Intersecting transcription networks constrain gene regulatory evolution

Nature

Volumn 523, Issue 7560, 2015, Pages 361-365

  Sorrells, Trevor R ^a,b   Booth, Lauren N ^a,b,c   Tuch, Brian B ^a,b,d   Johnson, Alexander D ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c STANFORD UNIVERSITY   (United States)

^d Loxo Oncology Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL DNA; PHEROMONE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR STE12; UNCLASSIFIED DRUG; DNA BINDING PROTEIN; MATING FACTOR; PEPTIDE; SACCHAROMYCES CEREVISIAE PROTEIN; STE12 PROTEIN, S CEREVISIAE;

ANCESTRY; EPISTASIS; EVOLUTIONARY BIOLOGY; GENE EXPRESSION; PHEROMONE; YEAST;

ARTICLE; BINDING SITE; CONTROLLED STUDY; FUNGAL CELL; GENE REGULATORY NETWORK; GENETIC TRANSCRIPTION; MATING TYPE; MOLECULAR EVOLUTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING; SACCHAROMYCES CEREVISIAE; DRUG EFFECTS; ENHANCER REGION; EPISTASIS; FUNGAL GENE; GENE EXPRESSION REGULATION; GENETICS; KLUYVEROMYCES; METABOLISM; NUCLEOTIDE SEQUENCE; PROMOTER REGION;

BASE SEQUENCE; BINDING SITES; DNA, FUNGAL; DNA-BINDING PROTEINS; ENHANCER ELEMENTS, GENETIC; EPISTASIS, GENETIC; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION, FUNGAL; GENE REGULATORY NETWORKS; GENES, FUNGAL; KLUYVEROMYCES; MATING FACTOR; PEPTIDES; PHEROMONES; PROMOTER REGIONS, GENETIC; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSCRIPTION FACTORS;

EID: 84937509257     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature14613     Document Type: Article

References (49)

