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How the Early Genetic Code Was Established?: Inference from the Analysis of Extant Animal Mitochondrial Decoding Systems

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Chemical Biology of Nucleic Acids

Part of the book series: RNA Technologies ((RNATECHN))

Abstract

Mitochondria are intracellular organelles in eukaryotic cells that have their own genome and translational apparatus. The vertebrate mitochondrial decoding system is thought to be the simplest among all extant living systems and to have originated by retrogression from the universal decoding system, induced mainly by genome economisation and directional mutation pressure during mitochondrial evolution. Thus, it is reasonable to speculate that the vertebrate genetic code table is a typical model for the early genetic code table.

In some metazoan mitochondrial decoding systems, it was found that unmodified anticodons of tRNA have the potential to base-pair with cognate codons and retain flexibility at the wobble pair, suggesting that the early decoding system consisted of unmodified RNA prior to the emergence of RNA-modifying systems. Competition would likely have occurred between G34-tRNA having GNN anticodons and U34-tRNA having UNN anticodons (or C34-tRNA having CNN anticodons for AUR codons) in their binding to the ribosomal A site, which would have resulted in the discrimination between NNY codons and NNR codons in the two-codon sets. Thus, the early genetic code table would have been established in such a way that eight family box codons were deciphered by U34-tRNA, and eight NNY and six NNR codons in the two-codon sets were deciphered by G34-tRNA and U34-tRNA (or C34-tRNA), respectively.

This review describes the characteristics of an early decoding system inferred from the genetic code of present vertebrate mitochondria, and how the present universal decoding system may have originated from the early decoding system during evolutionary history.

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References

  • Andachi Y, Yamao F, Iwami M et al (1987) Occurrence of unmodified adenine and uracil at the first position of anticodon in threonine tRNAs in Mycoplasma capricolum. Proc Natl Acad Sci U S A 84:7398–7402

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Andachi Y, Yamao F, Muto A et al (1989) Codon recognition patterns as deduced from sequences of the complete set of transfer RNA species in Mycoplasma capricolum: resemblance to mitochondria. J Mol Biol 209:37–54

    Article  CAS  PubMed  Google Scholar 

  • Anderson S, Bankier AT, Barerll BG et al (1981) Sequence and organization of the human mitochondrial genome. Nature 290:457–465

    Article  CAS  PubMed  Google Scholar 

  • Andersson SGE, Zomorodipour A, Andersson JO et al (1998) The genome sequence of Rickettsia prowazekii and the origin of mitochondria. Nature 396:133–143

    Article  CAS  PubMed  Google Scholar 

  • Barrell BG, Bankier AT, Drouin J (1979) A different genetic code in human mitochondria. Nature 282:189–194

    Article  CAS  PubMed  Google Scholar 

  • Bessho Y, Ohama T, Osawa S (1992) Planarian mitochondria II. The unique genetic code as deduced from cytochrome c oxydase subunit I gene sequence. J Mol Evol 34:331–335

    Article  CAS  PubMed  Google Scholar 

  • Himeno H, Masaki H, Kawai T et al (1987) Unusual genetic codes and a novel gene structure for tRNASer AGY in starfish mitochondria. Gene 56:219–230

    Article  CAS  PubMed  Google Scholar 

  • Huynen MA, Duarte I, Chrzanowska-Lightowlers ZMA et al (2012) Structure based hypothesis of a mitochondrial ribosome rescue mechanism. Biol Direct 7:14

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ikeuchi Y, Kimura S, Numata T et al (2010) Agmatine-containing cytidine in tRNA anticodon essential for AUA decoding in Archaea. Nat Chem Biol 6:277–282

    Article  CAS  PubMed  Google Scholar 

  • Inagaki Y, Kojima A, Bessho Y et al (1995) Translation of synonymous codons in family boxes by Mycoplasma capricolum tRNAs with unmodified uridine or adenosine at the first anticodon position. J Mol Biol 251:486–492

    Article  CAS  PubMed  Google Scholar 

  • Jacob JEM, Vanholme B, Van Leeuwen T et al (2009) A unique genetic code change in the mitochondrial genome of the parasitic nematode Radopholus similis. BMC Res Notes 2:192

    Article  PubMed Central  PubMed  Google Scholar 

  • Jukes TH (1983) Evolution of the amino acid code: inferences from mitochondrial codes. J Mol Evol 19:219–225

    Article  CAS  PubMed  Google Scholar 

  • Kurata S, Weixlbaumer A, Ohtsuki T et al (2008) Modified uridines with C5-methylene substituents at the first position of the tRNA anticodon stabilize U-G wobble pairing during decoding. J Biol Chem 283:18801–18811

