The evolution of combinatorial gene regulation in fungi
Open accessAbstract
It is widely suspected that gene regulatory networks are highly plastic. The rapid turnover of transcription factor binding sites has been predicted on theoretical grounds and has been experimentally demonstrated in closely related species. We combined experimental approaches with comparative genomics to focus on the role of combinatorial control in the evolution of a large transcriptional circuit in the fungal lineage. Our study centers on Mcm1, a transcriptional regulator that, in combination with five cofactors, binds roughly 4% of the genes in Saccharomyces cerevisiae and regulates processes ranging from the cell-cycle to mating. In Kluyveromyces lactis and Candida albicans, two other hemiascomycetes, we find that the Mcm1 combinatorial circuits are substantially different. This massive rewiring of the Mcm1 circuitry has involved both substantial gain and loss of targets in ancient combinatorial circuits as well as the formation of new combinatorial interactions. We have dissected the gains and losses on the global level into subsets of functionally and temporally related changes. One particularly dramatic change is the acquisition of Mcm1 binding sites in close proximity to Rap1 binding sites at 70 ribosomal protein genes in the K. lactis lineage. Another intriguing and very recent gain occurs in the C. albicans lineage, where Mcm1 is found to bind in combination with the regulator Wor1 at many genes that function in processes associated with adaptation to the human host, including the white-opaque epigenetic switch. The large turnover of Mcm1 binding sites and the evolution of new Mcm1-cofactor interactions illuminate in sharp detail the rapid evolution of combinatorial transcription networks.
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Changes in regulatory circuits that control gene expression are one of the major drivers of evolution.
“Changes in the regulatory circuits that control gene expression are one of the major drivers of evolution”
From Mitochondrial retrograde control of transcription evolves with respiratory stress, metabolic adaptation, and virulence in budding yeasts (2026) · cites this paper as Tuch et al. 2008
The Introduction describes changes in gene regulation as a potentially powerful mode of evolution and says their contribution to phenotypic variation has been demonstrated. The Discussion reports extensive rewiring of a fungal regulatory circuit. Neither passage establishes the stronger, unqualified claim that such changes are one of the major drivers of evolution generally. (LLM, conf=0.83)
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WebLogo: A Sequence Logo Generator: Figure 1Preprint
Crooks, G. E., Hon, G. C., Chandonia, J., & Brenner, S. E. (2004) · Genome Research · doi:10.1101/gr.849004 · Cited by 12,433 · see citing works
Fitting a mixture model by expectation maximization to discover motifs in biopolymers.
Bailey, T. L., & Elkan, C. (1994) · PubMed · Cited by 4,933 · see citing works
Spellman, P. T., Sherlock, G. J., Zhang, M. Q., Iyer, V. R., Anders, K. R., Eisen, M. B., Brown, P. O., Botstein, D., & Futcher, B. (1998) · Molecular Biology of the Cell · doi:10.1091/mbc.9.12.3273 · Cited by 4,724 · see citing works
King, M.-C., & Wilson, A. C. (1975) · Science · doi:10.1126/science.1090005 · Cited by 2,815 · see citing works
Jacob, F. (1977) · Science · doi:10.1126/science.860134 · Cited by 2,711 · see citing works
Transcriptional regulatory code of a eukaryotic genome
Harbison, C. T., Gordon, D. B., Lee, T. I., Rinaldi, N. J., MacIsaac, K. D., Danford, T., Hannett, N. M., Tagne, J., Reynolds, D. B., Yoo, J. Y., et al. (2004) · Nature · doi:10.1038/nature02800 · Cited by 2,116 · see citing works
Sequencing and comparison of yeast species to identify genes and regulatory elements
Kellis, M., Patterson, N. J., Endrizzi, M. G., Birren, B. W., & Lander, E. S. (2003) · Nature · doi:10.1038/nature01644 · Cited by 1,731 · see citing works
Dujon, B., Sherman, D., Fischer, G., Durrens, P., Casaregola, S., Lafontaine, I., de Montigny, J., Marck, C., Neuvéglise, C., Talla, E., et al. (2004) · Nature · doi:10.1038/nature02579 · Cited by 1,623 · see citing works
The evolutionary significance of cis-regulatory mutations
Wray, G. A. (2007) · Nature Reviews Genetics · doi:10.1038/nrg2063 · Cited by 1,521 · see citing works
Genome-scale approaches to resolving incongruence in molecular phylogenies.
