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

Molecular Biology and Evolution

Volumn 22, Issue 5, 2005, Pages 1345-1354

  Lemos, Bernardo ^a   Bettencourt, Brian R ^b   Meiklejohn, Colin D ^a   Hartl, Daniel L ^a  

^a HARVARD UNIVERSITY   (United States)

^b UNIVERSITY OF MASSACHUSETTS LOWELL   (United States)

Author keywords

Constraint; Correlation; Coupling; Drosophila; Network; Neutral; Selection

Indexed keywords

MESSENGER RNA;

AMINO ACID SUBSTITUTION; ARTICLE; CONTROLLED STUDY; DROSOPHILA; EVOLUTION; GENE EXPRESSION; GENOME ANALYSIS; MOLECULAR EVOLUTION; MOLECULAR PHYLOGENY; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION;

ANIMALS; DROSOPHILA; DROSOPHILA PROTEINS; EVOLUTION, MOLECULAR; GENE EXPRESSION; RNA, MESSENGER; SELECTION (GENETICS); VARIATION (GENETICS);

EID: 17744376961     PISSN: 07374038     EISSN: None     Source Type: Journal    
DOI: 10.1093/molbev/msi122     Document Type: Article

References (59)

1. Adams, M. D., S. E. Celniker, R. A. Holt et al. (195 co-authors). 2000. The genome sequence of Drosophila melanogaster. Science 287:2185-2195.
2. Albert, R., H. Jeong, and A. L. Barabasi. 2000. Error and attack tolerance of complex networks. Nature 406:378-382.
3. Akashi, H. 2003. Translational selection and yeast proteome evolutions. Genetics 164:1291-1303.
4. Bader, J. S., A. Chaudhuri, J. M. Rothberg, and J. Chant. 2004. Gaining confidence in high-throughput protein interaction networks. Nat. Biotech. 22:78-85.
5. Barabasi, A. L., and Z. N. Oltvai. 2004. Network biology: understanding the cell's functional organization. Nat. Rev. Genet. 5:101-113.
6. Bloom, J. D., and C. Adami. 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.
7. _. 2004. Evolutionary rate depends on number of protein-protein interactions independently of gene expression level: response. BMC Evol. Biol. 4:14.
8. Castillo-Davis, C. I., F. A. Kondrashov, D. L. Hartl, and R. J. Kulathinal. 2004. The functional genomic distribution of protein divergence in two animal phyla: coevolution, genomic conflict, and constraint. Genome Res. 14:802-811.
9. Coghlan, A., and Y. I. Wolfe. 2000. Relationship of codon bias to mRNA concentration and protein length in Saccharomyces cerevisiae. Yeast 16:1131-1145.
10. Covert, M. W., I. Famili, and B. O. Palsson. 2003. Identifying constraints that govern cell behavior: a key to converting conceptual to computational models in biology? Bioeng. 84:763-772.
11. Covert, M. W., E. M. Knight, J. L. Reed, M. J. Herrgard, and B. O. Palsson. 2004. Integrating high-throughput and computational data elucidates bacterial networks. Nature 429:92-96.
12. De Gregorio, E., P. T. Spellman, G. M. Rubin, and B. Lemaitre. 2001. Genome-wide analysis of the Drosophila immune response by using oligonucleotide microarrays. Proc. Natl. Acad. Sci. USA 98:12590-12595.
13. Duret, L., and D. Mouchiroud. 1999. Expression pattern and, surprisingly, gene length shape codon usage in Caenorhabditis, Drosophila, and Arabidopsis. Proc. Natl. Acad. Sci. USA 96:4482-4487.
14. _. 2000. Determinants of substitution rates in mammalian genes: expression pattern affects selection intensity but not mutation rate. Mol. Biol. Evol. 17:68-74.
15. Forster, J., I. Famili, P. Fu, B. O. Palsson, and J. Nielsen. 2003. Genome-scale reconstruction of the Saccharomyces cerevisiae metabolic network. Genome Res. 13:244-253.