    Article  CAS  PubMed  Google Scholar 

  • Lang BF, Burger G, O’Kelly CJ et al (1977) An ancestral mitochondrial DNA resembling a eubacterial genome in miniature. Nature 387:493–497

    Article  Google Scholar 

  • Margulis L (1970) Origin of eukaryotic cells. Yale University Press, New Haven, CT

    Google Scholar 

  • Margulis L (1993) Symbiosis in cell evolution: microbial communities in the Archean and Proterozoic eons, 2nd edn. W. H. Freeman, New York

    Google Scholar 

  • Matsuyama S, Ueda T, Crain PF et al (1998) A novel wobble rule found in starfish mitochondria. Presence of 7-methylguanosine at the anticodon wobble position expands decoding capability of tRNA. J Biol Chem 273:3363–3368

    Article  CAS  PubMed  Google Scholar 

  • Moriya J, Yokogawa T, Wakita K et al (1994) A novel modified nucleoside found at the first position of the anticodon of methionine tRNA from bovine liver mitochondria. Biochemistry 33:2234–2239

    Article  CAS  PubMed  Google Scholar 

  • Muramatsu T, Nishikawa K, Nemoto F et al (1988) Codon and amino acid specificities of a transfer RNA are both converted by a single post-transcriptional modification. Nature 294:187–188

    Google Scholar 

  • Näsvall SJ, Chen P, Björk GR (2007) The wobble hypothesis revisited: uridine-5-oxyacetic acid is critical for reading of G-ending codons. RNA 13:1–14

    Article  Google Scholar 

  • NCBI DB for Organelle genome. http://www.ncbi.nlm.gov/genomes/OrganelleResource,cgi?taxid=33208

  • Ohira T, Suzuki T, Miyauchi K et al (2013) Decoding mechanism of non-universal genetic codes in Loligo bleekeri mitochondria. J Biol Chem 288:7645–7652

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Osawa S (1995) Evolution of the genetic code. Oxford University Press, Tokyo

    Google Scholar 

  • Osawa S, Jukes TH (1989) Codon reassignment (codon capture) in evolution. J Mol Evol 28:271–278

    Article  CAS  PubMed  Google Scholar 

  • Osawa S, Jukes TH, Watanabe K et al (1992) Recent evidence for evolution of the genetic code. Microbiol Rev 56:229–264

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rogaiski M, Karcher D, Bock R (2008) Superwobbling facilitates translation with reduced tRNA sets. Nat Struct Mol Biol 15:192–198

    Article  Google Scholar 

  • Sakurai M, Ohtsuki T, Suzuki T et al (2005) Unusual usage of wobble modifications in mitochondrial tRNAs of the nematode Ascaris suum. FEBS Lett 579:2767–2772

    Article  CAS  PubMed  Google Scholar 

  • Schultz DW, Yarus M (1994) Transfer RNA mutation and the malleability of the genetic code. J Mol Biol 235:1377–1380

    Article  CAS  PubMed  Google Scholar 

  • Sengupta S, Yang X, Higgs PG (2007) The mechanisms of codon reassignments in mitochondrial genetic codes. J Mol Evol 64:662–688

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sibler AP, Dirheimer G, Martin RP (1986) Codon reading patterns in Saccharomyces cerevisiae mitochondria based on sequences of mitochondrial tRNAs. FEBS Lett 194:131–138

    Article  CAS  PubMed  Google Scholar 

  • Soleimanpour-Lichaei HR, Kühl I, Gaisne M et al (2007) mtRF1a is a human mitochondrial translation release factor decoding the major termination codons UAA and UAG. Mol Cell 27:745–757

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Soma A, Ikeuchi Y, Kanemasa S et al (2003) An RNA-modifying enzyme that governs both the codon and amino acid specificities of isoleucine tRNA. Mol Cell 12:689–698

    Article  CAS  PubMed  Google Scholar 

  • Stern L, Schulman LH (1978) The role of the minor base N4-acetylcytidine in the function of the Escherichia coli non-initiator methionine transfer RNA. J Biol Chem 253:6132–6139

    CAS  PubMed  Google Scholar 

  • Suzuki T, Terasaki M, Takemoto-Hori C et al (2001a) Structural compensation for the deficit of rRNA with proteins in the mammalian mitochondrial ribosome. J Biol Chem 276:21724–21736

    CAS  PubMed  Google Scholar 

  • Suzuki T, Terasaki M, Takemoto-Hori C et al (2001b) Proteomic analysis of the mammalian mitochondrial ribosome. J Biol Chem 276:33181–33195

    Article  CAS  PubMed  Google Scholar 

  • Suzuki T, Suzuki T, Wada T et al (2002) Taurine as a constituent of mitochondrial tRNAs: new insights into the function of taurine and human mitochondrial diseases. EMBO J 21:6581–6589

