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Cited by 98RNA and protein synthesis mechanismsOrigins and Evolution of LifeEvolution and Genetic Dynamics

On origin of genetic code and tRNA before translation

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Rodin, Andrei S, Szathmáry, Eörs, Rodin, Sergei N·2011·Biology Direct
DOI 10.1186/1745-6150-6-14PMC PMC3050877
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Abstract

BACKGROUND: Synthesis of proteins is based on the genetic code - a nearly universal assignment of codons to amino acids (aas). A major challenge to the understanding of the origins of this assignment is the archetypal "key-lock vs. frozen accident" dilemma. Here we re-examine this dilemma in light of 1) the fundamental veto on "foresight evolution", 2) modular structures of tRNAs and aminoacyl-tRNA synthetases, and 3) the updated library of aa-binding sites in RNA aptamers successfully selected in vitro for eight amino acids. RESULTS: The aa-binding sites of arginine, isoleucine and tyrosine contain both their cognate triplets, anticodons and codons. We have noticed that these cases might be associated with palindrome-dinucleotides. For example, one-base shift to the left brings arginine codons CGN, with CG at 1-2 positions, to the respective anticodons NCG, with CG at 2-3 positions. Formally, the concomitant presence of codons and anticodons is also expected in the reverse situation, with codons containing palindrome-dinucleotides at their 2-3 positions, and anticodons exhibiting them at 1-2 positions. A closer analysis reveals that, surprisingly, RNA binding sites for Arg, Ile and Tyr "prefer" (exactly as in the actual genetic code) the anticodon(2-3)/codon(1-2) tetramers to their anticodon(1-2)/codon(2-3) counterparts, despite the seemingly perfect symmetry of the latter. However, since in vitro selection of aa-specific RNA aptamers apparently had nothing to do with translation, this striking preference provides a new strong support to the notion of the genetic code emerging before translation, in response to catalytic (and possibly other) needs of ancient RNA life. Consistently with the pre-translation origin of the code, we propose here a new model of tRNA origin by the gradual, Fibonacci process-like, elongation of a tRNA molecule from a primordial coding triplet and 5'DCCA3' quadruplet (D is a base-determinator) to the eventual 76 base-long cloverleaf-shaped molecule. CONCLUSION: Taken together, our findings necessarily imply that primordial tRNAs, tRNA aminoacylating ribozymes, and (later) the translation machinery in general have been co-evolving to ''fit'' the (likely already defined) genetic code, rather than the opposite way around. Coding triplets in this primal pre-translational code were likely similar to the anticodons, with second and third nucleotides being more important than the less specific first one. Later, when the code was expanding in co-evolution with the translation apparatus, the importance of 2-3 nucleotides of coding triplets "transferred" to the 1-2 nucleotides of their complements, thus distinguishing anticodons from codons. This evolutionary primacy of anticodons in genetic coding makes the hypothesis of primal stereo-chemical affinity between amino acids and cognate triplets, the hypothesis of coding coenzyme handles for amino acids, the hypothesis of tRNA-like genomic 3' tags suggesting that tRNAs originated in replication, and the hypothesis of ancient ribozymes-mediated operational code of tRNA aminoacylation not mutually contradicting but rather co-existing in harmony.

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  • The redundancy of the universal genetic code optimized translation errors and mutations.

    “The redundancy of the universal genetic code optimized translation errors and mutations [108].”

    From The Origin of Prebiotic Information System in the Peptide/RNA World: A Simulation Model of the Evolution of Translation and the Genetic Code (2019) · cites this paper as [108]

    The Conclusions (page not provided) explicitly question the view that the genetic code was shaped by minimizing translation errors and instead emphasize that translation machinery evolved to fit an earlier code. The paper does not present redundancy as having optimized translation errors and mutations. (LLM, conf=0.87)

    Checked by a reasoning model — may be wrong.

    Experimental — accuracy not yet measured

  • GNC code evolved into the second generation of the genetic code, called an SNS type, where N denotes any four RNA bases and S denotes guanine and cytosine.

    “GNC code evolved into the second generation of the genetic code, called an SNS type, where N arbitrarily denotes any four RNA bases and S denotes guanine (G) and cytosine (S) [80,108].”

    From The Origin of Prebiotic Information System in the Peptide/RNA World: A Simulation Model of the Evolution of Translation and the Genetic Code (2019) · cites this paper as [108]

    The Background defines N as any of the four nucleotides, and the Results and discussion describe an early genetic code expanding alongside translation. The paper does not identify a GNC code evolving into a second-generation SNS code or define S as G and C (searched: GNC, SNS, and the proposed transition). (LLM, conf=0.77)

    Experimental — accuracy not yet measured

  • Phase 2 amino acids entered the code by means of biosynthesis from the Phase 1 amino acids with the emergence of tRNA molecules, aminoacyl transferase enzyme, and ribosomes.

    “Phase 2, the amino acids entered the code by means of biosynthesis from the Phase 1 amino acids with the emergence of tRNA molecules, aminoacyl transferase enzyme, and ribosomes [68,82,105,108].”

    From The Origin of Prebiotic Information System in the Peptide/RNA World: A Simulation Model of the Evolution of Translation and the Genetic Code (2019) · cites this paper as [108]

    The Conclusions (page unavailable) suggest that the order in which amino acids entered the code could have followed their biosynthetic pathways. The paper does not identify Phase 1 and Phase 2 amino acids or say that a second phase entered with the emergence of tRNAs, aminoacylating enzymes, and ribosomes; it instead describes an early, pre-translational code. (LLM, conf=0.85)

    Experimental — accuracy not yet measured

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Authors
Rodin, A. S., Szathmáry, E., & Rodin, S. N.
Affiliations
  • Eötvös Loránd University (HU)
  • Collegium Budapest (HU)
Corresponding author
Rodin, Sergei N
ORCID
Szathmáry, Eörs
Venue
Biology Direct
Publisher
Springer Science and Business Media LLC
Published
2011
Volume
6
Issue
1
Pages
14
ISSN
1745-6150 (ISSN-L)
DOI
10.1186/1745-6150-6-14
PMC
PMC3050877
OpenAlex
W1993599690
Cited by
98
References
97
Citations by year
2025: 6 · 2024: 1 · 2023: 6 · 2022: 8 · 2021: 5 · 2020: 7 · 2019: 7 · 2018: 7 · 2017: 9 · 2016: 6 · 2015: 5 · 2014: 8 · 2013: 8 · 2012: 10
FWCI
3.90
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • Biology Direct (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Repository of the Academy's Library (Library of the Hungarian Academy of Sciences) (acceptedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • ELTE Digital Institutional Repository (EDIT) (Eötvös Loránd University) (submittedVersion, other-oa)
Funders
  • Hungarian Scientific Research Fund (NK73047)
  • Nemzeti Kutatási és Technológiai Hivatal (KCKHA005, NAP 2005/KCKHA005)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA and protein synthesis mechanisms
  • Physical Sciences › Physics and Astronomy › Astronomy and Astrophysics › Origins and Evolution of Life
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
Keywords
origin of the genetic code, aminoacyl-tRNA synthetase, RNA aptamers, amino acid binding sites, tRNA evolution, RNA world, codon-anticodon pairing
MeSH terms
Amino Acids, Anticodon, Base Sequence, Binding Sites, Codon, Genetic Code, Models, Genetic, Molecular Sequence Data, Nucleic Acid Conformation, RNA, Transfer, Protein Biosynthesis, Dinucleotide Repeats, Dimerization, Aptamers, Nucleotide

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