Comparative studies of gene expression and the evolution of gene regulation

Nature Reviews Genetics

Volumn 13, Issue 7, 2012, Pages 505-516

  Romero, Irene Gallego ^a   Ruvinsky, Ilya ^a   Gilad, Yoav ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR;

ALTERNATIVE RNA SPLICING; CELL IMMORTALIZATION; COMPARATIVE STUDY; DNA METHYLATION; EPIGENETICS; EVOLUTIONARY ADAPTATION; GENE CONTROL; GENE EXPRESSION; GENETIC ASSOCIATION; HUMAN; NATURAL SELECTION; NONHUMAN; PHENOTYPE; PRIMATE; PRIORITY JOURNAL; PROTEIN BINDING; REVIEW; RNA INTERFERENCE; RNA SEQUENCE; SPECIES COMPARISON; TISSUE SPECIFICITY;

ADAPTATION, BIOLOGICAL; ANIMALS; BIOLOGICAL EVOLUTION; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION; GENETIC SPECIATION; MODELS, GENETIC; PHYSIOLOGY, COMPARATIVE; PRIMATES; SELECTION, GENETIC; SPECIES SPECIFICITY; TRANSCRIPTION FACTORS;

PRIMATES;

EID: 84863885448     PISSN: 14710056     EISSN: 14710064     Source Type: Journal    
DOI: 10.1038/nrg3229     Document Type: Review

References (120)

