How do regulatory networks evolve and expand throughout evolution?

Current Opinion in Biotechnology

Volumn 34, Issue , 2015, Pages 180-188

  Voordeckers, Karin ^a,b   Pougach, Ksenia ^a,b   Verstrepen, Kevin J ^a,b  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

GENES; TRANSCRIPTION FACTORS;

DNA BINDING; EVOLVABILITY; GENE FUNCTION; GENE NETWORKS; INTERACTION DOMAIN; NOVEL GENES; REGULATORY NETWORK; SUBFUNCTIONALIZATION;

TRANSCRIPTION;

TRANSCRIPTION FACTOR;

DNA BINDING; GENE; GENE DUPLICATION; GENE FUNCTION; GENE MUTATION; GENE REGULATORY NETWORK; MOLECULAR EVOLUTION; PRIORITY JOURNAL; PROMOTER REGION; REVIEW; ANIMAL; GENETIC TRANSCRIPTION; GENOME; HUMAN; MUTATION;

ANIMALS; EVOLUTION, MOLECULAR; GENE REGULATORY NETWORKS; GENOME; HUMANS; MUTATION; PROMOTER REGIONS, GENETIC; TRANSCRIPTION, GENETIC;

EID: 84923310169     PISSN: 09581669     EISSN: 18790429     Source Type: Journal    
DOI: 10.1016/j.copbio.2015.02.001     Document Type: Review

References (68)

