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Contact Density Affects Protein Evolutionary Rate from Bacteria to Animals

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Abstract

The density of contacts or the fraction of buried sites in a protein structure is thought to be related to a protein’s designability, and genes encoding more designable proteins should evolve faster than other genes. Several recent studies have tested this hypothesis but have found conflicting results. Here, we investigate how a gene’s evolutionary rate is affected by its protein’s contact density, considering the four species Escherichia coli, Saccharomyces cerevisiae, Drosophila melanogaster, and Homo sapiens. We find for all four species that contact density correlates positively with evolutionary rate, and that these correlations do not seem to be confounded by gene expression level. The strength of this signal, however, varies widely among species. We also study the effect of contact density on domain evolution in multidomain proteins and find that a domain’s contact density influences the domain’s evolutionary rate. Within the same protein, a domain with higher contact density tends to evolve faster than a domain with lower contact density. Our study provides evidence that contact density can increase evolutionary rates, and that it acts similarly on the level of entire proteins and of individual protein domains.

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References

  • Agrafioti I, Swire J, Abbott J, Huntley D, Butcher S, Stumpf MPH (2005) Comparative analysis of the Saccharomyces cerevisiae and Caenorhabditis elegans protein interaction networks. BMC Evol Biol 5:23

    Article  PubMed  CAS  Google Scholar 

  • Appelgren H, Kniola B, Ekwall K (2003) Distinct centromere domain structures with separate functions demonstrated in live fission yeast cells. J Cell Sci 116:4035–4042

    Article  PubMed  CAS  Google Scholar 

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy tat Soc B 57:289–300

    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

    Article  PubMed  Google Scholar 

  • Bloom JD, Drummond DA, Arnold FH, Wilke CO (2006) Structural determinants of the rate of protein evolution in yeast. Mol Biol Evol 23:1751–1761

    Article  PubMed  CAS  Google Scholar 

  • Bloom JD, Silberg JJ, Wilke CO, Drummond DA, Adami C, Arnold FH (2005) Thermodynamic prediction of protein neutrality. Proc Natl Acad Sci USA 102:606–611

    Article  PubMed  CAS  Google Scholar 

  • Covert MW, Knight EM, Reed JL, Herrgard MJ, Palsson BO (2004) Integrating high-throughput and computational data elucidates bacterial networks. Nature 429:92–96

    Article  PubMed  CAS  Google Scholar 

  • Creighton TE (1992) Proteins: structures and molecular properties, 2nd edn. Freeman, New York

    Google Scholar 

  • Dean AM, Neuhauser C, Grenier E, Golding GB (2002) The pattern of amino acid replacements in α\β-barrels. Mol Biol Evol 19:1846–1864

    PubMed  CAS  Google Scholar 

  • Dietmann S, Park J, Notredame C, Heger A, Lappe M, Holm L (2001) A fully automatic evolutionary classification of protein folds: Dali domain dictionary version 3. Nucleic Acids Res 29:55–57

    Article  PubMed  CAS  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

    Article  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

    Article  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

    Article  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 

  • Edgar RC (2004) Muscle: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    Article  PubMed  CAS  Google Scholar 

  • England JL, Shakhnovich EI (2003) Structural determinant of protein designability. Phys Rev Lett 90:218101

    Article  PubMed  CAS  Google Scholar 

  • England JL, Shakhnovich BE, Shakhnovich EI (2003) Natural selection of more designable folds: a mechanism for thermophilic adaptation. Proc Natl Acad Sci USA 100:8727–8731

    Article  PubMed  CAS  Google Scholar 

  • Fraser HB (2005) Modularity and evolutionary constraint on proteins. Nature Genet 37:351–352

    Article  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

    Article  PubMed  CAS  Google Scholar 

  • Goldman N, Thorne JL, Jones DT (1998) Assessing the impact of secondary structure and solvent accessibility on protein evolution. Genetics 149:445–458

    PubMed  CAS  Google Scholar 

  • Gu W, Zhou T, Ma J, Sun X, Lu Z (2004) The relationship between synonymous codon usage and protein structure in Escherichia coli and Homo sapiens. Biosystems 73:89–97

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Hakes L, Lovell SC, Oliver SG, Robertson DL (2007) Specificity in protein interactions and its relationship with sequence diversity and coevolution. Proc Natl Acad Sci USA 104:7999–8004

    Article  PubMed  CAS  Google Scholar 

  • Herbeck JT, Wall DP, Wernegreen JJ (2003) Gene expression level influences amino acid usage, but not codon usage, in the tsetse fly endosymbiont Wigglesworthia. Microbiology 149:2585–2596

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Holstege FCP, Jennings E, Wyrick JJ, Lee TI, Hengartner CJ, Green MR, Golub TR, Lander ES, Young RA (1998) Dissecting the regulatory circuitry of a eukaryotic genome. Cell 95:717–728

    Article  PubMed  CAS  Google Scholar 

  • Holstein SE, Ungewickell H, Ungewickell E (1996) Mechanism of clathrin basket dissociation: separate functions of protein domains of the DnaJ homologue auxilin. J Cell Biol 135:925–937

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Ihaka R, Gentleman R (1996) R: a language for data analysis and graphics. J Comput Graph Stat 5:299–314

    Article  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

    Article  PubMed  CAS  Google Scholar 

  • Kabsch W, Sander C (1983) Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22:2577–2637

