Skip to main content
SpringerLink
Log in

The Origin of Genetic Code and Translation in the Framework of Current Concepts on the Origin of Life

  • REVIEW
  • Published:
Biochemistry (Moscow) Aims and scope Submit manuscript

Abstract

The origin of genetic code and translation system is probably the central and most difficult problem in the investigations on the origin of life and one of the most complex problems in the evolutionary biology in general. There are multiple hypotheses on the emergence and development of existing genetic systems that propose the mechanisms for the origin and early evolution of genetic code, as well as for the emergence of replication and translation. Here, we discuss the most well-known of these hypotheses, although none of them provides a description of the early evolution of genetic systems without gaps and assumptions. The RNA world hypothesis is a currently prevailing scientific idea on the early evolution of biological and pre-biological structures, the main advantage of which is the assumption that RNAs as the first living systems were self-sufficient, i.e., capable of functioning as both catalysts and templates. However, this hypothesis has also significant limitations. In particular, no ribozymes with processive polymerase activity have been yet discovered or synthesized. Taking into account the mutual need of proteins and nucleic acids in each other in the current world, many authors propose the early evolution scenarios based on the co-evolution of these two classes of organic molecules. They postulate that the emergence of translation was necessary for the replication of nucleic acids, in contrast to the RNA world hypothesis, according to which the emergence of translation was preceded by the era of self-replicating RNAs. Although such scenarios are less parsimonious from the evolutionary point of view, since they require simultaneous emergence and evolution of two classes of organic molecules, as well as the emergence of synchronized replication and translation, their major advantage is that they explain the development of processive and much more accurate protein-dependent replication.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 5.
Fig. 6.
Fig. 7.

Similar content being viewed by others

Abbreviations

aaRS:

aminoacyl-tRNA synthetase

DRT:

direct RNA template

C-DRT:

DRT template complementary strand

GADV model:

GADV-protein world hypothesis on the origin of life

GARD model:

graded autocatalysis replication domain model

PR:

polar requirement, a measure of solubility of amino acids in aqueous solutions of pyridine

self-rARS:

self-aminoacylating ribozyme

SART:

self-aminoacylating ribozyme template

References

  1. Dodd, M. S., Papineau, D., Grenne, T., Slack, J. F., Rittner, M., et al. (2017) Evidence for early life in Earth’s oldest hydrothermal vent precipitates, Nature, 543, 60-64, https://doi.org/10.1038/nature21377.

    Article  CAS  PubMed  Google Scholar 

  2. Benner, S. A. (2010) Defining life, Astrobiology, 10, 1021-1030, https://doi.org/10.1089/ast.2010.0524.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Wolf, Y. I., and Koonin, E. V. (2007) On the origin of the translation system and the genetic code in the RNA world by means of natural selection, exaptation, and subfunctionalization, Biol. Direct, 2, 14, https://doi.org/10.1186/1745-6150-2-14.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Nikolaeva, D. D., Gelfand, M. S., and Garushyants, S. K. (2021) Simplification of ribosomes in bacteria with tiny genomes, Mol. Biol. Evol., 38, 58-66, https://doi.org/10.1093/molbev/msaa184.

    Article  CAS  PubMed  Google Scholar 

  5. Eigen, M. (1971) Selforganization of matter and the evolution of biological macromolecules, Naturwissenschaften, 58, 465-523, https://doi.org/10.1007/bf00623322.

    Article  CAS  PubMed  Google Scholar 

  6. Penny, D. (2005) An interpretive review of the origin of life research, Biol. Philos., 20, 633-671, https://doi.org/10.1007/s10539-004-7342-6.

    Article  Google Scholar 

  7. Eigen, M., and Schuster, P. (1977) The hypercycle. A principle of natural self-organization. Part A: Emergence of the hypercycle, Naturwissenschaften, 64, 541-565, https://doi.org/10.1007/BF00450633.

    Article  CAS  PubMed  Google Scholar 

  8. Szathmáry, E. (1986) Some remarks on hypercycles and the stochastic corrector model, Endocyt. Cell Res., 3, 337-339.

    Google Scholar 

  9. Szathmáry, E., and Demeter, L. (1987) Group selection of early replicators and the origin of life, J. Theor. Biol., 128, 463-486.

    Article  Google Scholar 

  10. Zintzaras, E., Santos, M., and Szathmáry, E. (2002) “Living” under the challenge of information decay: the stochastic corrector model vs. hypercycles, J. Theor. Biol., 217, 167-181.

