Evolutionary tinkering with conserved components of a transcriptional regulatory network

PLoS Biology

Volumn 8, Issue 3, 2010, Pages

  Lavoie, Hugo ^a,b   Hogues, Hervé ^a   Mallick, Jaideep ^a   Sellam, Adnane ^a,b   Nantel, André ^a,b   Whiteway, Malcolm ^a,b  

^a NATIONAL RESEARCH COUNCIL CANADA   (Canada)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN CBF1; PROTEIN HMO1; PROTEIN LFH1; PROTEIN TBF1; RAP1 PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; FUNGAL DNA; FUNGAL PROTEIN;

ARTICLE; CANDIDA ALBICANS; CELL FUNCTION; CIS ISOMER; DNA BINDING; GENE EXPRESSION PROFILING; GENE FUNCTION; GENE MAPPING; GENE REGULATORY NETWORK; MOLECULAR EVOLUTION; NONHUMAN; REGULON; SACCHAROMYCES CEREVISIAE; TRANS ISOMER; TRANSCRIPTION REGULATION; EVOLUTION; FUNGAL GENOME; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MICROARRAY ANALYSIS; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; RIBOSOME; SIGNAL TRANSDUCTION;

FUNGI;

BASE SEQUENCE; CANDIDA ALBICANS; DNA, FUNGAL; EVOLUTION; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; GENE REGULATORY NETWORKS; GENOME, FUNGAL; MICROARRAY ANALYSIS; MOLECULAR SEQUENCE DATA; REGULON; RIBOSOMES; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 77950553742     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1000329     Document Type: Article

References (122)

1. Abzhanov A, Kuo WP, Hartmann C, Grant BR, Grant PR, et al. (2006) The calmodulin pathway and evolution of elongated beak morphology in Darwin's finches. Nature 442: 563-567.
2. Abzhanov A, Protas M, Grant BR, Grant PR, Tabin CJ (2004) Bmp4 and morphological variation of beaks in Darwin's finches. Science 305: 1462-1465.
3. Coyle SM, Huntingford FA, Peichel CL (2007) Parallel evolution of Pitx1 underlies pelvic reduction in Scottish threespine stickleback (Gasterosteus aculeatus). J Hered 98: 581-586.
4. Shapiro MD, Marks ME, Peichel CL, Blackman BK, Nereng KS, et al. (2004) Genetic and developmental basis of evolutionary pelvic reduction in threespine sticklebacks. Nature 428: 717-723.
5. Carroll SB (2008) Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution. Cell 134: 25-36.
6. Prud'homme B, Gompel N, Carroll SB (2007) Emerging principles of regulatory evolution. Proc Natl Acad Sci U S A 104 Suppl 1: 8605-8612.
7. Gasch AP, Moses AM, Chiang DY, Fraser HB, Berardini M, et al. (2004) Conservation and evolution of cis-regulatory systems in ascomycete fungi. PLoS Biol 2: e398. doi:10.1371/journal.pbio.0020398.
8. Li X, Zhong S, Wong WH (2005) Reliable prediction of transcription factor binding sites by phylogenetic verification. Proc Natl Acad Sci U S A 102: 16945-16950.
9. Brown SJ, Cole MD, Erives AJ (2008) Evolution of the holozoan ribosome biogenesis regulon. BMC Genomics 9: 442.
10. Tanay A, Regev A, Shamir R (2005) Conservation and evolvability in regulatory networks: the evolution of ribosomal regulation in yeast. Proc Natl Acad Sci U S A 102: 7203-7208.
11. Ettwiller L, Budd A, Spitz F, Wittbrodt J (2008) Analysis of mammalian gene batteries reveals both stable ancestral cores and highly dynamic regulatory sequences. Genome Biol 9: R172.
12. Hauenschild A, Ringrose L, Altmutter C, Paro R, Rehmsmeier M (2008) Evolutionary plasticity of polycomb/trithorax response elements in Drosophila species. PLoS Biol 6: e261. doi:10.1371/journal.pbio.0060261.
13. Moses AM, Pollard DA, Nix DA, Iyer VN, Li XY, et al. (2006) Large-scale turnover of functional transcription factor binding sites in Drosophila. PLoS Comput Biol 2: e130. doi:10.1371/journal.pcbi.0020130.
