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Molecular evolution of transfer RNA from two precursor hairpins: Implications for the origin of protein synthesis

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Abstract

In this paper we are going to present a model for the coevolution of major components of the protein synthesis machinery in a primordial RNA world. We propose that the essential prerequisites for RNA-based protein synthesis, i.e., tRNA-like molecules, ribozymic charging catalysts, small-subunit(SSU) rRNA, and large-subunit(LSU) rRNA, evolved from the same ancestral RNA molecule. Several arguments are considered which suggest that tRNA-like molecules were derived by tandem joining of template-flanking hairpin structures involved in replication control. It is further argued that the ancestors of contemporary group I tRNA introns catalyzed such hairpin joining reactions, themselves also giving rise to the ribosomal RNAs. Our model includes a general stereochemical principle for the interaction between ribozymes and hairpin-derived recognition structures, which can be applied to such seemingly different processes as RNA polymerization, aminoacylation, tRNA decoding, and peptidyl transfer, implicating a common origin for these fundamental functions. These and other considerations suggest that generation and evolution of tRNA were coupled to the evolution of synthetases, ribosomal RNAs, and introns from the beginning and have been a consequence arising from the original function of tRNA precursor hairpins as replication and recombination control elements.

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References

  • Belfort M (1993) An expanding universe of introns. Science 262:1009–1010

    Google Scholar 

  • Benner SA, Ellington AD, Tauer A (1989) Modern metabolism as a palimpsest of the RNA world. Proc Natl Acad Sci USA 86:7054–7058

    Google Scholar 

  • Buechter DD, Schimmel P (1993) Aminoacylation of RNA minihelices: Implications for tRNA synthetase structural design and evolution. Crit Rev Biochem Mol Biol 28(4):309–322

    Google Scholar 

  • Cavalier-Smith T (1991) Intron phylogeny: a new hypothesis. Trends Genet 7:145–148

    Google Scholar 

  • De Duve C (1988) The second genetic code. Nature 333:117–118

    Google Scholar 

  • Eigen M, Lindemann BF, Tietze M, Winkler-Oswatitsch R, Dress A, von Haeseler A (1989) How old is the genetic code? Statistical geometry of tRNA provides an answer. Science 244:673–679

    Google Scholar 

  • Eigen M, Schuster P (1979) The hypercycle—a principle of natural self-organization. Springer, Berlin

    Google Scholar 

  • Eigen M, Winkler-Oswatitsch R (1981a) Transfer-RNA: the early adaptor. Naturwissenschaften 68:217–228

    Google Scholar 

  • Eigen M, Winkler-Oswatitsch R (1981b) Transfer-RNA, an early gene? Naturwissenschaften 68:82–292

    Google Scholar 

  • Forster AC, Altman S (1990) External Guide Sequence for an RNA enzyme. Science 249:783–786

    Google Scholar 

  • Gibson TJ, Lamond AI (1990) Metabolic complexity in the RNA world and implications for the origin of protein synthesis. J Mol Evol 30:7–15

    Google Scholar 

  • Gilbert W (1986) The RNA world. Nature 319:618

    Google Scholar 

  • Hausner TP, Geigenmueller U, Nierhaus KH (1988) The allosteric three-site model for the ribosomal elongation cycle. J Biol Chem 263:13103–13111

    Google Scholar 

  • Joyce GF (1989) RNA evolution and the origins of life. Nature 338: 217–224

    Article  Google Scholar 

  • Kikuchi Y (1990) Cleavage of tRNA within the mature tRNA sequence by the catalytic RNA of RNaseP: implications for the formation of the primer tRNA fragment for reverse transcription in copia retrovirus-like particles. Proc Natl Acad Sci USA 87:8105–8109

    Google Scholar 

  • Kuhsel MG, Strickland R, Palmer JD (1990) An ancient group I intron shared by eubacteria and chloroplasts. Science 250:1570–1573

    Google Scholar 

  • Lambowitz AM, Perlman PS (1990) Involvement of Amnoacyl-tRNA synthetases and other proteins in group I and group II intron splicing. Trends Biochem Sci 15:440–444

    Google Scholar 

  • Mans RMW, Pleij CWA, Bosch L (1991) tRNA-like structures. Eur J Biochem 201:303–324

    Google Scholar 

  • McClain WH (1993) Rules that govern tRNA identity in protein synthesis. J Mol Biol 234:257–280

    Google Scholar 

  • McPheeters DS, Abelson J (1992) Mutational analysis of the yeast U2 snRNA suggests a structural similarity to the catalytic core of group I introns. Cell 71:819–831