    Article  CAS  Google Scholar 

  11. Gago, S., Elena, S. F., Flores, R., and Sanjuan, R. (2009) Extremely high mutation rate of a hammerhead viroid, Science, 323, 1308, https://doi.org/10.1126/science.1169202.

    Article  CAS  PubMed  Google Scholar 

  12. Koonin, E. V., and Novozhilov, A. S. (2017) Origin and evolution of the universal genetic code, Annu. Rev. Genet., 51, 45-62, https://doi.org/10.1146/annurev-genet-120116-024713.

    Article  CAS  PubMed  Google Scholar 

  13. Rich, A. (1962) Horizons in Biochemistry (Kasha, M., and Pullman, B., eds.) Academic Press, New York.

  14. Crick, F. H. (1968) The origin of the genetic code, J. Mol. Biol., 38, 367-379, https://doi.org/10.1016/0022-2836(68)90392-6.

    Article  CAS  PubMed  Google Scholar 

  15. Orgel, L. E. (1968) Evolution of the genetic apparatus, J. Mol. Biol., 38, 381-393, https://doi.org/10.1016/0022-2836(68)90393-8.

    Article  CAS  PubMed  Google Scholar 

  16. Gilbert, W. (1986) Origin of life: The RNA world, Nature, 319, 618.

    Article  Google Scholar 

  17. Le Vay, K., and Mutschler, H. (2019) The difficult case of an RNA-only origin of life, Emerg. Top. Life Sci., 3, 469-475, https://doi.org/10.1042/etls20190024.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Kruger, K., Grabowski, P. J., Zaug, A. J., Sands, J., Gottschling, D. E., et al. (1982) Self-splicing RNA: Autoexcision and autocyclization of the ribosomal RNA intervening sequence of Tetrahymena, Cell, 31, 147-157, https://doi.org/10.1016/0092-8674(82)90414-7.

    Article  CAS  PubMed  Google Scholar 

  19. Robertson, H. D., Altman, S., and Smith, J. D. (1972) Purification and properties of a specific Escherichia coli ribonuclease which cleaves a tyrosine transfer ribonucleic acid presursor, J. Biol. Chem., 247, 5243-5251.

    Article  CAS  Google Scholar 

  20. Klemm, B. P., Wu, N., Chen, Y., Liu, X., Kaitany, K. J., et al. (2016) The diversity of ribonuclease P: Protein and RNA catalysts with analogous biological functions, Biomolecules, 6, 27, https://doi.org/10.3390/biom6020027.

    Article  CAS  PubMed Central  Google Scholar 

  21. Walter, N. G., and Engelke, D. R. (2002) Ribozymes: catalytic RNAs that cut things, make things, and do odd and useful jobs, Biologist, 49, 199-203.

    PubMed  Google Scholar 

  22. Johnston, W. K., Unrau, P. J., Lawrence, M. S., Glasner, M. E., and Bartel, D. P. (2001) RNA-catalyzed RNA polymerization: accurate and general RNA-templated primer extension, Science, 292, 1319-1325, https://doi.org/10.1126/science.1060786.

    Article  CAS  PubMed  Google Scholar 

  23. Wochner, A., Attwater, J., Coulson, A., and Holliger, P. (2011) Ribozyme-catalyzed transcription of an active ribozyme, Science, 332, 209-212, https://doi.org/10.1126/science.1200752.

    Article  CAS  PubMed  Google Scholar 

  24. Bowman, J. C., Hud, N. V., and Williams, L. D. (2015) The ribosome challenge to the RNA world, J. Mol. Evol., 80, 143-161, https://doi.org/10.1007/s00239-015-9669-9.

    Article  CAS  PubMed  Google Scholar 

  25. Ouzounis, C., and Kyrpides, N. (1996) The emergence of major cellular processes in evolution, FEBS Lett., 390, 119-123, https://doi.org/10.1016/0014-5793(96)00631-x.

    Article  CAS  PubMed  Google Scholar 

  26. Ganoza, M. C., Kiel, M. C., and Aoki, H. (2002) Evolutionary conservation of reactions in translation, Microbiol. Mol. Biol. Rev., 66, 460-485, https://doi.org/10.1128/mmbr.66.3.460-485.2002.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Melnikov, S., Ben-Shem, A., Garreau de Loubresse, N., Jenner, L., Yusupova, G., et al. (2012) One core, two shells: bacterial and eukaryotic ribosomes, Nat. Struct. Mol. Biol., 19, 560-567, https://doi.org/10.1038/nsmb.2313.

