Origins and Early Evolution of the tRNA Molecule

Tamura, Koji

doi:10.3390/life5041687

Cited by 57 publications

(50 citation statements)

References 91 publications

(118 reference statements)

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“…Transfer RNAs are typically 70–90 nucleotides in length with a cloverleaf-like secondary structure characterized by anticodon (AC), dihydrouridine (D) and thymidine–pseudouridine–cytidine (TΨC) stem-loops and an acceptor stem (ACC, orange circles) 127 . Although transcribed with the same nucleotide bases as mRNA (A, U, C, G), ribonucleosides of tRNAs undergo extensive post-transcriptional chemical modification (PTrM) at an average of 9–11% of bases per mature tRNA, representing the most highly modified RNA species within the cell 128 .…”

Section: Figurementioning

confidence: 99%

Translational fidelity and mistranslation in the cellular response to stress

2017

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Faithful translation of mRNA into the corresponding polypeptide is a complex multistep process, requiring accurate amino acid selection, transfer RNA (tRNA) charging and mRNA decoding on the ribosome. Key players in this process are aminoacyl-tRNA synthetases (aaRSs), which not only catalyse the attachment of cognate amino acids to their respective tRNAs, but also selectively hydrolyse incorrectly activated non-cognate amino acids and/or misaminoacylated tRNAs. This aaRS proofreading provides quality control checkpoints that exclude non-cognate amino acids during translation, and in so doing helps to prevent the formation of an aberrant proteome. However, despite the intrinsic need for high accuracy during translation, and the widespread evolutionary conservation of aaRS proofreading pathways, requirements for translation quality control vary depending on cellular physiology and changes in growth conditions, and translation errors are not always detrimental. Recent work has demonstrated that mistranslation can also be beneficial to cells, and some organisms have selected for a higher degree of mistranslation than others. The aims of this Review Article are to summarize the known mechanisms of protein translational fidelity and explore the diversity and impact of mistranslation events as a potentially beneficial response to environmental and cellular stress.

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Section: Figurementioning

confidence: 99%

Translational fidelity and mistranslation in the cellular response to stress

2017

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“…6E). The acceptor stem bases and the anticodon stem/loop bases in tRNA in tRNA 5´-half and 3´-half fit together with the doublehairpin folding; this suggests that the primordial double-hairpin RNA molecules could have evolved to the structure of modern tRNA by gene duplication, with subsequent mutations to form the familiar overleaf structure [56,61]. In other words, two pre-tRNA molecules somehow fused together to form a tRNA molecule.…”

Section: <Figure 6 About Here>mentioning

confidence: 99%

“…The half-sized pre-tRNA molecule with two loops (D-hairpin and T-hairpin) on one side, and anticodon and acceptor stem region of CCA end on the other side, is structurally and functionally independent and is more ancient than the other-half of the tRNA molecule [61]. This short, self-structured strand of pre-tRNA molecule possesses a template domain, which is chargeable through interaction with specific amino acids, is probably the predecessor of tRNA (Fig.…”

Section: <Figure 6 About Here>mentioning

confidence: 99%

The Origin of the Information System in the RNA/Protein World: A Simulation Model of the Evolution of Translation and the Genetic Code

