Evolution of reduced co-activator dependence led to target expansion of a starvation response pathway
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Abstract
Abstract In S. cerevisiae , the phosphate starvation (PHO) responsive transcription factors Pho4 and Pho2 are jointly required for induction of phosphate response genes and survival in phosphate starvation conditions. In the related human commensal and pathogen C. glabrata , Pho4 is required but Pho2 is dispensable for survival in phosphate-limited conditions and is only partially required for inducing the phosphate response genes. This reduced dependence on Pho2 evolved in C. glabrata and closely related species. Pho4 orthologs that are less dependent on Pho2 induce more genes when introduced into the S. cerevisiae background, and Pho4 in C. glabrata both binds to more sites and induces more genes with expanded functional roles compared to Pho4 in S. cerevisiae . Our work reveals an evolutionary mechanism for rapidly expanding the targets of a transcription factor by changing its dependence on a co-activator, potentially refining the physiological response it regulates.
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The CgPho4 target gene set includes genes involved in phosphate homeostasis, adherence, cell wall biosynthesis, non-phosphate-related stress response, and carbohydrate metabolism.
“This reduced dependence on CgPho2 appears to have substantially broadened the target gene set of CgPho4, which included genes involved in phosphate homeostasis as well as adherence, cell wall biosynthesis, non-phosphate-related stress response and carbohydrate metabolism [118].”
From Candida glabrata: A Lot More Than Meets the Eye (2019) · cites this paper as [118]
Reduced dependence on CgPho2 appears to have substantially broadened the target gene set of CgPho4.
“This reduced dependence on CgPho2 appears to have substantially broadened the target gene set of CgPho4, which included genes involved in phosphate homeostasis as well as adherence, cell wall biosynthesis, non-phosphate-related stress response and carbohydrate metabolism [118].”
From Candida glabrata: A Lot More Than Meets the Eye (2019) · cites this paper as [118]
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Cites
The Sequence Alignment/Map format and SAMtools
Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Marth, G., Abecasis, G., Durbin, R., & 1000 Genome Project Data Processing Subgroup (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp352 · Cited by 62,041 · see citing works
Robinson, M. D., McCarthy, D. J., & Smyth, G. K. (2010) · Bioinformatics · doi:10.1093/bioinformatics/btp616 · Cited by 41,364 · see citing works
limma powers differential expression analyses for RNA-sequencing and microarray studies
Ritchie, M. E., Phipson, B., Wu, D., Hu, Y., Law, C. W., Shi, W., & Smyth, G. K. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv007 · Cited by 40,458 · see citing works
BEDTools: a flexible suite of utilities for comparing genomic features
Quinlan, A. R., & Hall, I. M. (2010) · Bioinformatics · doi:10.1093/bioinformatics/btq033 · Cited by 27,437 · see citing works
Ultrafast and memory-efficient alignment of short DNA sequences to the human genome.
Langmead, B., Trapnell, C., Pop, M., & Salzberg, S. L. (2009) · Genome Biology · doi:10.1186/gb-2009-10-3-r25 · Cited by 21,849 · see citing works
Hierarchical Grouping to Optimize an Objective Function
Ward, J. H. (1963) · Journal of the American Statistical Association · doi:10.1080/01621459.1963.10500845 · Cited by 21,341 · see citing works
Model-based Analysis of ChIP-Seq (MACS)
Zhang, Y., Liu, T., Meyer, C. A., Eeckhoute, J., Johnson, D. S., Bernstein, B. E., Nusbaum, C., Myers, R. M., Brown, M., Li, W., et al. (2008) · Genome Biology · doi:10.1186/gb-2008-9-9-r137 · Cited by 18,386 · see citing works
A scaling normalization method for differential expression analysis of RNA-seq data
Robinson, M. D., & Oshlack, A. (2010) · Genome Biology · doi:10.1186/gb-2010-11-3-r25 · Cited by 7,876 · see citing works
voom: precision weights unlock linear model analysis tools for RNA-seq read counts
Law, C. W., Chen, Y., Shi, W., & Smyth, G. K. (2014) · Genome Biology · doi:10.1186/gb-2014-15-2-r29 · Cited by 6,155 · see citing works
Software for Computing and Annotating Genomic Ranges
Lawrence, M. F., Huber, W. K., Pagès, H., Aboyoun, P., Carlson, M. R. J., Gentleman, R. C., Morgan, M. T., & Carey, V. J. (2013) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1003118 · Cited by 4,438 · see citing works
Ward’s Hierarchical Agglomerative Clustering Method: Which Algorithms Implement Ward’s Criterion?
