ownloaded from genome. cshlp org on November 3, 2010- Published by Cold Spring Harbor Laboratory Press Coevolution within a transcriptional network Holt L, Tuch BB, Vi anson AD, Gygi SP, Morgan DO. 2009. Global elements in 12 Drosophila genomes using evolutionary signature phosphory lation sites provides insights into Storey JD, Tibshirani R. 2003. Statistical significance for genomewide Ihmels J, Bergmann S, Gerami-Nejad M, Yanai I, McClellan M, Berman J, studies. Proc Natl Acad Sci 100: 9440-9445 Storici F, Lewis LK, Resnick MA. 20 he evolution of mot ru 200o, Evoluti oligonucleotides. Nat Biotechnol 19: 773-77 trace analysis of TGF-beta nd related growth factors: Implications for site-directed mutagenesi and mutant Gcn4p in vivo can be different from the dNA ecificities of the corresponding bZip peptides Biol 276: C, Hariharan M, Asabere A, Waszak SM Suckow M, Kisters-Woike B, Hollenberg CP. 1999. A feature of dna 4p bzip peptide with dual DNA binding Kellis M, Patterson N, Endrizzi M, Birren B, Lander ES. 2003. Sequencing and ecificities dependent of half-site spacing. /Mol Biol 286: 983- Kim J, Struhl K. 1995. Determinants of half-site spacing preferences that Lee YC, Yang 1. 2009. Roles of trans a distinguish AP-1 and ATF/CREB bZIP domains. Nucleic Acids Res 23: traspecies evolution of gene expression. Mol Biol Evol 26: 2533-2538 clustering Genome Biol 11: R77. doi: 10. 1186/gb-2010-22-7-17 Landry CR, wittkopp PJ, Taubes CH, Ranz JM, Clark AG, Hartl DL 2005. Tanay A, Regev A, Shamir R. 2005. Conservation and evolvability in rks. Th evolution of ribosomal regulation in yeas expression specific hybrids of Drosophila Genetics 171: Proc Natl Acad Sci 102: 7203-7208 Lavoie H, Hogues H, Mallick J, Sellam A of a transcriptional gulatory network. PLos Biol 8: e1000329 do: 10. 1371/ ation. yeast 14: 565-57 1000329 Tirosh I, Reikhav S, Levy AA, Barkai N. 2009. A yeast hybrid provides insight ongtine MS, McKenzie A Ill, Demarini D, Shah NG, Wach A, Brachat A into the evolution of gene expression regulation. Science 324: 659- Additional modules for versatile and onomical PCR-based gene deletion and modification in Saccharomyces Tsong AE, Tuch BB, Li H, Johnson AD. 2006. Evolution of alt Maclsaac KD, Wang T, Gordon DB, Gifford DK, Stormo GD, Fraenkel E. Tuch BB, Galgoczy DJ, Hemday AD, LiH, onAD.2008. s:1o olutio 2006. An improved map of conserved regu gene regulation in fungi. PLos Biol 6: e38. doi: 10.1371/ MaerkI SJ, Quake SR. 2009. Experimental dete on of the evolvability Wagner GP, Lynch V]. 2008. The gene regulatory logic of transcription factor Trends Ecol Evol 23: 3 Mahony S, nith TJ, Benos PV. 2005. Improved detection of DNA Wapinski I, Pfe Regev A. 2007. Natural history and evolutionary principles of gene duplication in fungi. Nature 449: 54-61 Wapinski I, Pfiffner J, French C, Socha A, Thompson DA, Regev A. 201( Gene duplication and the evolution of ribosomal protein gene Rigaut G, Shevchenko A, Rutz B, wilm M, Mann M, Seraphin B. 1999. A Weng L, Dai H, Zhan Y, He Y, Stepaniants SB, Bassett DE. 2006. Rosetta error generic protein purification method for protein complex characterization model for gene expression analysis. Bioinformatics 22: 1111-112 d proteome exploration. Nat Biotechnol 17: 1030-1032 Rodrigues-Pousada C, Menezes RA, Pimentel C. 2010. The Yap family andits Tybulewicz VL, Fisher EM, Tavare S, Odom DT. 2008. Species-specifi ascription in mice carrying human chromosome 21. Science 322 Y ito m groud ing m bende m GC, Walkley Cr, Maika SD, Fujiwa ecies-divergent globin switching are driven by BCliiA Nature 460: Wittkopp Pl, Haerum BK, Clark AG. 2008. Regulatory changes underlying 093-1097 Kutter C, Watt S, Martinez-Jimenez CP, Mackay S, etau Nray GA. 2007. The evolutionary significan Genetic 1s. factor binding. Science 328: 1036-104onary dynamics of transcription Zheng w, Zhao H, Mancera E, Steinmetz LM, Snyder M. 