Changes in selective effects over time facilitate turnover of enhancer sequences

Genetics

Volumn 187, Issue 2, 2011, Pages 567-582

  Bullaughey, Kevin ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR;

ARTICLE; BEHAVIOR; BINDING SITE; ENHANCER REGION; FITNESS; GENE EXPRESSION; GENE MUTATION; GENETIC CONSERVATION; GENETIC DRIFT; HUMAN; MATHEMATICAL MODEL; MOLECULAR EVOLUTION; NATURAL SELECTION; NONHUMAN; PHENOTYPE; PHYLOGENY; PRIORITY JOURNAL; REGULATORY DNA SEQUENCE; TURNOVER TIME;

ANIMALS; COMPUTATIONAL BIOLOGY; DROSOPHILA; ENHANCER ELEMENTS, GENETIC; EVOLUTION, MOLECULAR; GENE EXPRESSION PROFILING; GENETIC DRIFT; MODELS, GENETIC; MUTATION; SELECTION, GENETIC;

EID: 79951548111     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.110.121590     Document Type: Article

References (77)

1. ANCEL, L. W., and W. FONTANA, 2000 Plasticity, evolvability, and modularity in RNA. J. Exp. Zool. 288(3): 242-283.
2. ANDOLFATTO, P., 2005 Adaptive evolution of non-coding DNA in Drosophila. Nature 437(7062): 1149-1152.
3. BREEDEN, L. L., 2003 Periodic transcription: a cycle within a cycle. Curr. Biol. 13(1): R31-R38.
4. BRODIE, E. D., 2000 Why evolutionary genetics does not always add up, pp. 3-19 in Epistasis and the Evolutionary Process, edited by J. B. WOLF, E. D. BRODIE and M. J. WADE. Oxford University Press, Oxford.
5. BROMHAM, L., and D. PENNY, 2003 The modern molecular clock. Nat. Rev. Genet. 4(3): 216-224.
6. BUSTAMANTE, C. D., A. FLEDEL-ALON, S. WILLIAMSON, R. NIELSEN, M. T. HUBISZ et al., 2005 Natural selection on protein-coding genes in the human genome. Nature 437(7062): 1153-1157.
7. CARROLL, S. B., J. K. GRENIER and S. D. WEATHERBEE, 2005 From DNA to Diversity: Molecular Genetics and the Evolution of Animal Design, Ed. 2. Blackwell, Malden, MA.
8. CLIFTEN, P., P. SUDARSANAM, A. DESIKAN, L. FULTON, B. FULTON et al., 2003 Finding functional features in Saccharomyces genomes by phylogenetic footprinting. Science 301(5629): 71-76.
9. CROW, J. F., and M. KIMURA, 1970 An Introduction to Population Genetics Theory. Harper & Row, New York.
10. DAVIDSON, E. H., 2006 The Regulatory Genome: Gene Regulatory Networks in Development and Evolution. Academic Press, Burlington, MA.
11. DELUNA, A., K. VETSIGIAN, N. SHORESH, M. HEGRENESS, M. COLÓN-GONZÁLEZ et al., 2008 Exposing the fitness contribution of duplicated genes. Nat. Genet. 40(5): 676-681.
12. DENVER, D. R., K. MORRIS, J. T. STREELMAN, S. K. KIM, M. LYNCH et al., 2005 The transcriptional consequences of mutation and natural selection in Caenorhabditis elegans. Nat. Genet. 37(5): 544-548.
13. DERMITZAKIS, E. T., C. M. BERGMAN and A. G. CLARK, 2003 Tracing the evolutionary history of Drosophila regulatory regions with models that identify transcription factor binding sites. Mol. Biol. Evol. 20(5): 703-714.
14. DRAGHI, J. A., T. L. PARSONS, G. P. WAGNER and J. B. PLOTKIN, 2010 Mutational robustness can facilitate adaptation. Nature 463(7279): 353-355.
15. DURRETT, R., and D. SCHMIDT, 2008 Waiting for two mutations: with applications to regulatory sequence evolution and the limits of Darwinian evolution. Genetics 180(3): 1501-1509.
16. EWENS, W. J., 2004 Mathematical Population Genetics, Ed. 2. Springer, New York.
17. EYRE-WALKER, A., and P. D. KEIGHTLEY, 1999 High genomic deleterious mutation rates in hominids. Nature 397(6717): 344-347.
