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Three Independent Determinants of Protein Evolutionary Rate

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Abstract

One of the most widely accepted ideas related to the evolutionary rates of proteins is that functionally important residues or regions evolve slower than other regions, a reasonable outcome of which should be a slower evolutionary rate of the proteins with a higher density of functionally important sites. Oddly, the role of functional importance, mainly measured by essentiality, in determining evolutionary rate has been challenged in recent studies. Several variables other than protein essentiality, such as expression level, gene compactness, protein–protein interactions, etc., have been suggested to affect protein evolutionary rate. In the present review, we try to refine the concept of functional importance of a gene, and consider three factors—functional importance, expression level, and gene compactness, as independent determinants of evolutionary rate of a protein, based not only on their known correlation with evolutionary rate but also on a reasonable mechanistic model. We suggest a framework based on these mechanistic models to correctly interpret the correlations between evolutionary rates and the various variables as well as the interrelationships among the variables.

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References

  • Agarwal SM (2005) Evolutionary rate variation in eukaryotic lineage specific human intronless proteins. Biochem Biophys Res Commun 337:1192–1197

    PubMed  CAS  Google Scholar 

  • Akashi H (1994) Synonymous codon usage in Drosophila melanogaster: natural selection and translational accuracy. Genetics 136:927–935

    PubMed  CAS  Google Scholar 

  • Akashi H (2001) Gene expression and molecular evolution. Curr Opin Genet Dev 11:660–666

    PubMed  CAS  Google Scholar 

  • Akashi H, Eyre-Walker A (1998) Translational selection and molecular evolution. Curr Opin Genet Dev 8:688–693

    PubMed  CAS  Google Scholar 

  • Alvarez-Ponce D (2012) The relationship between the hierarchical position of proteins in the human signal transduction network and their rate of evolution. BMC Evol Biol 12:192

    PubMed  CAS  Google Scholar 

  • Bergmiller T, Ackermann M, Silander OK (2012) Patterns of evolutionary conservation of essential genes correlate with their compensability. PLoS Genet 8:e1002803

    PubMed  CAS  Google Scholar 

  • Betancourt AJ, Welch JJ, Charlesworth B (2009) Reduced effectiveness of selection caused by a lack of recombination. Curr Biol 19:655–660

    PubMed  CAS  Google Scholar 

  • Bloom JD, Adami C (2003) Apparent dependence of protein evolutionary rate on number of interactions is linked to biases in protein–protein interactions data sets. BMC Evol Biol 3:21

    PubMed  Google Scholar 

  • Campos JL, Charlesworth B, Haddrill PR (2012) Molecular evolution in nonrecombining regions of the Drosophila melanogaster genome. Genome Biol Evol 4:278–288

    PubMed  CAS  Google Scholar 

  • Carmel L, Koonin EV (2009) A universal nonmonotonic relationship between gene compactness and expression levels in multicellular eukaryotes. Genome Biol Evol 1:382–390

    PubMed  Google Scholar 

  • Carvalho AB, Clark AG (1999) Intron size and natural selection. Nature 401:344

    PubMed  CAS  Google Scholar 

  • Castillo-Davis CI, Hartl DL (2003) Conservation, relocation and duplication in genome evolution. Trends Genet 19:593–597

    PubMed  CAS  Google Scholar 

  • Castillo-Davis CI, Mekhedov SL, Hartl DL, Koonin EV, Kondrashov FA (2002) Selection for short introns in highly expressed genes. Nat Genet 31:415–418

    PubMed  CAS  Google Scholar 

  • Charlesworth B, Betancourt AJ, Kaiser VB, Gordo I (2009) Genetic recombination and molecular evolution. Cold Spring Harb Symp Quant Biol 74:177–186

    PubMed  CAS  Google Scholar 

  • Chen Y, Dokholyan NV (2008) Natural selection against protein aggregation on self-interacting and essential proteins in yeast, fly, and worm. Mol Biol Evol 25:1530–1533

    PubMed  CAS  Google Scholar 

  • Chen Y, Xu D (2005) Understanding protein dispensability through machine-learning analysis of high-throughput data. Bioinformatics 21:575–581

    PubMed  CAS  Google Scholar 

  • Chen FC, Liao BY, Pan CL, Lin HY, Chang AY (2012) Assessing determinants of exonic evolutionary rates in mammals. Mol Biol Evol 29:3121–3129

    PubMed  CAS  Google Scholar 

  • Choi SS, Vallender EJ, Lahn BT (2006) Systematically assessing the influence of 3-dimensional structural context on the molecular evolution of mammalian proteomes. Mol Biol Evol 23:2131–2133

