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The Origin and Evolution of tRNA Inferred from Phylogenetic Analysis of Structure

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Abstract

The evolutionary history of the two structural and functional domains of tRNA is controversial but harbors the secrets of early translation and the genetic code. To explore the origin and evolution of tRNA, we reconstructed phylogenetic trees directly from molecular structure. Forty-two structural characters describing the geometry of 571 tRNAs and three statistical parameters describing thermodynamic and mechanical features of molecules quantitatively were used to derive phylogenetic trees of molecules and molecular substructures. Trees of molecules failed to group tRNA according to amino acid specificity and did not reveal the tripartite nature of life, probably due to loss of phylogenetic signal or because tRNA diversification predated organismal diversification. Trees of substructures derived from both structural and statistical characters support the origin of tRNA in the acceptor arm and the hypothesis that the top half domain composed of acceptor and pseudouridine (TΨC) arms is more ancient than the bottom half domain composed of dihydrouridine (DHU) and anticodon arms. This constitutes the cornerstone of the genomic tag hypothesis that postulates tRNAs were ancient telomeres in the RNA world. The trees of substructures suggest a model for the evolution of the major functional and structural components of tRNA. In this model, short RNA hairpins with stems homologous to the acceptor arm of present day tRNAs were extended with regions homologous to TΨC and anticodon arms. The DHU arm was then incorporated into the resulting three-stemmed structure to form a proto-cloverleaf structure. The variable region was the last structural addition to the molecular repertoire of evolving tRNA substructures.

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Acknowledgments

We thank Hee Shin Kim, Ajith Harish, Minglei Wang, and Jay Mittenthal for helpful discussions, Joe Felsenstein for comments on phylogenetic reconstruction, Paul Schimmel for suggestions, Sergei Rodin for many critical comments an suggestions that improved the manuscript, and Vegeir Knudsen for writing stoat, a program that codes statistical characters. Both authors designed and performed research, analyzed data, and wrote the paper. This work was supported by National Science Foundation Grant MCB-0343126 (to G.C.A.) and the Critical Research Initiative of the University of Illinois. Any opinions, findings, and conclusions and recommendations expressed in this material are those of the authors and do not necessarily reflect the views of the funding agencies.

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Correspondence to Gustavo Caetano-Anollés.

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Sun, FJ., Caetano-Anollés, G. The Origin and Evolution of tRNA Inferred from Phylogenetic Analysis of Structure. J Mol Evol 66, 21–35 (2008). https://doi.org/10.1007/s00239-007-9050-8

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  • DOI: https://doi.org/10.1007/s00239-007-9050-8

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