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PMID: 6429345 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't

Evolutionary implications of error amplification in the self-replicating and protein-synthesizing machinery.

Journal of molecular evolution ·Vol. 20 ·No. 1 ·1984-00-00 ·Pages 77-85

Hasegawa M, Yano T, Miyata T

Abstract

Evolutionary constraints operating on animal mitochondrial tRNA were estimated to be reduced to about 1/30 of those that apply to cytoplasmic tRNA. In the nuclear-cytoplasmic system, an effect of a mutation in tRNA is likely to be amplified through positive feedback loops consisting of DNA polymerases, RNA polymerases, ribosomal proteins, aminoacyl-tRNA synthetases, tRNA processing enzymes, and others. This amplification phenomenon is called an "error cascade" and the loops that cause it are called "error loops." The freedom of evolutionary change of cytoplasmic tRNA is expected to be severely restricted to avoid the error cascade. In fact, cytoplasmic tRNA is highly conserved during evolution. On the other hand, in the animal mitochondrial system, all of the proteins involved in error loops are coded for in the nuclear genome and imported from the cytoplasm, and accordingly the system is free from the error cascade. The difference in constraints operating on animal tRNA between cytoplasm and mitochondria is attributed to the presence or absence of error loops. It is shown that the constraints on mitochondrial tRNA in fungi are not as relaxed as those in animals. This observation is attributed to the presence of an error loop in fungal mitochondria, since at least one protein of the mitochondrial ribosome is coded for in the mitochondrial genome of fungi. The evolutionary rates of proteins involved in the processing of genetic information are discussed in relation to the error cascade.

