Modern mRNA proofreading and repair: Clues that the last universal common ancestor possessed an RNA genome?

Molecular Biology and Evolution

Volumn 22, Issue 6, 2005, Pages 1444-1455

  Poole, Anthony M ^a   Logan, Derek T ^b  

^a STOCKHOLM UNIVERSITY   (Sweden)

^b LUND UNIVERSITY   (Sweden)

Author keywords

DNA origins; Evolution; Last Universal Common Ancestor; Proofreading; RNA polymerase; RNA repair

Indexed keywords

DNA; MESSENGER RNA; PROTEIN; RNA POLYMERASE;

ARTICLE; DNA REPAIR; DNA REPLICATION; DNA TRANSCRIPTION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME STRUCTURE; GENOME ANALYSIS; MOLECULAR EVOLUTION; NONHUMAN; PHYLOGENY; PROGENOTE; REVERSE TRANSCRIPTION; RNA PROCESSING; SEQUENCE HOMOLOGY;

DNA REPAIR; DNA-DIRECTED RNA POLYMERASES; EVOLUTION; EVOLUTION, MOLECULAR; GENOME; MODELS, GENETIC; MODELS, MOLECULAR; MODELS, THEORETICAL; RNA; RNA EDITING; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, MESSENGER; SELECTION (GENETICS);

EID: 19544385261     PISSN: 07374038     EISSN: None     Source Type: Journal    
DOI: 10.1093/molbev/msi132     Document Type: Article

References (116)