2010 Shaulian E, Karin M. 2002. AP-1 as a regulator of cell life and death. Nat Cell analysis of variation in transcription factor binding in yeast. i aker M. 2003. M oxidization for microarray data. prediction. Nucleic Acids Res 31: 3406-3415. I biology solutions using R and Bioconductor (ed. VCR Gentleman et al. ) Pp. 397-420. Springer, New Yor Stark A, Lin ME, Kheradpour P, Pedersen Js, Par arison Jw, Crosby M. Rasmussen MD, Roy S, Deoras AN, et al. 2007. Discovery of functional Received June 15, 2010; in revised fonm September 20, 2010. Ger ResearchHolt LJ, Tuch BB, Villen J, Johnson AD, Gygi SP, Morgan DO. 2009. Global analysis of Cdk1 substrate phosphorylation sites provides insights into evolution. Science 325: 1682–1686. Ihmels J, Bergmann S, Gerami-Nejad M, Yanai I, McClellan M, Berman J, Barkai N. 2005. Rewiring of the yeast transcriptional network through the evolution of motif usage. Science 309: 938–940. Innis CA, Shi J, Blundell TL. 2000. Evolutionary trace analysis of TGF-beta and related growth factors: Implications for site-directed mutagenesis. Protein Eng 13: 839–847. Kasowski M, Grubert F, Heffelfinger C, Hariharan M, Asabere A, Waszak SM, Habegger L, Rozowsky J, Shi M, Urban AE, et al. 2010. Variation in transcription factor binding among humans. Science 328: 232–235. Kellis M, Patterson N, Endrizzi M, Birren B, Lander ES. 2003. Sequencing and comparison of yeast species to identify genes and regulatory elements. Nature 423: 241–254. Kim J, Struhl K. 1995. Determinants of half-site spacing preferences that distinguish AP-1 and ATF/CREB bZIP domains. Nucleic Acids Res 23: 2531–2537. Kuo D, Tan K, Zinman G, Ravasi T, Bar-Joseph Z, Ideker T. 2010. Evolutionary divergence in the fungal response to fluconazole revealed by soft clustering. Genome Biol 11: R77. doi: 10.1186/gb-2010-22-7-r77. Landry CR, Wittkopp PJ, Taubes CH, Ranz JM, Clark AG, Hartl DL. 2005. Compensatory cis-trans evolution and the dysregulation of gene expression in interspecific hybrids ofDrosophila. Genetics 171: 1813–1822. Lavoie H, Hogues H, Mallick J, Sellam A, Nantel A, Whiteway M. 2010. Evolutionary tinkering with conserved components of a transcriptional regulatory network. PLoS Biol 8: e1000329. doi: 10.1371/ journal.pbio.1000329. Longtine MS, McKenzie A III, Demarini DJ, Shah NG, Wach A, Brachat A, Philippsen P, Pringle JR. 1998. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14: 953–961. MacIsaac KD, Wang T, Gordon DB, Gifford DK, Stormo GD, Fraenkel E. 2006. An improved map of conserved regulatory sites for Saccharomyces cerevisiae. BMC Bioinformatics 7: 113. doi: 10.1186/1471-2105-7-113. Maerkl SJ, Quake SR. 2009. Experimental determination of the evolvability of a transcription factor. Proc Natl Acad Sci 106: 18650–18655. Mahony S, Golden A, Smith TJ, Benos PV. 2005. Improved detection of DNA motifs using a self-organized clustering of familial binding profiles. Bioinformatics 21: i283–i291. Pazos F, Valencia A. 2008. Protein co-evolution, co-adaptation and interactions. EMBO J 27: 2648–2655. Rigaut G, Shevchenko A, Rutz B, Wilm M, Mann M, Seraphin B. 1999. A generic protein purification method for protein complex characterization and proteome exploration. Nat Biotechnol 17: 1030–1032. Rodrigues-Pousada C, Menezes RA, Pimentel C. 2010. The Yap family and its role in stress response. Yeast 27: 245–258. Sankaran VG, Xu J, Ragoczy T, Ippolito GC, Walkley CR, Maika SD, Fujiwara Y, Ito M, Groudine M, Bender MA, et al. 2009. Developmental and species-divergent globin switching are driven by BCL11A. Nature 460: 1093–1097. Schmidt D, Wilson MD, Ballester B, Schwalie PC, Brown GD, Marshall A, Kutter C, Watt S, Martinez-Jimenez CP, Mackay S, et al. 2010. Five￾vertebrate ChIP-seq reveals the evolutionary dynamics of transcription factor binding. Science 328: 1036–1040. Shaulian E, Karin M. 2002. AP-1 as a regulator of cell life and death. Nat