    Article  CAS  PubMed  Google Scholar 

  28. Hsiao, C., Lenz, T. K., Peters, J. K., Fang, P. Y., Schneider, D. M., et al. (2013) Molecular paleontology: a biochemical model of the ancestral ribosome, Nucleic Acids Res., 41, 3373-3385, https://doi.org/10.1093/nar/gkt023.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Bernhardt, H. S. (2012) The RNA world hypothesis: the worst theory of the early evolution of life (except for all the others)(a), Biol. Direct, 7, 23, https://doi.org/10.1186/1745-6150-7-23.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Bregestovski, P. D. (2015) “RNA World”, a highly improbable scenario of the origin and early evolution of life on earth, J. Evol. Biochem. Physiol., 51, 72-84, https://doi.org/10.1134/S0022093015010111.

    Article  CAS  Google Scholar 

  31. Wills, P. R., and Carter, C. W., Jr. (2018) Insuperable problems of the genetic code initially emerging in an RNA world, Biosystems, 164, 155-166, https://doi.org/10.1016/j.biosystems.2017.09.006.

    Article  CAS  PubMed  Google Scholar 

  32. Orgel, L. E. (2004) Prebiotic chemistry and the origin of the RNA world, Crit. Rev. Biochem. Mol. Biol., 39, 99-123, https://doi.org/10.1080/10409230490460765.

    Article  CAS  PubMed  Google Scholar 

  33. Kim, H. J., Ricardo, A., Illangkoon, H. I., Kim, M. J., Carrigan, M. A., et al. (2011) Synthesis of carbohydrates in mineral-guided prebiotic cycles, J. Am. Chem. Soc., 133, 9457-9468, https://doi.org/10.1021/ja201769f.

    Article  CAS  PubMed  Google Scholar 

  34. Spirin, A. S. (2007) When, where, and in what environment could the RNA world appear and evolve? Paleontol. J., 41, 481-488.

    Article  Google Scholar 

  35. Tupper, A. S., Shi, K., and Higgs, P. G. (2017) The role of templating in the emergence of RNA from the prebiotic chemical mixture, Life, 7, 41, https://doi.org/10.3390/life7040041.

    Article  CAS  PubMed Central  Google Scholar 

  36. Szostak, J. W. (2012) The eightfold path to non-enzymatic RNA replication, J. Syst. Chem., 3, 2, https://doi.org/10.1186/1759-2208-3-2.

    Article  CAS  Google Scholar 

  37. Joyce, G. F., and Orgel, L. E. (1986) Non-enzymic template-directed synthesis on RNA random copolymers. Poly(C, G) templates, J. Mol. Biol., 188, 433-441, https://doi.org/10.1016/0022-2836(86)90166-x.

    Article  CAS  PubMed  Google Scholar 

  38. Joyce, G. F., and Szostak, J. W. (2018) Protocells and RNA self-replication, Cold Spring Harb. Perspect. Biol., 10, a034801, https://doi.org/10.1101/cshperspect.a034801.

    Article  PubMed  PubMed Central  Google Scholar 

  39. James, K. D., and Ellington, A. D. (1999) The fidelity of template-directed oligonucleotide ligation and the inevitability of polymerase function, Orig. Life Evol. Biosph., 29, 375-390, https://doi.org/10.1023/a:1006544611320.

    Article  CAS  PubMed  Google Scholar 

  40. Prywes, N., Blain, J. C., Del Frate, F., and Szostak, J. W. (2016) Nonenzymatic copying of RNA templates containing all four letters is catalyzed by activated oligonucleotides, eLife, 5, https://doi.org/10.7554/eLife.17756.

    Article  PubMed  PubMed Central  Google Scholar 

  41. Szostak, J. W. (2011) An optimal degree of physical and chemical heterogeneity for the origin of life? Philos. Trans. R. Soc. Lond. B Biol. Sci., 366, 2894-2901, https://doi.org/10.1098/rstb.2011.0140.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Bartel, D. P., and Szostak, J. W. (1993) Isolation of new ribozymes from a large pool of random sequences [see comment], Science, 261, 1411-1418, https://doi.org/10.1126/science.7690155.