14. Doniger SW, Fay JC (2007) Frequent gain and loss of functional transcription factor binding sites. PLoS Comput Biol 3: e99. doi:10.1371/journal.pcbi. 0030099.
15. Ihmels J, Bergmann S, Gerami-Nejad M, Yanai I, McClellan M, et al. (2005) Rewiring of the yeast transcriptional network through the evolution of motif usage. Science 309: 938-940.
16. Jeong S, Rebeiz M, Andolfatto P, Werner T, True J, et al. (2008) The evolution of gene regulation underlies a morphological difference between two Drosophila sister species. Cell 132: 783-793.
17. Prud'homme B, Gompel N, Rokas A, Kassner VA, Williams TM, et al. (2006) Repeated morphological evolution through cis-regulatory changes in a pleiotropic gene. Nature 440: 1050-1053.
18. Gompel N, Prud'homme B, Wittkopp PJ, Kassner VA, Carroll SB (2005) Chance caught on the wing: cis-regulatory evolution and the origin of pigment patterns in Drosophila. Nature 433: 481-487.
19. Borneman AR, Gianoulis TA, Zhang ZD, Yu H, Rozowsky J, et al. (2007) Divergence of transcription factor binding sites across related yeast species. Science 317: 815-819.
20. Field Y, Fondufe-Mittendorf Y, Moore IK, Mieczkowski P, Kaplan N, et al. (2009) Gene expression divergence in yeast is coupled to evolution of DNAencoded nucleosome organization. Nat Genet 41: 438-445.
21. Babu MM, Janga SC, de Santiago I, Pombo A (2008) Eukaryotic gene regulation in three dimensions and its impact on genome evolution. Curr Opin Genet Dev 18: 571-582.
22. 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.
23. Tuch BB, Li H, Johnson AD (2008) Evolution of eukaryotic transcription circuits. Science 319: 1797-1799.
24. Lynch VJ, Wagner GP (2008) Resurrecting the role of transcription factor change in developmental evolution. Evolution 62: 2131-2154.
25. Gerke J, Lorenz K, Cohen B (2009) Genetic interactions between transcription factors cause natural variation in yeast. Science 323: 498-501.
26. 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.
27. Rockman MV, Kruglyak L (2006) Genetics of global gene expression. Nat Rev Genet 7: 862-872.
28. Ihmels J, Bergmann S, Berman J, Barkai N (2005) Comparative gene expression analysis by differential clustering approach: application to the Candida albicans transcription program. PLoS Genet 1: e39. doi:10.1371/journal.pgen.0010039.
29. Powers T (2004) Ribosome biogenesis: giant steps for a giant problem. Cell 119: 901-902.
30. Wade JT, Hall DB, Struhl K (2004) The transcription factor Ifh1 is a key regulator of yeast ribosomal protein genes. Nature 432: 1054-1058.
31. Martin DE, Soulard A, Hall MN (2004) TOR regulates ribosomal protein gene expression via PKAand the Forkhead transcription factor FHL1. Cell 119: 969-979.
32. Schawalder SB, Kabani M, Howald I, Choudhury U, Werner M, et al. (2004) Growth-regulated recruitment of the essential yeast ribosomal protein gene activator Ifh1. Nature 432: 1058-1061.
33. Rudra D, Zhao Y, Warner JR (2005) Central role of Ifh1p-Fhl1p interaction in the synthesis of yeast ribosomal proteins. Embo J 24: 533-542.
34. Hall DB, Wade JT, Struhl K (2006) An HMG protein, Hmo1, associates with promoters of many ribosomal protein genes and throughout the rRNA gene locus in Saccharomyces cerevisiae. Mol Cell Biol 26: 3672-3679.
35. Zhao Y, McIntosh KB, Rudra D, Schawalder S, Shore D, et al. (2006) Finestructure analysis of ribosomal protein gene transcription. Mol Cell Biol 26: 4853-4862.
36. Kasahara K, Ohtsuki K, Ki S, Aoyama K, Takahashi H, et al. (2007) Assembly of regulatory factors on rRNA and ribosomal protein genes in Saccharomyces cerevisiae. Mol Cell Biol 27: 6686-6705.
