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Effect of Correlated tRNA Abundances on Translation Errors and Evolution of Codon Usage Bias


Despite the fact that tRNA abundances are thought to play a major role in determining translation error rates, their distribution across the genetic code and the resulting implications have received little attention. In general, studies of codon usage bias (CUB) assume that codons with higher tRNA abundance have lower missense error rates. Using a model of protein translation based on tRNA competition and intra-ribosomal kinetics, we show that this assumption can be violated when tRNA abundances are positively correlated across the genetic code. Examining the distribution of tRNA abundances across 73 bacterial genomes from 20 different genera, we find a consistent positive correlation between tRNA abundances across the genetic code. This work challenges one of the fundamental assumptions made in over 30 years of research on CUB that codons with higher tRNA abundances have lower missense error rates and that missense errors are the primary selective force responsible for CUB.


Vyšlo v časopise: Effect of Correlated tRNA Abundances on Translation Errors and Evolution of Codon Usage Bias. PLoS Genet 6(9): e32767. doi:10.1371/journal.pgen.1001128
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1001128

Souhrn

Despite the fact that tRNA abundances are thought to play a major role in determining translation error rates, their distribution across the genetic code and the resulting implications have received little attention. In general, studies of codon usage bias (CUB) assume that codons with higher tRNA abundance have lower missense error rates. Using a model of protein translation based on tRNA competition and intra-ribosomal kinetics, we show that this assumption can be violated when tRNA abundances are positively correlated across the genetic code. Examining the distribution of tRNA abundances across 73 bacterial genomes from 20 different genera, we find a consistent positive correlation between tRNA abundances across the genetic code. This work challenges one of the fundamental assumptions made in over 30 years of research on CUB that codons with higher tRNA abundances have lower missense error rates and that missense errors are the primary selective force responsible for CUB.


Zdroje

1. LobleyGE

MilneV

LovieJM

ReedsPJ

PennieK

1980 Whole body and tissue protein synthesis in cattle. Br J Nutr 43 491 502

2. PannevisMC

HoulihanDF

1992 The energetic cost of protein synthesis in isolated hepatocytes of rainbow trout (oncorhynchus mykiss). J Comp Physiol B, Biochem Syst Environ Physiol 162 393 400

3. WarnerJR

1999 The economics of ribosome biosynthesis in yeast. Trends Biochem Sci 24 437 40

4. AkashiH

GojoboriT

2002 Metabolic efficiency and amino acid composition in the proteomes of Escherichia coli and Bacillus subtilis. Proceedings of the National Academy of Sciences of the United States of America 99 3695 700

5. SharpPM

LiWH

1986 An evolutionary perspective on synonymous codon usage in unicellular organisms. J Mol Evol 24 28 38

6. BulmerM

1991 The selection-mutation-drift theory of synonymous codon usage. Genetics 129 897 907

7. BergOG

KurlandCG

1997 Growth rate-optimised tRNA abundance and codon usage. Journal of Molecular Biology 270 544 50

8. KanayaS

YamadaY

KudoY

IkemuraT

1999 Studies of codon usage and tRNA genes of 18 unicellular organisms and quantification of Bacillus subtilis tRNAs: gene expression level and species-specific diversity of codon usage based on multivariate analysis. Gene 238 143 55

9. RochaEPC

2004 Codon usage bias from tRNA's point of view: redundancy, specialization, and efficient decoding for translation optimization. Genome Research 14 2279 86

10. DrummondDA

WilkeCO

2009 The evolutionary consequences of erroneous protein synthesis. Nat Rev Genet 10 715 24

11. GilchristMA

ShahP

ZaretzkiR

2009 Measuring and detecting molecular adaptation in codon usage against nonsense errors during protein translation. Genetics 183 1493 505

12. AkashiH

1994 Synonymous codon usage in Drosophila melanogaster: natural selection and translational accuracy. Genetics 136 927 35

13. AkashiH

2001 Gene expression and molecular evolution. Current Opinion in Genetics & Development 11 660 6

14. AravaY

BoasFE

BrownPO

HerschlagD

2005 Dissecting eukaryotic translation and its control by ribosome density mapping. Nucleic Acids Research 33 2421 32

15. StoletzkiN

Eyre-WalkerA

2007 Synonymous codon usage in Escherichia coli: selection for translational accuracy. Molecular Biology and Evolution 24 374 81

16. GranthamR

1974 Amino acid difference formula to help explain protein evolution. Science 185 862 4

17. FreelandSJ

HurstLD

1998 The genetic code is one in a million. J Mol Evol 47 238 48

18. FreelandSJ

KnightRD

LandweberLF

HurstLD

2000 Early fixation of an optimal genetic code. Molecular Biology and Evolution 17 511 8

19. HiggsP

2009 A four-column theory for the origin of the genetic code: tracing the evolutionary pathways that gave rise to an optimized code. Biol Direct 4 16

20. AnderssonDI

BohmanK

IsakssonLA

KurlandCG

1982 Translation rates and misreading characteristics of rpsd mutants in Escherichia coli. Mol Gen Genet 187 467 72

21. BouadlounF

DonnerD

KurlandCG

1983 Codon-specific missense errors in vivo. EMBO J 2 1351 6

22. PrecupJ

ParkerJ

1987 Missense misreading of asparagine codons as a function of codon identity and context. J Biol Chem 262 11351 5

23. KurlandCG

EhrenbergM

1987 Growth-optimizing accuracy of gene expression. Annual review of biophysics and biophysical chemistry 16 291 317

24. JørgensenF

KurlandCG

1990 Processivity errors of gene expression in Escherichia coli. Journal of Molecular Biology 215 511 21

25. KramerEB

FarabaughPJ

2007 The frequency of translational misreading errors in e.coli is largely determined by tRNA competition. RNA 13 87 96

26. VarenneS

BucJ

LloubesR

LazdunskiC

1984 Translation is a non-uniform process. effect of trna availability on the rate of elongation of nascent polypeptide chains. Journal of Molecular Biology 180 549 76