Rokas, A., Williams, B. L., King, N., & Carroll, S. B. (2003) · Nature · doi:10.1038/nature02053 · Cited by 1,512 · see citing works
Kirschner, M., & Gerhart, J. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.15.8420 · Cited by 1,129 · see citing works
From DNA to diversity: molecular genetics and the evolution of animal design
Carroll, S., Grenier, J., & Weatherbee, S. D. (2002) · Choice Reviews Online · doi:10.5860/choice.39-5182 · Cited by 986 · see citing works
Genetic and developmental basis of evolutionary pelvic reduction in threespine sticklebacks
Shapiro, M. D., Marks, M. E., Peichel, C. L., Blackman, B. K., Nereng, K. S., Jónsson, B., Schluter, D., & Kingsley, D. M. (2004) · Nature · doi:10.1038/nature02415 · Cited by 843 · see citing works
The frailty of adaptive hypotheses for the origins of organismal complexity
Lynch, M. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0702207104 · Cited by 804 · see citing works
Repetitive and Non-Repetitive DNA Sequences and a Speculation on the Origins of Evolutionary Novelty
Britten, R. J., & Davidson, E. H. (1971) · The Quarterly Review of Biology · doi:10.1086/406830 · Cited by 789 · see citing works
Byrne, K. P., & Wolfe, K. H. (2005) · Genome Research · doi:10.1101/gr.3672305 · Cited by 720 · see citing works
On schemes of combinatorial transcription logic
Buchler, N. E. G., Gerland, U., & Terence Hwa, B. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0930314100 · Cited by 663 · see citing works
Chance caught on the wing: cis-regulatory evolution and the origin of pigment patterns in Drosophila
Gompel, N., Prud'homme, B., Wittkopp, P. J., Kassner, V. A., & Carroll, S. B. (2005) · Nature · doi:10.1038/nature03235 · Cited by 646 · see citing works
From DNA to Diversity: Molecular Genetics and the Evolution of Animal Design
Gostling, N. J. (2002) · Heredity · doi:10.1038/sj.hdy.6800154 · Cited by 620 · see citing works
Miller, M. G., & Johnson, A. D. (2002) · Cell · doi:10.1016/s0092-8674(02)00837-1 · Cited by 569 · see citing works
Self-citation"White-opaque transition": a second high-frequency switching system in Candida albicans
Slutsky, B., Staebell, M., Anderson, J., Risen, L., Pfaller, M. A., & Soll, D. R. (1987) · Journal of Bacteriology · doi:10.1128/jb.169.1.189-197.1987 · Cited by 564 · see citing works
Mechanisms of Haploinsufficiency Revealed by Genome-Wide Profiling in Yeast
Deutschbauer, A. M., Jaramillo, D. F., Proctor, M., Kumm, J., Hillenmeyer, M. E., Davis, R. W., Nislow, C., & Giaever, G. (2005) · Genetics · doi:10.1534/genetics.104.036871 · Cited by 535 · see citing works
Tissue-specific transcriptional regulation has diverged significantly between human and mouse
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. (2007) · Nature Genetics · doi:10.1038/ng2047 · Cited by 506 · see citing works
Buchman, A. R., Kimmerly, W. J., Rine, J., & Kornberg, R. D. (1988) · Molecular and Cellular Biology · doi:10.1128/mcb.8.1.210 · Cited by 493 · see citing works
Dermitzakis, E. T., & Clark, A. G. (2002) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a004169 · Cited by 463 · see citing works
Gene duplication and the adaptive evolution of a classic genetic switch
Hittinger, C. T., & Carroll, S. B. (2007) · Nature · doi:10.1038/nature06151 · Cited by 439 · see citing works
Dating divergences in the Fungal Tree of Life: review and new analyses
Taylor, J. W., & Berbee, M. L. (2006) · Mycologia · doi:10.3852/mycologia.98.6.838 · Cited by 424 · see citing works
Abundant Raw Material for Cis-Regulatory Evolution in Humans
Rockman, M. V., & Wray, G. A. (2002) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a004023 · Cited by 377 · see citing works
Divergence of Transcription Factor Binding Sites Across Related Yeast Species
Borneman, A. R., Gianoulis, T. A., Zhang, Z. D., Yu, H., Rozowsky, J. S., Seringhaus, M. R., Wang, L.-Y., Gerstein, M., & Snyder, M. P. (2007) · Science · doi:10.1126/science.1140748 · Cited by 335 · see citing works
Zordan, R. E., Galgoczy, D. J., & Johnson, A. D. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0605138103 · Cited by 306 · see citing works
Self-citationMessenguy, F., & Dubois, E. L. (2003) · Gene · doi:10.1016/s0378-1119(03)00747-9 · Cited by 299 · see citing works
Rewiring of the Yeast Transcriptional Network Through the Evolution of Motif Usage
Ihmels, J., Bergmann, S., Gerami‐Nejad, M., Yanai, I., McClellan, M., Berman, J. G., & Barkai, N. (2005) · Science · doi:10.1126/science.1113833 · Cited by 295 · see citing works
Bistable expression of WOR1 , a master regulator of white–opaque switching in Candida albicans
Huang, G., Wang, H., Chou, S., Nie, X., Chen, J., & Liu, H. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0605270103 · Cited by 293 · see citing works
Interlocking Transcriptional Feedback Loops Control White-Opaque Switching in Candida albicans
Zordan, R. E., Miller, M. G., Galgoczy, D. J., Tuch, B. B., & Johnson, A. D. (2007) · PLoS Biology · doi:10.1371/journal.pbio.0050256 · Cited by 292 · see citing works
Self-citationConservation and evolvability in regulatory networks: The evolution of ribosomal regulation in yeast
Tanay, A., Regev, A., & Ron Shamir, A. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0502521102 · Cited by 262 · see citing works
Evolution of alternative transcriptional circuits with identical logic
Tsong, A. E., Tuch, B. B., Li, H., & Johnson, A. D. (2006) · Nature · doi:10.1038/nature05099 · Cited by 255 · see citing works
Self-citationLarge-Scale Turnover of Functional Transcription Factor Binding Sites in Drosophila
