Abstract
We propose a phylogeny for the evolution of tRNA that is based on the ubiquity and conservation of tRNA-like structures in the replication of contemporary genomes. This phylogeny is unique in suggesting that the function of tRNA in replication dates back to the very beginnings of life on earth, before the advent of templated protein synthesis. The origin we propose for tRNA has distinct implications for the order in which other components of the modern translational apparatus evolved. We further suggest that the "top half" of modern tRNA-a coaxial stack of the acceptor stem on the T psi C arm--is the ancient structural and functional domain and that the "bottom half" of tRNA--a coaxial stack of the dihydrouracil arm on the anticodon arm--arose later to provide additional specificity.
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- Akins R. A., Kelley R. L., Lambowitz A. M. Characterization of mutant mitochondrial plasmids of Neurospora spp. that have incorporated tRNAs by reverse transcription. Mol Cell Biol. 1989 Feb;9(2):678–691. doi: 10.1128/mcb.9.2.678. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Benner S. A., Ellington A. D., Tauer A. Modern metabolism as a palimpsest of the RNA world. Proc Natl Acad Sci U S A. 1989 Sep;86(18):7054–7058. doi: 10.1073/pnas.86.18.7054. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Blackburn E. H. Structure and function of telomeres. Nature. 1991 Apr 18;350(6319):569–573. doi: 10.1038/350569a0. [DOI] [PubMed] [Google Scholar]
- Blumenthal T., Carmichael G. G. RNA replication: function and structure of Qbeta-replicase. Annu Rev Biochem. 1979;48:525–548. doi: 10.1146/annurev.bi.48.070179.002521. [DOI] [PubMed] [Google Scholar]
- Cavarelli J., Rees B., Ruff M., Thierry J. C., Moras D. Yeast tRNA(Asp) recognition by its cognate class II aminoacyl-tRNA synthetase. Nature. 1993 Mar 11;362(6416):181–184. doi: 10.1038/362181a0. [DOI] [PubMed] [Google Scholar]
- 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]
- Chapman K. B., Byström A. S., Boeke J. D. Initiator methionine tRNA is essential for Ty1 transposition in yeast. Proc Natl Acad Sci U S A. 1992 Apr 15;89(8):3236–3240. doi: 10.1073/pnas.89.8.3236. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Connell G. J., Illangesekare M., Yarus M. Three small ribooligonucleotides with specific arginine sites. Biochemistry. 1993 Jun 1;32(21):5497–5502. doi: 10.1021/bi00072a002. [DOI] [PubMed] [Google Scholar]
- Covey S. N., Turner D. S. Hairpin DNAs of cauliflower mosaic virus generated by reverse transcription in vivo. EMBO J. 1986 Nov;5(11):2763–2768. doi: 10.1002/j.1460-2075.1986.tb04565.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Crothers D. M., Seno T., Söll G. Is there a discriminator site in transfer RNA? Proc Natl Acad Sci U S A. 1972 Oct;69(10):3063–3067. doi: 10.1073/pnas.69.10.3063. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cusack S., Berthet-Colominas C., Härtlein M., Nassar N., Leberman R. A second class of synthetase structure revealed by X-ray analysis of Escherichia coli seryl-tRNA synthetase at 2.5 A. Nature. 1990 Sep 20;347(6290):249–255. doi: 10.1038/347249a0. [DOI] [PubMed] [Google Scholar]
- Eriani G., Delarue M., Poch O., Gangloff J., Moras D. Partition of tRNA synthetases into two classes based on mutually exclusive sets of sequence motifs. Nature. 1990 Sep 13;347(6289):203–206. doi: 10.1038/347203a0. [DOI] [PubMed] [Google Scholar]
- Green C. J., Vold B. S., Morch M. D., Joshi R. L., Haenni A. L. Ionic conditions for the cleavage of the tRNA-like structure of turnip yellow mosaic virus by the catalytic RNA of RNase P. J Biol Chem. 1988 Aug 25;263(24):11617–11620. [PubMed] [Google Scholar]
