Skip to main content
Log in

Information theory unveils the evolution of tRNA identity elements in the three domains of life

  • Original Article
  • Published:
Theory in Biosciences Aims and scope Submit manuscript

Abstract

We determined the identity elements of each tRNA isoacceptor for the three domains of life: Eubacteria, Archaea, and Eukarya. Our analyses encompass the most updated and curated available databases using an information theory approach. We obtained a collection of identity clusters for each of the isoacceptors of the 20 canonical amino acids for the three major domains of life. The identity clusters for all isoacceptors are compared within and among the three domains to determine their pattern of differentiation and to shed light on the evolution of the identity elements.

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

Access this article

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Sujatha Thankeswaran Parvathy, Varatharajalu Udayasuriyan & Vijaipal Bhadana

References

  • Abe T, Inokuchi H, Yamada Y, Muto A, Iwasaki Y, Ikemura T (2014) TRNADB-CE: TRNA gene database well-timed in the era of big sequence data. Front Genet 5:114

    Article  Google Scholar 

  • Ardell DH (2010) Computational analysis of tRNA identity. FEBS Lett 584:325–333

    Article  CAS  Google Scholar 

  • Arnez JG, Moras D (1997) Structural and functional considerations of the aminoacylation reaction. Trends Biochem Sci 22:211–216

    Article  CAS  Google Scholar 

  • Branciamore S, Gogoshin G, Di Giulio M, Rodin A (2018) Intrinsic properties of tRNA molecules as deciphered via bayesian network and distribution divergence analysis. Life 8:5

    Article  Google Scholar 

  • Carter CW, Wills PR (2018) Hierarchical groove discrimination by Class I and II aminoacyl-tRNA synthetases reveals a palimpsest of the operational RNA code in the tRNA acceptor-stem bases. Nucleic Acids Res 46:9667–9683

    Article  CAS  Google Scholar 

  • Chong YE, Guo M, Yang X-L, Kuhle B, Naganuma M, Sekine S-I, Yokoyama S, Schimmel P (2018) Distinct ways of G: U recognition by conserved tRNA binding motifs. Proc Natl Acad Sci 115:7527–7532

    Article  CAS  Google Scholar 

  • De Duve C (1988) The second genetic code. Nature 333:117–118

    Article  Google Scholar 

  • de Farias ST, Antonino D, Rêgo TG, José MV (2018) Structural evolution of Glycyl-tRNA synthetases alpha subunit and its implication in the initial organization of the decoding system. Prog Biophys Mol Biol 30:1e8

    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 motifs. Nature 347:203–206

    Article  CAS  Google Scholar 

  • Fujishima K, Kanai A (2014) tRNA gene diversity in the three domains of life. Front Genet 5:142

    Article  Google Scholar 

  • Giegé R, Sissler M, Florentz C (1998) Universal rules and idiosyncratic features in tRNA identity. Nucleic Acids Res 26:5017–5035

    Article  Google Scholar 

  • Hendrickson TL (2001) Recognizing the D-loop of transfer RNAs. Proc Natl Acad Sci 98:13473–13475

    Article  CAS  Google Scholar 

  • Hou Y-M (2010) CCA addition to tRNA: implications for tRNA quality control. IUBMB Life 62:251–260

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hou Y-M, Schimmel P (1988) A simple structural feature is a major determinant of the identity of a transfer RNA. Nature 333:140–145

    Article  CAS  Google Scholar 

  • Jühling F, Mörl M, Hartmann RK, Sprinzl M, Stadler PF, Pütz J (2009) tRNAdb 2009: compilation of tRNA sequences and tRNA genes. Nucleic Acids Res 37:D159–D162

    Article  Google Scholar 

  • Kuncha SK, Mazeed M, Singh R, Kattula B, Routh SB, Sankaranarayanan R (2018) A chiral selectivity relaxed paralog of DTD for proofreading tRNA mischarging in Animalia. Nat Commun 9:511

    Article  Google Scholar 

  • Lorenz C, Lünse C, Mörl M (2017) tRNA modifications: impact on structure and thermal adaptation. Biomolecules 7:35

    Article  Google Scholar 

  • Mcclain WH, Foss K (1988) Changing the identity of a tRNA by introducing a G-U wobble pair near the 3′ acceptor end. Science (80-) 240:793–796

    Article  CAS  Google Scholar 

  • Meilă M (2003) Comparing clusterings by the variation of information. In: Proceedings of learning theory and kernel machines: 16th annual conference on learning theory and 7th kernel workshop, COLT/Kernel 2003, Washington, DC, USA, August 24–27, 2003. Springer, Berlin, pp 173–187

