MBE Advance Access originally published online on October 19, 2005
Molecular Biology and Evolution 2006 23(2):327-337; doi:10.1093/molbev/msj038
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
Research Article |
A Single Determinant Dominates the Rate of Yeast Protein Evolution
,

* Program in Computation and Neural Systems, California Institute of Technology, Pasadena;
Keck Graduate Institute, Claremont;
School of Mathematical Sciences, Claremont Graduate University; and
Section of Integrative Biology and Center for Computational Biology and Bioinformatics, University of Texas at Austin
E-mail: cwilke{at}mail.utexas.edu.
A gene's rate of sequence evolution is among the most fundamental evolutionary quantities in common use, but what determines evolutionary rates has remained unclear. Here, we carry out the first combined analysis of seven predictors (gene expression level, dispensability, protein abundance, codon adaptation index, gene length, number of protein-protein interactions, and the gene's centrality in the interaction network) previously reported to have independent influences on protein evolutionary rates. Strikingly, our analysis reveals a single dominant variable linked to the number of translation events which explains 40-fold more variation in evolutionary rate than any other, suggesting that protein evolutionary rate has a single major determinant among the seven predictors. The dominant variable explains nearly half the variation in the rate of synonymous and protein evolution. We show that the two most commonly used methods to disentangle the determinants of evolutionary rate, partial correlation analysis and ordinary multivariate regression, produce misleading or spurious results when applied to noisy biological data. We overcome these difficulties by employing principal component regression, a multivariate regression of evolutionary rate against the principal components of the predictor variables. Our results support the hypothesis that translational selection governs the rate of synonymous and protein sequence evolution in yeast.
Key Words: Saccharomyces cerevisiae evolutionary rate gene expression protein-protein interactions dispensability translational selection
![]()
CiteULike
Connotea
Del.icio.us What's this?
This article has been cited by other articles:
![]() |
B.-Y. Liao, M.-P. Weng, and J. Zhang Impact of Extracellularity on the Evolutionary Rate of Mammalian Proteins Gen Biol Evol, January 22, 2010; 2010(0): 39 - 43. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. E. Vinogradov Systemic factors dominate mammal protein evolution Proc R Soc B, January 6, 2010; (2010) rspb.2009.1865v1. [Abstract] [Full Text] [PDF] |
||||
![]() |
K. Livingstone and S. Anderson Patterns of Variation in the Evolution of Carotenoid Biosynthetic Pathway Enzymes of Higher Plants J. Hered., November 1, 2009; 100(6): 754 - 761. [Abstract] [Full Text] [PDF] |
||||
![]() |
R. Carter and G. Drouin The Evolutionary Rates of Eukaryotic RNA Polymerases and of Their Transcription Factors Are Affected by the Level of Concerted Evolution of the Genes They Transcribe Mol. Biol. Evol., November 1, 2009; 26(11): 2515 - 2520. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. A. Franzosa and Y. Xia Structural Determinants of Protein Evolution Are Context-Sensitive at the Residue Level Mol. Biol. Evol., October 1, 2009; 26(10): 2387 - 2395. [Abstract] [Full Text] [PDF] |
||||
![]() |
C. C. Weber and L. D. Hurst Protein Rates of Evolution Are Predicted by Double-Strand Break Events, Independent of Crossing-over Rates Gen Biol Evol, September 23, 2009; 2009(0): 340 - 349. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. Melamud and J. Moult Stochastic noise in splicing machinery Nucleic Acids Res., August 1, 2009; 37(14): 4873 - 4886. [Abstract] [Full Text] [PDF] |
||||
![]() |
T. Zhou, M. Weems, and C. O. Wilke Translationally Optimal Codons Associate with Structurally Sensitive Sites in Proteins Mol. Biol. Evol., July 1, 2009; 26(7): 1571 - 1580. [Abstract] [Full Text] [PDF] |
||||
![]() |
Y. I. Wolf, P. S. Novichkov, G. P. Karev, E. V. Koonin, and D. J. Lipman Inaugural Article: The universal distribution of evolutionary rates of genes and distinct characteristics of eukaryotic genes of different apparent ages PNAS, May 5, 2009; 106(18): 7273 - 7280. [Abstract] [Full Text] [PDF] |
||||
![]() |
G. C. Conant and P. F. Stadler Solvent Exposure Imparts Similar Selective Pressures across a Range of Yeast Proteins Mol. Biol. Evol., May 1, 2009; 26(5): 1155 - 1161. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. V. Koonin Darwinian evolution in the light of genomics Nucleic Acids Res., March 1, 2009; 37(4): 1011 - 1034. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. X. C. N. Valente, S. B. Roberts, G. A. Buck, and Y. Gao Functional organization of the yeast proteome by a yeast interactome map PNAS, February 3, 2009; 106(5): 1490 - 1495. [Abstract] [Full Text] [PDF] |
||||
![]() |