Murtagh, F. D., & Legendre, P. (2014) · Journal of Classification · doi:10.1007/s00357-014-9161-z · Cited by 3,939 · see citing works
High-efficiency yeast transformation using the LiAc/SS carrier DNA/PEG method
Gietz, R. D., & Schiestl, R. H. (2007) · Nature Protocols · doi:10.1038/nprot.2007.13 · Cited by 2,785 · see citing works
Janke, C., Magiera, M., Rathfelder, N., Taxis, C., Reber, S., Maekawa, H., Moreno-Borchart, A. C., Doenges, G., Schwob, E., Schiebel, E., et al. (2004) · Yeast · doi:10.1002/yea.1142 · Cited by 2,251 · see citing works
The Galaxy platform for accessible, reproducible and collaborative biomedical analyses: 2016 update
Afgan, E., Baker, D., van den Beek, M., Blankenberg, D. J., Bouvier, D., Čech, M., Chilton, J. M., Clements, D., Coraor, N., Eberhard, C., et al. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw343 · Cited by 2,150 · see citing works
The genomic basis of adaptive evolution in threespine sticklebacks
Jones, F. C., Grabherr, M. G., Chan, Y. F., Russell, P. H., Mauceli, E., Johnson, J., Swofford, R., Pirun, M., Zody, M. C., White, S. J., et al. (2012) · Nature · doi:10.1038/nature10944 · Cited by 1,792 · 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
Use of within-array replicate spots for assessing differential expression in microarray experiments
Smyth, G. K., Michaud, J., & Scott, H. S. (2005) · Computer applications in the biosciences · doi:10.1093/bioinformatics/bti270 · Cited by 1,406 · 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
The limits of selection during maize domestication
Wang, R.-L., Stec, A., Hey, J., Lukens, L., & Doebley, J. (1999) · Nature · doi:10.1038/18435 · Cited by 740 · see citing works
Byrne, K. P., & Wolfe, K. H. (2005) · Genome Research · doi:10.1101/gr.3672305 · Cited by 720 · 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
Natural history and evolutionary principles of gene duplication in fungi
Wapinski, I., Pfeffer, A., Friedman, N., & Regev, A. (2007) · Nature · doi:10.1038/nature06107 · Cited by 614 · see citing works
Repeated morphological evolution through cis-regulatory changes in a pleiotropic gene
Prud'homme, B., Gompel, N., Rokas, A., Kassner, V. A., Williams, T. M., Yeh, S.-D., True, J. R., & Carroll, S. B. (2006) · Nature · doi:10.1038/nature04597 · Cited by 507 · see citing works
Cofactor Binding Evokes Latent Differences in DNA Binding Specificity between Hox Proteins
Slattery, M. G., Riley, T., Liu, P., Abe, N., Gomez-Alcala, P., Dror, I., Zhou, T., Rohs, R., Honig, B. H., Bussemaker, H. J., et al. (2011) · Cell · doi:10.1016/j.cell.2011.10.053 · Cited by 497 · see citing works
Ogawa, N., DeRisi, J. L., & Brown, P. O. (2000) · Molecular Biology of the Cell · doi:10.1091/mbc.11.12.4309 · Cited by 494 · see citing works
The evolution of hierarchical gene regulatory networks
Erwin, D. H., & Davidson, E. H. (2009) · Nature Reviews Genetics · doi:10.1038/nrg2499 · Cited by 454 · 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 · cited 2× · see citing works
“C. albicans strains All C. albicans strains used in this study are from the transcriptional regulatory deletion library made by Homann et al (Homann et al. 2009) and ordered from the Fungal Genetics Stock Center (http://www.fgsc.net/) Media and Growth Conditions Phosphate-free synthetic complete medium was prepared fr…”
MethodInfluentialThe plausibility of life: resolving Darwin's dilemma
(2006) · Choice Reviews Online · doi:10.5860/choice.43-4010 · Cited by 438 · see citing works
Evolution of Gene Regulatory Networks Controlling Body Plan Development
Peter, I. S., & Davidson, E. H. (2011) · Cell · doi:10.1016/j.cell.2011.02.017 · Cited by 417 · see citing works
