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Structure, function and evolution of seryl-tRNA synthetases: Implications for the evolution of aminoacyl-tRNA synthetases and the genetic code

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Abstract

Two aspects of the evolution of aminoacyl-tRNA synthetases are discussed. Firstly, using recent crystal structure information on seryl-tRNA synthetase and its substrate complexes, the coevolution of the mode of recognition between seryl-tRNA synthetase and tRNAser in different organisms is reviewed. Secondly, using sequence alignments and phylogenetic trees, the early evolution of class 2 Amnoacyl-tRNA synthetases is traced. Arguments are presented to suggest that synthetases are not the oldest of protein enzymes, but survived as RNA enzymes during the early period of the evolution of protein catalysts. In this view, the relatedness of the current synthetases, as evidenced by the division into two classes with their associated subclasses, reflects the replacement of RNA synthetases by protein synthetases. This process would have been triggered by the acquisition of tRNA 3′ end charging activity by early proteins capable of activating small molecules (e.g., amino acids) with ATP. If these arguments are correct, the genetic code was essentially frozen before the protein synthetases that we know today came into existence.

Correspondence to: S. Cusack

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References

  • Achsel T, Gross HJ (1993) Identity determinants of human tRNAser: sequence elements necessary for serylation and maturation of a tRNA with a long extra arm. EMBO J 12:3333–3338

    Google Scholar 

  • Artymiuk PJ, Rice DW, Poirrette AR, Willett P (1994) A tale of two synthetases. Nat Struc Biol 1:758–760

    Google Scholar 

  • Asahara H, Himeno M, Shimizu M (1991) A recognition model of tRNAser by seryl-tRNA synthetase in E. coli. Chem Lett 3:363–366

    Google Scholar 

  • Asahara H, Himeno H, Tamura K, Hasegawa T, Watenabe K, Shimizu M (1993) Recognition nucleotides of E. coli tRNAleu and its elements facilitating discrimination from tRNAser and tRNAtyr. J Mol Biol 231:219–229

    Google Scholar 

  • Asahara H, Himeno H, Tamura K, Nameki N, Hasegawa T, Shimizu M (1994) Escherichia coli seryl-tRNA synthetase recognizes tRNAser by its characteristic tertiary structure. J Mol Biol 236:738–748

    Google Scholar 

  • Baron C, Böck A (1991) The length of the aminoacyl-acceptor stem of the selenocysteine-specific tRNAsec of Escherichia coli is the determinant for binding to elongation factors SELB or Tu. J Biol Chem 266:20375–20379

    Google Scholar 

  • Baron C, Westhof E, Bock A, Giege R (1993) Solution structure of selenocysteine-inserting tRNAsec from Escherichia coli. Comparison with canonical tRNAser. J Mol Biol 231:274–292

    Google Scholar 

  • Belrhali H, Yaremchuk A, Tukalo M, Larsen K, Berthet-Colominas C, Leberman R, Beijer B, Sproat B, Als-Nielsen J, Grübel, Cusack S (1994) Crystal structures at 2.5 Å resolution of seryl-tRNA synthetase complexed with two analogs of seryl adenylate. Science 263:1432–1436

    Google Scholar 

  • Belrhali H, Yaremchuk AD, Tukalo M, Berther-Colominas C, Rasmussen B, Bösecke P, Diat O, Cusack S (1995) The structural basis for seryl-adenylate and Ap4A synthesis by seryl-tRNA synthetase. Structure (in press)

  • 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 

  • Benner SA, Cohen MA, Gonnet GH, Berkowitz DB, Johnsson KP (1993) Reading the palimpsest: contemporary biochemical data and the RNA world, In: Gesteland RF, Atkins JF (eds) The RNA World. Cold Spring Harbour Laboratory Press, Cold Spring Harbour, NY, pp 27–70

    Google Scholar 

  • Biou V, Yaremchuk A, Tukalo M, Cusack S (1994) The 2.9 A crystal structure of T. thermophilus seryl-tRNA synthetase complexed with tRNAser. Science 263:1404–1410

    Google Scholar 

  • Böck A, Forchhammer K, Heider J, Leinfelder W, Sawers G, Veprek B, Zinoni F (1991) Selenocysteine: the 21st amino acid. Mol Microbiol 5:515–520

    Google Scholar 

  • Borel F, Vincent C, Leberman R, Härtlein M (1994) Seryl-tRNA synthetase from Escherichia coli implication of its N-terminal domain in aminoacylation activity and specificity. Nucleic Acids Res 22: 2963–2969