Moses, A. M., Pollard, D. A., Nix, D. A., Iyer, V. N., Li, X., Biggin, M. D., & Eisen, M. B. (2006) · PLoS Computational Biology · doi:10.1371/journal.pcbi.0020130 · Cited by 251 · see citing works
Evolution of a Combinatorial Transcriptional Circuit
Tsong, A. E., Miller, M. G., Raisner, R. M., & Johnson, A. D. (2003) · Cell · doi:10.1016/s0092-8674(03)00885-7 · Cited by 250 · see citing works
Self-citationPassmore, S., Elble, R. C., & Tye, B. (1989) · Genes & Development · doi:10.1101/gad.3.7.921 · Cited by 241 · see citing works
Conservation and Evolution of Cis-Regulatory Systems in Ascomycete Fungi
Gasch, A. P., Moses, A. M., Chiang, D. Y., Fraser, H. B., Berardini, M. D., & Eisen, M. B. (2004) · PLoS Biology · doi:10.1371/journal.pbio.0020398 · Cited by 227 · see citing works
Rapid Evolution of cis-Regulatory Sequences via Local Point Mutations
Stone, J., & Wray, G. A. (2001) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a003964 · Cited by 224 · see citing works
Yeasts illustrate the molecular mechanisms of eukaryotic genome evolution
DUJON, B. (2006) · Trends in Genetics · doi:10.1016/j.tig.2006.05.007 · Cited by 224 · see citing works
TOS9 Regulates White-Opaque Switching in Candida albicans
Srikantha, T., Borneman, A. R., Daniels, K. J., Pujol, C., Wu, W., Seringhaus, M. R., Gerstein, M., Song, Y., Snyder, M. P., & Soll, D. R. (2006) · Eukaryotic Cell · doi:10.1128/ec.00252-06 · Cited by 209 · see citing works
Forkhead-like transcription factors recruit Ndd1 to the chromatin of G2/M-specific promoters
Koranda, M., Schleiffer, A., Endler, L., & Ammerer, G. (2000) · Nature · doi:10.1038/35017589 · Cited by 202 · see citing works
Plasticity of the cis-Regulatory Input Function of a Gene
Mayo, A., Setty, Y., Shavit, S., Zaslaver, A., & Alon, U. S. (2006) · PLoS Biology · doi:10.1371/journal.pbio.0040045 · Cited by 196 · see citing works
Fontana, W. (2002) · BioEssays · doi:10.1002/bies.10190 · Cited by 179 · see citing works
Transcriptional Rewiring of Fungal Galactose-Metabolism Circuitry
Martchenko, M., Levitin, A., Hogues, H., Nantel, A., & Whiteway, M. S. (2007) · Current Biology · doi:10.1016/j.cub.2007.05.017 · Cited by 172 · see citing works
Tata, P., Miles, S., GuhaThakurta, D., Jemiolo, D., & Breeden, L. L. (2002) · Genes & Development · doi:10.1101/gad.1034302 · Cited by 170 · see citing works
Smith, D. L., & Johnson, A. D. (1992) · Cell · doi:10.1016/0092-8674(92)90212-u · Cited by 169 · see citing works
Self-citationSonneborn, A., Tebarth, B., & Ernst, J. F. (1999) · Infection and Immunity · doi:10.1128/iai.67.9.4655-4660.1999 · Cited by 164 · see citing works
Frequent Gain and Loss of Functional Transcription Factor Binding Sites
Doniger, S. W., & Fay, J. C. (2007) · PLoS Computational Biology · doi:10.1371/journal.pcbi.0030099 · Cited by 153 · see citing works
Kvaal, C. A., Srikantha, T., & Soll, D. R. (1997) · Infection and Immunity · doi:10.1128/iai.65.11.4468-4475.1997 · Cited by 146 · see citing works
Ihmels, J., Bergmann, S., Berman, J. G., & Barkai, N. (2005) · PLoS Genetics · doi:10.1371/journal.pgen.0010039 · Cited by 131 · see citing works
Fedoroff, N. V. (1988) · Cell · doi:10.1016/0092-8674(88)90481-3 · Cited by 128 · see citing works
Skin Facilitates Candida albicans Mating
Lachke, S. A., Lockhart, S. R., Daniels, K. J., & Soll, D. R. (2003) · Infection and Immunity · doi:10.1128/iai.71.9.4970-4976.2003 · Cited by 127 · see citing works
The Closely Related Species Candida albicans and Candida dubliniensis Can Mate
Pujol, C., Daniels, K. J., Lockhart, S. R., Srikantha, T., Radke, J. B., Geiger, J., & Soll, D. R. (2004) · Eukaryotic Cell · doi:10.1128/ec.3.4.1015-1027.2004 · Cited by 120 · see citing works
SRF and MCM1 have related but distinct DNA binding specificities
Wynne, J., & Treisman, R. (1992) · Nucleic Acids Research · doi:10.1093/nar/20.13.3297 · Cited by 96 · see citing works
High-resolution computational models of genome binding events
Qi, Y., Rolfe, A., MacIsaac, K. D., Gerber, G. K., Pokholok, D., Zeitlinger, J., Danford, T., Dowell, R. D., Fraenkel, E., Jaakkola, T., et al. (2006) · Nature Biotechnology · doi:10.1038/nbt1233 · Cited by 89 · see citing works
Hollenhorst, P. C., Pietz, G. E., & Fox, C. A. (2001) · Genes & Development · doi:10.1101/gad.906201 · Cited by 84 · see citing works
Carter, A. J. R., & Wagner, G. P. (2002) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2002.1968 · Cited by 74 · see citing works
Expected Rates and Modes of Evolution of Enhancer Sequences
MacArthur, S. (2004) · Molecular Biology and Evolution · doi:10.1093/molbev/msh105 · Cited by 67 · see citing works
In vitro studies of the binding of the ARGR proteins to the ARG5,6 promoter.
Dubois, E., & Messenguy, F. (1991) · Molecular and Cellular Biology · doi:10.1128/mcb.11.4.2162 · Cited by 53 · see citing works
Chin, C.-S., Chuang, J. H., & Li, H. (2005) · Genome Research · doi:10.1101/gr.3243305 · Cited by 48 · see citing works
Self-citationRottmann, M., Dieter, S., Brunner, H., & Rupp, S. (2003) · Molecular Microbiology · doi:10.1046/j.1365-2958.2003.03358.x · Cited by 47 · see citing works
Zuckerkandi, E. (1997) · Journal of Molecular Evolution · doi:10.1007/pl00000048 · Cited by 41 · see citing works
Hagen, D. C., Bruhn, L., Westby, C. A., & Sprague, G. F. (1993) · Molecular and Cellular Biology · doi:10.1128/mcb.13.11.6866 · Cited by 36 · see citing works
Retrotransposons and regulatory suites
Shapiro, J. A. (2005) · BioEssays · doi:10.1002/bies.20192 · Cited by 27 · see citing works
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- Ptashne M Gann A 2002 Genes & signals Cold Spring Harbor (New York) Cold Spring Harbor Laboratory Press xvi, 192 p. p.