Kirschner, M. W., & Gerhart, J. C. (2017) · Yale University Press eBooks · doi:10.12987/9780300128673 · Cited by 408 · see citing works
High-resolution DNA-binding specificity analysis of yeast transcription factorsPreprint
Zhu, C., Byers, K. J. R. P., McCord, R. P., Shi, Z., Berger, M. F., Newburger, D. E., Saulrieta, K., Smith, Z. D., Shah, M. V., Radhakrishnan, M., et al. (2009) · Genome Research · doi:10.1101/gr.090233.108 · Cited by 399 · see citing works
Phosphorylation of the Transcription Factor PHO4 by a Cyclin-CDK Complex, PHO80-PHO85
Kaffman, A., Herskowitz, I., Tjian, R., & O’Shea, E. K. (1994) · Science · doi:10.1126/science.8108735 · Cited by 359 · see citing works
Nitta, K. R., Jolma, A., Yin, Y., Morgunova, E. Y., Kivioja, T., Akhtar, J., Hens, K., Toivonen, J., Deplancke, B., Furlong, E. E. M., et al. (2015) · eLife · doi:10.7554/elife.04837 · Cited by 358 · see citing works
Regulation of PHO4 Nuclear Localization by the PHO80-PHO85 Cyclin-CDK Complex
O’Neill, E., Kaffman, A., Jolly, E. R., & O’Shea, E. K. (1996) · Science · doi:10.1126/science.271.5246.209 · Cited by 330 · see citing works
Roles of Phosphorylation Sites in Regulating Activity of the Transcription Factor Pho4
Komeili, A., & O’Shea, E. K. (1999) · Science · doi:10.1126/science.284.5416.977 · Cited by 326 · 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
Disease Model of GATA4 Mutation Reveals Transcription Factor Cooperativity in Human Cardiogenesis
Ang, Y.-S., Rivas, R. N., Ribeiro, A. J. S., Srivas, R., Rivera, J., Stone, N. R., Pratt, K., Mohamed, T. M. A., Fu, J.-D., Spencer, C. I., et al. (2016) · Cell · doi:10.1016/j.cell.2016.11.033 · Cited by 294 · see citing works
Guo, Y., Mahony, S., & Gifford, D. K. (2012) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1002638 · Cited by 288 · see citing works
Species-Specific Transcription in Mice Carrying Human Chromosome 21
Wilson, M. D., Barbosa‐Morais, N. L., Schmidt, D., Conboy, C. B., Vanes, L., Tybulewicz, V. L. J., Fisher, E., Tavaré, S., & Odom, D. T. (2008) · Science · doi:10.1126/science.1160930 · Cited by 280 · see citing works
Struhl, K. (1987) · Cell · doi:10.1016/0092-8674(87)90511-3 · Cited by 259 · 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
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
Nicotinic Acid Limitation Regulates Silencing of <i>Candida</i> Adhesins During UTI
Domergue, R., Castaño, I., De Las Peñas, A., Zupancic, M., Lockatell, V., Hebel, J. R., Johnson, D., & Cormack, B. P. (2005) · Science · doi:10.1126/science.1108640 · Cited by 249 · see citing works
RSAT peak-motifs: motif analysis in full-size ChIP-seq datasets
Thomas‐Chollier, M., Herrmann, C., Defrance, M., Sand, O., Thieffry, D., & van Helden, J. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkr1104 · Cited by 239 · see citing works
Chromatin decouples promoter threshold from dynamic range
Lam, F. H., Steger, D. J., & O’Shea, E. K. (2008) · Nature · doi:10.1038/nature06867 · Cited by 237 · see citing works
Structure and function of a transcriptional network activated by the MAPK Hog1
Capaldi, A. P., Kaplan, T., Liu, Y., Habib, N., Regev, A., Friedman, N., & O’Shea, E. K. (2008) · Nature Genetics · doi:10.1038/ng.235 · Cited by 233 · see citing works
The evolution of combinatorial gene regulation in fungi
Tuch, B. B., Galgoczy, D. J., Hernday, A. D., Li, H., & Johnson, A. D. (2008) · PLoS Biology · doi:10.1371/journal.pbio.0060038 · Cited by 228 · see citing works
Inferring Binding Energies from Selected Binding Sites
Zhao, Y., Granas, D. M., & Stormo, G. D. (2009) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1000590 · Cited by 208 · see citing works
Comparative genomics of emerging pathogens in the Candida glabrata clade.