    PubMed  CAS  Google Scholar 

  • Comeron JM (2006) Weak selection and recent mutational changes influence polymorphic synonymous mutations in humans. Proc Natl Acad Sci USA 103:6940–6945

    PubMed  CAS  Google Scholar 

  • Comeron JM, Guthrie TB (2005) Intragenic Hill-Robertson interference influences selection intensity on synonymous mutations in Drosophila. Mol Biol Evol 22:2519–2530

    PubMed  CAS  Google Scholar 

  • Comeron JM, Kreitman M (2000) The correlation between intron length and recombination in Drosophila. Dynamic equilibrium between mutational and selective forces. Genetics 156:1175–1190

    PubMed  CAS  Google Scholar 

  • Comeron JM, Kreitman M (2002) Population, evolutionary and genomic consequences of interference selection. Genetics 161:389–410

    PubMed  CAS  Google Scholar 

  • Comeron JM, Kreitman M, Aguade M (1999) Natural selection on synonymous sites is correlated with gene length and recombination in Drosophila. Genetics 151:239–249

    PubMed  CAS  Google Scholar 

  • Comeron JM, Williford A, Kliman RM (2008) The Hill-Robertson effect: evolutionary consequences of weak selection and linkage in finite populations. Heredity (Edinb) 100:19–31

    CAS  Google Scholar 

  • Conant GC, Stadler PF (2009) Solvent exposure imparts similar selective pressures across a range of yeast proteins. Mol Biol Evol 26:1155–1161

    PubMed  CAS  Google Scholar 

  • Coulomb S, Bauer M, Bernard D, Marsolier-Kergoat MC (2005) Gene essentiality and the topology of protein interaction networks. Proc Biol Sci 272:1721–1725

    PubMed  CAS  Google Scholar 

  • Darwin C (1859) On the origin of species by means of natural selection. J. Murray, London

    Google Scholar 

  • Dotsch A, Klawonn F, Jarek M, Scharfe M, Blocker H, Haussler S (2010) Evolutionary conservation of essential and highly expressed genes in Pseudomonas aeruginosa. BMC Genomics 11:234

    PubMed  Google Scholar 

  • Drummond DA, Wilke CO (2008) Mistranslation-induced protein misfolding as a dominant constraint on coding-sequence evolution. Cell 134:341–352

    PubMed  CAS  Google Scholar 

  • Drummond DA, Wilke CO (2009) The evolutionary consequences of erroneous protein synthesis. Nat Rev Genet 10:715–724

    PubMed  Google Scholar 

  • Drummond DA, Bloom JD, Adami C, Wilke CO, Arnold FH (2005) Why highly expressed proteins evolve slowly. Proc Natl Acad Sci USA 102:14338–14343

    PubMed  CAS  Google Scholar 

  • Drummond DA, Raval A, Wilke CO (2006) A single determinant dominates the rate of yeast protein evolution. Mol Biol Evol 23:327–337

    PubMed  CAS  Google Scholar 

  • Duret L (2001) Why do genes have introns? Recombination might add a new piece to the puzzle. Trends Genet 17:172–175

    PubMed  CAS  Google Scholar 

  • Duret L, Mouchiroud D (1999) Expression pattern and, surprisingly, gene length shape codon usage in Caenorhabditis, Drosophila, and Arabidopsis. Proc Natl Acad Sci USA 96:4482–4487

    PubMed  CAS  Google Scholar 

  • Duret L, Mouchiroud D (2000) Determinants of substitution rates in mammalian genes: expression pattern affects selection intensity but not mutation rate. Mol Biol Evol 17:68–74

    PubMed  CAS  Google Scholar 

  • Eisenberg E, Levanon EY (2003) Human housekeeping genes are compact. Trends Genet 19:362–365

    PubMed  CAS  Google Scholar 

  • Ermakova EO, Nurtdinov RN, Gelfand MS (2006) Fast rate of evolution in alternatively spliced coding regions of mammalian genes. BMC Genomics 7:84

    PubMed  Google Scholar 

  • Fang G, Rocha E, Danchin A (2005) How essential are nonessential genes? Mol Biol Evol 22:2147–2156

    PubMed  CAS  Google Scholar 

  • Fedorova L, Fedorov A (2003) Introns in gene evolution. Genetica 118:123–131

    PubMed  CAS  Google Scholar 

  • Felsenstein J (1974) The evolutionary advantage of recombination. Genetics 78:737–756

    PubMed  CAS  Google Scholar 

  • Fitch DH, Strausbaugh LD (1993) Low codon bias and high rates of synonymous substitution in Drosophila hydei and D. melanogaster histone genes. Mol Biol Evol 10:397–413