18. FAKHOURI, W. D., A. AY, R. SAYAL, J. DRESCH, E. DAYRINGER et al., 2010 Deciphering a transcriptional regulatory code: modeling short-range repression in the Drosophila embryo. Mol. Syst. Biol. 6: 341.
19. FIELD, Y., Y. FONDUFE-MITTENDORF, I. K. MOORE, P. MIECZKOWSKI, N. KAPLAN et al., 2009 Gene expression divergence in yeast is coupled to evolution of DNA-encoded nucleosome organization. Nat. Genet. 41(4): 438-445.
20. FISHER, R. A., 1930 The Genetical Theory of Natural Selection. Clarendon Press, Oxford.
21. GASCH, A. P., P. T. SPELLMAN, C. M. KAO, O. CARMEL-HAREL, M. B. EISEN et al., 2000 Genomic expression programs in the response of yeast cells to environmental changes. Mol. Biol. Cell 11(12): 4241-4257.
22. GILAD, Y., A. OSHLACK and S. A. RIFKIN, 2006a Natural selection on gene expression. Trends Genet. 22(8): 456-461.
23. GILAD, Y., A. OSHLACK, G. K. SMYTH, T. P. SPEED and K. P. WHITE, 2006b Expression profiling in primates reveals a rapid evolution of human transcription factors. Nature 440(7081): 242-245.
24. GU, X., Y. WANG and J. GU, 2002 Age distribution of human gene families shows significant roles of both large- and small-scale duplications in vertebrate evolution. Nat. Genet. 31(2): 205-209.
25. HALLIGAN, D. L., and P. D. KEIGHTLEY, 2006 Ubiquitous selective constraints in the Drosophila genome revealed by a genome-wide interspecies comparison. Genome Res. 16(7): 875-884.
26. HALLIGAN, D. L., A. EYRE-WALKER, P. ANDOLFATTO and P. D. KEIGHTLEY, 2004 Patterns of evolutionary constraints in intronic and intergenic DNA of Drosophila. Genome Res. 14(2): 273-279.
27. HARE, E. E., B. K. PETERSON, V. N. IYER, R. MEIER and M. B. EISEN, 2008 Sepsid even-skipped enhancers are functionally conserved in Drosophila despite lack of sequence conservation. PLoS Genet. 4(6): e1000106.
28. HO, M. C. W., H. JOHNSEN, S. E. GOETZ, B. J. SCHILLER, E. BAE et al., 2009 Functional evolution of cis-regulatory modules at a homeotic gene in Drosophila. PLoS Genet. 5(11): e1000709.
29. HOFFMAN, M. M., and E. BIRNEY, 2010 An effective model for natural selection in promoters. Genome Res. 20(5): 685-692.
30. HUYNEN, M. A., P. F. STADLER and W. FONTANA, 1996 Smoothness within ruggedness: the role of neutrality in adaptation. Proc. Natl. Acad. Sci. USA 93(1): 397-401.
31. JAEGER, J., S. SURKOVA, M. BLAGOV, H. JANSSENS, D. KOSMAN et al., 2004 Dynamic control of positional information in the early Drosophila embryo. Nature 430(6997): 368-371.
32. KAPLAN, N., I. K. MOORE, Y. FONDUFE-MITTENDORF, A. J. GOSSETT, D. TILLO et al., 2009 The DNA-encoded nucleosome organization of a eukaryotic genome. Nature 458(7236): 362-366.
33. KAUFFMAN, S., and S. LEVIN, 1987 Towards a general theory of adaptive walks on rugged landscapes. J. Theor. Biol. 128(1): 11-45.
34. KELLIS, M., N. PATTERSON, M. ENDRIZZI, B. BIRREN and E. S. LANDER, 2003 Sequencing and comparison of yeast species to identify genes and regulatory elements. Nature 423(6937): 241-254.
35. KIM, J., X. HE and S. SINHA, 2009 Evolution of regulatory sequences in 12 Drosophila species. PLoS Genet. 5(1): e1000330.
36. KIMURA, M., 1977 Preponderance of synonymous changes as evidence for the neutral theory of molecular evolution. Nature 267(5608): 275-276.