Gabaldón, T., Martin, T., Marcet-Houben, M., Durrens, P., Bolotin-Fukuhara, M., Lespinet, O., Arnaise, S., Boisnard, S., Aguileta, G., Atanasova, R., et al. (2013) · BMC Genomics · doi:10.1186/1471-2164-14-623 · Cited by 198 · see citing works
Rhee, H. S., & Pugh, B. F. (2012) · Current Protocols in Molecular Biology · doi:10.1002/0471142727.mb2124s100 · Cited by 195 · see citing works
YeTFaSCo: a database of evaluated yeast transcription factor sequence specificities
de Boer, C. G., & Hughes, T. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkr993 · Cited by 193 · see citing works
Cormack, B. P., & Falkow, S. (1999) · Genetics · doi:10.1093/genetics/151.3.979 · Cited by 180 · see citing works
Molecular mechanisms of selector gene function and evolution
Mann, R. S. (2002) · Current Opinion in Genetics & Development · doi:10.1016/s0959-437x(02)00344-1 · Cited by 167 · see citing works
Vogel, K. D., Hörz, W., & Hinnen, A. (1989) · Molecular and Cellular Biology · doi:10.1128/mcb.9.5.2050 · Cited by 154 · see citing works
A Promiscuous Intermediate Underlies the Evolution of LEAFY DNA Binding Specificity
Sayou, C., Monniaux, M., Nanao, M., Moyroud, E., Brockington, S. F., Thévenon, E., Chahtane, H., Warthmann, N., Melkonian, M., Zhang, Y., et al. (2014) · Science · doi:10.1126/science.1248229 · Cited by 139 · see citing works
Phylogeny and Evolution of Medical Species of Candida and Related Taxa: a Multigenic Analysis
Diezmann, S., Cox, C. J., Schönian, G., Vilgalys, R. J., & Mitchell, T. G. (2004) · Journal of Clinical Microbiology · doi:10.1128/jcm.42.12.5624-5635.2004 · Cited by 135 · see citing works
MochiView: versatile software for genome browsing and DNA motif analysis
Homann, O. R., & Johnson, A. D. (2010) · BMC Biology · doi:10.1186/1741-7007-8-49 · Cited by 132 · see citing works
Silent chromatin determines target preference of the Saccharomyces retrotransposon Ty5
Zou, S., & Voytas, D. F. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.14.7412 · Cited by 128 · see citing works
Luo, G., & Samaranayake, L. P. (2002) · Apmis · doi:10.1034/j.1600-0463.2002.1100902.x · Cited by 121 · see citing works
Positive Feedback Regulates Switching of Phosphate Transporters in S. cerevisiae
Wykoff, D. D., Rizvi, A. H., Raser, J. M., Margolin, B., & O’Shea, E. K. (2007) · Molecular Cell · doi:10.1016/j.molcel.2007.07.022 · Cited by 119 · see citing works
Zhou, X., & O’Shea, E. K. (2011) · Molecular Cell · doi:10.1016/j.molcel.2011.05.025 · Cited by 119 · see citing works
Intracellular survival ofCandida glabratain macrophages: immune evasion and persistence
Kasper, L., Seider, K., & Hube, B. (2015) · FEMS Yeast Research · doi:10.1093/femsyr/fov042 · Cited by 115 · see citing works
Evolution of the hemiascomycete yeasts: on life styles and the importance of inbreeding
Knop, M. (2006) · BioEssays · doi:10.1002/bies.20435 · Cited by 112 · see citing works
Evolution of DNA specificity in a transcription factor family produced a new gene regulatory module
McKeown, A. N., Bridgham, J. T., Anderson, D. W., Murphy, M. N., Ortlund, E. A., & Thornton, J. W. (2014) · Cell · doi:10.1016/j.cell.2014.09.003 · Cited by 107 · see citing works
Cloning-free genome alterations in saccharomyces cereuisiae using adaptamer-mediated PCR
Reid, R. J. D., Lisby, M., & Rothstein, R. J. (2002) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(02)50968-x · Cited by 95 · see citing works