1. Aas, P. A., M. Otterlei, P. O. Falnes et al. (11 co-authors). 2003. Human and bacterial oxidative demethylases repair alkylation damage in both RNA and DNA. Nature 421:859-863.
2. Aravind, L., and E. V. Koonin. 2001. The DNA-repair protein AlkB, EGL-9, and leprecan define new families of 2-oxoglutarate- and iron-dependent dioxygenases. Genome Biol. 2:RESEARCH0007.
3. Astatke, M., K. Ng, N. D. Grindley, and C. M. Joyce. 1998. A single side chain prevents Escherichia coli DNA polymerase I (Klenow fragment) from incorporating ribonucleotides. Proc. Natl. Acad. Sci. USA 95:3402-3407.
4. Atkins, J. F. 1993. Contemporary RNA genomes. Pp. 535-556 in R. F. Gesteland and J. F. Atkins, eds. The RNA world. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
5. Beard, W. A., and S. H. Wilson. 2003. Structural insights into the origins of DNA polymerase fidelity. Structure (Camb.) 11:489-496.
6. Benner, S. A., A. D. Ellington, and A. Tauer. 1989. Modern metabolism as a palimpsest of the RNA world. Proc. Natl. Acad. Sci. USA 86:7054-7058.
7. Biebricher, C. K., and L. E. Orgel. 1973. An RNA that multiplies indefinitely with DNA-dependent RNA polymerase: selection from a random copolymer. Proc. Natl. Acad. Sci. USA 70:934-938.
8. Blattner, F. R., G. Plunkett III, C. A. Bloch et al. (17 co-authors). 1997. The complete genome sequence of Escherichia coli K-12. Science 277:1453-1474.
9. Börner, G. V., S. Yokobori, M. Mörl, M. Dörner, and S. Pääbo. 1997. RNA editing in metazoan mitochondria: staying fit without sex. FEBS Lett. 409:320-324.
10. Borukhov, S., V. Sagitov, and A. Goldfarb. 1993. Transcript cleavage factors from E. coli. Cell 72:459-466.
11. Chédin, S., M. Riva, P. Schultz, A. Sentenac, and C. Carles. 1998. The RNA cleavage activity of RNA polymerase III is mediated by an essential TFIIS-like subunit and is important for transcription termination. Genes Dev. 12:3857-3871.
12. Cramer, P. 2002a. Multisubunit RNA polymerases. Curr. Opin. Struct. Biol. 12:89-97.
13. -. 2002b. Common structural features of nucleic acid polymerases. Bioessays 24:724-729.
14. Crick, F. H. C. 1968. The origin of the genetic code. J. Mol. Biol. 38:367-379.
15. Crotty, S., and R. Andino. 2002. Implications of high RNA virus mutation rates: lethal mutagenesis and the antiviral drug ribavirin. Microbes Infect. 4:1301-1307.
16. Diener, T. O. 1971. Potato spindle tuber "virus." IV. A replicating, low molecular weight RNA. Virology 45:411-428.
17. Dworkin, J. P., A. Lazcano, and S. L. Miller. 2003. The roads to and from the RNA world. J. Theor. Biol. 222:127-134.
18. Erie, D. A., O. Hajiseyedjavadi, M. C. Young, and P. H. von Hippel. 1993. Multiple RNA polymerase conformations and GreA: control of the fidelity of transcription. Science 262: 867-873.
19. Esser, C., N. Ahmadinejad, C. Wiegand et al. (15 co-authors). 2004. A genome phylogeny for mitochondria among alpha-proteobacteria and a predominantly eubacterial ancestry of yeast nuclear genes. Mol. Biol. Evol. 21:1643-1660.
20. Fels, A., K. Hu, and D. Riesner. 2001. Transcription of potato spindle tuber viroid by RNA polymerase II starts predominantly at two specific sites. Nucleic Acids Res. 29:4589-4597.
21. Fijalkowska, I. J., R. L. Dunn, and R. M. Schaaper. 1993. Mutants of Escherichia coli with increased fidelity of DNA replication. Genetics 134:1023-1030.
22. Filée, J., P. Forterre, T. Sen-Lin, and J. Laurent. 2002. Evolution of DNA polymerase families: evidences for multiple gene exchange between cellular and viral proteins. J. Mol. Evol. 54:763-773.
23. Fish, R. N., and C. M. Kane. 2002. Promoting elongation with transcript cleavage stimulatory factors. Biochim. Biophys. Acta 1577:287-307.