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Evo-Devo and an Expanding Evolutionary Synthesis: A Genetic Theory of Morphological Evolution
Carroll, S. B. (2008) · Cell · doi:10.1016/j.cell.2008.06.030 · Cited by 2,067 · see citing works
Cis-regulatory elements: Molecular mechanisms and evolutionary processes underlying divergence
Wittkopp, P. J., & Kalay, G. (2012) · Nature Reviews Genetics · doi:10.1038/nrg3095 · Cited by 1,231 · see citing works
Evolution of pathogenicity and sexual reproduction in eight Candida genomes
Butler, G., Rasmussen, M. D., Lin, M. F., Santos, M. A. S., Sakthikumar, S., Munro, C. A., Rheinbay, E., Grabherr, M., Forche, A., Reedy, J. L., et al. (2009) · Nature · doi:10.1038/nature08064 · Cited by 1,065 · see citing works
Global Analysis of Cdk1 Substrate Phosphorylation Sites Provides Insights into Evolution
Holt, L. J., Tuch, B. B., Villén, J., Johnson, A. D., Gygi, S. P., & Morgan, D. O. (2009) · Science · doi:10.1126/science.1172867 · Cited by 859 · see citing works
Self-citationIdeker, T., & Krogan, N. J. (2012) · Molecular Systems Biology · doi:10.1038/msb.2011.99 · Cited by 784 · see citing works
A Recently Evolved Transcriptional Network Controls Biofilm Development in Candida albicans
Nobile, C. J., Fox, E. P., Nett, J. E., Sorrells, T. R., Mitrovich, Q. M., Hernday, A. D., Tuch, B. B., Andes, D. R., & Johnson, A. D. (2012) · Cell · doi:10.1016/j.cell.2011.10.048 · Cited by 711 · see citing works
Self-citationEvolution of the mammalian transcription factor binding repertoire via transposable elementsPreprint
Bourque, G., Leong, B., Vega, V. B., Chen, X., Lee, Y. L., Srinivasan, K. G., Chew, J.-L., Ruan, Y., Wei, C., Ng, H., et al. (2008) · Genome Research · doi:10.1101/gr.080663.108 · Cited by 579 · see citing works
A Phenotypic Profile of the Candida albicans Regulatory Network
Homann, O. R., Dea, J., Noble, S. M., & Johnson, A. D. (2009) · PLoS Genetics · doi:10.1371/journal.pgen.1000783 · Cited by 444 · see citing works
“Given the significant rewiring of transcriptional networks documented in the fungal lineages [4,5,35,63,64], the high degree of phenotypic conservation we observed between S.”
BackgroundSelf-citationConservation and divergence in the transcriptional programs of the human and mouse immune systems
Shay, T., Jojic, V., Zuk, O., Rothamel, K., Puyraimond-Zemmour, D., Feng, T., Wakamatsu, E., Benoist, C., Koller, D., Regev, A., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1222738110 · Cited by 359 · see citing works
Hahn, S., & Young, E. T. (2011) · Genetics · doi:10.1534/genetics.111.127019 · Cited by 341 · see citing works
Biofilm Matrix Regulation by Candida albicans Zap1
Nobile, C. J., Nett, J. E., Hernday, A. D., Homann, O. R., Deneault, J.-S., Nantel, A., Andes, D. R., Johnson, A. D., & Mitchell, A. P. (2009) · PLoS Biology · doi:10.1371/journal.pbio.1000133 · Cited by 337 · see citing works
Self-citationChen, C., Pande, K., French, S. D., Tuch, B. B., & Noble, S. M. (2011) · Cell Host & Microbe · doi:10.1016/j.chom.2011.07.005 · Cited by 314 · see citing works
Self-citationRegulation of multidrug resistance in pathogenic fungi
Morschhäuser, J. (2010) · Fungal Genetics and Biology · doi:10.1016/j.fgb.2009.08.002 · Cited by 300 · see citing works
Gladieux, P., Ropars, J., Badouin, H., Branca, A., Aguileta, G., de Vienne, D. M., de la Vega, R. C. R., Branco, S., & Giraud, T. (2013) · Molecular Ecology · doi:10.1111/mec.12631 · Cited by 270 · see citing works
Coevolution of Morphology and Virulence in Candida Species
Childers, D. S., Carlisle, P. L., & Kadosh, D. (2011) · Eukaryotic Cell · doi:10.1128/ec.05085-11 · Cited by 227 · see citing works
The Role of Nucleosome Positioning in the Evolution of Gene Regulation
Tsankov, A. M., Thompson, D. A., Socha, A. L., Regev, A., & Rando, O. J. (2010) · PLoS Biology · doi:10.1371/journal.pbio.1000414 · Cited by 217 · see citing works
RESURRECTING THE ROLE OF TRANSCRIPTION FACTOR CHANGE IN DEVELOPMENTAL EVOLUTION
Lynch, V. J., & Wagner, G. P. (2008) · Evolution · doi:10.1111/j.1558-5646.2008.00440.x · Cited by 206 · see citing works
Adaptation of cells to new environments
Brooks, A. N., Turkarslan, S., Beer, K. D., Lo, F. Y., & Baliga, N. S. (2010) · WIREs Systems Biology and Medicine · doi:10.1002/wsbm.136 · Cited by 197 · see citing works
Chung, D., Barker, B. M., Carey, C. C., Merriman, B., Werner, E. R., Lechner, B. E., Dhingra, S., Cheng, C., Xu, W., Blosser, S. J., et al. (2014) · PLoS Pathogens · doi:10.1371/journal.ppat.1004487 · Cited by 193 · see citing works