37. Merz K, Hondele M, Goetze H, Gmelch K, Stoeckl U, et al. (2008) Actively transcribed rRNA genes in S. cerevisiae are organized in a specialized chromatin associated with the high-mobility group protein Hmo1 and are largely devoid of histone molecules. Genes Dev 22: 1190-1204.
38. Tornow J, Zeng X, Gao W, Santangelo GM (1993) GCR1, a transcriptional activator in Saccharomyces cerevisiae, complexes with RAP1 and can function without its DNA binding domain. Embo J 12: 2431-2437.
39. Conrad MN, Wright JH, Wolf AJ, Zakian VA (1990) RAP1 protein interacts with yeast telomeres in vivo: overproduction alters telomere structure and decreases chromosome stability. Cell 63: 739-750.
40. Hogues H, Lavoie H, Sellam A, Mangos M, Roemer T, et al. (2008) Transcription factor substitution during the evolution of fungal ribosome regulation. Mol Cell 29: 552-562.
41. Wapinski I, Pfeffer A, Friedman N, Regev A (2007) Natural history and evolutionary principles of gene duplication in fungi. Nature 449: 54-61.
42. Marion RM, Regev A, Segal E, Barash Y, Koller D, et al. (2004) Sfp1 is a stress and nutrient-sensitive regulator of ribosomal protein gene expression. Proc Natl Acad Sci U S A 101: 14315-14322.
43. Jorgensen P, Rupes I, Sharom JR, Schneper L, Broach JR, et al. (2004) A dynamic transcriptional network communicates growth potential to ribosome synthesis and critical cell size. Genes Dev 18: 2491-2505.
44. Fingerman I, Nagaraj V, Norris D, Vershon AK (2003) Sfp1 plays a key role in yeast ribosome biogenesis. Eukaryot Cell 2: 1061-1068.
45. Ketel C, Wang HS, McClellan M, Bouchonville K, Selmecki A, et al. (2009) Neocentromeres form efficiently at multiple possible loci in Candida albicans. PLoS Genet 5: e1000400. doi:10.1371/journal.pgen.1000400.
46. Joglekar AP, Bouck D, Finley K, Liu X, Wan Y, et al. (2008) Molecular architecture of the kinetochore-microtubule attachment site is conserved between point and regional centromeres. J Cell Biol 181: 587-594.
47. Meraldi P, McAinsh AD, Rheinbay E, Sorger PK (2006) Phylogenetic and structural analysis of centromeric DNA and kinetochore proteins. Genome Biol 7: R23.
48. Berthiau AS, Yankulov K, Bah A, Revardel E, Luciano P, et al. (2006) Subtelomeric proteins negatively regulate telomere elongation in budding yeast. Embo J 25: 846-856.
49. Pina B, Fernandez-Larrea J, Garcia-Reyero N, Idrissi FZ (2003) The different (sur)faces of Rap1p. Mol Genet Genomics 268: 791-798.
50. Morse RH (2000) RAP, RAP, open up! New wrinkles for RAP1 in yeast. Trends Genet 16: 51-53.
51. Milo R, Shen-Orr S, Itzkovitz S, Kashtan N, Chklovskii D, et al. (2002) Network motifs: simple building blocks of complex networks. Science 298: 824-827.
52. Harbison CT, Gordon DB, Lee TI, Rinaldi NJ, Macisaac KD, et al. (2004) Transcriptional regulatory code of a eukaryotic genome. Nature 431: 99-104.
53. Lee TI, Rinaldi NJ, Robert F, Odom DT, Bar-Joseph Z, et al. (2002) Transcriptional regulatory networks in Saccharomyces cerevisiae. Science 298: 799-804.
54. Freckleton G, Lippman SI, Broach JR, Tavazoie S (2009) Microarray profiling of phage-display selections for rapid mapping of transcription factor-DNA interactions. PLoS Genet 5: e1000449. doi:10.1371/journal.pgen.1000449.
55. Zhu C, Byers KJ, McCord RP, Shi Z, Berger MF, et al. (2009) High-resolution DNA-binding specificity analysis of yeast transcription factors. Genome Res 19: 556-566.
56. Westholm JO, Nordberg N, Muren E, Ameur A, Komorowski J, et al. (2008) Combinatorial control of gene expression by the three yeast repressors Mig1, Mig2 and Mig3. BMC Genomics 9: 601.