    Article  PubMed  CAS  Google Scholar 

  • Kawabata T, Fukuchi S, Homma K, Ota M, Araki J, Ito T, Ichiyoshi N, Nishikawa K (2002) Gtop: a database of protein structures predicted from genome sequence. Nucleic Acids Res 30:294–298

    Article  PubMed  CAS  Google Scholar 

  • Kim PM, Lu LJ, Gerstein MB (2006) Relating three-dimensional structures to protein networks provides evolutionary insights. Science 314:1882–1883

    Article  Google Scholar 

  • Koshi JM, Goldstein RA (1995) Context-dependent optimal substitution matrices. Protein Eng 8:641–645

    Article  PubMed  CAS  Google Scholar 

  • Kussell E (2005) The designability hypothesis and protein evolution. Protein Peptide Lett 12:111–116

    Article  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

    Article  PubMed  CAS  Google Scholar 

  • Li H, Helling R, Tang C, Wingreen N (1996) Emergence of preferred structures in a simple model of protein folding. Science 273:666–669

    Article  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

    Article  PubMed  CAS  Google Scholar 

  • Mandel J (1982) Use of the singular value decomposition in regression analysis. Am Stat 36:15–24

    Article  Google Scholar 

  • Marais G, Duret L (2001) Synonymous codon usage, accuracy of translation, and gene length in Caenorhabditis elegans. J Mol Evol 52:275–280

    PubMed  CAS  Google Scholar 

  • Meyerguz L, Kleinberg J, Elber R (2007) The network of sequence flow between protein structures. Proc Natl Acad Sci USA 104:11627–11632

    Article  PubMed  CAS  Google Scholar 

  • Mintseris J, Weng Z (2005) Structure, function, and evolution of transient and obligate protein-protein interactions. Proc Natl Acad Sci USA 102:10930–10935

    Article  PubMed  CAS  Google Scholar 

  • Mirny LA, Shakhnovich EI (1999) Universally conserved positions in protein folds: reading evolutionary signals about stability, folding kinetics and function. J Mol Biol 291:177–196

    Article  PubMed  CAS  Google Scholar 

  • Orešič M, Shalloway D (1998) Specific correlations between relative synonymous codon usage and protein secondary structure. J Mol Biol 281:31–48

    Article  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, Hurst LD (2003) Rate of evolution and gene dispensability. Nature 421:496–497

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Ren M, Villamarin A, Shih A, Coutavas E, Moore MS, LoCurcio M, Clarke V, Oppenheim JD, D’Eustachio P, Rush MG (1995) Separate domains of the Ran GTPase interact with different factors to regulate nuclear protein import and RNA processing. Mol Cell Biol 15:2117–2124

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Shakhnovich BE (2006) Relative contributions of structural designability and functional diversity in molecular evolution of duplicates. Bioinformatics 22:e440–e445

    Article  PubMed  CAS  Google Scholar 

  • Shakhnovich BE, Deeds E, Delisi C, Shakhnovich E (2005) Protein structure and evolutionary history determine sequence space topology. Genome Res 15:385–392

    Article  PubMed  CAS  Google Scholar 

  • Shakhnovich EI (1998) Protein design: a perspective from simple tractable models. Fold Des 3:R45–R58

    Article  CAS  Google Scholar 

  • Stolc V, Gauhar Z, Mason C, Halasz G, van Batenburg MF, Rifkin SA, Hua S, Herreman T, Tongprasit W, Barbano PE, Bussemaker HJ, White KP (2004) A gene expression map for the euchromatic genome of Drosophila melanogaster. Science 306:655–660

    Article  PubMed  CAS  Google Scholar 

  • Su AI, Wiltshire T, Batalov S, Lapp H, Ching KA, Block D, Zhang J, Soden R, Hayakawa M, Kreiman G, Cooke MP, Walker JR, Hogenesch JB (2004) A gene atlas of the mouse and human protein-encoding transcriptomes. Proc Natl Acad Sci USA 101:6062–6067

    Article  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

    Article  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

    Article  PubMed  CAS  Google Scholar 

  • Wolynes PG (1996) Symmetry and the energy landscapes of biomolecules. Proc Natl Acad Sci USA 93:14249–14255

    Article  PubMed  CAS  Google Scholar 

  • Yang ZH (1997) PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 13:555–556

    PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This work was supported by NIH Grant AI 065960. D.A.D. received support through an NIH center grant to the FAS Center for Systems Biology. We would like to thank Jesse Bloom for helpful comments on this work.

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Authors and Affiliations

  1. Center for Computational Biology and Bioinformatics, Section of Integrative Biology, University of Texas at Austin, Austin, TX, 78731, USA

    Tong Zhou & Claus O. Wilke

  2. FAS Center for Systems Biology, Harvard University, Cambridge, MA, 02138, USA

    D. Allan Drummond

  3. Institute for Cell and Molecular Biology, University of Texas at Austin, Austin, TX, 78731, USA

    Claus O. Wilke

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  1. Tong Zhou
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  2. D. Allan Drummond
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Correspondence to Claus O. Wilke.

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Zhou, T., Drummond, D.A. & Wilke, C.O. Contact Density Affects Protein Evolutionary Rate from Bacteria to Animals. J Mol Evol 66, 395–404 (2008). https://doi.org/10.1007/s00239-008-9094-4

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  • DOI: https://doi.org/10.1007/s00239-008-9094-4

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