MeSH Terms
Animals Biological Evolution Cytoplasm/metabolism DNA Replication DNA-Directed DNA Polymerase/genetics Fungi/metabolism Mitochondria/metabolism Protein Biosynthesis Proteins/genetics RNA, Transfer/genetics Transcription, Genetic
Chemicals
Proteins RNA, Transfer DNA-Directed DNA Polymerase
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Hasegawa M
Yano T
Miyata T
References (57)
57 references, click to expand
  1. Ribosomal assembly influenced by growth in the presence of streptomycin.
    Proc Natl Acad Sci U S A. 1973 Oct;70(10):2762-6 PMID: 4583024
  2. Mechanisms of evolution in animal mitochondrial DNA.
    Ann N Y Acad Sci. 1981;361:119-34 PMID: 6941715
  3. Nucleotide sequence divergence and functional constraint in mRNA evolution.
    Proc Natl Acad Sci U S A. 1980 Dec;77(12):7328-32 PMID: 6938980
  4. The evolving tRNA molecule.
    CRC Crit Rev Biochem. 1981;11(1):35-104 PMID: 7030617
  5. Sequence and organization of the human mitochondrial genome.
    Nature. 1981 Apr 9;290(5806):457-65 PMID: 7219534
  6. Test of some aging hypotheses using two-dimensional protein mapping.
    Gerontology. 1978;24(6):426-33 PMID: 689377
  7. Mitochondrial DNA sequences of primates: tempo and mode of evolution.
    J Mol Evol. 1982;18(4):225-39 PMID: 6284948
  8. Mitochondrial nucleic acids and their relation to the biogenesis of mitochondria.
    Physiol Rev. 1970 Jul;50(3):376-427 PMID: 4912905
  9. Rapid evolutionary divergence of proteins in mammalian mitochondrial ribosomes.
    FEBS Lett. 1978 Feb 1;86(1):76-80 PMID: 620833
  10. Ageing of clones of mammalian cells.
    Nature. 1973 Jun 22;243(5408):441-5 PMID: 4591306
  11. The stability of the translation apparatus.
    J Mol Biol. 1975 Sep 15;97(2):257-65 PMID: 1177323
  12. On the specificity of DNA polymerase.
    Proc Natl Acad Sci U S A. 1967 Mar;57(3):650-7 PMID: 16591513
  13. Molecular clock of silent substitution: at least six-fold preponderance of silent changes in mitochondrial genes over those in nuclear genes.
    J Mol Evol. 1982;19(1):28-35 PMID: 7161808
  14. Failure of the Watson-Crick theory as a chemical explanation of inheritance.
    Nature. 1968 Oct 26;220(5165):334-40 PMID: 5684872
  15. The maintenance of the accuracy of protein synthesis and its relevance to ageing.
    Proc Natl Acad Sci U S A. 1963 Apr;49:517-21 PMID: 13940312
  16. On the origin of the genetic code and the stability of the translation apparatus.
    J Mol Biol. 1974 Jun 25;86(2):349-62 PMID: 4414916
  17. On some principles governing molecular evolution.
    Proc Natl Acad Sci U S A. 1974 Jul;71(7):2848-52 PMID: 4527913
  18. Evolution of ribosomal proteins.
    Eur J Biochem. 1973 Nov 1;39(1):305-12 PMID: 4543854
  19. Evolution of rRNA and origin of mitochondria.
    Nature. 1981 Oct 29;293(5835):751-5 PMID: 7027053
  20. Informational suppression.
    Annu Rev Genet. 1970;4:107-34 PMID: 4950057
  21. Comparison of the evolution rates of cytosolic and mitochondrial aspartate aminotransferase.
    Nature. 1978 Sep 14;275(5676):157-9 PMID: 692687
  22. Mitochondrial L-rRNA from Aspergillus nidulans: potential secondary structure and evolution.
    Nucleic Acids Res. 1982 Aug 11;10(15):4795-801 PMID: 6752884
  23. Complete sequence of bovine mitochondrial DNA. Conserved features of the mammalian mitochondrial genome.
    J Mol Biol. 1982 Apr 25;156(4):683-717 PMID: 7120390
  24. 3'-Terminal sequence of wheat mitochondrial 18S ribosomal RNA: further evidence of a eubacterial evolutionary origin.
    Nucleic Acids Res. 1982 Jul 10;10(13):3921-32 PMID: 7050913
  25. The maintenance of the accuracy of protein synthesis and its relevance to ageing: a correction.
    Proc Natl Acad Sci U S A. 1970 Nov;67(3):1476 PMID: 5274472
  26. Ribosomal discrimination of tRNAs.
    Nat New Biol. 1971 Dec 29;234(52):261-4 PMID: 4943838
  27. A semi-quantitative treatment of missense and nonsense suppression in the strA and ram ribosomal mutants of Escherichia coli. Evaluation of some molecular parameters of translation in vivo.
    J Mol Biol. 1974 Apr 5;84(2):297-313 PMID: 4598370
  28. A different genetic code in human mitochondria.
    Nature. 1979 Nov 8;282(5735):189-94 PMID: 226894
  29. Rearranged mitochondrial genes in the yeast nuclear genome.