1. Carroll, S. B. Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution. Cell 134, 25-36 (2008).
2. Hoekstra, H. E. & Coyne, J. A. The locus of evolution: evo devo and the genetics of adaptation. Evolution 61, 995-1016 (2007).
3. Stern, D. L. & Orgogozo, V. The loci of evolution: how predictable is genetic evolution? Evolution 62, 2155-2177 (2008).
4. Kleinjan, D. A. & van Heyningen, V. Long-range control of gene expression: emerging mechanisms and disruption in disease. Am. J. Hum. Genet. 76, 8-32 (2005).
5. Wray, G. A. The evolutionary significance of cis-regulatory mutations. Nature Rev. Genet. 8, 206-216 (2007).
6. Britten, R. J. & Davidson, E. H. Gene regulation for higher cells: a theory. Science 165, 349-357 (1969).
7. Britten, R. J. & Davidson, E. H. Repetitive and non-repetitive DNA sequences and a speculation on the origins of evolutionary novelty. Q. Rev. Biol. 46, 111-138 (1971).
8. King, M. C. & Wilson, A. C. Evolution at two levels in humans and chimpanzees. Science 188, 107-116 (1975).
9. Majewski, J. & Pastinen, T. The study of eQTL variations by RNA-seq: from SNPs to phenotypes. Trends Genet. 27, 72-79 (2011).
10. Gilad, Y., Rifkin, S. A. & Pritchard, J. K. Revealing the architecture of gene regulation: the promise of eQTL studies. Trends Genet. 24, 408-415 (2008).
11. Zheng, W., Gianoulis, T. A., Karczewski, K. J., Zhao, H. & Snyder, M. Regulatory variation within and between species. Annu. Rev. Genom. Hum. Genet. 12, 327-346 (2011).
12. Whitehead, A. & Crawford, D. L. Neutral and adaptive variation in gene expression. Proc. Natl Acad. Sci. USA 103, 5425-5430 (2006).
13. Gilad, Y., Oshlack, A. & Rifkin, S. A. Natural selection on gene expression. Trends Genet. 22, 456-461 (2006).
14. Wang, Z., Gerstein, M. & Snyder, M. RNA-seq: a revolutionary tool for transcriptomics. Nature Rev. Genet. 10, 57-63 (2009).
15. Brawand, D. et al. The evolution of gene expression levels in mammalian organs. Nature 478, 343-348 (2011).
16. Perry, G. H. et al. Comparative RNA sequencing reveals substantial genetic variation in endangered primates. Genome Res. 22, 602-610 (2012).
17. Gelfman, S. et al. Changes in exon-intron structure during vertebrate evolution affect the splicing pattern of exons. Genome Res. 22, 35-50 (2012).
18. Marioni, J. C., Mason, C. E., Mane, S. M., Stephens, M. & Gilad, Y. RNA-seq: an assessment of technical reproducibility and comparison with gene expression arrays. Genome Res. 18, 1509-1517 (2008).
19. Lemos, B., Meiklejohn, C. D., Caceres, M. & Hartl, D. L. Rates of divergence in gene expression profiles of primates, mice, and flies: stabilizing selection and variability among functional categories. Evolution 59, 126-137 (2005).
20. Rifkin, S. A., Kim, J. & White, K. P. Evolution of gene expression in the Drosophila melanogaster subgroup. Nature Genet. 33, 138-144 (2003).
21. Rifkin, S. A., Houle, D., Kim, J. & White, K. P. A mutation accumulation assay reveals extensive capacity for rapid gene expression evolution. Nature 438, 220-223 (2005).
22. Gilad, Y., Oshlack, A., Smyth, G. K., Speed, T. P. & White, K. P. Expression profiling in primates reveals a rapid evolution of human transcription factors. Nature 440, 242-245 (2006).
23. Wrangham, R. W., Jones, J. H., Laden, G., Pilbeam, D. & Conklin-Brittain, N. The raw and the stolen. Cooking and the ecology of human origins. Curr. Anthropol. 40, 567-594 (1999).
24. Finch, C. E. & Stanford, C. B. Meat-adaptive genes and the evolution of slower aging in humans. Q. Rev. Biol. 51, 3-50 (2004).
25. Nowick, K., Gernat, T., Almaas, E. & Stubbs, L. Differences in human and chimpanzee gene expression patterns define an evolving network of transcription factors in brain. Proc. Natl Acad. Sci. 106, 22358-22363 (2009).
26. Guohua Xu, A. et al. Intergenic and repeat transcription in human, chimpanzee and macaque brains measured by RNA-seq. PLoS Comput. Biol. 6, e1000843 (2010).
27. Somel, M. et al. Transcriptional neoteny in the human brain. Proc. Natl Acad. Sci. 106, 5743-5748 (2009).
28. Khaitovich, P. et al. A neutral model of transcriptome evolution. PLoS Biol. 2, e132 (2004).
29. Khaitovich, P., Enard, W., Lachmann, M. & Paabo, S. Evolution of primate gene expression. Nature Rev. Genet. 7, 693-702 (2006).
30. Blekhman, R., Marioni, J. C., Zumbo, P., Stephens, M. & Gilad, Y. Sex-specific and lineage-specific alternative splicing in primates. Genome Res. 20, 180-189 (2010).
31. Enard, W. et al. Intra-and interspecific variation in primate gene expression patterns. Science 296, 340-343 (2002).