    PubMed  CAS  Google Scholar 

  • Franzosa EA, Xia Y (2009) Structural determinants of protein evolution are context-sensitive at the residue level. Mol Biol Evol 26:2387–2395

    PubMed  CAS  Google Scholar 

  • Fraser HB, Hirsh AE, Steinmetz LM, Scharfe C, Feldman MW (2002) Evolutionary rate in the protein interaction network. Science 296:750–752

    PubMed  CAS  Google Scholar 

  • Fraser HB, Wall DP, Hirsh AE (2003) A simple dependence between protein evolution rate and the number of protein–protein interactions. BMC Evol Biol 3:11

    PubMed  Google Scholar 

  • Gerdes SY, Scholle MD, Campbell JW, Balazsi G, Ravasz E, Daugherty MD, Somera AL, Kyrpides NC, Anderson I, Gelfand MS, Bhattacharya A, Kapatral V, D’Souza M, Baev MV, Grechkin Y, Mseeh F, Fonstein MY, Overbeek R, Barabasi AL, Oltvai ZN, Osterman AL (2003) Experimental determination and system level analysis of essential genes in Escherichia coli MG1655. J Bacteriol 185:5673–5684

    PubMed  CAS  Google Scholar 

  • Gilbert W (1978) Why genes in pieces? Nature 271:501

    PubMed  CAS  Google Scholar 

  • Gingold H, Pilpel Y (2011) Determinants of translation efficiency and accuracy. Mol Sys Biol 7:481

    Google Scholar 

  • Goh KI, Cusick ME, Valle D, Childs B, Vidal M, Barabasi AL (2007) The human disease network. Proc Natl Acad Sci USA 104:8685–8690

    PubMed  CAS  Google Scholar 

  • Gong X, Fan S, Bilderbeck A, Li M, Pang H, Tao S (2008) Comparative analysis of essential genes and nonessential genes in Escherichia coli K12. Mol Genet Genomics 279:87–94

    PubMed  CAS  Google Scholar 

  • Gonzalez F, Romani S, Cubas P, Modolell J, Campuzano S (1989) Molecular analysis of the asense gene, a member of the achaete-scute complex of Drosophila melanogaster, and its novel role in optic lobe development. EMBO J 8:3553–3562

    PubMed  CAS  Google Scholar 

  • Gordo I, Charlesworth B (2001) Genetic linkage and molecular evolution. Curr Biol 11:R684–R686

    PubMed  CAS  Google Scholar 

  • Haddrill PR, Charlesworth B, Halligan DL, Andolfatto P (2005) Patterns of intron sequence evolution in Drosophila are dependent upon length and GC content. Genome Biol 6:R67

    PubMed  Google Scholar 

  • Hahn MW, Kern AD (2005) Comparative genomics of centrality and essentiality in three eukaryotic protein-interaction networks. Mol Biol Evol 22:803–806

    PubMed  CAS  Google Scholar 

  • Hahn MW, Conant GC, Wagner A (2004) Molecular evolution in large genetic networks: does connectivity equal constraint? J Mol Evol 58:203–211

    PubMed  CAS  Google Scholar 

  • Hao L, Ge X, Wan H, Hu S, Lercher MJ, Yu J, Chen WH (2010) Human functional genetic studies are biased against the medically most relevant primate-specific genes. BMC Evol Biol 10:316

    PubMed  Google Scholar 

  • He X, Zhang J (2006) Toward a molecular understanding of pleiotropy. Genetics 173:1885–1891

    PubMed  CAS  Google Scholar 

  • Hill WG, Robertson A (1966) The effect of linkage on limits to artificial selection. Genet Res 8:269–294

    PubMed  CAS  Google Scholar 

  • Hiraoka Y, Kawamata K, Haraguchi T, Chikashige Y (2009) Codon usage bias is correlated with gene expression levels in the fission yeast Schizosaccharomyces pombe. Genes Cells 14:499–509

    PubMed  CAS  Google Scholar 

  • Hirsh AE, Fraser HB (2001) Protein dispensability and rate of evolution. Nature 411:1046–1049

    PubMed  CAS  Google Scholar 

  • Huang YF, Niu DK (2008) Evidence against the energetic cost hypothesis for the short introns in highly expressed genes. BMC Evol Biol 8:154

    Google Scholar 

  • Hudson RR (1994) How can the low levels of DNA sequence variation in regions of the drosophila genome with low recombination rates be explained? Proc Natl Acad Sci USA 91:6815–6818

    PubMed  CAS  Google Scholar 

  • Hudson CM, Conant GC (2011) Expression level, cellular compartment and metabolic network position all influence the average selective constraint on mammalian enzymes. BMC Evol Biol 11:89