    Nature. 1983 Jan 27;301(5898):296-301 PMID: 6296698
  30. Intron within the large rRNA gene of N. crassa mitochondria: a long open reading frame and a consensus sequence possibly important in splicing.
    Cell. 1982 Dec;31(3 Pt 2):509-20 PMID: 6218884
  31. Ribosome structure and function emergent.
    Science. 1970 Sep 18;169(3951):1171-7 PMID: 4915895
  32. A rapid rise in cell variants during the senescence of populations of human fibroblasts.
    Cell. 1975 Sep;6(1):67-73 PMID: 1164734
  33. On the accuracy of protein synthesis in Drosophila melanogaster.
    Mech Ageing Dev. 1981 Jun;16(2):127-39 PMID: 6790882
  34. Compilation of sequences of tRNA genes.
    Nucleic Acids Res. 1983 Jan 11;11(1):r55-103 PMID: 6866761
  35. Novel features in the genetic code and codon reading patterns in Neurospora crassa mitochondria based on sequences of six mitochondrial tRNAs.
    Proc Natl Acad Sci U S A. 1980 Jun;77(6):3159-63 PMID: 6447871
  36. Molecular evolution of mRNA: a method for estimating evolutionary rates of synonymous and amino acid substitutions from homologous nucleotide sequences and its application.
    J Mol Evol. 1980 Sep;16(1):23-36 PMID: 6449605
  37. Decreased fidelity of DNA polymerase activity isolated from aging human fibroblasts.
    Proc Natl Acad Sci U S A. 1976 Aug;73(8):2818-22 PMID: 1066693
  38. Location and structure of the var1 gene on yeast mitochondrial DNA: nucleotide sequence of the 40.0 allele.
    Cell. 1982 Sep;30(2):617-26 PMID: 6754087
  39. Assembly of the mitochondrial membrane system. Analysis of the nucleotide sequence and transcripts in the oxi1 region of yeast mitochondrial DNA.
    J Biol Chem. 1981 Dec 25;256(24):12780-7 PMID: 7031051
  40. Rapid evolution of animal mitochondrial DNA.
    Proc Natl Acad Sci U S A. 1979 Apr;76(4):1967-71 PMID: 109836
  41. On the translational error theory of aging.
    Proc Natl Acad Sci U S A. 1977 Aug;74(8):3396-8 PMID: 333438
  42. On the role of DNA polymerase in base selection.
    Cold Spring Harb Symp Quant Biol. 1966;31:693-7 PMID: 5237208
  43. Sequence and gene organization of mouse mitochondrial DNA.
    Cell. 1981 Oct;26(2 Pt 2):167-80 PMID: 7332926
  44. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences.
    J Mol Evol. 1980 Dec;16(2):111-20 PMID: 7463489
  45. Altered enzymes in ageing human fibroblasts.
    Nature. 1972 Jul 7;238(5358):26-30 PMID: 12635262
  46. A mammalian tRNAHis-containing antigen is recognized by the polymyositis-specific antibody anti-Jo-1.
    Nucleic Acids Res. 1983 Feb 11;11(3):853-70 PMID: 6188108
  47. Genetic control of mutation rates in bacteriophageT4.
    Nature. 1969 Mar 22;221(5186):1128-32 PMID: 4975273
  48. Five TGA "stop" codons occur within the translated sequence of the yeast mitochondrial gene for cytochrome c oxidase subunit II.
    Proc Natl Acad Sci U S A. 1979 Dec;76(12):6534-8 PMID: 230513
  49. The structures of cytochrome c and the rates of molecular evolution.
    J Mol Evol. 1971;1(1):26-45 PMID: 4377446
  50. Transfer RNA: molecular structure, sequence, and properties.
    Annu Rev Biochem. 1976;45:805-60 PMID: 60910
  51. Different pattern of codon recognition by mammalian mitochondrial tRNAs.
    Proc Natl Acad Sci U S A. 1980 Jun;77(6):3164-6 PMID: 6932013
  52. Compilation of tRNA sequences.
    Nucleic Acids Res. 1983 Jan 11;11(1):r1-53 PMID: 6866759
  53. Biochemical evolution.
    Annu Rev Biochem. 1977;46:573-639 PMID: 409339
  54. Degradation of abnormal proteins in Escherichia coli (protein breakdown-protein structure-mistranslation-amino acid analogs-puromycin).
    Proc Natl Acad Sci U S A. 1972 Feb;69(2):422-6 PMID: 4551144
  55. Codon recognition rules in yeast mitochondria.
    Proc Natl Acad Sci U S A. 1980 Jun;77(6):3167-70 PMID: 6997870
  56. The error catastrophe hypothesis with reference to aging and the evolution of the protein synthesizing machinery.
    J Theor Biol. 1975 Nov;55(1):245-82 PMID: 1207158
  57. Error propagation in intracellular information transfer.
    J Theor Biol. 1980 Feb 7;82(3):363-82 PMID: 6988650
Article Info
Journal
Journal of molecular evolution
Abbr.
J Mol Evol
ISSN
0022-2844
Published
1984-00-00
Pages
77-85
Language
English
Region
Germany
NLM ID
0360051
Subset
IM
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