Bradley, R. K., Li, X., Trapnell, C., Davidson, S. M., Pachter, L. S., Chu, H. C., Tonkin, L. A., Biggin, M. D., & Eisen, M. B. (2010) · PLoS Biology · doi:10.1371/journal.pbio.1000343 · Cited by 190 · see citing works
Evolution of phosphoregulation: comparison of phosphorylation patterns across yeast species
Beltrao, P., Trinidad, J. C., Fiedler, D., Roguev, A., Lim, W. A., Shokat, K. M., Burlingame, A. L., & Krogan, N. J. (2009) · PLoS Biology · doi:10.1371/journal.pbio.1000134 · Cited by 188 · see citing works
Evolution of Transcriptional Regulatory Circuits in Bacteria
Pérez, J. C., & Groisman, E. A. (2009) · Cell · doi:10.1016/j.cell.2009.07.002 · Cited by 175 · see citing works
Comparative Analysis of Gene Regulatory Networks: From Network Reconstruction to Evolution
Thompson, D. A., Regev, A., & Roy, S. (2015) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-100913-012908 · Cited by 170 · see citing works
Why Transcription Factor Binding Sites Are Ten Nucleotides Long
Stewart, A. J., Hannenhalli, S. S., & Plotkin, J. B. (2012) · Genetics · doi:10.1534/genetics.112.143370 · Cited by 165 · see citing works
Quantitative Genetic Interactions Reveal Biological Modularity
Beltrão, P., Cagney, G., & Krogan, N. J. (2010) · Cell · doi:10.1016/j.cell.2010.05.019 · Cited by 156 · see citing works
Pérez, J. C., Kumamoto, C. A., & Johnson, A. D. (2013) · PLoS Biology · doi:10.1371/journal.pbio.1001510 · Cited by 156 · see citing works
Self-citationEvolution of Eukaryotic Transcription Circuits
Tuch, B. B., Li, H., & Johnson, A. D. (2008) · Science · doi:10.1126/science.1152398 · Cited by 156 · see citing works
Self-citationThe Robustness and Evolvability of Transcription Factor Binding Sites
Payne, J. L., & Wagner, A. (2014) · Science · doi:10.1126/science.1249046 · Cited by 154 · see citing works
Weirauch, M. T., & Hughes, T. R. (2010) · Trends in Genetics · doi:10.1016/j.tig.2009.12.002 · Cited by 146 · see citing works
Making Sense of Transcription Networks
Sorrells, T. R., & Johnson, A. D. (2015) · Cell · doi:10.1016/j.cell.2015.04.014 · Cited by 143 · see citing works
Self-citationSte12 and Ste12-Like Proteins, Fungal Transcription Factors Regulating Development and Pathogenicity
Hoi, J. W. S., & Dumas, B. (2010) · Eukaryotic Cell · doi:10.1128/ec.00333-09 · Cited by 140 · see citing works
Expandable and reversible copy number amplification drives rapid adaptation to antifungal drugs
Todd, R. T., & Selmecki, A. (2020) · eLife · doi:10.7554/elife.58349 · Cited by 138 · see citing works
Evolutionary Tinkering with Conserved Components of a Transcriptional Regulatory Network
Lavoie, H., Hogues, H., Mallick, J., Sellam, A., Nantel, A., & Whiteway, M. S. (2010) · PLoS Biology · doi:10.1371/journal.pbio.1000329 · Cited by 133 · see citing works
Wóycicki, R. K., Witkowicz, J., Gawroński, P., Dąbrowska‐Bronk, J., Lomsadze, A., Pawełkowicz, M. E., Siedlecka, E., Yagi, K., Pląder, W., Seroczyńska, A., et al. (2011) · PLoS ONE · doi:10.1371/journal.pone.0022728 · Cited by 128 · see citing works
Evolution of a Bacterial Regulon Controlling Virulence and Mg2+ Homeostasis
Pérez, J. C., Shin, D., Zwir, I. J. S., Latifi, T. N., Hadley, T. J., & Groisman, E. A. (2009) · PLoS Genetics · doi:10.1371/journal.pgen.1000428 · Cited by 126 · see citing works
A Temperature-Responsive Network Links Cell Shape and Virulence Traits in a Primary Fungal Pathogen
Beyhan, S., Gutierrez, M., Voorhies, M., & Sil, A. (2013) · PLoS Biology · doi:10.1371/journal.pbio.1001614 · Cited by 120 · see citing works
Porman, A. M., Alby, K., Hirakawa, M. P., & Bennett, R. J. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1112076109 · Cited by 116 · see citing works
Azole Drugs Are Imported By Facilitated Diffusion in Candida albicans and Other Pathogenic Fungi
Mansfield, B. E., Oltean, H. N., Oliver, B. G., Hoot, S. J., Leyde, S. E., Hedstrom, L., & White, T. C. (2010) · PLoS Pathogens · doi:10.1371/journal.ppat.1001126 · Cited by 111 · see citing works
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Baker, C. R., Hanson-Smith, V., & Johnson, A. D. (2013) · Science · doi:10.1126/science.1240810 · Cited by 113 · see citing works
Self-citationComparative Genomics and the Evolution of Pathogenicity in Human Pathogenic Fungi
Moran, G. P., Coleman, D. C., & Sullivan, D. J. (2010) · Eukaryotic Cell · doi:10.1128/ec.00242-10 · Cited by 108 · see citing works
Measuring the Evolutionary Rewiring of Biological Networks
Shou, C., Bhardwaj, N., Lam, H. Y. K., Yan, K., Kim, P. M., Snyder, M. P., & Gerstein, M. (2011) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1001050 · Cited by 101 · see citing works
Regulatory Factor X (RFX)-mediated transcriptional rewiring of ciliary genes in animals