    Article  CAS  PubMed  Google Scholar 

  43. Horning, D. P., and Joyce, G. F. (2016) Amplification of RNA by an RNA polymerase ribozyme, Proc. Natl. Acad. Sci. USA, 113, 9786-9791, https://doi.org/10.1073/pnas.1610103113.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Samanta, B., and Joyce, G. F. (2017) A reverse transcriptase ribozyme, eLife, 6, https://doi.org/10.7554/eLife.31153.

    Article  PubMed  PubMed Central  Google Scholar 

  45. Koonin, E. V. (2017) Frozen accident pushing 50: Stereochemistry, expansion, and chance in the evolution of the genetic code, Life (Basel), 7, 22, https://doi.org/10.3390/life7020022.

    Article  CAS  Google Scholar 

  46. Nirenberg, M. W., and Matthaei, J. H. (1961) The dependence of cell-free protein synthesis in E. coli upon naturally occurring or synthetic polyribonucleotides, Proc. Nat. Acad. Sci. USA, 47, 1588-1602.

    Article  CAS  Google Scholar 

  47. Gardner, R. S., Wahba, A. J., Basilio, C., Miller, R. S., et al. (1962) Synthetic polynucleotides and the amino acid code, VII, Proc. Natl. Acad. Sci. USA, 48, 2087.

    Article  CAS  Google Scholar 

  48. Wahba, A. J., Gardner, R. S., Basilio, C., Miller, R. S., Speyer, J. F., et al. (1963) Synthetic polynucleotides and the amino acid code, VIII, Proc. Natl. Acad. Sci. USA, 49, 116.

    Article  CAS  Google Scholar 

  49. Söll, D., Ohtsuka, E., Jones, D., Lohrmann, R., Hayatsu, H., et al. (1965) Studies on polynucleotides, XLIX. Stimulation of the binding of aminoacyl-sRNA’s to ribosomes by ribotrinucleotides and a survey of codon assignments for 20 amino acids, Proc. Natl. Acad. Sci. USA, 54, 1378.

    Article  Google Scholar 

  50. Woese, C. R., Dugre, D. H., Dugre, S. A., Kondo, M., and Saxinger, W. C. (1966) On the fundamental nature and evolution of the genetic code, Cold Spring Harb. Symp. Quant. Biol., 31, 723-736, https://doi.org/10.1101/sqb.1966.031.01.093.

    Article  CAS  PubMed  Google Scholar 

  51. Woese, C. R. (1968) The fundamental nature of the genetic code: prebiotic interactions between polynucleotides and polyamino acids or their derivatives, Proc. Natl. Acad. Sci. USA, 59, 110-117, https://doi.org/10.1073/pnas.59.1.110.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Yarus, M., Widmann, J. J., and Knight, R. (2009) RNA-amino acid binding: a stereochemical era for the genetic code, J. Mol. Evol., 69, 406-429, https://doi.org/10.1007/s00239-009-9270-1.

    Article  CAS  PubMed  Google Scholar 

  53. Yarus, M. (1998) Amino acids as RNA ligands: A direct-RNA-template theory for the code’s origin, J. Mol. Evol., 47, 109-117, https://doi.org/10.1007/pl00006357.

    Article  CAS  PubMed  Google Scholar 

  54. Yarus, M. (2000) RNA–ligand chemistry: a testable source for the genetic code, RNA, 6, 475-484, https://doi.org/10.1017/s1355838200002569.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Yarus, M., Caporaso, J. G., and Knight, R. (2005) Origins of the genetic code: the escaped triplet theory, Annu. Rev. Biochem., 74, 179-198, https://doi.org/10.1146/annurev.biochem.74.082803.133119.

    Article  CAS  PubMed  Google Scholar 

  56. Koonin, E. V., and Novozhilov, A. S. (2009) Origin and evolution of the genetic code: the universal enigma, IUBMB Life, 61, 99-111, https://doi.org/10.1002/iub.146.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Hajnic, M., Osorio, J. I., and Zagrovic, B. (2014) Computational analysis of amino acids and their sidechain analogs in crowded solutions of RNA nucleobases with implications for the mRNA–protein complementarity hypothesis, Nucleic Acids Res., 42, 12984-12994.

    Article  CAS  Google Scholar 

  58. Hlevnjak, M., Polyansky, A. A., and Zagrovic, B. (2012) Sequence signatures of direct complementarity between mRNAs and cognate proteins on multiple levels, Nucleic Acids Res., 40, 8874-8882, https://doi.org/10.1093/nar/gks679.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Polyansky, A. A., Hlevnjak, M., and Zagrovic, B. (2013) Analogue encoding of physicochemical properties of proteins in their cognate messenger RNAs, Nat. Commun., 4, 2784, https://doi.org/10.1038/ncomms3784.