Sérandour, A. A., Brown, G. D., Cohen, J. D., & Carroll, J. S. (2013) · Genome biology · doi:10.1186/gb-2013-14-12-r147 · Cited by 89 · 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
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
Barbarić, S., Münsterkötter, M., Goding, C. R., & Hörz, W. (1998) · Molecular and Cellular Biology · doi:10.1128/mcb.18.5.2629 · Cited by 74 · see citing works
Barbarić, S., Münsterkötter, M., Svaren, J. P., & Hörz, W. (1996) · Nucleic Acids Research · doi:10.1093/nar/24.22.4479 · Cited by 74 · see citing works
The structure and evolution of cis -regulatory regions: the shavenbaby story
Stern, D. L., & Frankel, N. (2013) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2013.0028 · Cited by 71 · see citing works
Huang, S., & O’Shea, E. K. (2005) · Genetics · doi:10.1534/genetics.104.038695 · Cited by 71 · see citing works
Romanowski, K. S. S., Zaborin, A., Valuckaite, V., Rolfes, R. J., BABROWSKI, T. A., Bethel, C., Olivas, A. D., Zaborina, O. Y., & Alverdy, J. C. (2012) · PLoS ONE · doi:10.1371/journal.pone.0030119 · Cited by 69 · see citing works
Variable gene expression in eukaryotes: a network perspective
Wittkopp, P. J. (2007) · Journal of Experimental Biology · doi:10.1242/jeb.002592 · Cited by 67 · 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
Experimental determination of the evolvability of a transcription factor
Maerkl, S. J., & Quake, S. R. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0907688106 · Cited by 66 · see citing works
Quenching of microbial samples for increased reliability of microarray data
Pieterse, B., Jellema, R. H., & WERF, M. J. V. D. (2005) · Journal of Microbiological Methods · doi:10.1016/j.mimet.2005.04.035 · Cited by 61 · see citing works
Espinosa, J., Boyd, J. S., Cantos, R., Salinas, P., Golden, S. S., & Contreras, A. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1424632112 · Cited by 60 · see citing works
Ikeh, M. A. C., Kastora, S. L., Day, A. M., Herrero-de-Dios, C. M., Tarrant, E., Waldron, K. J., Banks, A. P., Bain, J. M., Lydall, D. A., Veal, E. A., et al. (2016) · Molecular Biology of the Cell · doi:10.1091/mbc.e16-05-0266 · Cited by 60 · see citing works
van Werven, F. J. (2006) · Nucleic Acids Research · doi:10.1093/nar/gkl003 · Cited by 58 · see citing works
Elfving, N., Chereji, R. V., Bharatula, V., Björklund, S., Morozov, A. V., & Broach, J. R. (2014) · Nucleic Acids Research · doi:10.1093/nar/gku176 · Cited by 54 · see citing works
Jawhara, S., Mogensen, E. G., Maggiotto, F., Fradin, C., Sarazin, A., Dubuquoy, L., Maes, E., Guérardel, Y., Janbon, G., & Poulain, D. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.329300 · 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
Brayer, K. J., Lynch, V. J., & Wagner, G. P. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1100990108 · Cited by 44 · see citing works
Optimal use of tandem biotin and V5 tags in ChIP assays
Kolodziej, K. E., Pourfarzad, F., de Boer, E., Krpic, S., Grosveld, F. G., & Strouboulis, J. (2009) · BMC Molecular Biology · doi:10.1186/1471-2199-10-6 · Cited by 42 · see citing works
Kerwin, C. L., & Wykoff, D. D. (2009) · Genetics · doi:10.1534/genetics.109.101063 · Cited by 34 · see citing works
Jarvela, A. M. C., Brubaker, L., Vedenko, A., Gupta, A., Armitage, B. A., Bulyk, M. L., & Hinman, V. F. (2014) · Molecular Biology and Evolution · doi:10.1093/molbev/msu213 · Cited by 32 · see citing works
Shao, D., Creasy, C. L., & Bergman, L. W. (1996) · Molecular and General Genetics MGG · doi:10.1007/bf02172527 · Cited by 29 · see citing works