24. Flores, R., S. Delgado, M. E. Gas, A. Carbonell, D. Molina, S. Gago, and M. De la Pena. 2004. Viroids: the minimal non-coding RNAs with autonomous replication. FEBS Lett. 567:42-48.
25. Forterre, P. 1999. Displacement of cellular proteins by functional analogues from plasmids or viruses could explain puzzling phylogenies of many DNA informational proteins. Mol. Microbiol. 33:457-465.
26. -. 2001. Genomics and early cellular evolution. The origin of the DNA world. C. R. Acad. Sci. III 324:1067-1076.
27. -. 2002. The origin of DNA genomes and DNA replication proteins. Curr. Opin. Microbiol. 5:525-532.
28. Forterre, P., J. Filée, and H. Myllykallio. 2004. Origin and evolution of DNA and DNA replication machineries. Pp. 145-168 in L. R. de Pouplana, ed. The genetic code and the origin of life. Landes Bioscience, Georgetown, Tex.
29. Fraenkel-Conrat, H. 1956. The role of the nucleic acid in the reconstitution of active Tobacco Mosaic Virus. J. Am. Chem. Soc. 78:882-883.
30. Gao, G., M. Orlova, M. M. Georgiadis, W. A. Hendrickson, and S. P. Goff. 1997. Conferring RNA polymerase activity to a DNA polymerase: a single residue in reverse transcriptase controls substrate selection. Proc. Natl. Acad. Sci. USA 94: 407-411.
31. Gierer, A., and G. Schramm. 1956. Infectivity of ribonucleic acid from Tobacco Mosaic Virus. Nature 177:702-703.
32. Gilbert, W. 1986. The RNA world. Nature 319:618.
33. Gillet, R., and B. Felden. 2001. Emerging views on tmRNA-mediated protein tagging and ribosome rescue. Mol. Microbiol. 42:879-885.
34. Grabowski, B., and Z. Kelman. 2003. Archeal DNA replication: eukaryal proteins in a bacterial context. Annu. Rev. Microbiol. 57:487-516.
35. Guerrier-Takada, C., K. Gardiner, T. Marsh, N. Pace, and S. Altman. 1983. The RNA moiety of ribonuclease P is the catalytic subunit of the enzyme. Cell 35:849-857.
36. Hagler, J., and S. Shuman. 1993. Nascent RNA cleavage by purified ternary complexes of vaccinia RNA polymerase. J. Biol. Chem. 268:2166-2173.
37. Hansen, J. L., A. M. Long, and S. C. Schultz. 1997. Structure of the RNA-dependent RNA polymerase of poliovirus. Structure 5:1109-1122.
38. Harris, J. K., S. T. Kelley, G. B. Spiegelman, and N. R. Pace. 2003. The genetic core of the Universal Ancestor. Genome Res. 13:407-412.
39. Hausner, W., U. Lange, and M. Musfeldt. 2000. Transcription factor S, a cleavage induction factor of the archaeal RNA polymerase. J. Biol. Chem. 275:12393-12399.
40. Hutchison, C. A., S. N. Peterson, S. R. Gill, R. T. Cline, O. White, C. M. Fraser, H. O. Smith, and J. C. Venter. 1999. Global transposon mutagenesis and a minimal Mycoplasma genome. Science 286:2165-2169.
41. Ishihama, A. 1996. A multi-functional enzyme with RNA polymerase and RNase activities: molecular anatomy of influenza virus RNA polymerase. Biochimie 78:1097-1102.
42. Ishihama, A., K. Mizumoto, K. Kawakami, A. Kato, and A. Honda. 1986. Proofreading function associated with the RNA-dependent RNA polymerase from influenza virus. J. Biol. Chem. 261:10417-10421.
43. Ito, J., and D. K. Braithwaite. 1991. Compilation and alignment of DNA polymerase sequences. Nucleic Acids Res. 19:4045-4057.
44. Iyer, L. M., E. V. Koonin, and L. Aravind. 2003. Evolutionary connection between the catalytic subunits of DNA-dependent RNA polymerases and eukaryotic RNA-dependent RNA polymerases and the origin of RNA polymerases. BMC Struct. Biol. 3:1.
45. Jeffares, D. C., A. M. Poole, and D. Penny. 1998. Relics from the RNA world. J. Mol. Evol. 46:18-36.
46. Jeon, C., and K. Agarwal. 1996. Fidelity of RNA polymerase II transcription controlled by elongation factor TFIIS. Proc. Natl. Acad. Sci. USA 93:13677-13682.
47. Joyce, C. M., and T. A. Steitz. 1994. Function and structure relationships in DNA polymerases. Annu. Rev. Biochem. 63: 777-822.