16. Fraser, H. B., and A. E. Hirsh. 2004. Evolutionary rate depends on number of protein-protein interactions independently of gene expression level. BMC Evol. Biol. 4:13.
17. Fraser, H. B., A. E. Hirsh, L. M. Steinmetz, C. Scharfe, and M. W. Feldman. 2002. Evolutionary rate in the protein interaction network. Science 296:750-752.
18. Fraser, H. B., A. E. Hirsh, D. P. Wall, and M. B. Eisen. 2004. Coevolution of gene expression among interacting proteins. Proc. Natl. Acad. Sci. USA 101:9033-9038.
19. Fraser, H. B., D. P. Wall, and A. E. Hirsh. 2003. A simple dependence between protein evolution rate and the number of protein-protein interactions. BMC Evol. Biol. 3:11.
20. Giot, L., J. S. Bader, C. Brouwer et al. (49 co-authors). 2003. A protein interaction map of Drosophila melanogaster. Science 302:1727-1736.
21. Gu, Z., D. Nicolae, H. H. Lu, and W. H. Li. 2002. Rapid divergence in expression between duplicate genes inferred from microarray data. Trends Genet. 18:609-613.
22. Hahn, M. W., G. C. Conant, and A. Wagner. 2004. Molecular evolution in large genetic networks: does connectivity equal constraint? J. Mol. Evol. 58:203-211.
23. Holt, R. A., G. M. Subramanian, A. Halpern et al. (123 co-authors). 2002. The genome sequence of the malaria mosquito Anopheles gambiae. Science 298:129-149.
24. Jansen, R., and M. Gerstein. 2000. Analysis of the yeast transcriptome with structural and functional categories: characterizing highly expressed proteins. Nucleic Acids Res. 28:1481-1488.
25. Jeong, H., B. Tombor, R. Albert, Z. N. Oltvai, and A. L. Barabasi. 2000. The large-scale organization of metabolic networks. Nature 407:651-654.
26. Jordan, I. K., L. Marino-Ramirez, Y. I. Wolf, and E. V. Koonin. 2004. Conservation and coevolution in the scale-free human gene coexpression network. Mol. Biol. Evol. 21:2058-2070.
27. Jordan, I. K., Y. I. Wolf, and E. V. Koonin. 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.
28. Krylov, D. M., Y. I. Wolf, I. B. Rogozin, and E. V. Koonin. 2003. Gene loss, protein sequence divergence, gene dispensability, expression level, and interactivity are correlated in eukaryotic evolution. Genome Res. 13:2229-2235.
29. Lemos, B., C. D. Meiklejohn, M. Caceres, and D. L. Hartl. 2005. Rates of divergence in gene expression profiles of primates, mice and flies: stabilizing selection and variability among functional categories. Evolution 59:126-137.
30. Lemos, B., C. D. Meiklejohn, and D. L. Hartl. 2004. Regulatory evolution across the protein interaction network. Nat. Genet. 36:1059-1060.
31. Li, C., and W. H. Wong. 2001. Model-based analysis of oligonucleotide arrays: expression index computation and outlier detection. Proc. Natl. Acad. Sci. USA 98:31-36.
32. Makova, K. D., and W. H. Li. 2003. Divergence in the spatial pattern of gene expression between duplicate genes. Genome Res. 13:1638-1645.
33. Marais, G., and L. Duret. 2001. Synonymous codon usage, accuracy of translation, and gene length in Caenorhabditis elegans. J. Mol. Evol. 52:275-280.
34. Meiklejohn, C. D., J. Parsch, J. M. Ranz, and D. L. Hartl. 2003. Rapid evolution of male-biased gene expression in Drosophila. Proc. Natl. Acad. Sci. USA 100:9894-9899.
35. Moriyama, E. N., and D. L. Hartl. 1993. Codon usage bias and base composition of nuclear genes in Drosophila. Genetics 134:847-858.
36. Nuzhdin, S. V., M. L. Wayne, K. L. Harmon, and L. M. McIntyre. 2004. Common pattern of evolution of gene expression level and protein sequence in Drosophila. Mol. Biol. Evol. 21:1308-1317.