    Google Scholar 

  • Moeller W, Janssen GMC (1992) Statistical evidence for remnants of the primordial code in the acceptor stem of prokaryotic transfer RNA. J Mol Evol 34:471–477

    Google Scholar 

  • Noller HF, Hoffarth V, Zimniak L (1992) Unusual resistance of peptidyl transferase to protein extraction procedures. Science 256: 1420–1424

    Google Scholar 

  • Noller HF (1993) tRNA-rRNA interactions and peptidyl transferase. FASEB J 7:87–89

    Google Scholar 

  • Orgel LE (1987) Evolution of the genetic apparatus: a review. Cold Spring Harbor Symp Quant Biol 52:9–16

    Google Scholar 

  • Phizicky EM, Greer CL (1993) Pre-tRNA splicing: variation on a theme or exception to the rule? Trends Biochem Sci 18:31–34

    Google Scholar 

  • Piccirilli JA, McConnell TS, Zang AJ, Noller HF, Cech TR (1992) Aminoacyl esterase activity of the Tetrahymena ribozyme. Science 256:1416–1419

    Google Scholar 

  • Pyle AM, Cech TR (1991) Ribozyme recognition of RNA by tertiary interactions with specific ribose 2′-OH groups. Nature 350:628–631

    Google Scholar 

  • Pyle AM, Murphy FL, Cech TR (1992) RNA substrate binding site in the catalytic core of the Tetrahymena ribozyme. Nature 358:123–128

    Google Scholar 

  • Reinhold-Hurek B, Shub DA (1992) Self-splicing imrons in tRNA genes of widely divergent bacteria. Nature 357:173–176

    Google Scholar 

  • Saks ME, Sampson JR, Abelson JN (1994) The transfer RNA identity problem: a search for rules. Science 263:191–197

    Google Scholar 

  • Sargueil B, Tanner NK (1994) A shortened form of the Tetrahymena thermophila group I intron can catalyze the complete splicing reaction in trans. J Mol Biol 233:629–643

    Google Scholar 

  • Schimmel P, Giege R, Moras D, Yokoyama S (1993) An operational RNA code for amino acids and possible relationship to genetic code. Proc Natl Acad Sci USA 90:8763–8768

    Google Scholar 

  • Sharp PA (1991) “Five easy pieces.” Science 251:663

    Google Scholar 

  • Steitz TA, Steitz JA (1993) A general two-metal-ion mechanism for catalytic RNA. Proc Natl Acad Sci USA 90:6498–6502

    CAS  PubMed  Google Scholar 

  • Strobel SA, Cech TR (1994) Translocation of an RNA duplex on a ribozyme. Nature Struct Biol 1:13–17

    Google Scholar 

  • Thompson AJ, Herrin DL (1994) A chloroplast group I intron undergoes the first step of reverse splicing into host cytoplasmic 5.8S rRNA. J Mol Biol 236:455–468

    Google Scholar 

  • von Ahsen U, Noller HF (1993) Footprinting the sites of interaction of antibiotics with catalytic group I intron RNA. Science 260:1500–1503

    Google Scholar 

  • Voytas DF, Boeke JD (1993) Yeast retrotransposons and tRNAs. Trends Genet 9:421–426

    Google Scholar 

  • Wank H, Rogers J, Davies J, Schroeder R (1994) Peptide antibiotics of the tuberactinomycin family as inhibitors of group I intron RNA splicing. J Mol Biol 236:1001–1010

    Google Scholar 

  • Weiner AM (1988) Eukaryodc nuclear telomeres: molecular fossils of the RNP world? Cell 52:155–157

    Google Scholar 

  • Weiner AM (1993) mRNA splicing and autocatalytic introns: distant cousins or the product of chemical determinism? Cell 72:161–164

    Google Scholar 

  • Weiner AM, Maizels N (1987) tRNA-like structures tag the 3′ end of genomic RNA molecules for replication: implications for the origin of protein synthesis. Proc Natl Acad Sci USA 84:7383–7387

    Google Scholar 

  • Winkler-Oswatitsch R, Dress A, Eigen M (1986) Comparative sequence analysis, exemplified with tRNA and 5S rRNA. Chem Scr 26B:59–66

    Google Scholar 

  • Wise JA (1993) Guides to the heart of the spliceosome. Science 262: 1978–1979

    Google Scholar 

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Correspondence to: T.P. Dick

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Dick, T.P., Schamel, W.W.A. Molecular evolution of transfer RNA from two precursor hairpins: Implications for the origin of protein synthesis. J Mol Evol 41, 1–9 (1995). https://doi.org/10.1007/BF00174035

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  • DOI: https://doi.org/10.1007/BF00174035

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