- Guerrier-Takada C., van Belkum A., Pleij C. W., Altman S. Novel reactions of RNAase P with a tRNA-like structure in turnip yellow mosaic virus RNA. Cell. 1988 Apr 22;53(2):267–272. doi: 10.1016/0092-8674(88)90388-1. [DOI] [PubMed] [Google Scholar]
- Guerrier-Takada C., van Belkum A., Pleij C. W., Altman S. Novel reactions of RNAase P with a tRNA-like structure in turnip yellow mosaic virus RNA. Cell. 1988 Apr 22;53(2):267–272. doi: 10.1016/0092-8674(88)90388-1. [DOI] [PubMed] [Google Scholar]
- Haenni A. L., Joshi S., Chapeville F. tRNA-like structures in the genomes of RNA viruses. Prog Nucleic Acid Res Mol Biol. 1982;27:85–104. doi: 10.1016/s0079-6603(08)60598-x. [DOI] [PubMed] [Google Scholar]
- Hall T. C. Transfer RNA-like structures in viral genomes. Int Rev Cytol. 1979;60:1–26. doi: 10.1016/s0074-7696(08)61257-7. [DOI] [PubMed] [Google Scholar]
- Jaehning J. A. Sigma factor relatives in eukaryotes. Science. 1991 Aug 23;253(5022):859–859. doi: 10.1126/science.1876846. [DOI] [PubMed] [Google Scholar]
- Kikuchi Y., Ando Y., Shiba T. Unusual priming mechanism of RNA-directed DNA synthesis in copia retrovirus-like particles of Drosophila. 1986 Oct 30-Nov 5Nature. 323(6091):824–826. doi: 10.1038/323824a0. [DOI] [PubMed] [Google Scholar]
- Kuiper M. T., Lambowitz A. M. A novel reverse transcriptase activity associated with mitochondrial plasmids of Neurospora. Cell. 1988 Nov 18;55(4):693–704. doi: 10.1016/0092-8674(88)90228-0. [DOI] [PubMed] [Google Scholar]
- Lee B. J., Kang S. G., Hatfield D. Transcription of Xenopus selenocysteine tRNA Ser (formerly designated opal suppressor phosphoserine tRNA) gene is directed by multiple 5'-extragenic regulatory elements. J Biol Chem. 1989 Jun 5;264(16):9696–9702. [PubMed] [Google Scholar]
- Maizels N., Weiner A. M. Peptide-specific ribosomes, genomic tags, and the origin of the genetic code. Cold Spring Harb Symp Quant Biol. 1987;52:743–749. doi: 10.1101/sqb.1987.052.01.083. [DOI] [PubMed] [Google Scholar]
- Mans R. M., Guerrier-Takada C., Altman S., Pleij C. W. Interaction of RNase P from Escherichia coli with pseudoknotted structures in viral RNAs. Nucleic Acids Res. 1990 Jun 25;18(12):3479–3487. doi: 10.1093/nar/18.12.3479. [DOI] [PMC free article] [PubMed] [Google Scholar]
- McClain W. H., Guerrier-Takada C., Altman S. Model substrates for an RNA enzyme. Science. 1987 Oct 23;238(4826):527–530. doi: 10.1126/science.2443980. [DOI] [PubMed] [Google Scholar]
- McClain W. H. Rules that govern tRNA identity in protein synthesis. J Mol Biol. 1993 Nov 20;234(2):257–280. doi: 10.1006/jmbi.1993.1582. [DOI] [PubMed] [Google Scholar]
- Noller H. F., Hoffarth V., Zimniak L. Unusual resistance of peptidyl transferase to protein extraction procedures. Science. 1992 Jun 5;256(5062):1416–1419. doi: 10.1126/science.1604315. [DOI] [PubMed] [Google Scholar]
- Palmer J. R., Baltrus T., Reeve J. N., Daniels C. J. Transfer RNA genes from the hyperthermophilic Archaeon, Methanopyrus kandleri. Biochim Biophys Acta. 1992 Oct 20;1132(3):315–318. doi: 10.1016/0167-4781(92)90168-y. [DOI] [PubMed] [Google Scholar]
- Pan T., Gutell R. R., Uhlenbeck O. C. Folding of circularly permuted transfer RNAs. Science. 1991 Nov 29;254(5036):1361–1364. doi: 10.1126/science.1720569. [DOI] [PubMed] [Google Scholar]
- Piccirilli J. A., McConnell T. S., Zaug A. J., Noller H. F., Cech T. R. Aminoacyl esterase activity of the Tetrahymena ribozyme. Science. 1992 Jun 5;256(5062):1420–1424. doi: 10.1126/science.1604316. [DOI] [PubMed] [Google Scholar]