    PubMed  Google Scholar 

  • Hurst LD, Smith NG (1999) Do essential genes evolve slowly? Curr Biol 9:747–750

    PubMed  CAS  Google Scholar 

  • Iida K, Akashi H (2000) A test of translational selection at ‘silent’ sites in the human genome: base composition comparisons in alternatively spliced genes. Gene 261:93–105

    PubMed  CAS  Google Scholar 

  • Ingvarsson PK (2008) Molecular evolution of synonymous codon usage in Populus. BMC Evol Biol 8:307

    PubMed  Google Scholar 

  • Jeong H, Mason SP, Barabasi AL, Oltvai ZN (2001) Lethality and centrality in protein networks. Nature 411:41–42

    PubMed  CAS  Google Scholar 

  • Jordan IK, Rogozin IB, Wolf YI, Koonin EV (2002) Essential genes are more evolutionarily conserved than are nonessential genes in bacteria. Genome Res 12:962–968

    PubMed  CAS  Google Scholar 

  • Jordan IK, Wolf YI, Koonin EV (2003) No simple dependence between protein evolution rate and the number of protein–protein interactions: only the most prolific interactors tend to evolve slowly. BMC Evol Biol 3:1

    PubMed  Google Scholar 

  • Jovelin R, Phillips PC (2009) Evolutionary rates and centrality in the yeast gene regulatory network. Genome Biol 10:R35

    PubMed  Google Scholar 

  • Kawahara Y, Imanishi T (2007) A genome-wide survey of changes in protein evolutionary rates across four closely related species of Saccharomyces sensu stricto group. BMC Evol Biol 7:9

    Google Scholar 

  • Kim J, Copley SD (2007) Why metabolic enzymes are essential or nonessential for growth of Escherichia coli K12 on glucose. Biochemistry 46:12501–12511

    PubMed  CAS  Google Scholar 

  • Kim SH, Yi SV (2007) Understanding relationship between sequence and functional evolution in yeast proteins. Genetica 131:151–156

    PubMed  CAS  Google Scholar 

  • Kimura M, Ota T (1974) On some principles governing molecular evolution. Proc Natl Acad Sci USA 71:2848–2852

    PubMed  CAS  Google Scholar 

  • Kliman RM, Hey J (1993) Reduced natural selection associated with low recombination in Drosophila melanogaster. Mol Biol Evol 10:1239–1258

    PubMed  CAS  Google Scholar 

  • Koonin EV (2005) Systemic determinants of gene evolution and function. Mol Syst Biol 1(2005):0021

    PubMed  Google Scholar 

  • Koonin EV, Wolf YI (2006) Evolutionary systems biology: links between gene evolution and function. Curr Opin Biotechnol 17:481–487

    PubMed  CAS  Google Scholar 

  • Kotlar D, Lavner Y (2006) The action of selection on codon bias in the human genome is related to frequency, complexity, and chronology of amino acids. BMC Genomics 7:67

    PubMed  Google Scholar 

  • Kramer EB, Farabaugh PJ (2007) The frequency of translational misreading errors in E. coli is largely determined by tRNA competition. RNA 13:87–96

    PubMed  CAS  Google Scholar 

  • Krylov DM, Wolf YI, Rogozin IB, Koonin EV (2003) Gene loss, protein sequence divergence, gene dispensability, expression level, and interactivity are correlated in eukaryotic evolution. Genome Res 13:2229–2235

    PubMed  CAS  Google Scholar 

  • Larracuente AM, Clark AG, Eisen MB, Smith DR, Bergman CM, Oliver B, Markow TA, Kaufman TC, Kellis M, Gelbart W, Iyer VN, Pollard DA, Sackton TB, Singh ND, Abad JP, Abt DN, Adryan B, Aguade M, Akashi H, Anderson WW, Aquadro CF, Ardell DH, Arguello R, Artieri CG, Barbash DA, Barker D, Barsanti P, Batterham P, Batzoglou S, Begun D, Bhutkar A, Blanco E, Bosak SA, Bradley RK, Brand AD, Brent MR, Brooks AN, Brown RH, Butlin RK, Caggese C, Calvi BR, de Carvalho AB, Caspi A, Castrezana S, Celniker SE, Chang JL, Chapple C, Chatterji S, Chinwalla A, Civetta A, Clifton SW, Comeron JM, Costello JC, Coyne JA, Daub J, David RG, Delcher AL, Delehaunty K, Do CB, Ebling H, Edwards K, Eickbush T, Evans JD, Filipski A, Findeiss S, Freyhult E, Fulton L, Fulton R, Garcia AC, Gardiner A, Garfield DA, Garvin BE, Gibson G, Gilbert D, Gnerre S, Godfrey J, Good R, Gotea V, Gravely B, Greenberg AJ, Griffiths-Jones S, Gross S, Guigo R, Gustafson EA, Haerty W, Hahn MW, Halligan DL, Halpern AL, Halter GM, Han MV, Heger A, Hillier L, Hinrichs AS, Holmes I, Hoskins RA, Hubisz MJ, Hultmark D, Huntley MA, Jaffe DB, Jagadeeshan S et al (2007) Evolution of genes and genomes on the Drosophila phylogeny. Nature 450:203–218