  • Miller SL (1953) A production of amino acids under possible primitive earth conditions. Science (80-) 117:528–529

    Article  CAS  Google Scholar 

  • Miller SL (1957) The mechanism of synthesis of amino acids by electric discharges. Biochim Biophys Acta 23:480–489

    Article  CAS  Google Scholar 

  • Miller SL, Orgel LE (1974) The origins of life on the earth. Prentice-Hall, Upper Saddle River

    Google Scholar 

  • Motorin Y, Grosjean H (2005) tRNA modification. In: Encyclopedia of life sciences. Wiley. https://doi.org/10.1038/npgs.els0003866

  • Mukai T, Reynolds N, Crnković A, Söll D (2017) Bioinformatic analysis reveals archaeal tRNATyr and tRNATrp identities in bacteria. Life 7:8

    Article  Google Scholar 

  • Raina M, Ibba M (2014) tRNAs as regulators of biological processes. Front Genet 5:171

    Article  Google Scholar 

  • Ribas de Pouplana L, Schimmel P (2001) Operational RNA code for amino acids in relation to genetic code in evolution. J Biol Chem 276:6881–6884

    Article  CAS  Google Scholar 

  • Smith D, Yarus M (1989) Transfer RNA structure and coding specificity. I. Evidence that a D-arm mutation reduces tRNA dissociation from the ribosome. J Mol Biol 206:489–501

    Article  CAS  Google Scholar 

  • Sun L, Gomes AC, He W, Zhou H, Wang X, Pan DW, Schimmel P, Pan T, Yang XL (2016) Evolutionary gain of alanine mischarging to noncognate tRNAs with a G4:U69 base pair. J Am Chem Soc 138:12948–12955

    Article  CAS  Google Scholar 

  • Tamaki S, Tomita M, Suzuki H, Kanai A (2018) Systematic analysis of the binding surfaces between tRNAs and their respective aminoacyl tRNA synthetase based on structural and evolutionary data. Front Genet 8:227

    Article  Google Scholar 

  • Tamura K (2015) Origins and early evolution of the tRNA molecule. Life 5:1687–1699

    Article  CAS  Google Scholar 

  • Varani G, McClain WH (2000) The G·U wobble base pair. EMBO Rep 1:18–23

    Article  CAS  Google Scholar 

  • Wang C, Sobral B, Williams K (2007) Loss of a universal tRNA feature. J Bacteriol 189:1954–1962

    Article  CAS  Google Scholar 

  • Woese CR, Olsen GJ, Ibba M, Soll D (2000) Aminoacyl-tRNA synthetases, the genetic code, and the evolutionary process. Microbiol Mol Biol Rev 64:202–236

    Article  CAS  Google Scholar 

  • Zamudio GS, José MV (2018) Identity elements of tRNA as derived from information analysis. Orig Life Evol Biosph 48:73–81

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank Juan R. Bobadilla for technical computer support. We thank the anonymous reviewer for their helpful criticisms and suggestions. We thank Adhemar Liquitaya-Montiel for helpful discussions at the begining of this work.

Funding

GSZ is a doctoral student from Programa de Doctorado en Ciencias Biomédicas, Universidad Nacional Autónoma de México (UNAM), and received a doctoral fellowship from CONACYT (Number: 737920). MP is a doctoral student from Programa de Doctorado en Ciencias Biomédicas (PDCB), Universidad Nacional Autónoma de México (UNAM), and she receives the fellowship 694877 from CONACYT. MVJ was funded by Dirección General de Asuntos del Personal Académico (DGAPA), Universidad Nacional Autónoma de México, UNAM (PAPIIT-IN201019).

Author information

Authors and Affiliations

Authors

Contributions

GSZ and MVJ conceived and designed the experiments; GSZ performed the experiments and analyzed the identity clusters; MPP analyzed tRNA sites for posttranscriptional modifications; GSZ, MPP, and MVJ analyzed the data; GSZ and MVJ wrote the paper.

Corresponding authors

Correspondence to Gabriel S. Zamudio or Marco V. José.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Appendix

Appendix

figure a

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zamudio, G.S., Palacios-Pérez, M. & José, M.V. Information theory unveils the evolution of tRNA identity elements in the three domains of life. Theory Biosci. 139, 77–85 (2020). https://doi.org/10.1007/s12064-019-00301-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12064-019-00301-6

Keywords

Navigation