    Google Scholar 

  • Breitschopf K, Gross HJ (1994) The exchange of the discriminator base A73 for G is alone sufficient to convert human tRNAleu into a serine acceptor in vitro. EMBO J 13:3166–3169

    Google Scholar 

  • Cavarelli J, Rees B, Ruff M, Thierry JC, Moras D (1993) Yeast tRNAasp recognition by its cognate class II aminoacyl-tRNA synthetase. Nature 362:181–184

    Google Scholar 

  • Caverelli J, Eriani G, Rees B, Ruff M, Boeglin M, Mitschler A, Martin F, Gangloff J, Thierry JC, Moras D (1994) The active site of yeast aspartyl-tRNA synthetase: structural and functional aspects of the aminoacylation reaction. EMBO J 13:327–337

    Google Scholar 

  • Cusack S, Berthet-Colominas C, Härtlein M, Nassar N, Leberman R (1990) A second class of synthetase structure revealed by X-ray analysis of Escherichia coli seryl-tRNA synthetase at 2.5 Å. Nature 347:249–255

    Google Scholar 

  • Cusack S, Härtlein M, Leberman R (1991) Sequence, structure and evolutionary relationships between class 2 aminoacyl-tRNA synthetases. Nucleic Acids Res 19:3489–3498

    Google Scholar 

  • Cusack S (1993) Sequence, structure and evolutionary relationships between class 2 aminoacyl-tRNA synthetases: an update. Biochimic 75:1077–1081

    Google Scholar 

  • Delarue M, Poterszman A, Nikonov S, Garber M, Moras D, Thierry JC (1994) Crystal structure of a prokaryotic aspartyl-tRNA synthetase. EMBO J 13:3219–3229

    Google Scholar 

  • Delarue M, Moras D (1993) The aminoacyl-tRNA synthetase family: modules at work. Bioessays 15:675–687

    Google Scholar 

  • Dock-Bregeon AC, Garcia A, Giege R, Moras D (1990) The contacts of yeast tRNAser with seryl-tRNA synthetase studied by footprinting experiments. Eur J Biochem 188:283–290

    Google Scholar 

  • Dock-Bregeon AC, Westhof E, Giege R, Moras D (1989) Solution structure of a tRNA with a large variable arm: yeast tRNAser. J Mol Biol 206:707–722

    Google Scholar 

  • Eriani G, Delarue M, Poch O, Gangloff J, Moras D (1990) Partition of tRNA synthetases into two classes based on mutually exclusive sets of sequence motif. Nature 347:203–206

    Google Scholar 

  • Feng DF, Doolittle RF (1987) Progressive sequence alignment as a prerequisite to correct phylogenetic trees. J Mol Evol 25:351–360

    Google Scholar 

  • Fujinaga M, Berthet-Colominas C, Yaremchuk AD, Tukalo MA, Cusack S (1993) Refined crystal structure of the seryl-tRNA synthetase from Thermus thennophilus at 2.5 A resolution. J Mol Biol 234:222–323

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Härtlein M, Modern D, Leberman R (1987) Cloning and caracterization of the gene for Escherichia coli seryl-tRNA synthetase. Nucleic Acids Res 15:1005–1017

    Google Scholar 

  • Hartman H (1978) Speculations on the evolution of the genetic code. II. Orig Life 9:133–136

    Google Scholar 

  • Higgins DG, Sharp PM (1988) CLASTAL: a package for performing multiple sequence alignment on a microcomputer. Gene 73:237–244

    Article  CAS  PubMed  Google Scholar 

  • Himeno H, Hasegawa T, Ueda T, Watanabe K, Shimuzu M (1990) Conversion of aminoacylation specificity from tRNATyr to tRNASer in vitro. Nucleic Acids Res 18:6815–6819

    Google Scholar 

  • Hopfield JJ (1978) Origin of the genetic code: a testable hypothesis based on tRNA structure, sequence, and kinetic proofreading. Proc Natl Acad Sci USA 75:4334–4338

    Google Scholar 

  • Illangasekare M, Sanchez G, Nickles T, Yarus M (1995) AminoacylRNA synthesis catalyzed by an RNA. Science 267:643–647

    Google Scholar 

  • Joyce GF, Orgel LE (1993) Prospects for understanding the origin of the RNA world. In: Gesteland RF, Atkins JF (eds) The RNA world. Cold Spring Harbor Laboratory Press, Cold Spring Harbour, NY, pp 1–25