Fungal regulatory evolution: cis and trans in the balance
Thompson, D. A., & Regev, A. (2009) · FEBS Letters · doi:10.1016/j.febslet.2009.11.032 · Cited by 26 · see citing works
Peñas, A. D. L., Juárez‐Cepeda, J., López-Fuentes, E., Briones-Martín-del-Campo, M., Gutiérrez‐Escobedo, G., & Castaño, I. (2015) · FEMS Yeast Research · doi:10.1093/femsyr/fov056 · Cited by 25 · see citing works
Orkwis, B. R., Davies, D. L., Kerwin, C. L., Sanglard, D., & Wykoff, D. D. (2010) · Genetics · doi:10.1534/genetics.110.120824 · Cited by 21 · see citing works
Atanasova, R., Angoulvant, A., Tefit, M., Gay, F., Guitard, J., Mazier, D., Fairhead, C., & Hennequin, C. (2013) · PLoS ONE · doi:10.1371/journal.pone.0069664 · Cited by 20 · see citing works
Fabre, É., Sfihi-Loualia, G., Pourcelot, M., Coddeville, B., Krzewinski, F., Bouckaert, J. M. J., Maes, E., Hurtaux, T., Dubois, R., Fradin, C., et al. (2013) · Biochemical Journal · doi:10.1042/bj20131012 · Cited by 17 · see citing works
<i>De novo</i>generation of a phosphate starvation-regulated promoter in<i>Candida glabrata</i>
Kerwin, C. L., & Wykoff, D. D. (2012) · FEMS Yeast Research · doi:10.1111/1567-1364.12000 · Cited by 9 · see citing works
Orlando, K., Iosue, C. L., Leone, S. G., Davies, D. L., & Wykoff, D. D. (2015) · Biochemical Journal · doi:10.1042/bj20150611 · Cited by 2 · see citing works
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Bhalla, K., Qu, X., Kretschmer, M., & Kronstad, J. W. (2021) · Trends in Microbiology · doi:10.1016/j.tim.2021.08.002 · Cited by 77 · see citing works
Phosphate Acquisition and Virulence in Human Fungal Pathogens
Ikeh, M. A. C., Ahmed, Y., & Quinn, J. (2017) · Microorganisms · doi:10.3390/microorganisms5030048 · Cited by 58 · see citing works
Schwer, B., Sánchez, A. M., Garg, A., Chatterjee, D., & Shuman, S. (2017) · mBio · doi:10.1128/mbio.01218-17 · Cited by 32 · see citing works
Phosphate in Virulence of Candida albicans and Candida glabrata
Köhler, J. R., Acosta‐Zaldívar, M., & Qi, W. (2020) · Journal of Fungi · doi:10.3390/jof6020040 · Cited by 32 · see citing works
IP7-SPX Domain Interaction Controls Fungal Virulence by Stabilizing Phosphate Signaling Machinery
Desmarini, D., Lev, S., Furkert, D., Crossett, B., Saiardi, A., Kaufman‐Francis, K., Li, C., Sorrell, T. C., Wilkinson‐White, L. E., Matthews, J. M., et al. (2020) · mBio · doi:10.1128/mbio.01920-20 · Cited by 32 · see citing works
Lev, S., & Djordjevic, J. T. (2018) · PLoS Pathogens · doi:10.1371/journal.ppat.1007021 · Cited by 25 · see citing works
Gomes‐Vieira, A. L., Wideman, J. G., Vieira, L. P., Gomes, S. L., Richards, T. A., & Meyer‐Fernandes, J. R. (2018) · Fungal Genetics and Biology · doi:10.1016/j.fgb.2018.04.004 · Cited by 19 · see citing works
Candida albicans’ inorganic phosphate transport and evolutionary adaptation to phosphate scarcity
Acosta-Zaldívar, M., Qi, W., Mishra, A., Roy, U., King, W. R., Li, Y., Patton-Vogt, J., Anderson, M. Z., & Köhler, J. R. (2024) · PLOS Genetics · doi:10.1371/journal.pgen.1011156 · Cited by 14 · see citing works
King, W. R., Acosta‐Zaldívar, M., Qi, W., Cherico, N., Cooke, L., Köhler, J. R., & Patton, J. L. (2023) · mSphere · doi:10.1128/msphere.00231-23 · Cited by 10 · see citing works
Zheng, Q., Guan, G., Cao, C., Li, Q., & Huang, G. (2020) · Current Genetics · doi:10.1007/s00294-020-01100-z · Cited by 9 · see citing works