57. Futcher B (2002) Transcriptional regulatory networks and the yeast cell cycle. Curr Opin Cell Biol 14: 676-683.
58. Konig P, Giraldo R, Chapman L, Rhodes D (1996) The crystal structure of the DNA-binding domain of yeast RAP1 in complex with telomeric DNA. Cell 85: 125-136.
59. Taylor HO, O'Reilly M, Leslie AG, Rhodes D (2000) How the multifunctional yeast Rap1p discriminates between DNA target sites: a crystallographic analysis. J Mol Biol 303: 693-707.
60. Yu EY, Yen WF, Steinberg-Neifach O, Lue NF (2009) Rap1 in Candida albicans: an unusual structural organization and a critical function in suppressing telomere recombination. Mol Cell Biol.
61. McEachern MJ, Blackburn EH (1994) A conserved sequence motif within the exceptionally diverse telomeric sequences of budding yeasts. Proc Natl Acad Sci U S A 91: 3453-3457.
62. Lue NF (2009)Plasticity of telomere maintenance mechanisms in yeast. Trends Biochem Sci.
63. Lavoie H, Sellam A, Askew C, Nantel A, Whiteway M (2008) A toolbox for epitope-tagging and genome-wide location analysis in Candida albicans. BMC Genomics 9: 578.
64. Bastidas RJ, Heitman J, Cardenas ME (2009) The protein kinase Tor1 regulates adhesin gene expression in Candida albicans. PLoS Pathog 5: e1000294. doi:10.1371/journal.ppat.1000294.
65. Millar CB, Grunstein M (2006) Genome-wide patterns of histone modifications in yeast. Nat Rev Mol Cell Biol 7: 657-666.
66. Sandmeier JJ, French S, Osheim Y, Cheung WL, Gallo CM, et al. (2002) RPD3 is required for the inactivation of yeast ribosomal DNA genes in stationary phase. Embo J 21: 4959-4968.
67. Rohde JR, Cardenas ME (2003) The tor pathway regulates gene expression by linking nutrient sensing to histone acetylation. Mol Cell Biol 23: 629-635.
68. Robert F, Pokholok DK, Hannett NM, Rinaldi NJ, Chandy M, et al. (2004) Global position and recruitment of HATs and HDACs in the yeast genome. Mol Cell 16: 199-209.
69. Humphrey EL, Shamji AF, Bernstein BE, Schreiber SL (2004) Rpd3p relocation mediates a transcriptional response to rapamycin in yeast. Chem Biol 11: 295-299.
70. Wray GA (2007) The evolutionary significance of cis-regulatory mutations. Nat Rev Genet 8: 206-216.
71. Sellam A, Askew C, Epp E, Lavoie H, Whiteway M, et al. (2009) Genome-wide mapping of the coactivator Ada2p yields insight into the functional roles of SAGA/ADA complex in Candida albicans. Mol Biol Cell 20: 2389-2400.
72. Lavoie H, Hogues H, Whiteway M (2009) Rearrangements of the transcriptional regulatory networks of metabolic pathways in fungi. Curr Opin Microbiol.
73. Askew C, Sellam A, Epp E, Hogues H, Mullick A, et al. (2009) Transcriptional regulation of carbohydrate metabolism in the human pathogen Candida albicans. PLoS Pathog 5: e1000612. doi:10.1371/journal.ppat.1000612.
74. Erwin DH, Davidson EH (2009) The evolution of hierarchical gene regulatory networks. Nat Rev Genet 10: 141-148.
75. Davidson EH, Erwin DH (2006) Gene regulatory networks and the evolution of animal body plans. Science 311: 796-800.
76. Erwin DH, Davidson EH (2002) The last common bilaterian ancestor. Development 129: 3021-3032.
77. Seshasayee AS, Fraser GM, Babu MM, Luscombe NM (2009) Principles of transcriptional regulation and evolution of the metabolic system in E. coli. Genome Res 19: 79-91.
78. Haag ES, Doty AV (2005) Sex determination across evolution: connecting the dots. PLoS Biol 3: e21. doi:10.1371/journal.pbio.0030021.