Piasecki, B. P., Burghoorn, J., & Swoboda, P. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0914241107 · Cited by 100 · see citing works
Evolution of protein phosphorylation across 18 fungal species
Studer, R. A., Rodríguez‐Mias, R. A., Haas, K. M., Hsu, J. I., Viéitez, C., Solé, C., Swaney, D. L., Stanford, L. B., Liachko, I., Böttcher, R., et al. (2016) · Science · doi:10.1126/science.aaf2144 · Cited by 100 · see citing works
A toolbox for epitope-tagging and genome-wide location analysis in Candida albicans
Lavoie, H., Sellam, A., Askew, C., Nantel, A., & Whiteway, M. S. (2008) · BMC Genomics · doi:10.1186/1471-2164-9-578 · Cited by 94 · see citing works
Schmidt, S. F., Jørgensen, M., Chen, Y., Nielsen, R., Sandelin, A., & Mandrup, S. (2011) · BMC Genomics · doi:10.1186/1471-2164-12-152 · Cited by 94 · see citing works
Conserved and Divergent Roles of Bcr1 and CFEM Proteins in Candida parapsilosis and Candida albicans
Ding, C., Vidanes, G. M., Maguire, S. L., Guida, A., Synnott, J. M., Andes, D. R., & Butler, G. (2011) · PLoS ONE · doi:10.1371/journal.pone.0028151 · Cited by 93 · see citing works
Zheng, Q., Hou, R., Juanyu, Zhang, Ma, J., Wu, Z., Wang, G., Wang, C., & Xu, J. (2013) · PLoS ONE · doi:10.1371/journal.pone.0066980 · Cited by 92 · see citing works
Role of Ndt80p in Sterol Metabolism Regulation and Azole Resistance in <i>Candida albicans</i>
Sellam, A., Tebbji, F., & Nantel, A. (2009) · Eukaryotic Cell · doi:10.1128/ec.00074-09 · Cited by 91 · see citing works
Butler, G. (2010) · Clinical Microbiology Reviews · doi:10.1128/cmr.00053-09 · Cited by 87 · see citing works
Microevolution of Candida albicans in Macrophages Restores Filamentation in a Nonfilamentous Mutant
Wartenberg, A., Linde, J., Martin, R., Schreiner, M., Horn, F., Jacobsen, I. D., Jenull, S., Wolf, T., Kuchler, K., Guthke, R., et al. (2014) · PLoS Genetics · doi:10.1371/journal.pgen.1004824 · Cited by 85 · see citing works
Regulation of white-opaque switching in Candida albicans
Morschhäuser, J. (2010) · Medical Microbiology and Immunology · doi:10.1007/s00430-010-0147-0 · Cited by 86 · see citing works
Baker, C. R., Booth, L. N., Sorrells, T. R., & Johnson, A. D. (2012) · Cell · doi:10.1016/j.cell.2012.08.018 · Cited by 83 · see citing works
Self-citationTopology and Control of the Cell-Cycle-Regulated Transcriptional Circuitry
Haase, S. B., & Wittenberg, C. (2014) · Genetics · doi:10.1534/genetics.113.152595 · Cited by 83 · see citing works
Chemogenomic profiling predicts antifungal synergies
Jansen, G., Lee, A. Y., Epp, E., Fredette, A., Surprenant, J., Harcus, D., Scott, M. S., Tan, E., Nishimura, T., Whiteway, M. S., et al. (2009) · Molecular Systems Biology · doi:10.1038/msb.2009.95 · Cited by 79 · see citing works
Evolutionary principles of modular gene regulation in yeasts
Thompson, D. A., Roy, S., Chan, M., Styczynsky, M. P., Pfiffner, J., French, C., Socha, A., Thielke, A., Napolitano, S., Muller, P., et al. (2013) · eLife · doi:10.7554/elife.00603 · Cited by 78 · see citing works
Extensive DNA-binding specificity divergence of a conserved transcription regulator
Baker, C. R., Tuch, B. B., & Johnson, A. D. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1019177108 · Cited by 75 · see citing works
Self-citationGenetics and Molecular Biology in Candida albicans
Hernday, A. D., Noble, S. M., Mitrovich, Q. M., & Johnson, A. D. (2010) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(10)70031-8 · Cited by 77 · see citing works
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Benkhali, J. A., Coppin, E., Brun, S., Peraza‐Reyes, L., Martin, T., Dixelius, C., Lazar, N., TILBEURGH, H. V., & Debuchy, R. (2013) · PLoS Genetics · doi:10.1371/journal.pgen.1003642 · Cited by 77 · see citing works
Transcription factor function and promoter architecture govern the evolution of bacterial regulons
Pérez, J. C., & Groisman, E. A. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0810343106 · Cited by 74 · see citing works
ScerTF: a comprehensive database of benchmarked position weight matrices for Saccharomyces species
Spivak, A., & Stormo, G. D. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkr1180 · Cited by 76 · see citing works
Lind, A., Wisecaver, J. H., Smith, T. D., Feng, X., Calvo, A. M., & Rokas, A. (2015) · PLoS Genetics · doi:10.1371/journal.pgen.1005096 · Cited by 72 · see citing works
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Cain, C. W., Lohse, M. B., Homann, O. R., Sil, A., & Johnson, A. D. (2011) · Genetics · doi:10.1534/genetics.111.134080 · Cited by 75 · see citing works
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Booth, L. N., Tuch, B. B., & Johnson, A. D. (2010) · Nature · doi:10.1038/nature09560 · Cited by 75 · see citing works