32. Blekhman, R., Oshlack, A., Chabot, A. E., Smyth, G. K. & Gilad, Y. Gene regulation in primates evolves under tissue-specific selection pressures. PLoS Genet. 4, e1000271 (2008).
33. Valen, E. & Sandelin, A. Genomic and chromatin signals underlying transcription start-site selection. Trends Genet. 27, 475-485 (2011).
34. Cooper, G. M. & Shendure, J. Needles in stacks of needles: finding disease-causal variants in a wealth of genomic data. Nature Rev. Genet. 12, 628-640 (2011).
35. Schmidt, D. et al. Five-vertebrate ChIP-seq reveals the evolutionary dynamics of transcription factor binding. Science 328, 1036-1040 (2010).
36. Kasowski, M. et al. Variation in transcription factor binding among humans. Science 328, 232-235 (2010).
37. O'Doherty, A. et al. An aneuploid mouse strain carrying human chromosome 21 with Down syndrome phenotypes. Science 309, 2033-2037 (2005).
38. Wilson, M. D. et al. Species-specific transcription in mice carrying human chromosome 21. Science 322, 434-438 (2008).
39. Heintzman, N. D. et al. Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nature Genet. 39, 311-318 (2007).
40. Cain, C. E., Blekhman, R., Marioni, J. C. & Gilad, Y. Gene expression differences among primates are associated with changes in a histone epigenetic modification. Genetics 187, 1225-1234 (2011).
41. Schneider, R. et al. Histone H3 lysine 4 methylation patterns in higher eukaryotic genes. Nature Cell Biol. 6, 73-77 (2004).
42. Prabhakar, S. et al. Human-specific gain of function in a developmental enhancer. Science 321, 1346-1350 (2008).
43. Pai, A. A., Bell, J. T., Marioni, J. C., Pritchard, J. K. & Gilad, Y. A genome-wide study of DNA methylation patterns and gene expression levels in multiple human and chimpanzee tissues. PLoS Genet. 7, e1001316 (2011).
44. Molaro, A. et al. Sperm methylation profiles reveal features of epigenetic inheritance and evolution in primates. Cell 146, 1029-1041 (2011).
45. Martin, D. I. et al. Phyloepigenomic comparison of great apes reveals a correlation between somatic and germline methylation states. Genome Res. 21, 2049-2057 (2011).
46. Murrell, A., Rakyan, V. K. & Beck, S. From genome to epigenome. Hum. Mol. Genet. 14 (Suppl. 1), R3-R10 (2005).
47. Jaenisch, R. & Bird, A. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nature Genet. 33, 245-254 (2003).
48. Hu, H. Y. et al. MicroRNA expression and regulation in human, chimpanzee, and macaque brains. PLoS Genet. 7, e1002327 (2011).
49. Somel, M. et al. MicroRNA-driven developmental remodeling in the brain distinguishes humans from other primates. PLoS Biol. 9, e1001214 (2011).
50. McLean, C. Y. et al. Human-specific loss of regulatory DNA and the evolution of human-specific traits. Nature 471, 216-219 (2011).
51. Crocoll, A., Zhu, C. Q. C., Cato, A. C. B. & Blum, M. Expression of androgen receptor mRNA during mouse embryogenesis. Mech. Dev. 72, 175-178 (1998).
52. Dixson, A. F. Effects of testosterone on the sternal cutaneous glands and genitalia of the male greater galago (Galago crassicaudatus crassicaudatus). Folia Primatol. 26, 207-213 (1976).
53. Pollard, K. S. et al. An RNA gene expressed during cortical development evolved rapidly in humans. Nature 443, 167-172 (2006).
54. Enard, W. et al. A humanized version of Foxp2 affects cortico-basal ganglia circuits in mice. Cell 137, 961-971 (2009).
55. Enard, W. et al. Molecular evolution of FOXP2, a gene involved in speech and language. Nature 418, 869-872 (2002).
56. Sholtis, S. J. & Noonan, J. P. Gene regulation and the origins of human biological uniqueness. Trends Genet. 26, 110-118; erratum 26, 344 (2010).
57. Barrett, R. D. & Hoekstra, H. E. Molecular spandrels: tests of adaptation at the genetic level. Nature Rev. Genet. 12, 767-780 (2011);
58. corrigendum 13, 70 (2012).
59. Shapiro, M. D. et al. Genetic and developmental basis of evolutionary pelvic reduction in threespine sticklebacks. Nature 428, 717-723 (2004).
60. Chan, Y. F. et al. Adaptive evolution of pelvic reduction in sticklebacks by recurrent deletion of a Pitx1 enhancer. Science 327, 302-305 (2010).
61. Manceau, M., Domingues, V. S., Mallarino, R. & Hoekstra, H. E. The developmental role of Agouti in color pattern evolution. Science 331, 1062-1065 (2011).
62. Reed, R. D. et al. Optix drives the repeated convergent evolution of butterfly wing pattern mimicry. Science 333, 1137-1141 (2011).
63. Barriere, A., Gordon, K. L. & Ruvinsky, I. Distinct functional constraints partition sequence conservation in a cis-regulatory element. PLoS Genet. 7, e1002095 (2011).