    PubMed  Google Scholar 

  • Larracuente AM, Sackton TB, Greenberg AJ, Wong A, Singh ND, Sturgill D, Zhang Y, Oliver B, Clark AG (2008) Evolution of protein-coding genes in Drosophila. Trends Genet 24:114–123

    PubMed  CAS  Google Scholar 

  • Lee Y, Zhou T, Tartaglia GG, Vendruscolo M, Wilke CO (2010) Translationally optimal codons associate with aggregation-prone sites in proteins. Proteomics 10:4163–4171

    PubMed  CAS  Google Scholar 

  • Lemos B, Bettencourt BR, Meiklejohn CD, Hartl DL (2005) Evolution of proteins and gene expression levels are coupled in Drosophila and are independently associated with mRNA abundance, protein length, and number of protein–protein interactions. Mol Biol Evol 22:1345–1354

    PubMed  CAS  Google Scholar 

  • Li W-H (1997) Molecular evolution. Sinauer Associates, Sunderland, MA

    Google Scholar 

  • Li W-H, Graur D (1991) Fundamentals of molecular evolution. Sinauer Associates, Sunderland, MA

    Google Scholar 

  • Liao BY and Zhang J (2006) Low rates of expression profile divergence in highly expressed genes and tissue-specific genes in during mammalian evolution. Mol Biol Evol 23:1119–1128

    Google Scholar 

  • Liao BY, Scott NM, Zhang J (2006) Impacts of gene essentiality, expression pattern, and gene compactness on the evolutionary rate of mammalian proteins. Mol Biol Evol 23:2072–2080

    PubMed  CAS  Google Scholar 

  • Lin YS, Hsu WL, Hwang JK, Li WH (2007) Proportion of solvent-exposed amino acids in a protein and rate of protein evolution. Mol Biol Evol 24:1005–1011

    PubMed  CAS  Google Scholar 

  • Marais G, Mouchiroud D, Duret L (2001) Does recombination improve selection on codon usage? Lessons from nematode and fly complete genomes. Proc Natl Acad Sci USA 98:5688–5692

    PubMed  CAS  Google Scholar 

  • Marais G, Domazet-Loso T, Tautz D, Charlesworth B (2004) Correlated evolution of synonymous and nonsynonymous sites in Drosophila. J Mol Evol 59:771–779

    PubMed  CAS  Google Scholar 

  • Marais G, Nouvellet P, Keightley PD, Charlesworth B (2005) Intron size and exon evolution in Drosophila. Genetics 170:481–485

    PubMed  CAS  Google Scholar 

  • McLnerney JO, Creevey CJ, Keane TM, Pentony MM, Naughton TJ (2006) Assessment of methods for amino acid matrix selection and their use on empirical data shows that ad hoc assumptions for choice of matrix are not justified. BMC Evol Biol 6:29

    PubMed  Google Scholar 

  • Misawa K, Kikuno RF (2011) Relationship between amino acid composition and gene expression in the mouse genome. BMC Res Notes 4:20

    PubMed  CAS  Google Scholar 

  • Moriyama EN, Powell JR (1998) Gene length and codon usage bias in Drosophila melanogaster, Saccharomyces cerevisiae and Escherichia coli. Nucleic Acids Res 26:3188–3193

    PubMed  CAS  Google Scholar 

  • Ohta T (1992) The nearly neutral theory of molecular evolution. Annu Rev Ecol Syst 23:263–286

    Google Scholar 

  • Pal LR, Guda C (2006) Tracing the origin of functional and conserved domains in the human proteome: implications for protein evolution at the modular level. BMC Evol Biol 6:91

    PubMed  Google Scholar 

  • Pal C, Papp B, Hurst LD (2001) Highly expressed genes in yeast evolve slowly. Genetics 158:927–931

    PubMed  CAS  Google Scholar 

  • Pal C, Papp B, Lercher MJ (2006) An integrated view of protein evolution. Nat Rev Genet 7:337–348