1. Gu X., Zhang Z., Huang W. Rapid evolution of expression and regulatory divergences after yeast gene duplication. Proc Natl Acad Sci U S A 2005, 102:707-712.
2. Gu Z., Rifkin S.A., White K.P., Li W.H. Duplicate genes increase gene expression diversity within and between species. Nat Genet 2004, 36:577-579.
3. Arnoult L., Su K.F., Manoel D., Minervino C., Magrina J., Gompel N., Prud'homme B. Emergence and diversification of fly pigmentation through evolution of a gene regulatory module. Science 2013, 339:1423-1426.
4. King M.C., Wilson A.C. Evolution at two levels in humans and chimpanzees. Science 1975, 188:107-116.
5. Prud'homme B., Gompel N., Rokas A., Kassner V.A., Williams T.M., Yeh S.D., True J.R., Carroll S.B. Repeated morphological evolution through cis-regulatory changes in a pleiotropic gene. Nature 2006, 440:1050-1053.
6. Reed R.D., Papa R., Martin A., Hines H.M., Counterman B.A., Pardo-Diaz C., Jiggins C.D., Chamberlain N.L., Kronforst M.R., Chen R., et al. optix drives the repeated convergent evolution of butterfly wing pattern mimicry. Science 2011, 333:1137-1141.
7. Shapiro M.D., Marks M.E., Peichel C.L., Blackman B.K., Nereng K.S., Jonsson B., Schluter D., Kingsley D.M. Genetic and developmental basis of evolutionary pelvic reduction in threespine sticklebacks. Nature 2004, 428:717-723.
8. Wray G.A. The evolutionary significance of cis-regulatory mutations. Nat Rev Genet 2007, 8:206-216.
9. Tirosh I., Barkai N., Verstrepen K.J. Promoter architecture and the evolvability of gene expression. J Biol 2009, 8:95.
10. Ihmels J., Bergmann S., Gerami-Nejad M., Yanai I., McClellan M., Berman J., Barkai N. Rewiring of the yeast transcriptional network through the evolution of motif usage. Science 2005, 309:938-940.
11. Jones F.C., Grabherr M.G., Chan Y.F., Russell P., Mauceli E., Johnson J., Swofford R., Pirun M., Zody M.C., White S., et al. The genomic basis of adaptive evolution in threespine sticklebacks. Nature 2012, 484:55-61.
12. Babu M.M., Luscombe N.M., Aravind L., Gerstein M., Teichmann S.A. Structure and evolution of transcriptional regulatory networks. Curr Opin Struct Biol 2004, 14:283-291.
13. Borneman A.R., Gianoulis T.A., Zhang Z.D., Yu H., Rozowsky J., Seringhaus M.R., Wang L.Y., Gerstein M., Snyder M. Divergence of transcription factor binding sites across related yeast species. Science 2007, 317:815-819.
14. Bradley R.K., Li X.Y., Trapnell C., Davidson S., Pachter L., Chu H.C., Tonkin L.A., Biggin M.D., Eisen M.B. Binding site turnover produces pervasive quantitative changes in transcription factor binding between closely related Drosophila species. PLoS Biol 2010, 8:e1000343.
15. Odom D.T., Dowell R.D., Jacobsen E.S., Gordon W., Danford T.W., MacIsaac K.D., Rolfe P.A., Conboy C.M., Gifford D.K., Fraenkel E. Tissue-specific transcriptional regulation has diverged significantly between human and mouse. Nat Genet 2007, 39:730-732.
16. Carroll S.B. Evolution at two levels: on genes and form. PLoS Biol 2005, 3:e245.
17. Prud'homme B., Gompel N., Carroll S.B. Emerging principles of regulatory evolution. Proc Natl Acad Sci U S A 2007, 104(Suppl 1):8605-8612.
18. Hsia C.C., McGinnis W. Evolution of transcription factor function. Curr Opin Genet Dev 2003, 13:199-206.
19. Bustamante C.D., Fledel-Alon A., Williamson S., Nielsen R., Hubisz M.T., Glanowski S., Tanenbaum D.M., White T.J., Sninsky J.J., Hernandez R.D., et al. Natural selection on protein-coding genes in the human genome. Nature 2005, 437:1153-1157.
20. Yvert G., Brem R.B., Whittle J., Akey J.M., Foss E., Smith E.N., Mackelprang R., Kruglyak L. Trans-acting regulatory variation in Saccharomyces cerevisiae and the role of transcription factors. Nat Genet 2003, 35:57-64.
21. Brem R.B., Yvert G., Clinton R., Kruglyak L. Genetic dissection of transcriptional regulation in budding yeast. Science 2002, 296:752-755.
22. Grove C.A., De Masi F., Barrasa M.I., Newburger D.E., Alkema M.J., Bulyk M.L., Walhout A.J. A multiparameter network reveals extensive divergence between C. elegans bHLH transcription factors. Cell 2009, 138:314-327.