64. Crocker, J., Tamori, Y. & Erives, A. Evolution acts on enhancer organization to fine-tune gradient threshold readouts. PLoS Biol. 6, 2576-2587 (2008).
65. Fowlkes, C. C. et al. A conserved developmental patterning network produces quantitatively different output in multiple species of Drosophila. PLoS Genet. 7, e1002346 (2011).
66. Ludwig, M. Z., Manu, Kittler, R., White, K. P. & Kreitman, M. Consequences of eukaryotic enhancer architecture for gene expression dynamics, development, and fitness. PLoS Genet. 7, e1002364 (2011).
67. Ludwig, M. Z. et al. Functional evolution of a cis-regulatory module. PLoS Biol. 3, 588-598 (2005).
68. Bullard, J. H., Mostovoy, Y., Dudoit, S. & Brem, R. B. Polygenic and directional regulatory evolution across pathways in Saccharomyces. Proc. Natl Acad. Sci. 107, 5058-5063 (2010).
69. Gerke, J., Lorenz, K. & Cohen, B. Genetic interactions between transcription factors cause natural variation in yeast. Science 323, 498-501 (2009).
70. Gertz, J., Gerke, J. P. & Cohen, B. A. Epistasis in a quantitative trait captured by a molecular model of transcription factor interactions. Theoret. Popul. Biol. 77, 1-5 (2010).
71. Gerke, J., Lorenz, K., Ramnarine, S. & Cohen, B. Gene-environment interactions at nucleotide resolution. PLoS Genet. 6, e1001144 (2010).
72. Doebley, J., Stec, A. & Gustus, C. Teosinte Branched1 and the origin of maize-evidence for epistasis and the evolution of dominance. Genetics 141, 333-346 (1995).
73. Clark, R. M., Wagler, T. N., Quijada, P. & Doebley, J. A distant upstream enhancer at the maize domestication gene tb1 has pleiotropic effects on plant and inflorescent architecture. Nature Genet. 38, 594-597 (2006).
74. Studer, A., Zhao, Q., Ross-Ibarra, J. & Doebley, J. Identification of a functional transposon insertion in the maize domestication gene tb1. Nature Genet. 43, 1160-1164 (2011).
75. Rebeiz, M., Jikomes, N., Kassner, V. A. & Carroll, S. B. Evolutionary origin of a novel gene expression pattern through co option of the latent activities of existing regulatory sequences. Proc. Natl Acad. Sci. 108, 10036-10043 (2011).
76. Hoekstra, H. E., Hirschmann, R. J., Bundey, R. A., Insel, P. A. & Crossland, J. P. A single amino acid mutation contributes to adaptive beach mouse color pattern. Science 313, 101-104 (2006).
77. Will, J. L. et al. Incipient balancing selection through adaptive loss of aquaporins in natural Saccharomyces cerevisiae populations. PLoS Genet. 6, e1000893 (2010).
78. Brem, R. B., Yvert, G., Clinton, R. & Kruglyak, L. Genetic dissection of transcriptional regulation in budding yeast. Science 296, 752-755 (2002).
79. Ronald, J., Brem, R. B., Whittle, J. & Kruglyak, L. Local regulatory variation in Saccharomyces cerevisiae. PLoS Genet. 1, e25 (2005).
80. Tirosh, I., Reikhav, S., Levy, A. A. & Barkai, N. A. Yeast hybrid provides insight into the evolution of gene expression regulation. Science 324, 659-662 (2009).
81. Wittkopp, P. J., Haerum, B. K. & Clark, A. G. Regulatory changes underlying expression differences within and between Drosophila species. Nature Genet. 40, 346-350 (2008).
82. Doniger, S. W. & Fay, J. C. Frequent gain and loss of functional transcription factor binding sites. PLoS Comput. Biol. 3, 932-942 (2007).
83. Bradley, R. K. et al. Binding site turnover produces pervasive quantitative changes in transcription factor binding between closely related Drosophila species. PLoS Biol. 8, e1000343 (2010).
84. Tirosh, I., Sigal, N. & Barkai, N. Divergence of nucleosome positioning between two closely related yeast species: genetic basis and functional consequences. Mol. Syst. Biol. 6, 365 (2010).
85. Gordon, K. L. & Ruvinsky, I. Tempo and mode in evolution of transcriptional regulation. PLoS Genet. 8, e1002432 (2012).
86. Landry, C. R. et al. Compensatory cis-trans evolution and the dysregulation of gene expression in interspecific hybrids of Drosophila. Genetics 171, 1813-1822 (2005).
87. Ernst, J. et al. Mapping and analysis of chromatin state dynamics in nine human cell types. Nature 473, 43-49 (2011).
88. Degner, J. F. et al. DNase I sensitivity QTLs are a major determinant of human expression variation. Nature 482, 390-394 (2012).
89. Field, Y. et al. Gene expression divergence in yeast is coupled to evolution of DNA-encoded nucleosome organization. Nature Genet. 41, 438-445 (2009).
90. Tsankov, A., Yanagisawa, Y., Rhind, N., Regev, A. & Rando, O. J. Evolutionary divergence of intrinsic and trans-regulated nucleosome positioning sequences reveals plastic rules for chromatin organization. Genome Res. 21, 1851-1862 (2011).
