Molecular Biology and Evolution 17:68-070 (2000)
© 2000 Society for Molecular Biology and Evolution
Article |
Determinants of Substitution Rates in Mammalian Genes: Expression Pattern Affects Selection Intensity but Not Mutation Rate
Laboratoire de Biométrie, Génétique et Biologie des Populations, Unité Mixte de Recherche Centre National de la Recherche Scientifique 5558, Université Claude Bernard, Villeurbanne, France
To determine whether gene expression patterns affect mutation rates and/or selection intensity in mammalian genes, we studied the relationships between substitution rates and tissue distribution of gene expression. For this purpose, we analyzed 2,400 human/rodent and 834 mouse/rat orthologous genes, and we measured (using expressed sequence tag data) their expression patterns in 19 tissues from three development states. We show that substitution rates at nonsynonymous sites are strongly negatively correlated with tissue distribution breadth: almost threefold lower in ubiquitous than in tissue-specific genes. Nonsynonymous substitution rates also vary considerably according to the tissues: the average rate is twofold lower in brain-, muscle-, retina- and neuron-specific genes than in lymphocyte-, lung-, and liver-specific genes. Interestingly, 5' and 3' untranslated regions (UTRs) show exactly the same trend. These results demonstrate that the expression pattern is an essential factor in determining the selective pressure on functional sites in both coding and noncoding regions. Conversely, silent substitution rates do not vary with expression pattern, even in ubiquitously expressed genes. This latter result thus suggests that synonymous codon usage is not constrained by selection in mammals. Furthermore, this result also indicates that there is no reduction of mutation rates in genes expressed in the germ line, contrary to what had been hypothesized based on the fact that transcribed DNA is more efficiently repaired than nontranscribed DNA.
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  T. Kasuga and N. L. Glass Dissecting Colony Development of Neurospora crassa Using mRNA Profiling and Comparative Genomics Approaches Eukaryot. Cell, September 1, 2008; 7(9): 1549 - 1564. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 L. M. Turner, E. B. Chuong, and H. E. Hoekstra Comparative Analysis of Testis Protein Evolution in Rodents Genetics, August 1, 2008; 179(4): 2075 - 2089. [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]
|
|
|
|
 |
|
 K. Bullaughey, M. Przeworski, and G. Coop No effect of recombination on the efficacy of natural selection in primates Genome Res., April 1, 2008; 18(4): 544 - 554. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Subramanian Nearly Neutrality and the Evolution of Codon Usage Bias in Eukaryotic Genomes Genetics, April 1, 2008; 178(4): 2429 - 2432. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 E. W. Ganko, B. C. Meyers, and T. J. Vision Divergence in Expression between Duplicated Genes in Arabidopsis Mol. Biol. Evol., October 1, 2007; 24(10): 2298 - 2309. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
I. Gitelman Evolution of the vertebrate twist family and synfunctionalization: a mechanism for differential gene loss through merging of expression domains Mol. Biol. Evol., September 1, 2007; 24(9): 1912 - 1925. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
N. Osada Inference of Expression-Dependent Negative Selection Based on Polymorphism and Divergence in the Human Genome Mol. Biol. Evol., August 1, 2007; 24(8): 1622 - 1626. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. M. Resch, L. Carmel, L. Marino-Ramirez, A. Y. Ogurtsov, S. A. Shabalina, I. B. Rogozin, and E. V. Koonin Widespread Positive Selection in Synonymous Sites of Mammalian Genes Mol. Biol. Evol., August 1, 2007; 24(8): 1821 - 1831. [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. E. Mank, E. Axelsson, and H. Ellegren Fast-X on the Z: Rapid evolution of sex-linked genes in birds Genome Res., May 1, 2007; 17(5): 618 - 624. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 N. Georgelis, E. L. Braun, J. R. Shaw, and L. C. Hannah The Two AGPase Subunits Evolve at Different Rates in Angiosperms, yet They Are Equally Sensitive to Activity-Altering Amino Acid Changes When Expressed in Bacteria PLANT CELL, May 1, 2007; 19(5): 1458 - 1472. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 H. Anthoni, M. Zucchelli, H. Matsson, B. Muller-Myhsok, I. Fransson, J. Schumacher, S. Massinen, P. Onkamo, A. Warnke, H. Griesemann, et al. A locus on 2p12 containing the co-regulated MRPL19 and C2ORF3 genes is associated to dyslexia Hum. Mol. Genet., March 15, 2007; 16(6): 667 - 677. [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]
|
|
|
|
|
|