D. Alvarez-Ponce, M. Aguade, and J. Rozas Network-level molecular evolutionary analysis of the insulin/TOR signal transduction pathway across 12 Drosophila genomes Genome Res., February 1, 2009; 19(2): 234 - 242. [Abstract] [Full Text] [PDF] |
||||
![]() |
P. Mukhopadhyay, S. Basak, and T. C. Ghosh Differential Selective Constraints Shaping Codon Usage Pattern of Housekeeping and Tissue-specific Homologous Genes of Rice and Arabidopsis DNA Res, December 1, 2008; 15(6): 347 - 356. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. J. Greenberg, S. R. Stockwell, and A. G. Clark Evolutionary Constraint and Adaptation in the Metabolic Network of Drosophila Mol. Biol. Evol., December 1, 2008; 25(12): 2537 - 2546. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. M. Guisinger, J. V. Kuehl, J. L. Boore, and R. K. Jansen Genome-wide analyses of Geraniaceae plastid DNA reveal unprecedented patterns of increased nucleotide substitutions PNAS, November 25, 2008; 105(47): 18424 - 18429. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. K. Holloway, D. J. Begun, A. Siepel, and K. S. Pollard Accelerated sequence divergence of conserved genomic elements in Drosophila melanogaster Genome Res., October 1, 2008; 18(10): 1592 - 1601. [Abstract] [Full Text] [PDF] |
||||
![]() |
G. C. Conant and K. H. Wolfe Probabilistic Cross-Species Inference of Orthologous Genomic Regions Created by Whole-Genome Duplication in Yeast Genetics, July 1, 2008; 179(3): 1681 - 1692. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. Semon and K. H. Wolfe Preferential subfunctionalization of slow-evolving genes after allopolyploidization in Xenopus laevis PNAS, June 17, 2008; 105(24): 8333 - 8338. [Abstract] [Full Text] [PDF] |
||||
![]() |
G. M. Cooper and C. D. Brown Qualifying the relationship between sequence conservation and molecular function Genome Res., February 1, 2008; 18(2): 201 - 205. [Abstract] [Full Text] [PDF] |
||||
![]() |
D. R. Scannell and K. H. Wolfe A burst of protein sequence evolution and a prolonged period of asymmetric evolution follow gene duplication in yeast Genome Res., January 1, 2008; 18(1): 137 - 147. [Abstract] [Full Text] [PDF] |
||||
![]() |
L. Carmel, I. B. Rogozin, Y. I. Wolf, and E. V. Koonin Evolutionarily conserved genes preferentially accumulate introns Genome Res., July 1, 2007; 17(7): 1045 - 1050. [Abstract] [Full Text] [PDF] |
||||
![]() |
L. Hakes, S. C. Lovell, S. G. Oliver, and D. L. Robertson Specificity in protein interactions and its relationship with sequence diversity and coevolution PNAS, May 8, 2007; 104(19): 7999 - 8004. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. B. Plotkin and H. B. Fraser Assessing the Determinants of Evolutionary Rates in the Presence of Noise Mol. Biol. Evol., May 1, 2007; 24(5): 1113 - 1121. [Abstract] [Full Text] [PDF] |
||||
![]() |
Y.-S. Lin, W.-L. Hsu, J.-K. Hwang, and W.-H. Li Proportion of Solvent-Exposed Amino Acids in a Protein and Rate of Protein Evolution Mol. Biol. Evol., April 1, 2007; 24(4): 1005 - 1011. [Abstract] [Full Text] [PDF] |
||||
![]() |
B. P. Cusack and K. H. Wolfe Not Born Equal: Increased Rate Asymmetry in Relocated and Retrotransposed Rodent Gene Duplicates Mol. Biol. Evol., March 1, 2007; 24(3): 679 - 686. [Abstract] [Full Text] [PDF] |
||||
![]() |
P. K. Ingvarsson Gene Expression and Protein Length Influence Codon Usage and Rates of Sequence Evolution in Populus tremula Mol. Biol. Evol., March 1, 2007; 24(3): 836 - 844. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. K. Choi, S. C. Kim, J. Seo, S. Kim, and J. Bhak Impact of Transcriptional Properties on Essentiality and Evolutionary Rate Genetics, January 1, 2007; 175(1): 199 - 206. [Abstract] [Full Text] [PDF] |
||||
![]() |
B. E. Shakhnovich and E. V. Koonin Origins and impact of constraints in evolution of gene families Genome Res., December 1, 2006; 16(12): 1529 - 1536. [Abstract] [Full Text] [PDF] |
||||
![]() |
B.-Y. Liao, N. M. Scott, and J. Zhang Impacts of Gene Essentiality, Expression Pattern, and Gene Compactness on the Evolutionary Rate of Mammalian Proteins Mol. Biol. Evol., November 1, 2006; 23(11): 2072 - 2080. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. D. Bloom, D. A. Drummond, F. H. Arnold, and C. O. Wilke Structural Determinants of the Rate of Protein Evolution in Yeast Mol. Biol. Evol., September 1, 2006; 23(9): 1751 - 1761. [Abstract] [Full Text] [PDF] |
||||
![]() |
X. He and J. Zhang Toward a Molecular Understanding of Pleiotropy Genetics, August 1, 2006; 173(4): 1885 - 1891. [Abstract] [Full Text] [PDF] |
||||
![]() |
B.-Y. Liao and J. Zhang Low Rates of Expression Profile Divergence in Highly Expressed Genes and Tissue-Specific Genes During Mammalian Evolution Mol. Biol. Evol., June 1, 2006; 23(6): 1119 - 1128. [Abstract] [Full Text] [PDF] |
||||
![]() |
C. O. Wilke and D. A. Drummond Population Genetics of Translational Robustness Genetics, May 1, 2006; 173(1): 473 - 481. [Abstract] [Full Text] [PDF] |
||||
![]() |
S.-H. Kim and S. V. Yi Correlated Asymmetry of Sequence and Functional Divergence Between Duplicate Proteins of Saccharomyces cerevisiae Mol. Biol. Evol., May 1, 2006; 23(5): 1068 - 1075. [Abstract] [Full Text] [PDF] |
||||