Liang, J., Tang, H., Snyder, L. F., Youngstrom, C. E., & He, B. (2023) · PLoS Pathogens · doi:10.1371/journal.ppat.1011748 · Cited by 7 · see citing works
Grf10 regulates the response to copper, iron, and phosphate in Candida albicans
Wangsanut, T., Arnold, S. J. Y., Jilani, S. Z., Marzec, S., Monsour, R. C., & Rolfes, R. J. (2023) · G3 Genes Genomes Genetics · doi:10.1093/g3journal/jkad070 · Cited by 7 · see citing works
Snyder, L. F., O'Brien, E. M., Zhao, J., Liang, J., Bruce, B. J., Zhang, Y., Zhu, W., Cassier, T., Schnicker, N., Zhou, X., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-59244-w · Cited by 6 · see citing works
Iosue, C. L., Gulotta, A. P., Selhorst, K. B., Mody, A. C., Barbour, K. M., Marcotte, M. J., Bui, L. N., Leone, S. G., Lang, E. C., Hughes, G. H., et al. (2019) · G3 Genes Genomes Genetics · doi:10.1534/g3.119.400897 · Cited by 4 · see citing works
The PHO pathway involved in phosphate metabolism in Yeast for efficient phosphorus removal
Hu, M., Qiu, L., & Wang, Y. (2018) · E3S Web of Conferences · doi:10.1051/e3sconf/20185304023 · Cited by 3 · see citing works
Tup1 Paralog CgTUP11 Is a Stronger Repressor of Transcription than CgTUP1 in Candida glabrata
Bui, L. N., Iosue, C. L., & Wykoff, D. D. (2022) · mSphere · doi:10.1128/msphere.00765-21 · Cited by 3 · see citing works
Dahbi, Y., Benhida, R., & Danouche, M. (2026) · Reviews in Environmental Science and Bio/Technology · doi:10.1007/s11157-026-09775-5 · Cited by 1 · see citing works
Functional analysis of a Phytophthora host-translocated effector using the yeast model system
Wilson, A. C., & Morgan, W. R. (2021) · PeerJ · doi:10.7717/peerj.12576
Ariño, J. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms262311450
Zhao, J., & He, B. (2020) · Figshare · doi:10.6084/m9.figshare.13140446
Genetic Tools in the Nakaseomyces clade for Evolutionary Comparisons of Signal Transduction Pathways
Abraham, M., Iosue, C. L., & Wykoff, D. D. (2026) · Yeast · doi:10.1002/yea.70029
Komagataella phaffii Encodes Two Functional Pho4 Transcription Factors
Albacar, M., González, A., Wang, R., Casamayor, A., & Ariño, J. (2026) · International Journal of Molecular Sciences · doi:10.3390/ijms27156561
- Authors
- He, B. Z., Zhou, X., & O’Shea, E. K.
- Affiliations
- Howard Hughes Medical Institute (US)
- Venue
- eLife
- Publisher
- eLife Sciences Publications, Ltd
- Published
- 2017-05-09
- Volume
- 6
- ISSN
- 2050-084X (ISSN-L)
- PMC
- PMC5446240
- OpenAlex
- W2580493040
- Cited by
- 27
- References
- 96
- Citations by year
- 2026: 3 · 2025: 2 · 2024: 1 · 2023: 3 · 2022: 1 · 2021: 5 · 2020: 4 · 2019: 2 · 2018: 3 · 2017: 3
- FWCI
- 1.34
- Type
- journal article
- Language
- en
- Update notices
- correction (2022-10-20)
- Open access
- gold
- doi.org
- Licence
- Locations
- eLife (publishedVersion, cc-by)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Howard Hughes Medical Institute
- 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 › Genetics › Bacterial Genetics and Biotechnology
- Keywords
- combinatorial gene regulation, transcription factor evolution, Pho4, PHO2, phosphate starvation response, Candida glabrata, Saccharomyces cerevisiae, orthologs, transcriptional activation, phylogenetic analysis
- MeSH terms
- Phosphates, Phylogeny, Saccharomyces cerevisiae, Transcription Factors, Gene Expression Regulation, Fungal, Evolution, Molecular, Candida glabrata, Microbial Viability, Gene Regulatory Networks
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