    Google Scholar 

  • Kawaguchi Y, Honda H, Taniguchi-Morimura J, Iwasaki S (1989) The codon CUG is read as serine in an asporogenic yeast Candida cylindracea. Nature 341:164–169

    Google Scholar 

  • Khan AS, Wilcox AS, Polymeropoulos, Hopfins JA, Stevens TJ, Robinson M, Orpana AK, Sikela JM (1992) Single pass sequencing and physical and genetic mapping of human brain cDNAc. Nature Genet 2:180–185

    Google Scholar 

  • Kumazawa Y, Himeno H, Miura K, Watanabe K (1991) Unilateral aminoacylation specificity between bovine mitochondria and eubacteria. J Biochem 109:421–427

    Google Scholar 

  • Lehman H, Jukes TH (1988) Genetic code development by stop codon takeover. J Theor Biol 135:203–214

    Google Scholar 

  • Lunel C, Buttin G, de Saint Vincent BR (1992) A seryl-tRNA synthetase gene is coamplified with the adenylate deaminase 2 gene in coformycin resistant Chinese hamster fibroblasts. Nucleic Acids Res 20:2597

    Google Scholar 

  • Mayerfeld I, Yarns M (1994) An RNA pocket for an aliphatic hydroprobe. Nature Struct Biol 1:287–292

    Google Scholar 

  • Mirande M, Lazard M, Kerjan P, Bee G, Agou F, Quevilo S, Waller JP (1993) The Amnoacyl-tRNA synthetase family: an evolutionary view of their structural organisation. In: Nierhaus KH, Franceschi F, Subramanian AR, Erdmann VA, Wittmann-Liebold B (eds) The translation apparatus: structure, function, regulation, evolution. pp 657–668

  • Miseta A, Woodley CL, Greenberg JR, Slobin LI (1991) Mammalian seryl-tRNA synthetase associates with mRNA in vivo and has homology to elongation factor 1 alpha. J Biol Chem 266:19158–19161

    Google Scholar 

  • Mosyak L, Reshetnikova L, Safro M (1993) Phenylalanyl-tRNA synthetase from Thermus thermophilus has four antiparallel folds of which only two are catalytically functional. Biochimie 75:1091–1098

    Google Scholar 

  • Murzin AG (1993) Oligonucleotide/oligosaccharide binding-fold: common structural and functional solution for non-homologous sequences. EMBO J 12:861–867

    Google Scholar 

  • Noller HF, Hoffarth V, Zimniak L (1992) Unusual resistance of peptidyl transferase to protein extraction procedures. Science 256: 1416–1419

    Google Scholar 

  • Normanly J, Ogden RC, Horvath SJ, Abelson J (1986) Changing the identity of a transfer RNA. Nature 321:213–219

    Google Scholar 

  • Normanly J, Ollick T, Abelson J (1992) Eight base changes are sufficient to convert a leucine-inserting tRNA into a serine-inserting tRNA. Proc Natl Acad Sci USA 89:5680–5684

    Google Scholar 

  • Onesti S, Miller AD, Brick P (1995) The crystal structure of the lysyl-tRNA synthetase (LysU) from Escherichia coli. Structure 3:163–176

    Google Scholar 

  • Orgel LE (1989) The origin of polynucleotide-directed protein synthesis. J Mol Evol 29:465–474

    Google Scholar 

  • Piccirilli JA, McConnell TS, Zaug AJ, Noller HF, Cech TR (1992) Aminoacyl esterase activity of the Tetrahymena ribozyme. Science 256:1420–1424

    Google Scholar 

  • Price S, Cusack S, Borel F, Berthet-Colominas C, Leberman R (1993) Crystallization of the seryl-tRNA synthetase: tRNAser complex of Escherichia coli. FEBS Lett 324:167–170

    Google Scholar 

  • Rich A (1965) Evolving genes and proteins. ed. Bryson V, Vogel HG Academic, New York, pp 453–468

    Google Scholar 

  • Rogg H, Staehelin M (1971) Nucleotide sequences of rat liver serine-tRNA1. Products of digestion with pancreatic ribonuclease. Eur J Biochem 21:235–242

    Google Scholar 

  • Ruff M, Krishnaswamy S, Boeglin M, Poterszman A, Mitschler A, Podjamy A, Rees B, Thierry JC, Moras D (1991) Class II aminoacyl-tRNA synthetases: crystal structure of yeast aspartyl-tRNA synthetase complexed with tRNAasp. Science 252:1682–1689