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Suzuki T, Nagao A, Suzuki T (2011a) Human mitochondrial tRNAs: biogenesis, function, structural aspects, and diseases. Annu Rev Genet 45:299–329

    Article  CAS  PubMed  Google Scholar 

  • Suzuki T, Miyauchi K, Suzuki T et al (2011b) Taurine-containing uridine modifications in tRNA anticodons are required to decipher non-universal genetic codes in ascidian mitochondria. J Biol Chem 286:35494–35498

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Takai K, Horie N, Yamaizumi Z et al (1994) Recognition of UUN codons by two leucine tRNA species from Escherichia coli. FEBS Lett 344:31–34

    Article  CAS  PubMed  Google Scholar 

  • Takemoto C, Spremulli LL, Benkowski LA et al (2009) Unconventional decoding of the AUA codon as methionine by mitochondrial tRNAMet with the anticodon f5CAU as revealed with a mitochondrial in vitro translation system. Nucleic Acids Res 37:1616–1627

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Telford MJ, Herniou EA, Russel RB et al (2000) Changes in mitochondrial genetic codes as phylogenetic characters: two examples from the flatworms. Proc Natl Acad Sci U S A 97:11359–11364

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Temperley R, Richter R, Denneriein S et al (2010) Hungry codons promote frameshifting in human mitochondrial ribosomes. Science 327:301

    Article  CAS  PubMed  Google Scholar 

  • Tomita K, Ueda T, Watanabe K (1998) 7-methylguanosine at the anticodon wobble position of squid mitochondrial tRNASerGCU: molecular basis for assignment of AGA/AGG codons as serine in invertebrate mitochondria. Biochim Biophys Acta 1399:78–82

    Article  CAS  PubMed  Google Scholar 

  • Tomita K, Ueda T, Ishiwa S, Crain PF, McCloskey JA, Watanabe K (1999a) Codon reading patterns in Drosophila melanogaster mitochondria based on their tRNA sequences: a unique wobble rule in animal mitochondria. Nucleic Acids Res 27:4291–4297

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tomita K, Ueda T, Watanabe K (1999b) The presence of pseudouridine in the anticodon alters the genetic code: a possible mechanism for assignment of the AAA lysine codon as asparagine in echinoderm mitochondria. Nucleic Acids Res 27:1683–1689

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Watanabe K (2010) Unique features of animal mitochondrial translation systems. The non-universal genetic code, unusual features of the translational apparatus and their relevance to human mitochondrial diseases. Proc Jpn Acad Ser B Phys Biol Sci 86:11–39

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Watanabe K, Yokobori S (2011) tRNA modification and genetic code variations in animal mitochondria. J Nucleic Acids 2011:Article ID 623095

    Article  Google Scholar 

  • Watanabe Y, Tsurui H, Ueda T et al (1994) Primary and higher order structures of nematode (Ascaris suum) mitochondrial tRNAs lacking either the T or D stem. J Biol Chem 269:22902–22906

    CAS  PubMed  Google Scholar 

  • Watanabe Y, Tsurui H, Ueda T et al (1997) Primary sequence of mitochondrial tRNAArg of a nematode Ascaris suum: occurrence of unmodified adenosine at the first position of the anticodon. Biochim Biophys Acta 1350:119–122

    Article  CAS  PubMed  Google Scholar 

  • Yamao F, Muto A, Kawauchi Y et al (1985) UGA is read as tryptophan in Mycoplasma capricolum. Proc Natl Acad Sci U S A 82:2306–2309

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yokobori S, Ueda T, Watanabe K (1993) Codons AGA and AGG are read as glycine in ascidian mitochondria. J Mol Evol 36:1–8

    Article  CAS  PubMed  Google Scholar 

  • Yokoyama S, Nishimura S (1995) Modified nucleosides and codon recognition. In: Söll D, RajBhandary UL (eds) tRNA: structure, biosynthesis and function. ASM, Washington, DC, pp 207–223

    Google Scholar 

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Acknowledgements

We thank Dr. Tsutomu Suzuki of the University of Tokyo for supplying us with analytical data of mitochondrial tRNAs and his wholehearted support of this study. We also thank Dr. Akira Muto, Hirosaki University, for Mycoplasma ribosome data, and Dr. Takeo Suzuki, University of Tokyo, for E. coli tRNA data.

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Correspondence to Kimitsuna Watanabe .

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Watanabe, K., Yokobori, Si. (2014). How the Early Genetic Code Was Established?: Inference from the Analysis of Extant Animal Mitochondrial Decoding Systems. In: Erdmann, V., Markiewicz, W., Barciszewski, J. (eds) Chemical Biology of Nucleic Acids. RNA Technologies. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-54452-1_2

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