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PMID: 20044587 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

A novel method to detect proteins evolving at correlated rates: identifying new functional relationships between coevolving proteins.

Molecular biology and evolution ·Vol. 27 ·No. 5 ·2010-05-00 ·Pages 1152-61

Clark NL, Aquadro CF

Abstract

Interacting proteins evolve at correlated rates, possibly as the result of evolutionary pressures shared by functional groups and/or coevolution between interacting proteins. This evolutionary signature can be exploited to learn more about protein networks and to infer functional relationships between proteins on a genome-wide scale. Multiple methods have been introduced that detect correlated evolution using amino acid distances. One assumption made by these methods is that the neutral rate of nucleotide substitution is uniform over time; however, this is unlikely and such rate heterogeneity would adversely affect amino acid distance methods. We explored alternative methods that detect correlated rates using protein-coding nucleotide sequences in order to better estimate the rate of nonsynonymous substitution at each branch (d(N)) normalized by the underlying synonymous substitution rate (d(S)). Our novel likelihood method, which was robust to realistic simulation parameters, was tested on Drosophila nuclear pore proteins, which form a complex with well-documented physical interactions. The method revealed significantly correlated evolution between nuclear pore proteins, where members of a stable subcomplex showed stronger correlations compared with those proteins that interact transiently. Furthermore, our likelihood approach was better able to detect correlated evolution among closely related species than previous methods. Hence, these sequence-based methods are a complementary approach for detecting correlated evolution and could be applied genome-wide to provide candidate protein-protein interactions and functional group assignments using just coding sequences.