- Raabe T., Bollum F. J., Manley J. L. Primary structure and expression of bovine poly(A) polymerase. Nature. 1991 Sep 19;353(6341):229–234. doi: 10.1038/353229a0. [DOI] [PubMed] [Google Scholar]
- Rao A. L., Dreher T. W., Marsh L. E., Hall T. C. Telomeric function of the tRNA-like structure of brome mosaic virus RNA. Proc Natl Acad Sci U S A. 1989 Jul;86(14):5335–5339. doi: 10.1073/pnas.86.14.5335. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rasmussen N. J., Wikman F. P., Clark B. F. Crosslinking of tRNA containing a long extra arm to elongation factor Tu by trans-diamminedichloroplatinum(II). Nucleic Acids Res. 1990 Aug 25;18(16):4883–4890. doi: 10.1093/nar/18.16.4883. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ruff M., Krishnaswamy S., Boeglin M., Poterszman A., Mitschler A., Podjarny A., Rees B., Thierry J. C., Moras D. Class II aminoacyl transfer RNA synthetases: crystal structure of yeast aspartyl-tRNA synthetase complexed with tRNA(Asp). Science. 1991 Jun 21;252(5013):1682–1689. doi: 10.1126/science.2047877. [DOI] [PubMed] [Google Scholar]
- Saks M. E., Sampson J. R., Abelson J. N. The transfer RNA identity problem: a search for rules. Science. 1994 Jan 14;263(5144):191–197. doi: 10.1126/science.7506844. [DOI] [PubMed] [Google Scholar]
- Sanfaçon H., Hohn T. Proximity to the promoter inhibits recognition of cauliflower mosaic virus polyadenylation signal. Nature. 1990 Jul 5;346(6279):81–84. doi: 10.1038/346081a0. [DOI] [PubMed] [Google Scholar]
- Schimmel P., Giegé R., Moras D., Yokoyama S. An operational RNA code for amino acids and possible relationship to genetic code. Proc Natl Acad Sci U S A. 1993 Oct 1;90(19):8763–8768. doi: 10.1073/pnas.90.19.8763. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tse W. T., Forget B. G. Reverse transcription and direct amplification of cellular RNA transcripts by Taq polymerase. Gene. 1990 Apr 16;88(2):293–296. doi: 10.1016/0378-1119(90)90047-u. [DOI] [PubMed] [Google Scholar]
- Wang H., Lambowitz A. M. The Mauriceville plasmid reverse transcriptase can initiate cDNA synthesis de novo and may be related to reverse transcriptase and DNA polymerase progenitor. Cell. 1993 Dec 17;75(6):1071–1081. doi: 10.1016/0092-8674(93)90317-j. [DOI] [PubMed] [Google Scholar]
- Watson J. D. Origin of concatemeric T7 DNA. Nat New Biol. 1972 Oct 18;239(94):197–201. doi: 10.1038/newbio239197a0. [DOI] [PubMed] [Google Scholar]
- 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]
- Wigley P. L., Sheets M. D., Zarkower D. A., Whitmer M. E., Wickens M. Polyadenylation of mRNA: minimal substrates and a requirement for the 2' hydroxyl of the U in AAUAAA. Mol Cell Biol. 1990 Apr;10(4):1705–1713. doi: 10.1128/mcb.10.4.1705. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Woese C. R. Evolutionary questions: the "progenote". Science. 1990 Feb 16;247(4944):789–789. doi: 10.1126/science.2305249. [DOI] [PubMed] [Google Scholar]
- Woese C. R., Kandler O., Wheelis M. L. Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci U S A. 1990 Jun;87(12):4576–4579. doi: 10.1073/pnas.87.12.4576. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Xiong Y., Eickbush T. H. Origin and evolution of retroelements based upon their reverse transcriptase sequences. EMBO J. 1990 Oct;9(10):3353–3362. doi: 10.1002/j.1460-2075.1990.tb07536.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yuan Y., Altman S. Selection of guide sequences that direct efficient cleavage of mRNA by human ribonuclease P. Science. 1994 Mar 4;263(5151):1269–1273. doi: 10.1126/science.8122108. [DOI] [PubMed] [Google Scholar]