X. Gu and Z. Su Tissue-driven hypothesis of genomic evolution and sequence-expression correlations PNAS, February 20, 2007; 104(8): 2779 - 2784. [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]
|
|
|
|
|
|
A. Aouacheria, C. Geourjon, N. Aghajari, V. Navratil, G. Deleage, C. Lethias, and J.-Y. Exposito Insights into Early Extracellular Matrix Evolution: Spongin Short Chain Collagen-Related Proteins Are Homologous to Basement Membrane Type IV Collagens and Form a Novel Family Widely Distributed in Invertebrates Mol. Biol. Evol., December 1, 2006; 23(12): 2288 - 2302. [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]
|
|
|
|
|
|
K. Julenius and A. G. Pedersen Protein Evolution Is Faster Outside the Cell Mol. Biol. Evol., November 1, 2006; 23(11): 2039 - 2048. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. P. Ponting and G. Lunter Signatures of adaptive evolution within human non-coding sequence Hum. Mol. Genet., October 15, 2006; 15(suppl_2): R170 - R175. [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]
|
|
|
|
|
|
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]
|
|
|
|
|
|
C. E. Popescu, T. Borza, J. P. Bielawski, and R. W. Lee Evolutionary Rates and Expression Level in Chlamydomonas Genetics, March 1, 2006; 172(3): 1567 - 1576. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. A. Drummond, A. Raval, and C. O. Wilke A Single Determinant Dominates the Rate of Yeast Protein Evolution Mol. Biol. Evol., February 1, 2006; 23(2): 327 - 337. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. Zhang and W.-H. Li Human SNPs Reveal No Evidence of Frequent Positive Selection Mol. Biol. Evol., December 1, 2005; 22(12): 2504 - 2507. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
B. P. Cusack and K. H. Wolfe Changes in Alternative Splicing of Human and Mouse Genes Are Accompanied by Faster Evolution of Constitutive Exons Mol. Biol. Evol., November 1, 2005; 22(11): 2198 - 2208. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. A. Drummond, J. D. Bloom, C. Adami, C. O. Wilke, and F. H. Arnold Why highly expressed proteins evolve slowly PNAS, October 4, 2005; 102(40): 14338 - 14343. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
N. Osada, M. Hirata, R. Tanuma, J. Kusuda, M. Hida, Y. Suzuki, S. Sugano, T. Gojobori, C.-K. J. Shen, C.-I Wu, et al. Substitution Rate and Structural Divergence of 5'UTR Evolution: Comparative Analysis Between Human and Cynomolgus Monkey cDNAs Mol. Biol. Evol., October 1, 2005; 22(10): 1976 - 1982. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. Yang, A. I. Su, and W.-H. Li Gene Expression Evolves Faster in Narrowly Than in Broadly Expressed Mammalian Genes Mol. Biol. Evol., October 1, 2005; 22(10): 2113 - 2118. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 P. Khaitovich, I. Hellmann, W. Enard, K. Nowick, M. Leinweber, H. Franz, G. Weiss, M. Lachmann, and S. Paabo Parallel Patterns of Evolution in the Genomes and Transcriptomes of Humans and Chimpanzees Science, September 16, 2005; 309(5742): 1850 - 1854. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Sironi, G. Menozzi, G. P. Comi, R. Cagliani, N. Bresolin, and U. Pozzoli Analysis of intronic conserved elements indicates that functional complexity might represent a major source of negative selection on non-coding sequences Hum. Mol. Genet., September 1, 2005; 14(17): 2533 - 2546. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
G. Marais, P. Nouvellet, P. D. Keightley, and B. Charlesworth Intron Size and Exon Evolution in Drosophila Genetics, May 1, 2005; 170(1): 481 - 485. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
B. Lemos, B. R. Bettencourt, C. D. Meiklejohn, and D. L. Hartl 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., May 1, 2005; 22(5): 1345 - 1354. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. Pfeufer, S. Jalilzadeh, S. Perz, J. C. Mueller, M. Hinterseer, T. Illig, M. Akyol, C. Huth, A. Schopfer-Wendels, B. Kuch, et al. Common Variants in Myocardial Ion Channel Genes Modify the QT Interval in the General Population: Results From the KORA Study Circ. Res., April 1, 2005; 96(6): 693 - 701. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. M. Good and M. W. Nachman Rates of Protein Evolution Are Positively Correlated with Developmental Timing of Expression During Mouse Spermatogenesis Mol. Biol. Evol., April 1, 2005; 22(4): 1044 - 1052. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. Zhang and X. He Significant Impact of Protein Dispensability on the Instantaneous Rate of Protein Evolution Mol. Biol. Evol., April 1, 2005; 22(4): 1147 - 1155. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. M. Alba and J. Castresana Inverse Relationship Between Evolutionary Rate and Age of Mammalian Genes Mol. Biol. Evol., March 1, 2005; 22(3): 598 - 606. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. G. Torgerson and R. S. Singh Rapid Evolution Through Gene Duplication and Subfunctionalization of the Testes-Specific {alpha}4 Proteasome Subunits in Drosophila Genetics, November 1, 2004; 168(3): 1421 - 1432. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