48. Joyce, G. F., and L. E. Orgel. 1999. Prospects for understanding the origin of the RNA world. Pp. 49-77 in R. F. Gesteland, T. R. Cech, and J. F. Atkins, eds. The RNA world. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N. Y.
49. Kettenberger, H., K. J. Armache, and P. Cramer. 2003. Architecture of the RNA polymerase II-TFIIS complex and implications for mRNA cleavage. Cell 114:347-357.
50. -. 2004. Complete RNA polymerase II elongation complex structure and its interactions with NTP and TFIIS. Mol. Cell 16:955-965.
51. Koonin, E. V. 2003. Comparative genomics, minimal gene-sets and the Last Universal Common Ancestor. Nat. Rev. Microbiol. 1:127.
52. Kornberg, A., and T. A. Baker. 1992. DNA replication. Pp. 90-93. W. H. Freeman and Company, New York.
53. Kruger, K., P. J. Grabowski, A. J. Zaug, J. Sands, D. E. Gottschling, and T. R. Cech. 1982. Self-splicing RNA: autoexcision and autocyclization of the ribosomal RNA intervening sequence of Tetrahymena. Cell 31:147-157.
54. Labeit, S., and B. Kolmerer. 1995. Titins: giant proteins in charge of muscle ultrastructure and elasticity. Science 270:293-296.
55. Lange, U., and W. Hausner. 2004. Transcriptional fidelity and proofreading in Archaea and implications for the mechanism of TFS-induced RNA cleavage. Mol. Microbiol. 52:1133-1143.
56. Larsson, K. M., A. Jordan, R. Eliasson, P. Reichard, D. T. Logan, and P. Nordlund. 2004. Structural mechanism of allosteric substrate specificity regulation in a ribonucleotide reductase. Nat. Struct. Mol. Biol. 11:1142-1149.
57. Lehman, N. 2003. A case for the extreme antiquity of recombination. J. Mol. Evol. 56:770-777.
58. Leipe, D. D., L. Aravind, and E. V. Koonin. 1999. Did DNA replication evolve twice independently? Nucleic Acids Res. 27:3389-3401.
59. Logan, D. T., J. Andersson, B. M. Sjoberg, and P. Nordlund. 1999. A glycyl radical site in the crystal structure of a class III ribonucleotide reductase. Science 283:1499-1504.
60. Lynch, M. 1996. Mutation accumulation in transfer RNAs: molecular evidence for Muller's ratchet in mitochondrial genomes. Mol. Biol. Evol. 13:209-220.
61. Marra, M. A., S. J. Jones, C. R. Astell et al. (59 co-authors). 2003. The genome sequence of the SARS-associated coronavirus. Science 300:1399-1404.
62. Mirkin, B. G., T. I. Fenner, M. Y. Galperin, and E. V. Koonin. 2003. Algorithms for computing parsimonious evolutionary scenarios for genome evolution, the last universal common ancestor and dominance of horizontal gene transfer in the evolution of prokaryotes. BMC Evol. Biol. 3:2.
63. Moore, P. B., and T. A. Steitz. 2002. The involvement of RNA in ribosome function. Nature 418:229-235.
64. Mühlbach, H. P., and H. L. Sanger. 1979. Viroid replication is inhibited by alpha-amanitin. Nature 278:185-188.
65. Mushegian, A. R., and E. V. Koonin. 1996. A minimal gene set for cellular life derived by comparison of complete bacterial genomes. Proc. Natl. Acad. Sci. USA 93:10268-10273.
66. Noller, H. F. 2004. The driving force for molecular evolution of translation. RNA 10:1833-1837.
67. Opalka, N., M. Chlenov, P. Chacon, W. J. Rice, W. Wriggers, and S. A. Darst. 2003. Structure and function of the transcription elongation factor GreB bound to bacterial RNA polymerase. Cell 114:335-345.
68. Orgel, L. E. 1968. Evolution of the genetic apparatus. J. Mol. Biol. 38:381-393.
69. Orlova, M., J. Newlands, A. Das, A. Goldfarb, and S. Borukhov. 1995. Intrinsic transcript cleavage activity of RNA polymerase. Proc. Natl. Acad. Sci. USA 92:4596-4600.
70. Ougland, R., C. M. Zhang, A. Liiv, R. F. Johansen, E. Seeberg, Y. M. Hou, J. Remme, and P. O. Falnes. 2004. AlkB restores the biological function of mRNA and tRNA inactivated by chemical methylation. Mol. Cell 16:107-116.