Self-citationWang, A., Raniga, P. P., Lane, S., Lü, Y., & Liu, H. (2009) · Molecular and Cellular Biology · doi:10.1128/mcb.01502-08 · Cited by 75 · see citing works
Lohse, M. B., Hernday, A. D., Fordyce, P. M., Noiman, L., Sorrells, T. R., Hanson-Smith, V., Nobile, C. J., DeRisi, J. L., & Johnson, A. D. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1221734110 · Cited by 74 · see citing works
Self-citationJiménez-López, C., Collette, J. R., Brothers, K. M., Shepardson, K. M., Cramer, R. A., Wheeler, R. T., & Lorenz, M. C. (2012) · Eukaryotic Cell · doi:10.1128/ec.00290-12 · Cited by 72 · see citing works
Transcriptional Analysis of the <i>Candida albicans</i> Cell Cycle
Côte, P., Hogues, H., & Whiteway, M. (2009) · Molecular Biology of the Cell · doi:10.1091/mbc.e09-03-0210 · Cited by 72 · see citing works
Sabouri, N., Capra, J. A., & Zakian, V. A. (2014) · BMC Biology · doi:10.1186/s12915-014-0101-5 · Cited by 72 · see citing works
Gene duplication and the evolution of ribosomal protein gene regulation in yeast
Wapinski, I. N., Pfiffner, J., French, C. E., Socha, A. L., Thompson, D. A., & Regev, A. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0911905107 · Cited by 67 · see citing works
Intersecting transcription networks constrain gene regulatory evolution
Sorrells, T. R., Booth, L. N., Tuch, B. B., & Johnson, A. D. (2015) · Nature · doi:10.1038/nature14613 · Cited by 69 · see citing works
Self-citationRegulatory Variation Within and Between Species
Zheng, W., Gianoulis, T. A., Karczewski, K. J., Zhao, H., & Snyder, M. P. (2011) · Annual Review of Genomics and Human Genetics · doi:10.1146/annurev-genom-082908-150139 · Cited by 67 · see citing works
Rearrangements of the transcriptional regulatory networks of metabolic pathways in fungi.
Lavoie, H., Hogues, H., & Whiteway, M. (2009) · Current Opinion in Microbiology · doi:10.1016/j.mib.2009.09.015 · Cited by 74 · see citing works
Coevolution within a transcriptional network by compensatory trans and cis mutationsPreprint
Kuo, D., Licon, K., Bandyopadhyay, S., Chuang, R. J., Luo, C., Catalana, J., Ravasi, T., Tan, K., & Ideker, T. E. (2010) · Genome Research · doi:10.1101/gr.111765.110 · Cited by 67 · see citing works
Tempo and Mode in Evolution of Transcriptional Regulation
Gordon, K. L., & Ruvinsky, I. (2012) · PLoS Genetics · doi:10.1371/journal.pgen.1002432 · Cited by 62 · see citing works
Sellam, A., van het Hoog, M., Tebbji, F., Beaurepaire, C., Whiteway, M., & Nantel, A. (2014) · Eukaryotic Cell · doi:10.1128/ec.00292-13 · Cited by 63 · see citing works
Dalal, C. K., Zuleta, I. A., Mitchell, K. F., Andes, D. R., El-Samad, H., & Johnson, A. D. (2016) · eLife · doi:10.7554/elife.18981 · Cited by 62 · see citing works
Self-citationTranscription factor binding variation in the evolution of gene regulation
Dowell, R. D. (2010) · Trends in Genetics · doi:10.1016/j.tig.2010.08.005 · Cited by 61 · see citing works
Sellam, A., Hogues, H., Askew, C., Tebbji, F., Hoog, M. V. H., Lavoie, H., Kumamoto, C. A., Whiteway, M. S., & Nantel, A. (2010) · Genome biology · doi:10.1186/gb-2010-11-7-r71 · Cited by 58 · see citing works
14 Mating-Type Structure, Function, Regulation and Evolution in the Pezizomycotina
Dyer, P. S., Inderbitzin, P., & Debuchy, R. (2016) · The mycota · doi:10.1007/978-3-319-25844-7_14 · Cited by 58 · see citing works
Crawford, E. D., Seaman, J. E., Barber, A. E., David, D. C., Babbitt, P. C., Burlingame, A. L., & Wells, J. A. (2012) · Cell Death and Differentiation · doi:10.1038/cdd.2012.99 · Cited by 57 · see citing works
Lelandais, G., Tanty, V., Geneix, C., Etchebest, C., Jacq, C., & Devaux, F. (2008) · Genome biology · doi:10.1186/gb-2008-9-11-r164 · Cited by 56 · see citing works
Sensing the environment: Response of Candida albicans to the X factor
Cottier, F., & Mühlschlegel, F. A. (2009) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.2009.01564.x · Cited by 56 · see citing works
“Reverse genomics” predicts function of human conserved noncoding elements
Marcovitz, A., Jia, R., & Bejerano, G. (2016) · Molecular Biology and Evolution · doi:10.1093/molbev/msw001 · Cited by 53 · see citing works
Histoplasma capsulatum pathogenesis: making a lifestyle switch
Holbrook, E. D., & Rappleye, C. A. (2008) · Current Opinion in Microbiology · doi:10.1016/j.mib.2008.05.010 · Cited by 56 · see citing works
Signatures of combinatorial regulation in intrinsic biological noise
Warmflash, A., & Dinner, A. R. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0809314105 · Cited by 55 · see citing works
Evolutionary Conservation and Diversification of Puf RNA Binding Proteins and Their mRNA Targets