79. Haag ES, True JR (2007) Evolution and development: anchors away! Curr Biol 17: R172-R174.
80. Hill RC, de Carvalho CE, Salogiannis J, Schlager B, Pilgrim D, et al. (2006) Genetic flexibility in the convergent evolution of hermaphroditism in Caenorhabditis nematodes. Dev Cell 10: 531-538.
81. Nayak S, Goree J, Schedl T (2005) fog-2 and the evolution of self-fertile hermaphroditism in Caenorhabditis. PLoS Biol 3: e6. doi:10.1371/journal.pbio.0030006.
82. Stauber M, Prell A, Schmidt-Ott U (2002) A single Hox3 gene with composite bicoid and zerknullt expression characteristics in non-Cyclorrhaphan flies. Proc Natl Acad Sci U S A 99: 274-279.
83. Wittkopp PJ, Haerum BK, Clark AG (2008) Regulatory changes underlying expression differences within and between Drosophila species. Nat Genet 40: 346-350.
84. Wittkopp PJ, Haerum BK, Clark AG (2004) Evolutionary changes in cis and trans gene regulation. Nature 430: 85-88.
85. Balaji S, Babu MM, Iyer LM, Luscombe NM, Aravind L (2006) Comprehensive analysis of combinatorial regulation using the transcriptional regulatory network of yeast. J Mol Biol 360: 213-227.
86. Lopez MC, Smerage JB, Baker HV (1998) Multiple domains of repressor activator protein 1 contribute to facilitated binding of glycolysis regulatory protein 1. Proc Natl Acad Sci U S A 95: 14112-14117.
87. Mizuno T, Kishimoto T, Shinzato T, Haw R, Chambers A, et al. (2004) Role of the N-terminal region of Rap1p in the transcriptional activation of glycolytic genes in Saccharomyces cerevisiae. Yeast 21: 851-866.
88. Hemmerich P, Stoyan T, Wieland G, Koch M, Lechner J, et al. (2000) Interaction of yeast kinetochore proteins with centromere-protein/transcription factor Cbf1. Proc Natl Acad Sci U S A 97: 12583-12588.
89. Stoyan T, Gloeckner G, Diekmann S, Carbon J (2001) Multifunctional centromere binding factor 1 is essential for chromosome segregation in the human pathogenic yeast Candida glabrata. Mol Cell Biol 21: 4875-4888.
90. Vernis L, Poljak L, Chasles M, Uchida K, Casaregola S, et al. (2001) Only centromeres can supply the partition system required for ARS function in the yeast Yarrowia lipolytica. J Mol Biol 305: 203-217.
91. Dujon B, Sherman D, Fischer G, Durrens P, Casaregola S, et al. (2004) Genome evolution in yeasts. Nature 430: 35-44.
92. Sanyal K, Baum M, Carbon J (2004) Centromeric DNA sequences in the pathogenic yeast Candida albicans are all different and unique. Proc Natl Acad Sci U S A 101: 11374-11379.
93. Kuriyan J, Eisenberg D (2007) The origin of protein interactions and allostery in colocalization. Nature 450: 983-990.
94. Babu MM, Balaji S, Iyer LM, Aravind L (2006) Estimating the prevalence and regulatory potential of the telomere looping effect in yeast transcription regulation. Cell Cycle 5: 2354-2363.
95. Janga SC, Collado-Vides J, Babu MM (2008) Transcriptional regulation constrains the organization of genes on eukaryotic chromosomes. Proc Natl Acad Sci U S A 105: 15761-15766.
96. Batada NN, Hurst LD (2007) Evolution of chromosome organization driven by selection for reduced gene expression noise. Nat Genet 39: 945-949.
97. Martchenko M, Levitin A, Hogues H, Nantel A, Whiteway M (2007) Transcriptional rewiring of fungal galactose-metabolism circuitry. Curr Biol 17: 1007-1013.
98. Fontana W, Schuster P (1998) Continuity in evolution: on the nature of transitions. Science 280: 1451-1455.
99. Chialvo DR, Jalife J (1987) Non-linear dynamics of cardiac excitation and impulse propagation. Nature 330: 749-752.
100. Battogtokh D, Tyson JJ (2004) Bifurcation analysis of a model of the budding yeast cell cycle. Chaos 14: 653-661.
101. Fung E, Wong WW, Suen JK, Bulter T, Lee SG, et al. (2005) A synthetic genemetabolic oscillator. Nature 435: 118-122.