37. Pal, C., B. Papp, and L. D. Hurst. 2001. Highly expressed genes in yeast evolve slowly. Genetics 158:927-931.
38. Papp, B., C. Pal, and L. D. Hurst. 2003. Dosage sensitivity and the evolution of gene families in yeast. Nature 424:194-196.
39. Price, N. D., J. L. Reed, and B. O. Palsson. 2004. Genome-scale models of microbial cells: evaluating the consequences of constraints. Nat. Rev. Microbiol. 2:886-897.
40. Ranz, J. M., C. I. Castillo-Davis, C. D. Meiklejohn, and D. L. Hartl. 2003. Sex-dependent gene expression and evolution of the Drosophila transcriptome. Science 300:1742-1745.
41. Richards, S., Y. Liu, B. R. Bettencourt et al. (52 co-authors). 2005. Comparative sequencing and analysis of Drosophila pseudoobscura. Genome Res. 15:1-18.
42. Rifkin, S. A., J. Kim, and K. P. White. 2003. Evolution of gene expression in the Drosophila melanogaster subgroup. Nat. Genet. 33:138-144.
43. Rocha, E. P. C., and A. Danchin. 2004. An analysis of determinants of amino acids substitution rates in bacterial proteins. Mol. Biol. Evol. 21:108-116.
44. Sharp, P. M., and W. H. Li. 1989. On the rate of DNA sequence evolution in Drosophila. J. Mol. Evol. 28:398-402.
45. Shipley, B. 2000. Cause and correlation in biology: a user's guide to path analysis, structural equations and causal inference. Cambridge University Press, Cambridge, UK.
46. Subramanian, S., and S. Kumar. 2004. Gene expression intensity shapes evolutionary rates of the proteins encoded by the vertebrate genome. Genetics 168:373-381.
47. Tatusov, R. L., E. V. Koonin, and D. J. Lipman. 1997. A genomic perspective on protein families. Science 278:631-637.
48. Teichmann, S. A. 2002. The constraints protein-protein interactions place on sequence divergence. J. Mol. Biol. 324:399-407.
49. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CLUSTALW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
50. Townsend, J. P. 2003. Multifactorial experimental design and the transitivity of ratios with spotted DNA microarrays. BMC Genomics 4:41.
51. Townsend, J. P., and D. L. Hartl. 2002. Bayesian analysis of gene expression levels: statistical quantification of relative mRNA levels across multiple strains or treatments. Genome Biol. 3:RESEARCH0071.
52. Urrutia, A. O., and L. D. Hurst. 2003. The signature of selection mediated by expression on humans genes. Genome Res. 13:2260-2264.
53. Veitia, R. A. 2002. Exploring the etiology of haploinsufficiency. Bioessays 24:175-184.
54. Wagner, A. 2000. Decoupled evolution of coding region and mRNA expression patterns after gene duplication: implications for the neutralist-selectionist debate. Proc. Natl. Acad. Sci. USA 97:6579-6584.
55. Williams, E. J. B., and L. D. Hurst. 2000. The proteins of linked genes evolve at similar rates. Nature 407:900-903.
56. Yang, Z. 1997. PAML: a program package for phylogenetic analysis by maximum likelihood. CABIOS 13:555-556.
57. _. 2002. Phylogenetic analysis by maximum likelihood (PAML) version 3.0. (http://abacus.gene.ucl.ac.uk/software/paml.html).
58. Yang, Z., and R. Nielsen. 2000. Estimating synonymous and non-synonymous substitution rates under realistic evolutionary models. Mol. Biol. Evol. 17:32-43.
59. Zhang, Z., T. M. Hambuch, and J. Parsch. 2004. Molecular evolution of sex-biased genes in Drosophila. Mol. Biol. Evol. 21:2130-2139.