Hogan, G. J., Brown, P. O., & Herschlag, D. (2015) · PLoS Biology · doi:10.1371/journal.pbio.1002307 · Cited by 55 · see citing works
Becker, K., Beer, C., Freitag, M., & Kück, U. (2015) · Molecular Microbiology · doi:10.1111/mmi.12987 · Cited by 54 · see citing works
Exploitation of Latent Allostery Enables the Evolution of New Modes of MAP Kinase Regulation
Coyle, S. M., Flores, J. A., & Lim, W. A. (2013) · Cell · doi:10.1016/j.cell.2013.07.019 · Cited by 54 · see citing works
Nocedal, I., Mancera, E., & Johnson, A. D. (2017) · eLife · doi:10.7554/elife.23250 · Cited by 53 · see citing works
Self-citationFrom elements to modules: regulatory evolution in Ascomycota fungi
Wohlbach, D. J., Thompson, D. A., Gasch, A. P., & Regev, A. (2009) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2009.09.007 · Cited by 50 · see citing works
Evolution of transcriptional control in mammals
Wilson, M. D., & Odom, D. T. (2009) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2009.10.003 · Cited by 51 · see citing works
Barrière, A., Gordon, K. L., & Ruvinsky, I. (2012) · PLoS Genetics · doi:10.1371/journal.pgen.1002961 · Cited by 50 · see citing works
The zinc cluster transcription factor Ahr1p directs Mcm1p regulation of Candida albicans adhesion
Askew, C., Sellam, A., Epp, E., Mallick, J., Hogues, H., Mullick, A., Nantel, A., & Whiteway, M. S. (2010) · Molecular Microbiology · doi:10.1111/j.1365-2958.2010.07504.x · Cited by 51 · see citing works
The ancestral levels of transcription and the evolution of sexual phenotypes in filamentous fungi
Trail, F., Wang, Z., Stefanko, K., Cubba, C., & Townsend, J. P. (2017) · PLoS Genetics · doi:10.1371/journal.pgen.1006867 · Cited by 51 · see citing works
Habib, N., Wapinski, I., Margalit, H., Regev, A., & Friedman, N. (2012) · Molecular Systems Biology · doi:10.1038/msb.2012.50 · Cited by 50 · see citing works
Mogavero, S., Tavanti, A., Senesi, S., Rogers, P. D., & Morschhäuser, J. (2011) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.01467-10 · Cited by 49 · see citing works
Inference and Evolutionary Analysis of Genome-Scale Regulatory Networks in Large Phylogenies
Koch, C., Konieczka, J. H., Delorey, T. M., Lyons, A. M., Socha, A. L., Davis, K., Knaack, S., Thompson, D. A., O’Shea, E. K., Regev, A., et al. (2017) · Cell Systems · doi:10.1016/j.cels.2017.04.010 · Cited by 48 · see citing works
Evolution of biological interaction networks: from models to real data
Sun, M. G., & Kim, P. M. (2011) · Genome biology · doi:10.1186/gb-2011-12-12-235 · Cited by 49 · see citing works
Znaidi, S., van Wijlick, L., Hernández-Cervantes, A., Sertour, N., Desseyn, J., Vincent, F., Atanasova, R., Gouyer, V., Munro, C. A., Bachellier‐Bassi, S., et al. (2018) · Cellular Microbiology · doi:10.1111/cmi.12890 · Cited by 45 · see citing works
Porman, A. M., Hirakawa, M. P., Jones, S. K., Wang, N., & Bennett, R. J. (2013) · PLoS Genetics · doi:10.1371/journal.pgen.1003369 · Cited by 45 · see citing works
- Authors
- Tuch, B. B., Galgoczy, D. J., Hernday, A. D., Li, H., & Johnson, A. D.
- Affiliations
- University of California, San Francisco (US)
- Corresponding author
- Li, Hao
- Johnson, Alexander D
- Venue
- PLoS Biology
- Publisher
- Public Library of Science (PLoS)
- Published
- 2008-02-26
- Volume
- 6
- Issue
- 2
- Pages
- e38
- ISSN
- 1544-9173 (ISSN-L)
- 1545-7885
- PMC
- PMC2253631
- OpenAlex
- W2084695584
- Cited by
- 228
- References
- 66
- Citations by year
- 2026: 3 · 2025: 3 · 2024: 3 · 2023: 1 · 2022: 4 · 2021: 4 · 2020: 5 · 2019: 3 · 2018: 10 · 2017: 9 · 2016: 16 · 2015: 15 · 2014: 15 · 2013: 15 · 2012: 21
- FWCI
- 13.70
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS Biology (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- eScholarship (California Digital Library) (submittedVersion, cc-by)
- Figshare (submittedVersion, cc-by)
- Funders
- National Science Foundation
- Broad Institute
- Joint Genome Institute
- National Institutes of Health
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gene Regulatory Network Analysis
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Keywords
- combinatorial gene regulation, transcription factor binding sites, MCM1, Rap1, Wor1, hemiascomycetes, Kluyveromyces lactis, Candida albicans, Saccharomyces cerevisiae, ribosomal protein genes, host adaptation, cofactor interactions
- MeSH terms
- Genes, Fungal, Species Specificity, Transcription Factors, Gene Expression Regulation, Enzymologic, Evolution, Molecular, Minichromosome Maintenance 1 Protein, Saccharomyces cerevisiae Proteins, Epigenesis, Genetic
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