I. K. Jordan, L. Marino-Ramirez, Y. I. Wolf, and E. V. Koonin Conservation and Coevolution in the Scale-Free Human Gene Coexpression Network Mol. Biol. Evol., November 1, 2004; 21(11): 2058 - 2070. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. Huminiecki and K. H. Wolfe Divergence of Spatial Gene Expression Profiles Following Species-Specific Gene Duplications in Human and Mouse Genome Res., October 1, 2004; 14(10a): 1870 - 1879. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. T. Webster, N. G.C. Smith, M. J. Lercher, and H. Ellegren Gene Expression, Synteny, and Local Similarity in Human Noncoding Mutation Rates Mol. Biol. Evol., October 1, 2004; 21(10): 1820 - 1830. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Subramanian and S. Kumar Gene Expression Intensity Shapes Evolutionary Rates of the Proteins Encoded by the Vertebrate Genome Genetics, September 1, 2004; 168(1): 373 - 381. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. I. Wright, C. B. K. Yau, M. Looseley, and B. C. Meyers Effects of Gene Expression on Molecular Evolution in Arabidopsis thaliana and Arabidopsis lyrata Mol. Biol. Evol., September 1, 2004; 21(9): 1719 - 1726. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. M. Comeron Selective and Mutational Patterns Associated With Gene Expression in Humans: Influences on Synonymous Composition and Intron Presence Genetics, July 1, 2004; 167(3): 1293 - 1304. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. J. Lercher, J.-V. Chamary, and L. D. Hurst Genomic Regionality in Rates of Evolution Is Not Explained by Clustering of Genes of Comparable Expression Profile Genome Res., June 1, 2004; 14(6): 1002 - 1013. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. Johannesson, P. Vidal, J. Guarro, R. A. Herr, G. T. Cole, and J. W. Taylor Positive Directional Selection in the Proline-Rich Antigen (PRA) Gene Among the Human Pathogenic Fungi Coccidioides immitis, C. posadasii and Their Closest Relatives Mol. Biol. Evol., June 1, 2004; 21(6): 1134 - 1145. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. L. Halligan, A. Eyre-Walker, P. Andolfatto, and P. D. Keightley Patterns of Evolutionary Constraints in Intronic and Intergenic DNA of Drosophila Genome Res., February 1, 2004; 14(2): 273 - 279. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. Zhang and W.-H. Li Mammalian Housekeeping Genes Evolve More Slowly than Tissue-Specific Genes Mol. Biol. Evol., February 1, 2004; 21(2): 236 - 239. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 P. J. Stover Nutritional genomics Physiol Genomics, January 15, 2004; 16(2): 161 - 165. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
E. E. Winter, L. Goodstadt, and C. P. Ponting Elevated Rates of Protein Secretion, Evolution, and Disease Among Tissue-Specific Genes Genome Res., January 1, 2004; 14(1): 54 - 61. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. S. Choi and B. T. Lahn Adaptive Evolution of MRG, a Neuron-Specific Gene Family Implicated in Nociception Genome Res., October 1, 2003; 13(10): 2252 - 2259. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. Akashi Translational Selection and Yeast Proteome Evolution Genetics, August 1, 2003; 164(4): 1291 - 1303. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
P. K. Tucker, R. M. Adkins, and J. S. Rest Differential Rates of Evolution for the ZFY-Related Zinc Finger Genes, Zfy, Zfx, and Zfa in the Mouse Genus Mus Mol. Biol. Evol., June 1, 2003; 20(6): 999 - 1005. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
I. Hellmann, S. Zollner, W. Enard, I. Ebersberger, B. Nickel, and S. Paabo Selection on Human Genes as Revealed by Comparisons to Chimpanzee cDNA Genome Res., May 1, 2003; 13(5): 831 - 837. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. Duan, M. S. Wainwright, J. M. Comeron, N. Saitou, A. R. Sanders, J. Gelernter, and P. V. Gejman Synonymous mutations in the human dopamine receptor D2 (DRD2) affect mRNA stability and synthesis of the receptor Hum. Mol. Genet., February 1, 2003; 12(3): 205 - 216. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. Grassot, G. Mouchiroud, and G. Perriere RTKdb: database of receptor tyrosine kinase Nucleic Acids Res., January 1, 2003; 31(1): 353 - 358. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. H. Woelk and E. C. Holmes Reduced Positive Selection in Vector-Borne RNA Viruses Mol. Biol. Evol., December 1, 2002; 19(12): 2333 - 2336. [Full Text] [PDF]
|
|
|
|
|
|
D. G. Torgerson, R. J. Kulathinal, and R. S. Singh Mammalian Sperm Proteins Are Rapidly Evolving: Evidence of Positive Selection in Functionally Diverse Genes Mol. Biol. Evol., November 1, 2002; 19(11): 1973 - 1980. [Abstract] [Full Text] [PDF]
|
|