    Article  CAS  PubMed  Google Scholar 

  60. Polyansky, A. A., Hlevnjak, M., and Zagrovic, B. (2013) Proteome-wide analysis reveals clues of complementary interactions between mRNAs and their cognate proteins as the physicochemical foundation of the genetic code, RNA Biol., 10, 1248-1254, https://doi.org/10.4161/rna.25977.

    Article  PubMed  PubMed Central  Google Scholar 

  61. Gamow, G. (1954) Possible relation between deoxyribonucleic acid and protein structures, Nature, 173, 318.

    Article  CAS  Google Scholar 

  62. Melcher, G. (1974) Stereospecificity of the genetic code, J. Mol. Evol., 3, 121-140, https://doi.org/10.1007/bf01796558.

    Article  CAS  PubMed  Google Scholar 

  63. Hendry, L., Bransome, E., Hutson, M., and Campbell, L. (1981) First approximation of a stereochemical rationale for the genetic code based on the topography and physicochemical properties of “cavities” constructed from models of DNA, Proc. Nat. Acad. Sci. USA, 78, 7440-7444, https://doi.org/10.1073/pnas.78.12.7440.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Balasubramanian, R., Seetharamulu, P., and Raghunathan, G. (1980) A conformational rationale for the origin of the mechanism of nucleic acid-directed protein synthesis of “living” organisms, Orig. Life, 10, 15-30, https://doi.org/10.1007/bf00928940.

    Article  CAS  PubMed  Google Scholar 

  65. Shimizu, M. (1982) Molecular basis for the genetic code, J. Mol. Evol., 18, 297-303, https://doi.org/10.1007/bf01733895.

    Article  CAS  PubMed  Google Scholar 

  66. Massey, S. E. (2006) A sequential “2-1-3” model of genetic code evolution that explains codon constraints, J. Mol. Evol., 62, 809-810, https://doi.org/10.1007/s00239-005-0222-0.

    Article  CAS  PubMed  Google Scholar 

  67. Wong, J. T. (1975) A co-evolution theory of the genetic code, Proc. Natl. Acad. Sci. USA, 72, 1909-1912, https://doi.org/10.1073/pnas.72.5.1909.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Wong, J. T. (2005) Coevolution theory of the genetic code at age thirty, Bioessays, 27, 416-425, https://doi.org/10.1002/bies.20208.

    Article  CAS  PubMed  Google Scholar 

  69. Amirnovin, R. (1997) An analysis of the metabolic theory of the origin of the genetic code, J. Mol. Evol., 44, 473-476, https://doi.org/10.1007/pl00006170.

    Article  CAS  PubMed  Google Scholar 

  70. Ronneberg, T. A., Landweber, L. F., and Freeland, S. J. (2000) Testing a biosynthetic theory of the genetic code: fact or artifact? Proc. Natl. Acad. Sci. USA, 97, 13690-13695, https://doi.org/10.1073/pnas.250403097.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Woese, C. R. (1965) On the evolution of the genetic code, Proc. Natl. Acad. Sci. USA, 54, 1546-1552, https://doi.org/10.1073/pnas.54.6.1546.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Haig, D., and Hurst, L. D. (1991) A quantitative measure of error minimization in the genetic code, J. Mol. Evol., 33, 412-417, https://doi.org/10.1007/BF02103132.

    Article  CAS  PubMed  Google Scholar 

  73. Novozhilov, A. S., Wolf, Y. I., and Koonin, E. V. (2007) Evolution of the genetic code: partial optimization of a random code for robustness to translation error in a rugged fitness landscape, Biol. Direct, 2, 24, https://doi.org/10.1186/1745-6150-2-24.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Mukai, T., Lajoie, M. J., Englert, M., and Söll, D. (2017) Rewriting the genetic code, Annu. Rev. Microbiol., 71, 557-577.

    Article  CAS  Google Scholar 

  75. Spirin, A. (2001) Protein biosynthesis, the world of RNA, and the origin of life, Vestnik Rossiiskoi Akademii Nauk, 71, 320-328.

    CAS  Google Scholar 

  76. Spirin, A. (2013) The emergence of molecular machines as a prerequisite of the ancient RNA world evolution, Paleontol. J., 47, 1016-1029.

    Article  Google Scholar 

  77. Schimmel, P. (2011) The RNP bridge between two worlds, Nat. Rev. Mol. Cell. Biol., 12, 135, https://doi.org/10.1038/nrm3061.

