introns. Nature. 1985 May 23;315(6017):283–284. doi: 10.1038/315283b0. [DOI] [PubMed] [Google Scholar]
  4. Cech T. R. A model for the RNA-catalyzed replication of RNA. Proc Natl Acad Sci U S A. 1986 Jun;83(12):4360–4363. doi: 10.1073/pnas.83.12.4360. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cech T. R. RNA chemistry. Ribozyme self-replication? Nature. 1989 Jun 15;339(6225):507–508. doi: 10.1038/339507a0. [DOI] [PubMed] [Google Scholar]
  6. Cech T. R. The chemistry of self-splicing RNA and RNA enzymes. Science. 1987 Jun 19;236(4808):1532–1539. doi: 10.1126/science.2438771. [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. Crick F. Split genes and RNA splicing. Science. 1979 Apr 20;204(4390):264–271. doi: 10.1126/science.373120. [DOI] [PubMed] [Google Scholar]
  9. 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]
  10. Diener T. O. Potato spindle tuber "virus". IV. A replicating, low molecular weight RNA. Virology. 1971 Aug;45(2):411–428. doi: 10.1016/0042-6822(71)90342-4. [DOI] [PubMed] [Google Scholar]
  11. Diener T. O. Viroid processing: a model involving the central conserved region and hairpin I. Proc Natl Acad Sci U S A. 1986 Jan;83(1):58–62. doi: 10.1073/pnas.83.1.58. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Dinter-Gottlieb G. Viroids and virusoids are related to group I introns. Proc Natl Acad Sci U S A. 1986 Sep;83(17):6250–6254. doi: 10.1073/pnas.83.17.6250. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Doudna J. A., Szostak J. W. RNA-catalysed synthesis of complementary-strand RNA. Nature. 1989 Jun 15;339(6225):519–522. doi: 10.1038/339519a0. [DOI] [PubMed] [Google Scholar]
  14. Eigen M. Selforganization of matter and the evolution of biological macromolecules. Naturwissenschaften. 1971 Oct;58(10):465–523. doi: 10.1007/BF00623322. [DOI] [PubMed] [Google Scholar]
  15. Feldstein P. A., Buzayan J. M., Bruening G. Two sequences participating in the autolytic processing of satellite tobacco ringspot virus complementary RNA. Gene. 1989 Oct 15;82(1):53–61. doi: 10.1016/0378-1119(89)90029-2. [DOI] [PubMed] [Google Scholar]
  16. Forster A. C., Jeffries A. C., Sheldon C. C., Symons R. H. Structural and ionic requirements for self-cleavage of virusoid RNAs and trans self-cleavage of viroid RNA. Cold Spring Harb Symp Quant Biol. 1987;52:249–259. doi: 10.1101/sqb.1987.052.01.030. [DOI] [PubMed] [Google Scholar]
  17. Forster A. C., Symons R. H. Self-cleavage of plus and minus RNAs of a virusoid and a structural model for the active sites. Cell. 1987 Apr 24;49(2):211–220. doi: 10.1016/0092-8674(87)90562-9. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. Guerrier-Takada C., Gardiner K., Marsh T., Pace N., Altman S. The RNA moiety of ribonuclease P is the catalytic subunit of the enzyme. Cell. 1983 Dec;35(3 Pt 2):849–857. doi: 10.1016/0092-8674(83)90117-4. [DOI] [PubMed] [Google Scholar]
  20. Hammond R. W., Diener T. O., Owens R. A. Infectivity of chimeric viroid transcripts reveals the presence of alternative processing sites in potato spindle tuber viroid. Virology. 1989 Jun;170(2):486–495. doi: 10.1016/0042-6822(89)90440-6. [DOI] [PubMed] [Google Scholar]
  21. Haseloff J., Gerlach W. L. Simple RNA enzymes with new and highly specific endoribonuclease activities. Nature. 1988 Aug 18;334(6183):585–591. doi: 10.1038/334585a0. [DOI] [PubMed] [Google Scholar]
  22. Hashimoto J., Koganezawa H. Nucleotide sequence and secondary structure of apple scar skin viroid. Nucleic Acids Res. 1987 Sep 11;15(17):7045–7052. doi: 10.1093/nar/15.17.7045. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Hutchins C. J., Rathjen P. D., Forster A. C., Symons R. H. Self-cleavage of plus and minus RNA transcripts of avocado sunblotch viroid. Nucleic Acids Res. 1986 May 12;14(9):3627–3640. doi: 10.1093/nar/14.9.3627. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Inoue T., Orgel L. E. A nonenzymatic RNA polymerase model. Science. 1983 Feb 18;219(4586):859–862. doi: 10.1126/science.6186026. [DOI] [PubMed] [Google Scholar]
  25. Joyce G. F. RNA evolution and the origins of life. Nature. 1989 Mar 16;338(6212):217–224. doi: 10.1038/338217a0. [DOI] [PubMed] [Google Scholar]
  26. Juhász A., Hegyi H., Solymosy F. A novel aspect of the information content of viroids. Biochim Biophys Acta. 1988 Sep 7;950(3):455–458. doi: 10.1016/0167-4781(88)90145-5. [DOI] [PubMed] [Google Scholar]
  27. 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]
  28. Koltunow A. M., Rezaian M. A. Grapevine viroid 1B, a new member of the apple scar skin viroid group contains the left terminal region of tomato planta macho viroid. Virology. 1989 Jun;170(2):575–578. doi: 10.1016/0042-6822(89)90450-9. [DOI] [PubMed] [Google Scholar]
  29. Koltunow A. M., Rezaian M. A. Grapevine yellow speckle viroid: structural features of a new viroid group. Nucleic Acids Res. 1988 Feb 11;16(3):849–864. doi: 10.1093/nar/16.3.849. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. 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]
  31. Lambowitz A. M. Infectious introns. Cell. 1989 Feb 10;56(3):323–326. doi: 10.1016/0092-8674(89)90232-8. [DOI] [PubMed] [Google Scholar]
  32. 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]
  33. Reanney D. Genetic noise in evolution? 1984 Jan 26-Feb 1Nature. 307(5949):318–319. doi: 10.1038/307318a0. [DOI] [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. 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]
  35. Schneider I. R. Satellite-like particle of tobacco ringspot virus that resembles tobacco ringspot virus. Science. 1969 Dec 26;166(3913):1627–1629. doi: 10.1126/science.166.3913.1627. [DOI] [PubMed] [Google Scholar]
  36. Sharp P. A. On the origin of RNA splicing and introns. Cell. 1985 Sep;42(2):397–400. doi: 10.1016/0092-8674(85)90092-3. [DOI] [PubMed] [Google Scholar]
  37. 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. 1987 Aug;6(8):2173–2183. doi: 10.1002/j.1460-2075.1987.tb02488.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Uhlenbeck O. C. A small catalytic oligoribonucleotide. Nature. 1987 Aug 13;328(6131):596–600. doi: 10.1038/328596a0. [DOI] [PubMed] [Google Scholar]
  39. Weiner A. M., Maizels N. tRNA-like structures tag the 3' ends of genomic RNA molecules for replication: implications for the origin of protein synthesis. Proc Natl Acad Sci U S A. 1987 Nov;84(21):7383–7387. doi: 10.1073/pnas.84.21.7383. [DOI] [PMC free article] [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