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Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1979 Sep;76(9):4507–4510. doi: 10.1073/pnas.76.9.4507

On the evolution of accuracy and cost of proofreading tRNA aminoacylation.

M A Savageau, R R Freter
PMCID: PMC411606  PMID: 388443

Abstract

Aminoacylation of tRNA occurs with a high degree of accuracy in many cases because misacylated molecules are effectively proofread on the aminoacyl-tRNA synthetase by preferential hydrolysis. This hydrolysis releases an ATP equivalent of energy. An explicit relationship between cost of proofreading and the resulting degree of accuracy is presented. Experimental data from Escherichia coli for isoleucyl-tRNA synthetase proofreading valyl-tRNAIle are examined by means of this relationship, and a conjecture concerning the natural selection of accuracy and proofreading costs is put forth and tested. We have found the energy cost of accurate proofreading to be high. The minimum error, derived in previous theoretical studies, is never actually reached. Instead, higher values, determined by the balance between energy wasted in the cell as a consequence of error and the energy cost of proofreading, appear to be selected. The total cost of proofreading all types of tRNA aminoacylations is estimated to be approximately 2% of the energy required to synthesize a bacterial cell.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Baldwin A. N., Berg P. Transfer ribonucleic acid-induced hydrolysis of valyladenylate bound to isoleucyl ribonucleic acid synthetase. J Biol Chem. 1966 Feb 25;241(4):839–845. [PubMed] [Google Scholar]
  2. Beckman D., Cooper S. Temperature-sensitive nonsense mutations in essential genes of Escherichia coli. J Bacteriol. 1973 Dec;116(3):1336–1342. doi: 10.1128/jb.116.3.1336-1342.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Davies J., Jones D. S., Khorana H. G. A further study of misreading of codons induced by streptomycin and neomycin using ribopolynucleotides containing two nucleotides in alternating sequence as templates. J Mol Biol. 1966 Jun;18(1):48–57. doi: 10.1016/s0022-2836(66)80075-x. [DOI] [PubMed] [Google Scholar]
  4. Edelmann P., Gallant J. On the translational error theory of aging. Proc Natl Acad Sci U S A. 1977 Aug;74(8):3396–3398. doi: 10.1073/pnas.74.8.3396. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Hopfield J. J. Kinetic proofreading: a new mechanism for reducing errors in biosynthetic processes requiring high specificity. Proc Natl Acad Sci U S A. 1974 Oct;71(10):4135–4139. doi: 10.1073/pnas.71.10.4135. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Hopfield J. J., Yamane T., Yue V., Coutts S. M. Direct experimental evidence for kinetic proofreading in amino acylation of tRNAIle. Proc Natl Acad Sci U S A. 1976 Apr;73(4):1164–1168. doi: 10.1073/pnas.73.4.1164. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. LOFTFIELD R. B. THE FREQUENCY OF ERRORS IN PROTEIN BIOSYNTHESIS. Biochem J. 1963 Oct;89:82–92. doi: 10.1042/bj0890082. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Loftfield R. B., Eigner E. A. The specificity of enzymic reactions. Aminoacyl-soluble RNA ligases. Biochim Biophys Acta. 1966 Dec 28;130(2):426–448. doi: 10.1016/0304-4165(66)90239-x. [DOI] [PubMed] [Google Scholar]
  9. Loftfield R. B., Vanderjagt D. The frequency of errors in protein biosynthesis. Biochem J. 1972 Aug;128(5):1353–1356. doi: 10.1042/bj1281353. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Mulvey R. S., Fersht A. R. Editing mechanisms in aminoacylation of tRNA: ATP consumption and the binding of aminoacyl-tRNA by elongation factor Tu. Biochemistry. 1977 Oct 18;16(21):4731–4737. doi: 10.1021/bi00640a031. [DOI] [PubMed] [Google Scholar]
  11. Ninio J. Kinetic amplification of enzyme discrimination. Biochimie. 1975;57(5):587–595. doi: 10.1016/s0300-9084(75)80139-8. [DOI] [PubMed] [Google Scholar]
  12. Oeschger M. P., Woods S. L. A temperature-sensitive suppressor enabling the manipulation of the level of individual proteins in intact cells. Cell. 1976 Feb;7(2):205–212. doi: 10.1016/0092-8674(76)90019-2. [DOI] [PubMed] [Google Scholar]
  13. Raunio R., Rosenqvist H. Amino acid pool of Escherichia coli during the different phases of growth. Acta Chem Scand. 1970;24(8):2737–2744. doi: 10.3891/acta.chem.scand.24-2737. [DOI] [PubMed] [Google Scholar]
  14. Schreier A. A., Schimmel P. R. Transfer ribonucleic acid synthetase catalyzed deacylation of aminoacyl transfer ribonucleic acid in the absence of adenosine monophosphate and pyrophosphate. Biochemistry. 1972 Apr 25;11(9):1582–1589. doi: 10.1021/bi00759a006. [DOI] [PubMed] [Google Scholar]
  15. Yarus M. Phenylalanyl-tRNA synthetase and isoleucyl-tRNA Phe : a possible verification mechanism for aminoacyl-tRNA. Proc Natl Acad Sci U S A. 1972 Jul;69(7):1915–1919. doi: 10.1073/pnas.69.7.1915. [DOI] [PMC free article] [PubMed] [Google Scholar]

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