    Article  CAS  PubMed  Google Scholar 

  78. Nissen, P., Hansen, J., Ban, N., Moore, P. B., and Steitz, T. A. (2000) The structural basis of ribosome activity in peptide bond synthesis, Science, 289, 920-930, https://doi.org/10.1126/science.289.5481.920.

    Article  CAS  PubMed  Google Scholar 

  79. Dunn, I. S. (2011) RNA templating of molecular assembly and covalent modification patterning in early molecular evolution and modern biosystems, J. Theor. Biol., 284, 32-41, https://doi.org/10.1016/j.jtbi.2011.06.009.

    Article  CAS  PubMed  Google Scholar 

  80. Ma, W. (2010) The scenario on the origin of translation in the RNA world: in principle of replication parsimony, Biol. Direct, 5, 65, https://doi.org/10.1186/1745-6150-5-65.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Rodin, S., Rodin, A., and Ohno, S. (1996) The presence of codon-anticodon pairs in the acceptor stem of tRNAs, Proc. Natl. Acad. Sci. USA, 93, 4537-4542, https://doi.org/10.1073/pnas.93.10.4537.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Tamura, K. (2015) Origins and early evolution of the tRNA molecule, Life (Basel), 5, 1687-1699, https://doi.org/10.3390/life5041687.

    Article  CAS  Google Scholar 

  83. Di Giulio, M. (1992) On the origin of the transfer RNA molecule, J. Theor. Biol., 159, 199-214, https://doi.org/10.1016/s0022-5193(05)80702-7.

    Article  CAS  PubMed  Google Scholar 

  84. Widmann, J., Di Giulio, M., Yarus, M., and Knight, R. (2005) tRNA creation by hairpin duplication, J. Mol. Evol., 61, 524-530, https://doi.org/10.1007/s00239-004-0315-1.

    Article  CAS  PubMed  Google Scholar 

  85. Caetano-Anolles, D., and Caetano-Anolles, G. (2016) Piecemeal buildup of the genetic code, ribosomes, and genomes from primordial tRNA building blocks, Life (Basel), 6, 43, https://doi.org/10.3390/life6040043.

    Article  CAS  Google Scholar 

  86. De Farias, S. T., Rêgo, T. G., and José, M. V. (2021) Origin of the 16S ribosomal molecule from ancestor tRNAs, J. Mol. Evol., 89, 249-256, https://doi.org/10.1007/s00239-021-10002-8.

    Article  CAS  PubMed  Google Scholar 

  87. Petrov, A. S., Gulen, B., Norris, A. M., Kovacs, N. A., Bernier, C. R., et al. (2015) History of the ribosome and the origin of translation, Proc. Natl. Acad. Sci. USA, 112, 15396-15401, https://doi.org/10.1073/pnas.1509761112.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Demongeot, J., and Seligmann, H. (2020) Comparisons between small ribosomal RNA and theoretical minimal RNA ring secondary structures confirm phylogenetic and structural accretion histories, Sci. Rep., 10, 1-14.

    Article  Google Scholar 

  89. Amunts, A., Brown, A., Toots, J., Scheres, S. H., and Ramakrishnan, V. (2015) The structure of the human mitochondrial ribosome, Science, 348, 95-98.

    Article  CAS  Google Scholar 

  90. Seligmann, H., and Raoult, D. (2018) Stem-loop RNA hairpins in giant viruses: invading rRNA-like repeats and a template free RNA, Front. Microbiol., 9, 101.

    Article  Google Scholar 

  91. De Farias, S. T., Rego, T. G., and Jose, M. V. (2016) tRNA core hypothesis for the transition from the RNA world to the ribonucleoprotein world, Life (Basel), 6, 15, https://doi.org/10.3390/life6020015.

    Article  CAS  Google Scholar 

  92. Noller, H. F. (2012) Evolution of protein synthesis from an RNA world, Cold Spring Harb. Perspect. Biol., 4, a003681, https://doi.org/10.1101/cshperspect.a003681.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Wong, J. T. (2014) Emergence of life: From functional RNA selection to natural selection and beyond, Front. Biosci. (Landmark Ed), 19, 1117-1150, https://doi.org/10.2741/4271.

    Article  CAS  Google Scholar 

  94. Wong, J. T., Ng, S. K., Mat, W. K., Hu, T., and Xue, H. (2016) Coevolution theory of the genetic code at age forty: Pathway to translation and synthetic life, Life (Basel), 6, https://doi.org/10.3390/life6010012.