    PubMed  CAS  Google Scholar 

  • Park SG, Choi SS (2010) Expression breadth and expression abundance behave differently in correlations with evolutionary rates. BMC Evol Biol 10:241

    Google Scholar 

  • Park K, Kim D (2009) Localized network centrality and essentiality in the yeast-protein interaction network. Proteomics 9:5143–5154

    PubMed  CAS  Google Scholar 

  • Parmley JL, Urrutia AO, Potrzebowski L, Kaessmann H, Hurst LD (2007) Splicing and the evolution of proteins in mammals. PLoS Biol 5:e14

    PubMed  Google Scholar 

  • Parra G, Bradnam K, Rose AB, Korf I (2011) Comparative and functional analysis of intron-mediated enhancement signals reveals conserved features among plants. Nucleic Acids Res 39:5328–5337

    PubMed  CAS  Google Scholar 

  • Peralta H, Guerrero G, Aguilar A, Mora J (2011) Sequence variability of Rhizobiales orthologs and relationship with physico-chemical characteristics of proteins. Biol Direct 6:48

    Google Scholar 

  • Plass M, Eyras E (2006) Differentiated evolutionary rates in alternative exons and the implications for splicing regulation. BMC Evol Biol 6:50

    PubMed  Google Scholar 

  • Plotkin JB, Fraser HB (2007) Assessing the determinants of evolutionary rates in the presence of noise. Mol Biol Evol 24:1113–1121

    PubMed  CAS  Google Scholar 

  • Plotkin and Kudla (2011) Synonymous but not the same: the causes and consequences of codon bias. Nat Rev Genet 12:32–42

    Google Scholar 

  • Podder S, Mukhopadhyay P, Ghosh TC (2009) Multifunctionality dominantly determines the rate of human housekeeping and tissue specific interacting protein evolution. Gene 439:11–16

    PubMed  CAS  Google Scholar 

  • Popescu CE, Borza T, Bielawski JP, Lee RW (2006) Evolutionary rates and expression level in Chlamydomonas. Genetics 172:1567–1576

    PubMed  CAS  Google Scholar 

  • Prachumwat A, DeVincentis L, Palopoli MF (2004) Intron size correlates positively with recombination rate in Caenorhabditis elegans. Genetics 166:1585–1590

    PubMed  CAS  Google Scholar 

  • Precup J, Parker J (1987) Missense misreading of asparagine codons as a function of codon identity and context. J Biol Chem 262:11351–11355

    PubMed  CAS  Google Scholar 

  • Presgraves DC (2006) Intron length evolution in Drosophila. Mol Biol Evol 23:2203–2213

    PubMed  CAS  Google Scholar 

  • Ramsey DC, Scherrer MP, Zhou T, Wilke CO (2011) The relationship between relative solvent accessibility and evolutionary rate in protein evolution. Genetics 188:479–488

    PubMed  CAS  Google Scholar 

  • Rao YS, Wang ZF, Chai XW, Wu GZ, Zhou M, Nie QH, Zhang XQ (2010) Selection for the compactness of highly expressed genes in Gallus gallus. Biol Direct 5:35

    Google Scholar 

  • Razeto-Barry P, Diaz J, Cotoras D, Vasquez RA (2011) Molecular evolution, mutation size and gene pleiotropy: a geometric reexamination. Genetics 187:877–885

    PubMed  CAS  Google Scholar 

  • Ren XY, Vorst O, Fiers MW, Stiekema WJ, Nap JP (2006) In plants, highly expressed genes are the least compact. Trends Genet 22:528–532

    Google Scholar 

  • Rocha EP (2006) The quest for the universals of protein evolution. Trends Genet 22:412–416

    PubMed  CAS  Google Scholar 

  • Rocha EP, Danchin A (2004) An analysis of determinants of amino acids substitution rates in bacterial proteins. Mol Biol Evol 21:108–116

    PubMed  CAS  Google Scholar 

  • Rodgers-Melnick E, Mane SP, Dharmawardhana P, Slavov GT, Crasta OR, Strauss SH, Brunner AM, DiFazio SP (2012) Contrasting patterns of evolution following whole genome versus tandem duplication events in Populus. Genome Res 22:95–105

    PubMed  CAS  Google Scholar 

  • Saeed R, Deane CM (2006) Protein protein interactions, evolutionary rate, abundance and age. BMC Bioinformatics 7:128

    Google Scholar 

  • Sällström B, Arnaout RA, Davids W, Bjelkmar P, Andersson SG (2006) Protein evolutionary rates correlate with expression independently of synonymous substitutions in Helicobacter pylori. J Mol Evol 62:600–614