    Google Scholar 

  • Sassanfar M, Szostak JW (1993) An RNA motif that binds ATP. Nature 364:550–552

    Google Scholar 

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

    Google Scholar 

  • Saks ME, Sampson JR, (submitted) Patterns and modes of tRNA sequence evolution. J Mol Evol

  • Sampson JR, Saks ME (1993) Contributions of discrete tRNAser domains to amino-acylation by E. coli seryl-tRNA synthetase: a kinetic analysis using model RNA substrates. Nucleic Acids Res 21:4467–4475

    Google Scholar 

  • Schimmel P, Giegé 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 

  • Schulman LH (1991) recognition of tRNAs by Amnoacyl-tRNA synthetases. Prog Nucleic Acid Res Mol Biol 41:23–47

    Google Scholar 

  • Sidorik LL, Gudzera OI, Dragovoz VA, Tukalo MA, Beresten SF (1991) Immuno-chemical non-cross-reactivity between eukaryotic and prokaryotic seryl-tRNA synthetases. FEBS Lett 292:76–78

    Google Scholar 

  • Steinberg S, Gautheret G, Cedergren R (1994) Fitting the structurally diverse animal mitochondrial tRNAs to common three-dimensional constraints. J Mol Biol 236:982–989

    Google Scholar 

  • Ueda T, Yotsumoto Y, Ikeda K, Watanabe K (1992) The T-loop region of animal mitochondrial tRNAser(AGY) is a main recognition site for homologous seryl-tRNA synthetase. Nucleic Acids Res 20: 2217–2222

    Google Scholar 

  • Wetzel R (1978) Aminoacyl-tRNA synthetase families and their significance to the origin of the genetic code. Orig Life 9:39–50

    Google Scholar 

  • Weygand-Durasevic I, Johnson-Burke D, Söll D (1987) Cloning and characterization of the gene coding for cytoplasmic seryl-tRNA synthetase from Saccharomyces cerevisiae. Nucleic Acids Res 15: 1887–1904

    Google Scholar 

  • Weygand-Durasevic I, Ban N, Jahn D, Söll D (1993) Yeast seryl-tRNA synthetase expressed in Escherichia coli recognizes bacterial serine-specific tRNA in vivo. Eur J Biochem 214:869–877

    Google Scholar 

  • Weygand-Durasevic I, Nalaskowska M, Söll D (1994) Coexpression of eukaryotic tRNASer and yeast seryl-tRNA synthetase leads to functional amber suppression in Escherichia coli. J Bacteriol 176:232–239

    Google Scholar 

  • Wilson KP, Shewchuk LM, Brennan RG, Otsuka AJ, Matthews BW (1992) E. coli biotin holoenzyme synthetase/bio repressor crystal structure delineates the biotin- and DNA-binding domains. Proc Natl Acad Sci USA 89:9257–9261

    Google Scholar 

  • Wu XQ, Gross HJ (1993) The long extra arms of human tRNA ((Ser)Sec) and tRNA(Ser) function as major identity elements for serylation in an orientation-dependent, but not sequence specific manner. Nucleic Acids Res 21:5589–5594

    Google Scholar 

  • Yarus M (1989) Specificity of arginine binding by the Tetrahymena intron. Biochemistry 28:980–988

    Google Scholar 

  • Yokogawa T, Suzuki T, Ueda T, Mori M, Ohama T, Kuchino Y, Yoshinari S, Motoki I, Nishikawa K, Osawa S (1992) Serine tRNA complementary to the nonuniversal serine codon CUG in Candida cylindracea: evolutionary implications. Proc Natl Acad Sci USA 89:7408–7411

    Google Scholar 

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  1. European Molecular Biology Laboratory, Grenoble Outstation, c/o ILL, 156X, 38042, Grenoble Cedex, France

    Michael Härtlein & Stephen Cusack

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  1. Michael Härtlein
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  2. Stephen Cusack
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Based on a presentation made at a workshop-“Aminoacyl-tRNA Synthetases and the Evolution of the Genetic Code”-held at Berkeley, CA, July 17–20, 1994

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Härtlein, M., Cusack, S. Structure, function and evolution of seryl-tRNA synthetases: Implications for the evolution of aminoacyl-tRNA synthetases and the genetic code. J Mol Evol 40, 519–530 (1995). https://doi.org/10.1007/BF00166620

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