71. Pelchat, M., C. Grenier, and J. P. Perreault. 2002. Characterization of a viroid-derived RNA promoter for the DNA-dependent RNA polymerase from Escherichia coli. Biochemistry 41:6561-6571.
72. Pelchat, M., and J. P. Perreault. 2004. Binding site of Escherichia coli RNA polymerase to an RNA promoter. Biochem. Biophys. Res. Commun. 319:636-642.
73. Peleg, O., V. Kirzhner, E. Trifonov, and A. Bolshoy. 2004. Overlapping messages and survivability. J. Mol. Evol. 59: 520-527.
74. Penny, D., and A. Poole. 1999. The nature of the last universal common ancestor. Curr. Opin. Genet. Dev. 9:672-677.
75. Pfeiffer, J. K., and K. Kirkegaard. 2003. A single mutation in poliovirus RNA-dependent RNA polymerase confers resistance to mutagenic nucleotide analogs via increased fidelity. Proc. Natl. Acad. Sci. USA 100:7289-7294.
76. Poole, A., D. Jeffares, and D. Penny. 1999. Early evolution: prokaryotes, the new kids on the block. Bioessays 21:880-889.
77. Poole, A., D. Penny, and B.-M. Sjöberg. 2000. Methyl-RNA: an evolutionary bridge between RNA and DNA? Chem. Biol. 7:R207-R216.
78. Poole, A. M., D. C. Jeffares, and D. Penny. 1998. The path from the RNA world. J. Mol. Evol. 46:1-17.
79. Poole, A. M., D. T. Logan, and B.-M. Sjöberg. 2002. The evolution of the ribonucleotide reductases: much ado about oxygen. J. Mol. Evol. 55:180-196.
80. Pugachev, K. V., F. Guirakhoo, S. W. Ocran et al. (11 co-authors). 2004. High fidelity of yellow fever virus RNA polymerase. J. Virol. 78:1032-1038.
81. Reanney, D. C. 1987. Genetic error and genome design. Cold Spring Harb. Symp. Quant. Biol. 52:751-757.
82. Reichert, A. S., and M. Mörl. 2000. Repair of tRNAs in metazoan mitochondria. Nucleic Acids Res. 28:2043-2048.
83. Rosales, R., N. Harris, B. Y. Ahn, and B. Moss. 1994. Purification and identification of a vaccinia virus-encoded intermediate stage promoter-specific transcription factor that has homology to eukaryotic transcription factor SII (TFIIS) and an additional role as a viral RNA polymerase subunit. J. Biol. Chem. 269:14260-14267.
84. Rota, P. A., M. S. Oberste, S. S. Monroe et al. (35 co-authors). 2003. Characterization of a novel coronavirus associated with severe acute respiratory syndrome. Science 300:1394-1399.
85. Santos, M., E. Zintzaras, and E. Szathmáry. 2004. Recombination in primeval genomes: a step forward but still a long leap from maintaining a sizable genome. J. Mol. Evol. 59:507-519.
86. Sastry, S. S., and B. M. Ross. 1997. Nuclease activity of T7 RNA polymerase and the heterogeneity of transcription elongation complexes. J. Biol. Chem. 272:8644-8652.
87. Scheuring, I. 2000. Avoiding catch-22 of early evolution by step-wise increase in copying fidelity. Selection 1:135-145.
88. Schindler, I.-M., and H.-P. Mühlbach. 1992. Involvement of nuclear DNA-dependent RNA polymerases in potato spindle tuber viroid replication: a reevaluation. Plant Sci. 84: 221-229.
89. Schnapp, G., B. R. Graveley, and I. Grummt. 1996. TFIIS binds to mouse RNA polymerase I and stimulates transcript elongation and hydrolytic cleavage of nascent rRNA. Mol. Gen. Genet. 252:412-419.
90. Shaevitz, J. W., E. A. Abbondanzieri, R. Landick, and S. M. Block. 2003. Backtracking by single RNA polymerase molecules observed at near-base-pair resolution. Nature 426:684-687.
91. Shirai, T., and M. Go. 1991. RNase-like domain in DNA-directed RNA polymerase II. Proc. Natl. Acad. Sci. USA 88:9056-9060.
92. Siegel, R. W., L. Bellon, L. Beigelman, and C. C. Kao. 1999. Use of DNA, RNA, and chimeric templates by a viral RNA-dependent RNA polymerase: evolutionary implications for the transition from the RNA to the DNA world. J. Virol. 73:6424-6429.