91. Tsankov, A. M., Thompson, D. A., Socha, A., Regev, A. & Rando, O. J. The role of nucleosome positioning in the evolution of gene regulation. PLoS Biol. 8, e1000414 (2010).
92. Tsui, K. et al. Evolution of nucleosome occupancy: conservation of global properties and divergence of gene-specific patterns. Mol. Cell. Biol. 31, 4348-4355 (2011).
93. Vinces, M. D., Legendre, M., Caldara, M., Hagihara, M. & Verstrepen, K. J. Unstable tandem repeats in promoters confer transcriptional evolvability. Science 324, 1213-1216 (2009).
94. Tirosh, I., Reikhav, S., Sigal, N., Assia, Y. & Barkai, N. Chromatin regulators as capacitors of interspecies variations in gene expression. Mol. Syst. Biol. 6, 435 (2010).
95. Bourque, G. et al. Evolution of the mammalian transcription factor binding repertoire via transposable elements. Genome Res. 18, 1752-1762 (2008).
96. Lynch, V. J., Leclerc, R. D., May, G. & Wagner, G. P. Transposon-mediated rewiring of gene regulatory networks contributed to the evolution of pregnancy in mammals. Nature Genet. 43, 1154-1158 (2011).
97. Smith, A. M. et al. A novel mode of enhancer evolution: the Tal1 stem cell enhancer recruited a MIR element to specifically boost its activity. Genome Res. 18, 1422-1432 (2008).
98. Eichenlaub, M. P. & Ettwiller, L. De novo genesis of enhancers in vertebrates. PLoS Biol. 9, e1001188 (2011).
99. Alonso, C. R. & Wilkins, A. S. The molecular elements that underlie developmental evolution. Nature Rev. Genet. 6, 709-715 (2005).
100. Dori-Bachash, M., Shema, E. & Tirosh, I. Coupled evolution of transcription and mRNA degradation. PLoS Biol. 9, e1001106 (2011).
101. Segal, E. & Widom, J. From DNA sequence to transcriptional behaviour: a quantitative approach. Nature Rev. Genet. 10, 443-456 (2009).
102. Janssens, H. et al. Quantitative and predictive model of transcriptional control of the Drosophila melanogaster even skipped gene. Nature Genet. 38, 1159-1165 (2006).
103. Segal, E., Raveh-Sadka, T., Schroeder, M., Unnerstall, U. & Gaul, U. Predicting expression patterns from regulatory sequence in Drosophila segmentation. Nature 451, 535-540 (2008).
104. Raveh-Sadka, T., Levo, M. & Segal, E. Incorporating nucleosomes into thermodynamic models of transcription regulation. Genome Res. 19, 1480-1496 (2009).
105. Wasson, T. & Hartemink, A. J. An ensemble model of competitive multi-factor binding of the genome. Genome Res. 19, 2101-2112 (2009).
106. Landolin, J. M. et al. Sequence features that drive human promoter function and tissue specificity. Genome Res. 20, 890-898 (2010).
107. Kimura, M. Genetic variability maintained in a finite population due to mutational production of neutral and nearly neutral isoalleles. Genet. Res. 11, 247-269 (1968).
108. Kimura, M. in The Neutral Theory 34-55 (Cambridge Univ. Press, 1983).
109. Lande, R. Natural-selection and random genetic drift in phenotypic evolution. Evolution 30, 314-334 (1976).
110. Lynch, M. & Hill, W. G. Phenotypic evolution by neutral mutation. Evolution 40, 915-935 (1986).
111. Pickrell, J. K. et al. Signals of recent positive selection in a worldwide sample of human populations. Genome Res. 19, 826-837 (2009).
112. Sabeti, P. C. et al. Genome-wide detection and characterization of positive selection in human populations. Nature 449, 913-918 (2007).
113. Voight, B. F., Kudaravalli, S., Wen, X. & Pritchard, J. K. A map of recent positive selection in the human genome. PLoS Biol. 4, e72 (2006).
114. Williamson, S. H. et al. Localizing recent adaptive evolution in the human genome. PLoS Genet. 3, e90 (2007).
115. Teshima, K. M., Coop, G. & Przeworski, M. How reliable are empirical genomic scans for selective sweeps? Genome Res. 16, 702-712 (2006).
116. Akey, J. M. Constructing genomic maps of positive selection in humans: where do we go from here? Genome Res. 19, 711-722 (2009).
117. Tan, C. L. & Drake, J. H. Evidence of tree gouging and exudate eating in pygmy slow lorises (Nycticebus pygmaeus). Folia Primatol. 72, 37-39 (2001).
118. Swapna, N., Radhakrishna, S., Gupta, A. K. & Kumar, A. Exudativory in the Bengal slow loris (Nycticebus bengalensis) in Trishna Wildlife Sanctuary, Tripura, northeast India. Am. J. Primatol. 72, 113-121 (2010).
119. Sakabe, N. J. & Nobrega, M. A. Genome-wide maps of transcription regulatory element. Wiley Interdiscip. Rev. Syst. Biol. Med. 2, 422-437 (2010).
120. Scally, A. et al. Insights into hominid evolution from the gorilla genome sequence. Nature 483, 169-175 (2012).