    Article  CAS  Google Scholar 

  95. Illangasekare, M., Sanchez, G., Nickles, T., and Yarus, M. (1995) Aminoacyl-RNA synthesis catalyzed by an RNA, Science, 267, 643-647, https://doi.org/10.1126/science.7530860.

    Article  CAS  PubMed  Google Scholar 

  96. Lee, N., Bessho, Y., Wei, K., Szostak, J. W., and Suga, H. (2000) Ribozyme-catalyzed tRNA aminoacylation, Nat. Struct. Biol., 7, 28-33, https://doi.org/10.1038/71225.

    Article  CAS  PubMed  Google Scholar 

  97. Suga, H., Hayashi, G., and Terasaka, N. (2011) The RNA origin of transfer RNA aminoacylation and beyond, Philos. Trans. R. Soc. B, 366, 2959-2964, https://doi.org/10.1098/rstb.2011.0137.

    Article  CAS  Google Scholar 

  98. Turk, R. M., Chumachenko, N. V., and Yarus, M. (2010) Multiple translational products from a five-nucleotide ribozyme, Proc. Natl. Acad. Sci. USA, 107, 4585-4589, https://doi.org/10.1073/pnas.0912895107.

    Article  PubMed  PubMed Central  Google Scholar 

  99. Szathmary, E. (1993) Coding coenzyme handles: a hypothesis for the origin of the genetic code, Proc. Natl. Acad. Sci. USA, 90, 9916-9920, https://doi.org/10.1073/pnas.90.21.9916.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Szathmary, E. (1999) The origin of the genetic code: Amino acids as cofactors in an RNA world, Trends Genet., 15, 223-229, https://doi.org/10.1016/s0168-9525(99)01730-8.

    Article  CAS  PubMed  Google Scholar 

  101. Kazakov, S., and Altman, S. (1992) A trinucleotide can promote metal ion-dependent specific cleavage of RNA, Proc. Natl. Acad. Sci. USA, 89, 7939-7943, https://doi.org/10.1073/pnas.89.17.7939.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Rodin, S. N., and Ohno, S. (1997) Four primordial modes of tRNA-synthetase recognition, determined by the (G,C) operational code, Proc. Natl. Acad. Sci. USA, 94, 5183-5188, https://doi.org/10.1073/pnas.94.10.5183.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Di Giulio, M. (2008) An extension of the coevolution theory of the origin of the genetic code, Biol. Direct, 3, 37, https://doi.org/10.1186/1745-6150-3-37.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Saad, N. Y. (2018) A ribonucleopeptide world at the origin of life, J. Syst. Evol., 56, 1-13, https://doi.org/10.1111/jse.12287.

    Article  Google Scholar 

  105. Altstein, A. D., and Efimov, A. V. (1988) Physico-chemical basis of the genetic code origin: stereochemical analysis of interactions of amino acids and nucleotides based on the progene hypothesis, Mol. Biol. (Mosk), 22, 1411-1429.

    Google Scholar 

  106. Fox, G. E. (2010) Origin and evolution of the ribosome, Cold Spring Harb. Perspect. Biol., 2, a003483, https://doi.org/10.1101/cshperspect.a003483.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Altstein, A. D. (2015) The progene hypothesis: the nucleoprotein world and how life began, Biol. Direct, 10, 67, https://doi.org/10.1186/s13062-015-0096-z.

    Article  PubMed  PubMed Central  Google Scholar 

  108. Lambowitz, A. M., and Zimmerly, S. (2011) Group II introns: Mobile ribozymes that invade DNA, Cold Spring Harb. Perspect. Biol., 3, a003616, https://doi.org/10.1101/cshperspect.a003616.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Kunin, V. (2000) A system of two polymerases – a model for the origin of life, Orig. Life. Evol. Biosph., 30, 459-466, https://doi.org/10.1023/a:1006672126867.

    Article  CAS  PubMed  Google Scholar 

  110. Altshtein, A. D., and Kaverin, N. N. (1980) On the origin of viral genetic systems, Zhurn. Vses. Khim. O-va im. D.I. Mendeleeva, 25, 383-390.

