Abstract
In the course of evolving variants of the Tetrahymena thermophila Group I ribozyme for improved DNA cleavage in vitro, we witnessed the unexpected emergence of a derived molecular species, capable of acting as a partner for the ribozyme, but no longer autocatalytic. This new RNA species exhibits a deletion in the catalytic core and participates in a productive intermolecular interaction with an active ribozyme, thus insuring its survival in the population. These novel RNA molecules have evolved a precise catalytic interaction with the Group I ribozyme and depend for their survival on the continued presence of active catalysts. This interaction hints at the complexity that may inevitably arise even in simple evolving systems.
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Selected References
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- Bartel D. P., Szostak J. W. Isolation of new ribozymes from a large pool of random sequences [see comment]. Science. 1993 Sep 10;261(5127):1411–1418. doi: 10.1126/science.7690155. [DOI] [PubMed] [Google Scholar]
- Beaudry A. A., Joyce G. F. Directed evolution of an RNA enzyme. Science. 1992 Jul 31;257(5070):635–641. doi: 10.1126/science.1496376. [DOI] [PubMed] [Google Scholar]
- Cech T. R., Damberger S. H., Gutell R. R. Representation of the secondary and tertiary structure of group I introns. Nat Struct Biol. 1994 May;1(5):273–280. doi: 10.1038/nsb0594-273. [DOI] [PubMed] [Google Scholar]
- Eigen M. New concepts for dealing with the evolution of nucleic acids. Cold Spring Harb Symp Quant Biol. 1987;52:307–320. doi: 10.1101/sqb.1987.052.01.036. [DOI] [PubMed] [Google Scholar]
- Ekland E. H., Szostak J. W., Bartel D. P. Structurally complex and highly active RNA ligases derived from random RNA sequences. Science. 1995 Jul 21;269(5222):364–370. doi: 10.1126/science.7618102. [DOI] [PubMed] [Google Scholar]
- Ellington A. D., Szostak J. W. Selection in vitro of single-stranded DNA molecules that fold into specific ligand-binding structures. Nature. 1992 Feb 27;355(6363):850–852. doi: 10.1038/355850a0. [DOI] [PubMed] [Google Scholar]
- Furuya T., Macnaughton T. B., La Monica N., Lai M. M. Natural evolution of coronavirus defective-interfering RNA involves RNA recombination. Virology. 1993 May;194(1):408–413. doi: 10.1006/viro.1993.1277. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Green R., Szostak J. W. Selection of a ribozyme that functions as a superior template in a self-copying reaction. Science. 1992 Dec 18;258(5090):1910–1915. doi: 10.1126/science.1470913. [DOI] [PubMed] [Google Scholar]
- Herschlag D., Cech T. R. DNA cleavage catalysed by the ribozyme from Tetrahymena. Nature. 1990 Mar 29;344(6265):405–409. doi: 10.1038/344405a0. [DOI] [PubMed] [Google Scholar]
- Hirao I., Ellington A. D. Re-creating the RNA world. Curr Biol. 1995 Sep 1;5(9):1017–1022. doi: 10.1016/s0960-9822(95)00205-3. [DOI] [PubMed] [Google Scholar]
- Kirkwood T. B., Bangham C. R. Cycles, chaos, and evolution in virus cultures: a model of defective interfering particles. Proc Natl Acad Sci U S A. 1994 Aug 30;91(18):8685–8689. doi: 10.1073/pnas.91.18.8685. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kramer F. R., Mills D. R., Cole P. E., Nishihara T., Spiegelman S. Evolution in vitro: sequence and phenotype of a mutant RNA resistant to ethidium bromide. J Mol Biol. 1974 Nov 15;89(4):719–736. doi: 10.1016/0022-2836(74)90047-3. [DOI] [PubMed] [Google Scholar]
- Lehman N., Joyce G. F. Evolution in vitro of an RNA enzyme with altered metal dependence. Nature. 1993 Jan 14;361(6408):182–185. doi: 10.1038/361182a0. [DOI] [PubMed] [Google Scholar]
- Lehman N., Joyce G. F. Evolution in vitro: analysis of a lineage of ribozymes. Curr Biol. 1993;3(11):723–734. doi: 10.1016/0960-9822(93)90019-k. [DOI] [PubMed] [Google Scholar]
- Meyers G., Thiel H. J. Cytopathogenicity of classical swine fever virus caused by defective interfering particles. J Virol. 1995 Jun;69(6):3683–3689. doi: 10.1128/jvi.69.6.3683-3689.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Michel F., Westhof E. Modelling of the three-dimensional architecture of group I catalytic introns based on comparative sequence analysis. J Mol Biol. 1990 Dec 5;216(3):585–610. doi: 10.1016/0022-2836(90)90386-Z. [DOI] [PubMed] [Google Scholar]
- Nadeau J. G., Singleton C. K., Kelly G. B., Weith H. L., Gough G. R. Use of ribonucleosides as protecting groups in synthesis of polynucleotides with phosphorylated terminals. Biochemistry. 1984 Dec 4;23(25):6153–6159. doi: 10.1021/bi00320a040. [DOI] [PubMed] [Google Scholar]
- Norkin L. C., Tirrell S. M. Emergence of simian virus 40 variants during serial passage of plaque isolates. J Virol. 1982 May;42(2):730–733. doi: 10.1128/jvi.42.2.730-733.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Szathmáry E. Natural selection and dynamical coexistence of defective and complementing virus segments. J Theor Biol. 1992 Aug 7;157(3):383–406. doi: 10.1016/s0022-5193(05)80617-4. [DOI] [PubMed] [Google Scholar]
- Tsang J., Joyce G. F. Evolutionary optimization of the catalytic properties of a DNA-cleaving ribozyme. Biochemistry. 1994 May 17;33(19):5966–5973. doi: 10.1021/bi00185a038. [DOI] [PubMed] [Google Scholar]
- Tsang J., Joyce G. F. Specialization of the DNA-cleaving activity of a group I ribozyme through in vitro evolution. J Mol Biol. 1996 Sep 13;262(1):31–42. doi: 10.1006/jmbi.1996.0496. [DOI] [PubMed] [Google Scholar]
- Tuerk C., Gold L. Systematic evolution of ligands by exponential enrichment: RNA ligands to bacteriophage T4 DNA polymerase. Science. 1990 Aug 3;249(4968):505–510. doi: 10.1126/science.2200121. [DOI] [PubMed] [Google Scholar]
- Wlotzka B., McCaskill J. S. A molecular predator and its prey: coupled isothermal amplification of nucleic acids. Chem Biol. 1997 Jan;4(1):25–33. doi: 10.1016/s1074-5521(97)90234-9. [DOI] [PubMed] [Google Scholar]
- Woodworth-Gutai M., Celeste A., Sheflin L., Sclair M. Naturally arising recombinants that are missing portions of the simian virus 40 regulatory region. Mol Cell Biol. 1983 Nov;3(11):1930–1936. doi: 10.1128/mcb.3.11.1930. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zaug A. J., Cech T. R. The intervening sequence RNA of Tetrahymena is an enzyme. Science. 1986 Jan 31;231(4737):470–475. doi: 10.1126/science.3941911. [DOI] [PubMed] [Google Scholar]