23. Reece-Hoyes J.S., Pons C., Diallo A., Mori A., Shrestha S., Kadreppa S., Nelson J., Diprima S., Dricot A., Lajoie B.R., et al. Extensive rewiring and complex evolutionary dynamics in a C. elegans multiparameter transcription factor network. Mol Cell 2013, 51:116-127.
24. Lynch V.J., May G., Wagner G.P. Regulatory evolution through divergence of a phosphoswitch in the transcription factor CEBPB. Nature 2011, 480:383-386.
25. Sayou C., Monniaux M., Nanao M.H., Moyroud E., Brockington S.F., Thevenon E., Chahtane H., Warthmann N., Melkonian M., Zhang Y., et al. A promiscuous intermediate underlies the evolution of LEAFY DNA binding specificity. Science 2014, 343:645-648.
26. Madan Babu M., Teichmann S.A., Aravind L. Evolutionary dynamics of prokaryotic transcriptional regulatory networks. J Mol Biol 2006, 358:614-633.
27. Weirauch M.T., Yang A., Albu M., Cote A.G., Montenegro-Montero A., Drewe P., Najafabadi H.S., Lambert S.A., Mann I., Cook K., et al. Determination and inference of eukaryotic transcription factor sequence specificity. Cell 2014, 158:1431-1443.
28. Hoekstra H.E., Coyne J.A. The locus of evolution: evo devo and the genetics of adaptation. Evolution 2007, 61:995-1016.
29. Falciani F., Hausdorf B., Schroder R., Akam M., Tautz D., Denell R., Brown S. Class 3 Hox genes in insects and the origin of zen. Proc Natl Acad Sci U S A 1996, 93:8479-8484.
30. Hernandez-Hernandez T., Martinez-Castilla L.P., Alvarez-Buylla E.R. Functional diversification of B MADS-box homeotic regulators of flower development: adaptive evolution in protein-protein interaction domains after major gene duplication events. Mol Biol Evol 2007, 24:465-481.
31. Teichmann S.A., Babu M.M. Gene regulatory network growth by duplication. Nat Genet 2004, 36:492-496.
32. Thompson D.A., Roy S., Chan M., Styczynsky M.P., Pfiffner J., French C., Socha A., Thielke A., Napolitano S., Muller P., et al. Evolutionary principles of modular gene regulation in yeasts. Elife (Cambridge) 2013, 2:e00603.
33. Wapinski I., Pfeffer A., Friedman N., Regev A. Natural history and evolutionary principles of gene duplication in fungi. Nature 2007, 449:54-61.
34. Wapinski I., Pfiffner J., French C., Socha A., Thompson D.A., Regev A. Gene duplication and the evolution of ribosomal protein gene regulation in yeast. Proc Natl Acad Sci U S A 2010, 107:5505-5510.
35. Conant G.C., Wolfe K.H. Turning a hobby into a job: how duplicated genes find new functions. Nat Rev Genet 2008, 9:938-950.
36. Lynch M., Conery J.S. The evolutionary fate and consequences of duplicate genes. Science 2000, 290:1151-1155.
37. Madan Babu M., Teichmann S.A. Evolution of transcription factors and the gene regulatory network in Escherichia coli. Nucleic Acids Res 2003, 31:1234-1244.
38. Teichmann S.A., Park J., Chothia C. Structural assignments to the Mycoplasma genitalium proteins show extensive gene duplications and domain rearrangements. Proc Natl Acad Sci U S A 1998, 95:14658-14663.
39. Ohno S. Evolution by Gene Duplication 1970, Springer-Verlag, Berlin.
40. Lynch M., Force A. The probability of duplicate gene preservation by subfunctionalization. Genetics 2000, 154:459-473.
41. Bridgham J.T., Brown J.E., Rodriguez-Mari A., Catchen J.M., Thornton J.W. Evolution of a new function by degenerative mutation in cephalochordate steroid receptors. PLoS Genet 2008, 4:e1000191.
42. Perez J.C., Fordyce P.M., Lohse M.B., Hanson-Smith V., DeRisi J.L., Johnson A.D. How duplicated transcription regulators can diversify to govern the expression of nonoverlapping sets of genes. Genes Dev 2014, 28:1272-1277.
43. Pougach K., Voet A., Kondrashov F.A., Voordeckers K., Christiaens J.F., Baying B., Benes V., Sakai R., Aerts J., Zhu B., et al. Duplication of a promiscuous transcription factor drives the emergence of a new regulatory network. Nat Commun 2014, 5:4868.
44. Voordeckers K., Brown C.A., Vanneste K., van der Zande E., Voet A., Maere S., Verstrepen K.J. Reconstruction of ancestral metabolic enzymes reveals molecular mechanisms underlying evolutionary innovation through gene duplication. PLoS Biol 2012, 10:e1001446.
45. Baker C.R., Hanson-Smith V., Johnson A.D. Following gene duplication, paralog interference constrains transcriptional circuit evolution. Science 2013, 342:104-108.