37. KIMURA, M., 1985 The role of compensatory neutral mutations in molecular evolution. J. Genet. 64(1): 7-19.
38. KIRCHHAMER, C. V., C. H. YUH and E. H. DAVIDSON, 1996 Modular cis-regulatory organization of developmentally expressed genes: two genes transcribed territorially in the sea urchin embryo, and additional examples. Proc. Natl. Acad. Sci. USA 93(18): 9322-9328.
39. KREITMAN, M., 1996 The neutral theory is dead. Long live the neutral theory. BioEssays 18(8): 678-683.
40. KRYAZHIMSKIY, S., G. TKACIK and J. B. PLOTKIN, 2009 The dynamics of adaptation on correlated fitness landscapes. Proc. Natl. Acad. Sci. USA 106(44): 18638-18643.
41. KRYUKOV, G. V., S. SCHMIDT and S. SUNYAEV, 2005 Small fitness effect of mutations in highly conserved non-coding regions. Hum. Mol. Genet. 14(15): 2221-2229.
42. LENORMAND, T., D. ROZE and F. ROUSSET, 2009 Stochasticity in evolution. Trends Ecol. Evol. (Amst.) 24(3): 157-165.
43. LI, B., M. CAREY and J. WORKMAN, 2007 The role of chromatin during transcription. Cell 128: 707-719.
44. LI, X.-Y., S. MACARTHUR, R. BOURGON, D. NIX, D. A. POLLARD et al., 2008 Transcription factors bind thousands of active and inactive regions in the Drosophila blastoderm. PLoS Biol. 6(2): e27.
45. LUDWIG, M. Z., N. H. PATEL and M. KREITMAN, 1998 Functional analysis of eve stripe 2 enhancer evolution in Drosophila: rules governing conservation and change. Development 125(5): 949-958.
46. LUDWIG, M. Z., C. BERGMAN, N. H. PATEL and M. KREITMAN, 2000 Evidence for stabilizing selection in a eukaryotic enhancer element. Nature 403(6769): 564-567.
47. LUDWIG,M. Z., A. PALSSON, E. ALEKSEEVA, C. M. BERGMAN, J. NATHAN et al., 2005 Functional evolution of a cis-regulatory module. PLoS Biol. 3(4): e93.
48. LUSK, R. W., and M. B. EISEN, 2010 Evolutionary mirages: selection on binding site composition creates the illusion of conserved grammars in Drosophila enhancers. PLoS Genet. 6(1): e1000829.
49. MARTIN, G., and T. LENORMAND, 2006 A general multivariate extension of Fisher's geometrical model and the distribution of mutation fitness effects across species. Evolution 60(5): 893-907.
50. MCDONALD, J. H., and M. KREITMAN, 1991 Adaptive protein evolution at the Adh locus in Drosophila. Nature 351(6328): 652-654.
51. MIRNY, L., 2009 Nucleosome-mediated cooperativity between transcription factors. Available from Nature Precedings. http://hdl.handle.net/10101/npre.
52. MOSES, A. M., D. Y. CHIANG, M. KELLIS, E. S. LANDER and M. B. EISEN, 2003 Position specific variation in the rate of evolution in transcription factor binding sites. BMC Evol. Biol. 3: 19.
53. MOSES, A. M., D. A. POLLARD, D. A. NIX, V. N. IYER, X.-Y. LI et al., 2006 Large-scale turnover of functional transcription factor binding sites in Drosophila. PLoS Comput. Biol. 2(10): e130.
54. NOBREGA, M. A., I. OVCHARENKO, V. AFZAL and E. M. RUBIN, 2003 Scanning human gene deserts for long-range enhancers. Science 302(5644): 413.
55. ORR, H. A., 2005 The genetic theory of adaptation: a brief history. Nat. Rev. Genet. 6(2): 119-127.
56. ORR, H. A., 2006 The population genetics of adaptation on correlated fitness landscapes: the block model. Evolution 60(6): 1113-1124.
57. PETERSON, B. K., E. E. HARE, V. N. IYER, S. STORAGE, L. CONNER et al., 2009 Big genomes facilitate the comparative identification of regulatory elements. PLoS ONE 4(3): e4688.