102. Swat M, Kel A, Herzel H (2004) Bifurcation analysis of the regulatory modules of the mammalian G1/S transition. Bioinformatics 20: 1506-1511.
103. Madan Babu M, Teichmann SA, Aravind L (2006) Evolutionary dynamics of prokaryotic transcriptional regulatory networks. J Mol Biol 358: 614-633.
104. Gonzalez Perez AD, Gonzalez E, Espinosa Angarica V, Vasconcelos AT, Collado-Vides J (2008) Impact of transcription units rearrangement on the evolution of the regulatory network of gamma-proteobacteria. BMC Genomics 9: 128.
105. Perez JC, Groisman EA (2009) Evolution of transcriptional regulatory circuits in bacteria. Cell 138: 233-244.
106. Price MN, Dehal PS, Arkin AP (2007) Orthologous transcription factors in bacteria have different functions and regulate different genes. PLoS Comput Biol 3: 1739-1750. doi:10.1371/journal.pcbi.0030175.
107. Lozada-Chavez I, Janga SC, Collado-Vides J (2006) Bacterial regulatory networks are extremely flexible in evolution. Nucleic Acids Res 34: 3434-3445.
108. Perez JC, Shin D, Zwir I, Latifi T, Hadley TJ, et al. (2009) Evolution of a bacterial regulon controlling virulence and Mg(2+) homeostasis. PLoS Genet 5: e1000428. doi:10.1371/journal.pgen.1000428.
109. Osborne SE, Walthers D, Tomljenovic AM, Mulder DT, Silphaduang U, et al. (2009) Pathogenic adaptation of intracellular bacteria by rewiring a cisregulatory input function. Proc Natl Acad Sci U S A 106: 3982-3987.
110. Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, et al. (1992) Current protocols in molecular biology. New York: John Wiley and Sons.
111. Roemer T, Jiang B, Davison J, Ketela T, Veillette K, et al. (2003) Large-scale essential gene identification in Candida albicans and applications to antifungal drug discovery. Mol Microbiol 50: 167-181.
112. Ghaemmaghami S, Huh WK, Bower K, Howson RW, Belle A, et al. (2003) Global analysis of protein expression in yeast. Nature 425: 737-741.
113. James P (2001) Yeast two-hybrid vectors and strains. Methods Mol Biol 177: 41-84.
114. Guillemette B, Bataille AR, Gevry N, Adam M, Blanchette M, et al. (2005) Variant histone H2A.Z is globally localized to the promoters of inactive yeast genes and regulates nucleosome positioning. PLoS Biol 3: e384. doi:10.1371/journal.pbio.0030384.
115. Nantel A, Rigby T, Hogues H, Whiteway M (2006) Microarrays for studying pathology in Candida albicans. In: Kavanaugh K, ed. Medical mycology: cellular and molecular techniques Wiley Press.
116. Chenna R, Sugawara H, Koike T, Lopez R, Gibson TJ, et al. (2003) Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res 31: 3497-3500.
117. Galtier N, Gouy M, Gautier C (1996) SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny. Comput Appl Biosci 12: 543-548.
118. Felsenstein J (2004) PHYLIP. 3.6 ed. Seattle: Distributed by the author. Department of Genome Sciences, University of Washington. pp. Phylogeny Inference Package.
119. Bailey TL, Elkan C (1994) Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc Int Conf Intell Syst Mol Biol 2: 28-36.
120. Boyle EI, Weng S, Gollub J, Jin H, Botstein D, et al. (2004) GO:TermFinder-open source software for accessing Gene Ontology information and finding significantly enriched Gene Ontology terms associated with a list of genes. Bioinformatics 20: 3710-3715.
121. Monteiro PT, Mendes ND, Teixeira MC, d'Orey S, Tenreiro S, et al. (2008) YEASTRACT-DISCOVERER: new tools to improve the analysis of transcriptional regulatory associations in Saccharomyces cerevisiae. Nucleic Acids Res 36: D132-D136.
122. Moses AM, Chiang DY, Eisen MB (2004) Phylogenetic motif detection by expectation-maximization on evolutionary mixtures. Pac Symp Biocomput. Pp 324-335.