27. GromadskiKB

RodninaMV

2004 Kinetic determinants of high-fidelity tRNA discrimination on the ribosome. Mol Cell 13 191 200

28. OgleJM

BrodersenDE

ClemonsWM

TarryMJ

CarterAP

2001 Recognition of cognate transfer RNA by the 30S ribosomal subunit. Science 292 897 902

29. FluittA

PienaarE

ViljoenH

2007 Ribosome kinetics and aa-tRNA competition determine rate and fidelity of peptide synthesis. Computational Biology and Chemistry 31 335 46

30. ZaherHS

GreenR

2009 Fidelity at the molecular level: lessons from protein synthesis. Cell 136 746 62

31. DongH

NilssonL

KurlandCG

1996 Co-variation of tRNA abundance and codon usage in Escherichia coli at different growth rates. Journal of Molecular Biology 260 649 63

32. CognatV

DeragonJM

VinogradovaE

SalinasT

RemacleC

2008 On the evolution and expression of Chlamydomonas reinhardtii nucleus-encoded transfer RNA genes. Genetics 179 113 23

33. ChanPP

LoweTM

2009 GtRNAdb: a database of transfer RNA genes detected in genomic sequence. Nucleic Acids Research 37 D93 7

34. LimVI

CurranJF

2001 Analysis of codon:anticodon interactions within the ribosome provides new insights into codon reading and the genetic code structure. RNA 7 942 57

35. IkemuraT

1985 Codon usage and tRNA content in unicellular and multicellular organisms. Molecular Biology and Evolution 2 13 34

36. CurranJF

YarusM

1989 Rates of aminoacyl-tRNA selection at 29 sense codons in vivo. Journal of Molecular Biology 209 65 77

37. IkemuraT

1981 Correlation between the abundance of Escherichia coli transfer RNAs and the occurrence of the respective codons in its protein genes: a proposal for a synonymous codon choice that is optimal for the e.coli translational system. Journal of Molecular Biology 151 389 409

38. DrummondDA

WilkeCO

2008 Mistranslation-induced protein misfolding as a dominant constraint on coding-sequence evolution. Cell 134 341 52

39. GilchristMA

2007 Combining models of protein translation and population genetics to predict protein production rates from codon usage patterns. Molecular Biology and Evolution 24 2362 72

40. DrummondDA

BloomJD

AdamiC

WilkeCO

ArnoldFH

2005 Why highly expressed proteins evolve slowly. Proc Natl Acad Sci USA 102 14338 43

41. DrummondDA

RavalA

WilkeCO

2006 A single determinant dominates the rate of yeast protein evolution. Molecular Biology and Evolution 23 327 37

42. GilchristMA

WagnerA

2006 A model of protein translation including codon bias, nonsense errors, and ribosome recycling. Journal of Theoretical Biology 239 417 34

43. Kimchi-SarfatyC

OhJM

KimIW

SaunaZE

CalcagnoAM

2007 A “silent” polymorphism in the mdr1 gene changes substrate specificity. Science 315 525 8

44. TsaiCJ

SaunaZE

Kimchi-SarfatyC

AmbudkarSV

GottesmanMM

2008 Synonymous mutations and ribosome stalling can lead to altered folding pathways and distinct minima. J Mol Biol 383 281 91

45. MarinM

2008 Folding at the rhythm of the rare codon beat. Biotechnol J 3 1047 57

46. GreenbaumD

ColangeloC

WilliamsK

GersteinM

2003 Comparing protein abundance and mRNA expression levels on a genomic scale. Genome Biol 4 117

47. KelloggE

JulianoN

1997 The structure and function of rubisco and their implications for systematic studies. American journal of botany

48. WilkeCO

DrummondDA

2006 Population genetics of translational robustness. Genetics 173 473 81

49. WongJT

1975 A co-evolution theory of the genetic code. Proc Natl Acad Sci USA 72 1909 12

50. ArdellDH

SellaG

2001 On the evolution of redundancy in genetic codes. J Mol Evol 53 269 81

51. VetsigianK

GoldenfeldN

2009 Genome rhetoric and the emergence of compositional bias. Proc Natl Acad Sci USA 106 215 20

52. BlanchardSC

KimHD

GonzalezRL

PuglisiJD

ChuS

2004 tRNA dynamics on the ribosome during translation. Proc Natl Acad Sci USA 101 12893 8

53. BlanchardSC

GonzalezRL

KimHD

ChuS

PuglisiJD

2004 tRNA selection and kinetic proofreading in translation. Nat Struct Mol Biol 11 1008 14

54. KotheU

RodninaMV

2007 Codon reading by tRNA-ala with modified uridine in the wobble position. Mol Cell 25 167 74

55. AgrisPF

1991 Wobble position modified nucleosides evolved to select transfer RNA codon recognition: a modified-wobble hypothesis. Biochimie 73 1345 9

56. AgrisPF

VendeixFAP

GrahamWD

2007 tRNA's wobble decoding of the genome: 40 years of modification. J Mol Biol 366 1 13

57. SørensenMA

KurlandCG

PedersenS

1989 Codon usage determines translation rate in Escherichia coli. Journal of Molecular Biology 207 365 77

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