Chatterjee¹,

Yadav²

2018

Preprint

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The Late Heavy Bombardment Period (4.1 to 3.8 billion years ago) of heightened impact cratering activity on young Earth is likely the driving force for the origin of life. During the Eoarchean, asteroids such as carbonaceous chondrites delivered the building blocks of life and water to early Earth. Asteroid collisions created innumerable hydrothermal crater lakes in the Eoarchean crust which inadvertently became the perfect cradle for prebiotic chemistry. These hydrothermal crater lakes were filled with cosmic water and the building blocks of life. forming a thick prebiotic soup. The unique combination of exogenous delivery of extraterrestrial building blocks of life, and the endogenous biosynthesis in hydrothermal impact crater lakes very likely gave rise to life. A new symbiotic model for the origin of life within the hydrothermal crater lakes is here proposed. In this scenario, life arose around four billion years ago through five hierarchical stages of increasing molecular complexity: cosmic, geologic, chemical, information, and biological. During the prebiotic synthesis, membranes first appeared in the hydrothermal crater lakes, followed by the simultaneous origin of RNA and protein molecules, creating the RNA/protein world. These proteins were noncoded protein enzymes that facilitated chemical reactions. RNA molecules formed in the hydrothermal crater basin by polymerization of the nucleotides on the montmorillonite mineral substrate. Similarly, the initial synthesis of abiotic protein enzymes was mediated by the condensation of amino acids on pyrite surfaces. The regular wet-dry cycles within the crater lakes assisted further concentration, condensation, and polymerization of the RNAs and proteins. Lipid membranes randomly encapsulated amino acids, RNA, and protein molecules from the prebiotic soup to initiate a molecular symbiosis inside the protocells, this led to the hierarchical emergence of several cell components. As the role of protein enzymes became essential for catalytic process in the RNA/protein world, Darwinian selection from noncoded to coded protein synthesis led to translation systems and the genetic code, heralding the information stage. In this stage, the biochemical pathways suggest the successive emergence of translation machineries such as tRNAs, aaRS, mRNAs, and of ribosomes for protein synthesis. The molecular attraction between tRNA and amino acid led to the emergence of translation machinery and the genetic code.  tRNA is an ancient molecule that created mRNA for the purpose of storing amino acid information like a digital strip. Each mRNA strand became the storage device for genetic information that encoded the amino acid sequences in triplet nucleotides. As information became available in the digital languages of the codon within mRNA, biosynthesis became less random and more organized and directional. The original translation machinery was simpler before the emergence of the ribosome than that of today. We review three main concepts on the origin and evolution of the genetic code: the stereochemical theory, the coevolution theory, and adaptive theory. We believe that these three theories are not mutually exclusive, but are compatible with our coevolution model of translations machines and the genetic code. We suggest biosynthetic pathways as the origin of the translation machine that provided the framework for the origin of the genetic code. During translation, the genetic code developed in three stages coincident with the refinement of the translation machinery: GNC code with four codons and four amino acids during interactions of pre-tRNA/pre-aaRS /pre-mRNA, SNS code consisting of 16 codons and 10 amino acids appeared during the tRNA/aaRS/mRNA interaction, and finally the universal genetic code evolved with the emergence of the tRNA/aaRS/mRNA/ribosome machine. The universal code consists of 64 codons and 20 amino acids, with a redundancy that minimizes errors in translation. To address the question of the origin of the biological information system in the RNA/protein world, we converted letter codons into numerical codons in the Universal Genetic Code Table. We developed a software called CATI (Codon-Amino Acid-Translator-Imitator) to translate randomly chosen numerical codons into corresponding amino acids and vice versa, gaining insight into how translation might have worked in the RNA/protein world. We simulated the likely biochemical pathways for the origin of translation and the genetic code using the Model-View-Controller (MVC) software framework, and the translation machinery step-by-step. We used AnyLogic software to simulate and visualize the evolution of the translation machines and the genetic code. We conclude that the emergence of the information age from the RNA/protein world was a watershed event in the origin of life about four billion years ago.

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“…The conclusion that the mRNA decoding in the early translation system was performed by RNA molecules, conceivably, evolutionary precursors of modern tRNAs (prototRNAs) [89], implies a stereochemical model of code origin and evolution, but one that differs from the traditional models of this type in an important way ( Figure 2). Under this model, the proto-RNA-amino acid interactions that defined the specificity of translation would not involve the anticodon (let alone codon) that therefore could be chosen arbitrarily and fixed through frozen accident.…”

Section: Primordial Expansion Of the Codementioning

confidence: 99%

Frozen Accident Pushing 50: Stereochemistry, Expansion and Chance in the Evolution of the Genetic Code

Koonin¹

2017

Preprint

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Nearly 50 years ago, Francis Crick propounded the frozen accident scenario for the evolution of the genetic code along with the hypothesis that the early translation system consisted primarily of RNA. Under the frozen accident perspective, the code is universal among modern life forms because any change in codon assignment would be highly deleterious. The frozen accident can be considered the default theory of code evolution because it does not imply any specific interactions between amino acids and the cognate codons or anticodons, or any particular properties of the code. The subsequent 49 years of code studies have elucidated notable features of the standard code, such as high robustness to errors, but failed to develop a compelling explanation for codon assignments. In particular, stereochemical affinity between amino acids and the cognate codons or anticodons does not seem to account for the origin and evolution of the code.Here I expand Crick's hypothesis on RNA-only translation system by presenting evidence that this early translation already attained high fidelity that allowed protein evolution. I outline an experimentally testable scenario for the evolution of the code that combines a distinct version of the stereochemical hypothesis, in which amino acids are recognized via unique sites in the tertiary structure of proto-tRNAs, rather than by anticodons, expansion of the code via proto-tRNA duplication and the frozen accident.

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Origins and Early Evolution of the tRNA Molecule

Cited by 57 publications

References 91 publications

Translational fidelity and mistranslation in the cellular response to stress

Translational fidelity and mistranslation in the cellular response to stress

The Origin of the Information System in the RNA/Protein World: A Simulation Model of the Evolution of Translation and the Genetic Code

Frozen Accident Pushing 50: Stereochemistry, Expansion and Chance in the Evolution of the Genetic Code

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