MeSH Terms
Animals Computer Simulation Databases, Protein Drosophila/genetics Drosophila Proteins/genetics,metabolism Evolution, Molecular Likelihood Functions Models, Genetic Nuclear Pore Complex Proteins/genetics,metabolism Phylogeny Sequence Analysis, Protein/methods
Chemicals
Drosophila Proteins Nuclear Pore Complex Proteins
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Clark Nathaniel L
Department of Molecular Biology and Genetics, Cornell University, USA. [email protected]
Aquadro Charles F
References (48)
48 references, click to expand
  1. DNA variability and divergence at the notch locus in Drosophila melanogaster and D. simulans: a case of accelerated synonymous site divergence.
    Genetics. 2004 May;167(1):171-85 PMID: 15166145
  2. Mutation rate variation in the mammalian genome.
    Curr Opin Genet Dev. 2003 Dec;13(6):562-8 PMID: 14638315
  3. Hearing silence: non-neutral evolution at synonymous sites in mammals.
    Nat Rev Genet. 2006 Feb;7(2):98-108 PMID: 16418745
  4. Evolution of reproductive proteins from animals and plants.
    Reproduction. 2006 Jan;131(1):11-22 PMID: 16388004
  5. PAML 4: phylogenetic analysis by maximum likelihood.
    Mol Biol Evol. 2007 Aug;24(8):1586-91 PMID: 17483113
  6. Strong evidence for lineage and sequence specificity of substitution rates and patterns in Drosophila.
    Mol Biol Evol. 2009 Jul;26(7):1591-605 PMID: 19351792
  7. Coevolution of gene expression among interacting proteins.
    Proc Natl Acad Sci U S A. 2004 Jun 15;101(24):9033-8 PMID: 15175431
  8. Dynamic nuclear pore complexes: life on the edge.
    Cell. 2006 Jun 16;125(6):1041-53 PMID: 16777596
  9. Exploiting the co-evolution of interacting proteins to discover interaction specificity.
    J Mol Biol. 2003 Mar 14;327(1):273-84 PMID: 12614624
  10. Structure, function, and evolution of transient and obligate protein-protein interactions.
    Proc Natl Acad Sci U S A. 2005 Aug 2;102(31):10930-5 PMID: 16043700
  11. Determinants of substitution rates in mammalian genes: expression pattern affects selection intensity but not mutation rate.
    Mol Biol Evol. 2000 Jan;17(1):68-74 PMID: 10666707
  12. Co-evolutionary analysis reveals insights into protein-protein interactions.
    J Mol Biol. 2002 Nov 15;324(1):177-92 PMID: 12421567
  13. A codon-based model of nucleotide substitution for protein-coding DNA sequences.
    Mol Biol Evol. 1994 Sep;11(5):725-36 PMID: 7968486
  14. Maximum likelihood estimation of ancestral codon usage bias parameters in Drosophila.
    Mol Biol Evol. 2007 Jan;24(1):228-35 PMID: 17041152
  15. Co-evolution of proteins with their interaction partners.
    J Mol Biol. 2000 Jun 2;299(2):283-93 PMID: 10860738
  16. Correlated mutations contain information about protein-protein interaction.
    J Mol Biol. 1997 Aug 29;271(4):511-23 PMID: 9281423
  17. Similarity of phylogenetic trees as indicator of protein-protein interaction.
    Protein Eng. 2001 Sep;14(9):609-14 PMID: 11707606
  18. A relationship between gene expression and protein interactions on the proteome scale: analysis of the bacteriophage T7 and the yeast Saccharomyces cerevisiae.
    Nucleic Acids Res. 2001 Sep 1;29(17):3513-9 PMID: 11522820
  19. Cellular reactions to gene dosage imbalance: genomic, transcriptomic and proteomic effects.
    Trends Genet. 2008 Aug;24(8):390-7 PMID: 18585818
  20. High-confidence prediction of global interactomes based on genome-wide coevolutionary networks.
    Proc Natl Acad Sci U S A. 2008 Jan 22;105(3):934-9 PMID: 18199838
  21. A single determinant dominates the rate of yeast protein evolution.
    Mol Biol Evol. 2006 Feb;23(2):327-37 PMID: 16237209
  22. Patterns of mutation and selection at synonymous sites in Drosophila.
    Mol Biol Evol. 2007 Dec;24(12):2687-97 PMID: 18000010
  23. Locus-specific decoupling of base composition evolution at synonymous sites and introns along the Drosophila melanogaster and Drosophila sechellia lineages.
    Genome Biol Evol. 2009 May 25;1:67-74 PMID: 20333178
  24. Why highly expressed proteins evolve slowly.
    Proc Natl Acad Sci U S A. 2005 Oct 4;102(40):14338-43 PMID: 16176987
  25. ROCR: visualizing classifier performance in R.
    Bioinformatics. 2005 Oct 15;21(20):3940-1 PMID: 16096348
  26. Evolution of genes and genomes on the Drosophila phylogeny.
    Nature. 2007 Nov 8;450(7167):203-18 PMID: 17994087
  27. Adaptive evolution drives divergence of a hybrid inviability gene between two species of Drosophila.
    Nature. 2003 Jun 12;423(6941):715-9 PMID: 12802326
  28. Evolution of protein-coding genes in Drosophila.
    Trends Genet. 2008 Mar;24(3):114-23 PMID: 18249460
  29. Specificity in protein interactions and its relationship with sequence diversity and coevolution.
    Proc Natl Acad Sci U S A. 2007 May 8;104(19):7999-8004 PMID: 17468399
  30. Modular self-assembly of a Y-shaped multiprotein complex from seven nucleoporins.
    EMBO J. 2002 Feb 1;21(3):387-97 PMID: 11823431
  31. Positive selection of yeast nonhomologous end-joining genes and a retrotransposon conflict hypothesis.
    Proc Natl Acad Sci U S A. 2006 Nov 21;103(47):17614-9 PMID: 17101967
  32. Evolution of the Drosophila nuclear pore complex results in multiple hybrid incompatibilities.
    Science. 2009 Feb 6;323(5915):779-82 PMID: 19197064
  33. Correlation between transcriptome and interactome mapping data from Saccharomyces cerevisiae.
    Nat Genet. 2001 Dec;29(4):482-6 PMID: 11694880
  34. Cluster analysis and display of genome-wide expression patterns.
    Proc Natl Acad Sci U S A. 1998 Dec 8;95(25):14863-8 PMID: 9843981
  35. Molecular phylogeny of the Drosophila melanogaster species subgroup.
    J Mol Evol. 2003 Nov;57(5):562-73 PMID: 14738315
  36. Gene expression intensity shapes evolutionary rates of the proteins encoded by the vertebrate genome.
    Genetics. 2004 Sep;168(1):373-81 PMID: 15454550
  37. Assessing protein co-evolution in the context of the tree of life assists in the prediction of the interactome.
    J Mol Biol. 2005 Sep 30;352(4):1002-15 PMID: 16139301
  38. Coevolution of interacting fertilization proteins.
    PLoS Genet. 2009 Jul;5(7):e1000570 PMID: 19629160
  39. Comparing patterns of natural selection across species using selective signatures.
    PLoS Genet. 2008 Feb;4(2):e23 PMID: 18266472
  40. Steady progress and recent breakthroughs in the accuracy of automated genome annotation.
    Nat Rev Genet. 2008 Jan;9(1):62-73 PMID: 18087260
  41. Highly expressed genes in yeast evolve slowly.
    Genetics. 2001 Jun;158(2):927-31 PMID: 11430355
  42. Novel vertebrate nucleoporins Nup133 and Nup160 play a role in mRNA export.
    J Cell Biol. 2001 Oct 29;155(3):339-54 PMID: 11684705
  43. ADVICE: Automated Detection and Validation of Interaction by Co-Evolution.
    Nucleic Acids Res. 2004 Jul 1;32(Web Server issue):W69-72 PMID: 15215353
  44. Phylogenetic incongruence in the Drosophila melanogaster species group.
    Mol Phylogenet Evol. 2007 Jun;43(3):1138-50 PMID: 17071113
  45. The inference of protein-protein interactions by co-evolutionary analysis is improved by excluding the information about the phylogenetic relationships.
    Bioinformatics. 2005 Sep 1;21(17):3482-9 PMID: 15994190
  46. HyPhy: hypothesis testing using phylogenies.
    Bioinformatics. 2005 Mar 1;21(5):676-9 PMID: 15509596
  47. Pervasive adaptive evolution among interactors of the Drosophila hybrid inviability gene, Nup96.
    Mol Biol Evol. 2007 Jan;24(1):306-14 PMID: 17056646
  48. A likelihood approach for comparing synonymous and nonsynonymous nucleotide substitution rates, with application to the chloroplast genome.
    Mol Biol Evol. 1994 Sep;11(5):715-24 PMID: 7968485
Article Info
Journal
Molecular biology and evolution
Abbr.
Mol Biol Evol
ISSN
1537-1719
Published
2010-05-00
Epub
2009-00-31
Pages
1152-61
Language
English
Region
United States
NLM ID
8501455
PMCID
PMC2877527
Subset
IM
Grants
NIGMS NIH HHS · F32 GM084592 · United States
NIGMS NIH HHS · R01 GM036431 · United States
NIGMS NIH HHS · GM36431 · United States
NIGMS NIH HHS · GM084592 · United States
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