    Google Scholar 

  • Schaber J, Rispe C, Wernegreen J, Buness A, Delmotte F, Silva FJ, Moya A (2005) Gene expression levels influence amino acid usage and evolutionary rates in endosymbiotic bacteria. Gene 352:109–117

    Google Scholar 

  • Scholle MD, Gerdes SY (2008) Whole-genome detection of conditionally essential and dispensable genes in Escherichia coli via genetic footprinting. Methods Mol Biol 416:83–102

    PubMed  CAS  Google Scholar 

  • Shabalina SA, Ogurtsov AY, Spiridonov AN, Novichkov PS, Spiridonov NA, Koonin EV (2010) Distinct patterns of expression and evolution of intronless and intron-containing mammalian genes. Mol Biol Evol 27:1745–1749

    PubMed  CAS  Google Scholar 

  • Sharp PM, Stenico M, Peden JF, Lloyd AT (1993) Codon usage: mutational bias, translational selection, or both? Biochem Soc Trans 21:835–841

    PubMed  CAS  Google Scholar 

  • Stenoien HK (2007) Compact genes are highly expressed in the moss Physcomitrella patens. J Evol Biol 20:1223–1229

    PubMed  CAS  Google Scholar 

  • Stoletzki N, Eyre-Walker A (2007) Synonymous codon usage in Escherichia coli: selection for translational accuracy. Mol Biol Evol 24:374–381

    PubMed  CAS  Google Scholar 

  • Subramanian S, Kumar S (2004) Gene expression intensity shapes evolutionary rates of the proteins encoded by the vertebrate genome. Genetics 168:373–381

    PubMed  CAS  Google Scholar 

  • Teichmann SA (2002) The constraints protein–protein interactions place on sequence divergence. J Mol Biol 324:399–407

    PubMed  CAS  Google Scholar 

  • Toth-Petroczy A, Tawfik DS (2011) Slow protein evolutionary rates are dictated by surface-core association. Proc Natl Acad Sci USA 108:11151–11156

    PubMed  CAS  Google Scholar 

  • Tudor M, Murray PJ, Onufryk C, Jaenisch R, Young RA (1999) Ubiquitous expression and embryonic requirement for RNA polymerase II coactivator subunit Srb7 in mice. Genes Dev 13:2365–2368

    PubMed  CAS  Google Scholar 

  • Tuller T, Kupiec M, Ruppin E (2008) Evolutionary rate and gene expression across different brain regions. Genome Biol 9:R142

    PubMed  Google Scholar 

  • Urrutia AO, Hurst LD (2001) Codon usage bias covaries with expression breadth and the rate of synonymous evolution in humans, but this is not evidence for selection. Genetics 159:1191–1199

    PubMed  CAS  Google Scholar 

  • Urrutia AO, Hurst LD (2003) The signature of selection mediated by expression on human genes. Genome Res 13:2260–2264

    PubMed  CAS  Google Scholar 

  • Vinogradov AE (2001) Intron length and codon usage. J Mol Evol 52:2–5

    PubMed  CAS  Google Scholar 

  • Vinogradov AE (2004) Compactness of human housekeeping genes: selection for economy or genomic design? Trends Genet 20:248–253

    PubMed  CAS  Google Scholar 

  • Vinogradov AE (2006) “Genome design” model: evidence from conserved intronic sequence in human-mouse comparison. Genome Res 16:347–354

    PubMed  CAS  Google Scholar 

  • Vinogradov AE (2010) Systemic factors dominate mammal protein evolution. Proc R Soc B Biol Sci 277:1403–1408

    CAS  Google Scholar 

  • Wagner A (2005) Energy constraints on the evolution of gene expression. Mol Biol Evol 22:1365–1374

    PubMed  CAS  Google Scholar 

  • Waldman YY, Tuller T, Keinan A, Ruppin E (2011) Selection for translation efficiency on synonymous polymorphisms in recent human evolution. Genome Biol Evol 3:749–961

    PubMed  CAS  Google Scholar 

  • Wall DP, Hirsh AE, Fraser HB, Kumm J, Giaever G, Eisen MB, Feldman MW (2005) Functional genomic analysis of the rates of protein evolution. Proc Natl Acad Sci USA 102:5483–5488

    PubMed  CAS  Google Scholar 

  • Wang Z, Zhang J (2009) Why is the correlation between gene importance and gene evolutionary rate so weak? PLoS Genet 5:e1000329

    PubMed  Google Scholar 

  • Warringer J, Blomberg A (2006) Evolutionary constraints on yeast protein size. BMC Evol Biol 6:61