93. Sintchak, M. D., G. Arjara, B. A. Kellogg, J. Stubbe, and C. L. Drennan. 2002. The crystal structure of class II ribonucleotide reductase reveals how an allosterically regulated monomer mimics a dimer. Nat. Struct. Biol. 9:293-300.
94. Skovgaard, M., L. J. Jensen, S. Brunak, D. Ussery, and A. Krogh. 2001. On the total number of genes and their length distribution in complete microbial genomes. Trends Genet. 17:425-428.
95. Sosunov, V., E. Sosunova, A. Mustaev, I. Bass, V. Nikiforov, and A. Goldfarb. 2003. Unified two-metal mechanism of RNA synthesis and degradation by RNA polymerase. EMBO J. 22: 2234-2244.
96. Sosunova, E., V. Sosunov, M. Kozlov, V. Nikiforov, A. Goldfarb, and A. Mustaev. 2003. Donation of catalytic residues to RNA polymerase active center by transcription factor Gre. Proc. Natl. Acad. Sci. USA 100:15469-15474.
97. Steitz, T. A. 1998. A mechanism for all polymerases. Nature 391:231-232.
98. -. 1999. DNA polymerases: structural diversity and common mechanisms. J. Biol. Chem. 274:17395-17398.
99. Steitz, T. A., and J. A. Steitz. 1993. A general two-metal-ion mechanism for catalytic RNA. Proc. Natl. Acad. Sci. USA 90:6498-6502.
100. Tauer, A., and S. A. Benner. 1997. The B12-dependent ribonucleotide reductase from the archaebacterium Thermoplasma acidophila: an evolutionary solution to the ribonucleotide reductase conundrum. Proc. Natl. Acad. Sci. USA 94:53-58.
101. Thomas, M. J., A. A. Platas, and D. K. Hawley. 1998. Transcriptional fidelity and proofreading by RNA polymerase II. Cell 93:627-637.
102. Torrents, E., P. Aloy, I. Gibert, and F. Rodriguez-Trelles. 2002. Ribonucleotide reductases: divergent evolution of an ancient enzyme. J. Mol. Evol. 55:138-152.
103. Tourasse, N. J., and M. Gouy. 1999. Accounting for evolutionary rate variation among sequence sites consistently changes universal phylogenies deduced from rRNA and protein-coding genes. Mol. Phylogenet. Evol. 13:159-168.
104. Tschochner, H. 1996. A novel RNA polymerase I-dependent RNase activity that shortens nascent transcripts from the 3′ end. Proc. Natl. Acad. Sci. USA 93:12914-12919.
105. Uhlin, U., and H. Eklund. 1994. Structure of ribonucleotide reductase protein R1. Nature 370:533-539.
106. Vasudevan, S., S. W. Peltz, and C. J. Wilusz. 2002. Non-stop decay - a new mRNA surveillance pathway. Bioessays 24:785-788.
107. Villarreal, L. P., and V. R. DeFilippis. 2000. A hypothesis for DNA viruses as the origin of eukaryotic replication proteins. J. Virol. 74:7079-7084.
108. Wang, D., and D. K. Hawley. 1993. Identification of a 3′ → 5′ exonuclease activity associated with human RNA polymerase II. Proc. Natl. Acad. Sci. USA 90:843-847.
109. Wettich, A., and C. K. Biebricher. 2001. RNA species that replicate with DNA-dependent RNA polymerase from Escherichia coli. Biochemistry 40:3308-3315.
110. White, H. B. III. 1976. Coenzymes as fossils of an earlier metabolic state. J. Mol. Evol. 7:101-104.
111. Whitehall, S. K., C. Bardeleben, and G. A. Kassavetis. 1994. Hydrolytic cleavage of nascent RNA in RNA polymerase III ternary transcription complexes. J. Biol. Chem. 269:2299-2306.
112. Wilusz, C. J., W. Wang, and S. W. Peltz. 2001. Curbing the nonsense: the activation and regulation of mRNA surveillance. Genes Dev. 15:2781-2785.
113. Wind, M., and D. Reines. 2000. Transcription elongation factor SII. Bioessays 22:327-336.
114. Woese, C. R. 1967. The genetic code: The molecular basis of genetic expression. Harper and Row, New York.
115. Yarus, M. 2002. Primordial genetics: phenotype of the ribocyte. Annu. Rev. Genet. 36:125-151.
116. Zanotto, P. M., M. J. Gibbs, E. A. Gould, and E. C. Holmes. 1996. A reevaluation of the higher taxonomy of viruses based on RNA polymerases. J. Virol. 70:6083-6096.