58. PRUD'HOMME, B., N. GOMPEL and S. B. CARROLL, 2007 Emerging principles of regulatory evolution. Proc. Natl. Acad. Sci. USA 104(Suppl. 1): 8605-8612.
59. RAVEH-SADKA, T., M. LEVO and E. SEGAL, 2009 Incorporating nucleosomes into thermodynamic models of transcription regulation. Genome Res. 19(8): 1480-1496.
60. RIFKIN, S. A., J. KIM and K. P. WHITE, 2003 Evolution of gene expression in the Drosophila melanogaster subgroup. Nat. Genet. 33(2): 138-144.
61. ROCKMAN,M. V., and G. A.WRAY, 2002 Abundant rawmaterial for cis-regulatory evolution in humans. Mol. Biol. Evol. 19(11): 1991-2004.
62. SAWYER, S. A., and D. L. HARTL, 1992 Population genetics of polymorphism and divergence. Genetics 132(4): 1161-1176.
63. SCHUSTER, P., W. FONTANA, P. F. STADLER and I. L. HOFACKER, 1994 From sequences to shapes and back: a case study in RNA secondary structures. Proc. Biol. Sci. 255(1344): 279-284.
64. SEGAL, E., T. RAVEH-SADKA, M. SCHROEDER, U. UNNERSTALL and U. GAUL, 2008 Predicting expression patterns from regulatory sequence in Drosophila segmentation. Nature 451(7178): 535-540.
65. SHABALINA, S. A., A. Y. OGURTSOV, V. A. KONDRASHOV and A. S. KONDRASHOV, 2001 Selective constraint in intergenic regions of human and mouse genomes. Trends Genet. 17(7): 373-376.
66. TAGLE, D. A., B. F. KOOP, M. GOODMAN, J. L. SLIGHTOM, D. L. HESS et al., 1988 Embryonic epsilon and gamma globin genes of a prosimian primate (Galago crassicaudatus). Nucleotide and amino acid sequences, developmental regulation and phylogenetic footprints. J. Mol. Biol. 203(2): 439-455.
67. TANAY, A., 2006 Extensive low-affinity transcriptional interactions in the yeast genome. Genome Res. 16(8): 962-972.
68. TAYLOR, M. S., C. KAI, J. KAWAI, P. CARNINCI, Y. HAYASHIZAKI et al., 2006 Heterotachy in mammalian promoter evolution. PLoS Genet. 2(4): e30.
69. TIROSH, I., and N. BARKAI, 2008 Two strategies for gene regulation by promoter nucleosomes. Genome Res. 18(7): 1084-1091.
70. TOMPA, M., N. LI, T. L. BAILEY, G. M. CHURCH, B. D. MOOR et al., 2005 Assessing computational tools for the discovery of transcription factor binding sites. Nat. Biotechnol. 23(1): 137-144.
71. TORGERSON, D. G., A. R. BOYKO, R. D. HERNANDEZ, A. INDAP, X. HU et al., 2009 Evolutionary processes acting on candidate cis-regulatory regions in humans inferred from patterns of polymorphism and divergence. PLoS Genet. 5(8): e1000592.
72. VISEL, A., S. PRABHAKAR, J. A. AKIYAMA, M. SHOUKRY, K. D. LEWIS et al., 2008 Ultraconservation identifies a small subset of extremely constrained developmental enhancers. Nat. Genet. 40(2): 158-160.
73. WAGNER, A., 2008 Neutralism and selectionism: a network-based reconciliation. Nat. Rev. Genet. 9(12): 965-974.
74. WASSON, T., and A. J. HARTEMINK, 2009 An ensemble model of competitive multi-factor binding of the genome. Genome Res. 19(11): 2101-2112.
75. WORKMAN, J. L., andR.E.KINGSTON, 1992 Nucleosome core displacement in vitro via a metastable transcription factor-nucleosome complex. Science 258(5089): 1780-1784.
76. WRAY, G. A., M. W. HAHN, E. ABOUHEIF, J. P. BALHOFF, M. PIZER et al., 2003 The evolution of transcriptional regulation in eukaryotes. Mol. Biol. Evol. 20(9): 1377-1419.
77. YANG, Z., and J. BIELAWSKI, 2000 Statistical methods for detecting molecular adaptation. Trends Ecol. Evol. (Amst.) 15(12): 496-503.