    CAS  Google Scholar 

  111. Altshtein, A. D. (1987) The origin of genetic system: progene hypothesis, Molek. Biol., 21, 309-321.

    CAS  Google Scholar 

  112. Li, L., Francklyn, C., and Carter, C. W., Jr. (2013) Aminoacylating urzymes challenge the RNA world hypothesis, J. Biol. Chem., 288, 26856-26863, https://doi.org/10.1074/jbc.M113.496125.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Rodin, A. S., Rodin, S. N., and Carter, C. W., Jr. (2009) On primordial sense-antisense coding, J. Mol. Evol., 69, 555-567, https://doi.org/10.1007/s00239-009-9288-4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Carter, C. W., Jr., and Kraut, J. (1974) A proposed model for interaction of polypeptides with RNA, Proc. Natl. Acad. Sci. USA, 71, 283-287, https://doi.org/10.1073/pnas.71.2.283.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Carter, C. W. (2015) What RNA world? Why a peptide/RNA partnership merits renewed experimental attention, Life (Basel), 5, 294-320, https://doi.org/10.3390/life5010294.

    Article  CAS  Google Scholar 

  116. Koonin, E. V. (2011) The Logic of Chance: The Nature and Origin of Biological Evolution, FT Press.

  117. Ikehara, K. (2002) Origins of gene, genetic code, protein and life: comprehensive view of life systems from a GNC-SNS primitive genetic code hypothesis, J. Biosci., 27, 165-186, https://doi.org/10.1007/BF02703773.

    Article  CAS  PubMed  Google Scholar 

  118. Ikehara, K. (2005) Possible steps to the emergence of life: the [GADV]-protein world hypothesis, Chem. Record, 5, 107-118, https://doi.org/10.1002/tcr.20037.

    Article  CAS  Google Scholar 

  119. Ikehara, K., Omori, Y., Arai, R., and Hirose, A. (2002) A novel theory on the origin of the genetic code: a GNC-SNS hypothesis, J. Mol. Evol., 54, 530-538, https://doi.org/10.1007/s00239-001-0053-6.

    Article  CAS  PubMed  Google Scholar 

  120. Trifonov, E. N. (2004) The triplet code from first principles, J. Biomol. Struct. Dyn., 22, 1-11, https://doi.org/10.1080/07391102.2004.10506975.

    Article  CAS  PubMed  Google Scholar 

  121. Ikehara, K. (2014) [GADV]-protein world hypothesis on the origin of life, Orig. Life Evol., 44, 299-302, https://doi.org/10.1007/s11084-014-9383-4.

    Article  CAS  Google Scholar 

  122. Segre, D., Ben-Eli, D., Deamer, D. W., and Lancet, D. (2001) The lipid world, Orig. Life Evol., 31, 119-145, https://doi.org/10.1023/a:1006746807104.

    Article  CAS  Google Scholar 

  123. Mallik, S., and Kundu, S. (2012) The lipid–RNA world, arXiv preprint arXiv:1211.0413.

  124. Lancet, D., Zidovetzki, R., and Markovitch, O. (2018) Systems protobiology: origin of life in lipid catalytic networks, J. R. Soc. Interface, 15, 20180159, https://doi.org/10.1098/rsif.2018.0159.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Krebs, J. E., Goldstein, E. S., and Kilpatrick, S. T. (2017) Lewin’s genes XII, Jones & Bartlett Learning.

  126. Miller, S. L., Schopf, J. W., and Lazcano, A. (1997) Oparin’s “Origin of Life”: sixty years later, J. Mol. Evol., 44, 351-353.

    Article  CAS  Google Scholar 

Download references

Funding

This study has been supported by the RUDN University Strategic Academic Leadership Program.

Author information

Authors and Affiliations

  1. Shemyakin–Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences, 117997, Moscow, Russia

    Liya G. Kondratyeva

  2. Vavilov Institute of General Genetics, 119991, Moscow, Russia

    Marina S. Dyachkova

  3. Peoples’ Friendship University of Russia (RUDN University), 117198, Moscow, Russia

    Alexey V. Galchenko

Authors
  1. Liya G. Kondratyeva
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marina S. Dyachkova
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Alexey V. Galchenko
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Alexey V. Galchenko.

Ethics declarations

The authors declare no conflicts of interest in financial or any other sphere. This article does not contain any studies with human participants or animals performed by any of the authors.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kondratyeva, L.G., Dyachkova, M.S. & Galchenko, A.V. The Origin of Genetic Code and Translation in the Framework of Current Concepts on the Origin of Life. Biochemistry Moscow 87, 150–169 (2022). https://doi.org/10.1134/S0006297922020079

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0006297922020079

Keywords

Search

Navigation