    PubMed  Google Scholar 

  • Wilke CO, Drummond DA (2006) Population genetics of translational robustness. Genetics 173:473–481

    PubMed  CAS  Google Scholar 

  • Wilson AC, Carlson SS, White TJ (1977) Biochemical evolution. Annu Rev Biochem 46:573–639

    PubMed  CAS  Google Scholar 

  • Wolf MY, Wolf YI, Koonin EV (2008) Comparable contributions of structural-functional constraints and expression level to the rate of protein sequence evolution. Biol Direct 3:40

    PubMed  Google Scholar 

  • Woody JL, Severin AJ, Bolon YT, Joseph B, Diers BW, Farmer AD, Weeks N, Muehlbauer GJ, Nelson RT, Grant D, Specht JE, Graham MA, Cannon SB, May GD, Vance CP, Shoemaker RC (2011) Gene expression patterns are correlated with genomic and genic structure in soybean. Genome 54:10–18

    PubMed  CAS  Google Scholar 

  • Wright SI, Yau CB, Looseley M, Meyers BC (2004) Effects of gene expression on molecular evolution in Arabidopsis thaliana and Arabidopsis lyrata. Mol Biol Evol 21:1719–1726

    PubMed  CAS  Google Scholar 

  • Wu GCT, Chen FC (2012) Determinants of exon-level evolutionary rates in Arabidopsis species. Evol Bioinf 8:389–415

    CAS  Google Scholar 

  • Wuchty S (2002) Interaction and domain networks of yeast. Proteomics 2:1715–1723

    PubMed  CAS  Google Scholar 

  • Yang J, Gu Z, Li WH (2003) Rate of protein evolution versus fitness effect of gene deletion. Mol Biol Evol 20:772–774

    PubMed  Google Scholar 

  • Yang J, Su AI, Li WH (2005) Gene expression evolves faster in narrowly than in broadly expressed mammalian genes. Mol Biol Evol 22:2113–2118

    PubMed  CAS  Google Scholar 

  • Yang JR, Liao BY, Zhuang SM, Zhang JZ (2012) Protein misinteraction avoidance causes highly expressed proteins to evolve slowly. Proc Natl Acad Sci USA 109:E831–E840

    PubMed  CAS  Google Scholar 

  • Yu H, Zhu X, Greenbaum D, Karro J, Gerstein M (2004) TopNet: a tool for comparing biological sub-networks, correlating protein properties with topological statistics. Nucleic Acids Res 32:328–337

    PubMed  CAS  Google Scholar 

  • Zeng Y, Gu X (2010) Genome factor and gene pleiotropy hypotheses in protein evolution. Biol Direct 5:37

    Google Scholar 

  • Zhang J, He X (2005) Significant impact of protein dispensability on the instantaneous rate of protein evolution. Mol Biol Evol 22:1147–1155

    PubMed  CAS  Google Scholar 

  • Zhang L, Li WH (2004) Mammalian housekeeping genes evolve more slowly than tissue-specific genes. Mol Biol Evol 21:236–239

    PubMed  Google Scholar 

  • Zhou T, Drummond DA, Wilke CO (2008) Contact density affects protein evolutionary rate from bacteria to animals. J Mol Evol 66:395–404

    PubMed  CAS  Google Scholar 

  • Zhou T, Weems M, Wilke CO (2009) Translationally optimal codons associate with structurally sensitive sites in proteins. Mol Biol Evol 26:1571–1580

    PubMed  CAS  Google Scholar 

  • Zhu J, He F, Hu S, Yu J (2008) On the nature of human housekeeping genes. Trends Genet 24:481–484

    PubMed  CAS  Google Scholar 

  • Zotenko E, Mestre J, O’Leary DP, Przytycka TM (2008) Why do hubs in the yeast protein interaction network tend to be essential: reexamining the connection between the network topology and essentiality. PLoS Comput Biol 4:e1000140

    PubMed  Google Scholar 

  • Zuckerkandl E (1976) Evolutionary processes and evolutionary noise at the molecular level. I. Functional density in proteins. J Mol Evol 7:167–183

    PubMed  CAS  Google Scholar 

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Acknowledgments

This research was supported by Kangwon National University and Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education, Science and Technology (NRF-2011-0010679). SH is funded by NIH R01GM085226. Authors would like to thank the anonymous reviewers for their very generous comments, and Dr. Leonid Sukharnikov and Justin Malin for additional comments on the revised version.

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Correspondence to Sun Shim Choi.

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Choi, S.S., Hannenhalli, S. Three Independent Determinants of Protein Evolutionary Rate. J Mol Evol 76, 98–111 (2013). https://doi.org/10.1007/s00239-013-9543-6

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