46. Bridgham J.T., Carroll S.M., Thornton J.W. Evolution of hormone-receptor complexity by molecular exploitation. Science 2006, 312:97-101.
47. Carroll S.M., Ortlund E.A., Thornton J.W. Mechanisms for the evolution of a derived function in the ancestral glucocorticoid receptor. PLoS Genet 2011, 7:e1002117.
48. Conant G.C., Wolfe K.H. Functional partitioning of yeast co-expression networks after genome duplication. PLoS Biol 2006, 4:e109.
49. Brown C.A., Murray A.W., Verstrepen K.J. Rapid expansion and functional divergence of subtelomeric gene families in yeasts. Curr Biol 2010, 20:895-903.
50. McKeown A.N., Bridgham J.T., Anderson D.W., Murphy M.N., Ortlund E.A., Thornton J.W. Evolution of DNA specificity in a transcription factor family produced a new gene regulatory module. Cell 2014, 159:58-68.
51. Tzeng S.R., Kalodimos C.G. Protein activity regulation by conformational entropy. Nature 2012, 488:236-240.
52. Aharoni A., Gaidukov L., Khersonsky O., Mc Q.G.S., Roodveldt C., Tawfik D.S. The 'evolvability' of promiscuous protein functions. Nat Genet 2005, 37:73-76.
53. Khersonsky O., Tawfik D.S. Enzyme promiscuity: a mechanistic and evolutionary perspective. Annu Rev Biochem 2010, 79:471-505.
54. Badis G., Berger M.F., Philippakis A.A., Talukder S., Gehrke A.R., Jaeger S.A., Chan E.T., Metzler G., Vedenko A., Chen X., et al. Diversity and complexity in DNA recognition by transcription factors. Science 2009, 324:1720-1723.
55. Nakagawa S., Gisselbrecht S.S., Rogers J.M., Hartl D.L., Bulyk M.L. DNA-binding specificity changes in the evolution of forkhead transcription factors. Proc Natl Acad Sci U S A 2013, 110:12349-12354.
56. 2 zinc finger DNA binding. Mol Cell 2014, 55:640-648.
57. Lynch M., Katju V. The altered evolutionary trajectories of gene duplicates. Trends Genet 2004, 20:544-549.
58. Hittinger C.T., Carroll S.B. Gene duplication and the adaptive evolution of a classic genetic switch. Nature 2007, 449:677-681.
59. Babu M.M., Iyer L.M., Balaji S., Aravind L. The natural history of the WRKY-GCM1 zinc fingers and the relationship between transcription factors and transposons. Nucleic Acids Res 2006, 34:6505-6520.
60. Balaji S., Babu M.M., Iyer L.M., Aravind L. Discovery of the principal specific transcription factors of Apicomplexa and their implication for the evolution of the AP2-integrase DNA binding domains. Nucleic Acids Res 2005, 33:3994-4006.
61. Bourque G., Leong B., Vega V.B., Chen X., Lee Y.L., Srinivasan K.G., Chew J.L., Ruan Y., Wei C.L., Ng H.H., et al. Evolution of the mammalian transcription factor binding repertoire via transposable elements. Genome Res 2008, 18:1752-1762.
62. Jacques P.E., Jeyakani J., Bourque G. The majority of primate-specific regulatory sequences are derived from transposable elements. PLoS Genet 2013, 9:e1003504.
63. Jordan I.K., Rogozin I.B., Glazko G.V., Koonin E.V. Origin of a substantial fraction of human regulatory sequences from transposable elements. Trends Genet 2003, 19:68-72.
64. Kunarso G., Chia N.Y., Jeyakani J., Hwang C., Lu X., Chan Y.S., Ng H.H., Bourque G. Transposable elements have rewired the core regulatory network of human embryonic stem cells. Nat Genet 2010, 42:631-634.
65. Xie D., Chen C.C., Ptaszek L.M., Xiao S., Cao X., Fang F., Ng H.H., Lewin H.A., Cowan C., Zhong S. Rewirable gene regulatory networks in the preimplantation embryonic development of three mammalian species. Genome Res 2010, 20:804-815.
66. Cheatle Jarvela A.M., Brubaker L., Vedenko A., Gupta A., Armitage B.A., Bulyk M.L., Hinman V.F. Modular evolution of DNA-binding preference of a Tbrain transcription factor provides a mechanism for modifying gene regulatory networks. Mol Biol Evol 2014, 31:2672-2688.
67. Brockington S.F., Moyroud E., Sayou C., Monniaux M., Nanao M.H., Thevenon E., Chahtane H., Warthmann N., Melkonian M., Zhang Y., et al. Evolution. Response to Comment on "A promiscuous intermediate underlies the evolution of LEAFY DNA binding specificity". Science 2015, 347:621.
68. Brunkard J.O., Runkel A.M., Zambryski P.C. Evolution. Comment on "A promiscuous intermediate underlies the evolution of LEAFY DNA binding specificity". Science 2015, 347:621.