Cell Biol 4: E131–E136. Smyth GK. 2005. Limma: Linear models for microarray data. In Bioinformatics and computational biology solutions using R and Bioconductor (ed. VCR Gentleman et al.), pp. 397–420. Springer, New York. Stark A, Lin MF, Kheradpour P, Pedersen JS, Parts L, Carlson JW, Crosby MA, Rasmussen MD, Roy S, Deoras AN, et al. 2007. Discovery of functional elements in 12 Drosophila genomes using evolutionary signatures. Nature 450: 219–232. Storey JD, Tibshirani R. 2003. Statistical significance for genomewide studies. Proc Natl Acad Sci 100: 9440–9445. Storici F, Lewis LK, Resnick MA. 2001. In vivo site-directed mutagenesis using oligonucleotides. Nat Biotechnol 19: 773–776. Suckow M, Hollenberg CP. 1998. The activation specificities of wild-type and mutant Gcn4p in vivo can be different from the DNA binding specificities of the corresponding bZip peptides in vitro. J Mol Biol 276: 887–902. Suckow M, Kisters-Woike B, Hollenberg CP. 1999. A novel feature of DNA recognition: A mutant Gcn4p bZip peptide with dual DNA binding specificities dependent of half-site spacing. J Mol Biol 286: 983– 987. Sung HM, Wang TY, Wang D, Huang YS, Wu JP, Tsai HK, Tzeng J, Huang CJ, Lee YC, Yang P, et al. 2009. Roles of trans and cis variation in yeast intraspecies evolution of gene expression. Mol Biol Evol 26: 2533–2538. Tan K, Feizi H, Luo C, Fan SH, Ravasi T, Ideker TG. 2008. A systems approach to delineate functions of paralogous transcription factors: Role of the Yap family in the DNA damage response. Proc Natl Acad Sci 105: 2934– 2939. Tanay A, Regev A, Shamir R. 2005. Conservation and evolvability in regulatory networks: The evolution of ribosomal regulation in yeast. Proc Natl Acad Sci 102: 7203–7208. Thompson JR, Register E, Curotto J, Kurtz M, Kelly R. 1998. An improved protocol for the preparation of yeast cells for transformation by electroporation. Yeast 14: 565–571. Tirosh I, Reikhav S, Levy AA, Barkai N. 2009. A yeast hybrid provides insight into the evolution of gene expression regulation. Science 324: 659– 662. Tsong AE, Tuch BB, Li H, Johnson AD. 2006. Evolution of alternative transcriptional circuits with identical logic. Nature 443: 415–420. Tuch BB, Galgoczy DJ, Hernday AD, Li H, Johnson AD. 2008. The evolution of combinatorial gene regulation in fungi. PLoS Biol 6: e38. doi: 10.1371/ journal.pbio.0060038. Wagner GP, Lynch VJ. 2008. The gene regulatory logic of transcription factor evolution. Trends Ecol Evol 23: 377–385. Wapinski I, Pfeffer A, Friedman N, Regev A. 2007. Natural history and evolutionary principles of gene duplication in fungi. Nature 449: 54–61. Wapinski I, Pfiffner J, French C, Socha A, Thompson DA, Regev A. 2010. Gene duplication and the evolution of ribosomal protein gene regulation in yeast. Proc Natl Acad Sci 107: 5505–5510. Weng L, Dai H, Zhan Y, He Y, Stepaniants SB, Bassett DE. 2006. Rosetta error model for gene expression analysis. Bioinformatics 22: 1111–1121. Wilson MD, Barbosa-Morais NL, Schmidt D, Conboy CM, Vanes L, Tybulewicz VL, Fisher EM, Tavare S, Odom DT. 2008. Species-specific transcription in mice carrying human chromosome 21. Science 322: 434–438. Wittkopp PJ, Haerum BK, Clark AG. 2008. Regulatory changes underlying expression differences within and between Drosophila species. Nat Genet 40: 346–350. Wray GA. 2007. The evolutionary significance of cis-regulatory mutations. Nat Rev Genet 8: 206–216. Zheng W, Zhao H, Mancera E, Steinmetz LM, Snyder M. 2010. Genetic analysis of variation in transcription factor binding in yeast. Nature 464: 1187–1191. Zuker M. 2003. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31: 3406–3415. Received June 15, 2010; accepted in revised form September 20, 2010. Coevolu tion wi thin a transcrip tional ne twork Genome Research 7 www.genome.org Downloaded from genome.cshlp.org on November 3, 2010 - Published by Cold Spring Harbor Laboratory Press