1. Blount, Z. D., Borland, C. Z. & Lenski, R. E. Historical contingency and the evolution of a key innovation in an experimental population of Escherichia coli. Proc. Natl Acad. Sci. USA 105, 7899-7906 (2008).
2. Harms, M. J. & Thornton, J. W. Historical contingency and its biophysical basis in glucocorticoid receptor evolution. Nature 512, 203-207 (2014).
3. Mohrig, J. R. et al. Importance of historical contingency in the stereochemistry of hydratase-dehydratase enzymes. Science 269, 527-529 (1995).
4. Harms, M. J. & Thornton, J. W. Evolutionary biochemistry: revealing the historical and physical causes of protein properties. Nature Rev. Genet. 14, 559-571 (2013).
5. Ortlund, E. A., Bridgham, J. T., Redinbo, M. R. & Thornton, J. W. Crystal structure of an ancient protein: evolution by conformational epistasis. Science 317, 1544-1548 (2007).
6. Bershtein, S., Segal, M., Bekerman, R., Tokuriki, N. & Tawfik, D. S. Robustnessepistasis link shapes the fitness landscape of a randomly drifting protein. Nature 444, 929-932 (2006).
7. Bloom, J. D., Labthavikul, S. T., Otey, C. R. & Arnold, F. H. Protein stability promotes evolvability. Proc. Natl Acad. Sci. USA 103, 5869-5874 (2006).
8. Gerke, J., Lorenz, K. & Cohen, B. Genetic interactions between transcription factors cause natural variation in yeast. Science 323, 498-501 (2009).
9. Ren, B. et al. Genome-wide location and function of DNAbinding proteins. Science 290, 2306-2309 (2000).
10. Payne, J. L. & Wagner, A. Constraint and contingency in multifunctional gene regulatory circuits. PLOS Comput. Biol. 9, e1003071 (2013).
11. Dolan, J. W., Kirkman, C. & Fields, S. The yeast STE12 protein binds to the DNA sequence mediating pheromone induction. Proc. Natl Acad. Sci. USA 86, 5703-5707 (1989).
12. Herskowitz, I. MAP kinase pathways in yeast: for mating and more. Cell 80, 187-197 (1995).
13. Coria, R. et al. The pheromone response pathway of Kluyveromyces lactis. FEMS Yeast Res. 6, 336-344 (2006).
14. Kensche, P. R., Oti, M., Dutilh, B. E. & Huynen, M. A. Conservation of divergent transcription in fungi. Trends Genet. 24, 207-211 (2008).
15. Bennett, R. J., Uhl, M. A., Miller, M. G. & Johnson, A. D. Identification and characterization of a Candida albicans mating pheromone. Mol. Cell. Biol. 23, 8189-8201 (2003).
16. Tsong, A. E., Tuch, B. B., Li, H. & Johnson, A. D. Evolution of alternative transcriptional circuits with identical logic. Nature 443, 415-420 (2006).
17. Herskowitz, I. A regulatory hierarchy for cell specialization in yeast. Nature 342, 749-757 (1989).
18. Borneman, A. R. et al. Divergence of transcription factor binding sites across related yeast species. Science 317, 815-819 (2007).
19. Ramos, A. I. & Barolo, S. Low-affinity transcription factor binding sites shape morphogen responses and enhancer evolution. Phil. Trans. R. Soc. Lond. B 368, 20130018 (2013).
20. Crocker, J. et al. Low affinity binding site clusters confer Hox specificity and regulatory robustness. Cell 160, 191-203 (2015).
21. Tsong, A.E., Miller, M. G., Raisner, R.M. & Johnson, A. D. Evolutionof a combinatorial transcriptional circuit: a case study in yeasts. Cell 115, 389-399 (2003).
22. Tuch, B. B., Galgoczy, D. J., Hernday, A. D., Li, H. & Johnson, A. D. The evolution of combinatorial gene regulation in fungi. PLoS Biol. 6, e38 (2008).
23. Baker, C. R., Booth, L. N., Sorrells, T. R. & Johnson, A. D. Protein modularity, cooperative binding, and hybrid regulatory states underlie transcriptional network diversification. Cell 151, 80-95 (2012).
24. Strathern, J., Hicks, J. & Herskowitz, I. Control of cell type in yeast by the mating type locus. The a1-a2 hypothesis. J. Mol. Biol. 147, 357-372 (1981).
25. Galgoczy, D. J. et al. Genomic dissection of the cell-type-specification circuit in Saccharomyces cerevisiae. Proc. Natl Acad. Sci. USA 101, 18069-18074 (2004).
26. Wray, G. A. et al. The evolution of transcriptional regulation in eukaryotes. Mol. Biol. Evol. 20, 1377-1419 (2003).
27. Otto, W. et al. Measuring transcription factor-binding site turnover: a maximum likelihood approach using phylogenies. Genome Biol. Evol. 1, 85-98 (2009).
28. Hubisz, M. J., Pollard, K. S. & Siepel, A. PHAST and RPHAST: phylogenetic analysis with space/time models. Brief. Bioinform. 12, 41-51 (2011).
29. Hare, E. E., Peterson, B. K., Iyer, V. N., Meier, R. & Eisen, M. B. Sepsid even-skipped enhancers are functionally conserved in Drosophila despite lack of sequence conservation. PLoS Genet. 4, e1000106 (2008).
30. Swanson, C. I., Schwimmer, D. B. & Barolo, S. Rapid evolutionary rewiring of a structurally constrained eye enhancer. Curr. Biol. 21, 1186-1196 (2011).
31. Tirosh, I., Weinberger, A., Bezalel, D., Kaganovich, M. & Barkai, N. On the relation between promoter divergence and gene expression evolution. Mol. Syst. Biol. 4, 159 (2008).
32. Wapinski, I., Pfeffer, A., Friedman, N. & Regev, A. Natural history and evolutionary principles of gene duplication in fungi. Nature 449, 54-61 (2007).
33. Gordon, J. L. et al. Evolutionary erosion of yeast sex chromosomes by mating-type switching accidents. Proc. Natl Acad. Sci. USA 108, 20024-20029 (2011).
34. Lusk, R. W. & Eisen, M. B. Spatial promoter recognition signatures may enhance transcription factor specificity in yeast. PLoS ONE 8, e53778 (2013).
35. D'haeseleer, P. What are DNA sequence motifs? Nature Biotechnol. 24, 423-425 (2006).
36. Wach, A. PCR-synthesis of marker cassettes with long flanking homology regions for gene disruptions in S. cerevisiae. Yeast 12, 259-265 (1996).
37. Cormack, B. P. et al. Yeast-enhanced green fluorescent protein (yEGFP): a reporter of gene expression in Candida albicans. Microbiology 143, 303-311 (1997).
38. Tagwerker, C. et al. HB tag modules for PCR-based gene tagging and tandem affinity purification in Saccharomyces cerevisiae. Yeast 23, 623-632 (2006).
39. Kooistra, R., Hooykaas, P. J. J. & Steensma, H. Y. Efficient gene targeting in Kluyveromyces lactis. Yeast 21, 781-792 (2004).
40. Gojkovic, Z., Jahnke, K., Schnackerz, K. D. & Piskur, J. PYD2 encodes 5,6-dihydropyrimidine amidohydrolase, which participates in a novel fungal catabolic pathway. J. Mol. Biol. 295, 1073-1087 (2000).
41. Mitrovich, Q. M., Tuch, B. B., Guthrie, C. & Johnson, A. D. Computational and experimental approaches double the number of known introns in the pathogenic yeast Candida albicans. Genome Res. 17, 492-502 (2007).
42. Booth, L. N., Tuch, B. B. & Johnson, A. D. Intercalation of a new tier of transcription regulation into an ancient circuit. Nature 468, 959-963 (2010).
43. Borneman, A. R. et al. Target hub proteins serve as master regulators of development in yeast. Genes Dev. 20, 435-448 (2006).
44. Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nature Methods 9, 357-359 (2012).
45. Li, H. et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078-2079 (2009).
46. Zhang, Y. et al. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 9, R137 (2008).
47. Homann, O. R. & Johnson, A.D. Mochi View: versatile software for genome browsing and DNA motif analysis. BMC Biol. 8, 49 (2010).
48. Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792-1797 (2004).
49. Posada, D. & Crandall, K. A. Selecting models of nucleotide substitution: an application to human immunodeficiency virus 1 (HIV-1). Mol. Biol. Evol. 18, 897-906 (2001).