Unexpected repertoire of metazoan transcription factors in the unicellular holozoan Capsaspora owczarzaki
Open accessAbstract
How animals (metazoans) originated from their single-celled ancestors remains a major question in biology. As transcriptional regulation is crucial to animal development, deciphering the early evolution of associated transcription factors (TFs) is critical to understanding metazoan origins. In this study, we uncovered the repertoire of 17 metazoan TFs in the amoeboid holozoan Capsaspora owczarzaki, a representative of a unicellular lineage that is closely related to choanoflagellates and metazoans. Phylogenetic and comparative genomic analyses with the broadest possible taxonomic sampling allowed us to formulate new hypotheses regarding the origin and evolution of developmental metazoan TFs. We show that the complexity of the TF repertoire in C. owczarzaki is strikingly high, pushing back further the origin of some TFs formerly thought to be metazoan specific, such as T-box or Runx. Nonetheless, TF families whose beginnings antedate the origin of the animal kingdom, such as homeodomain or basic helix-loop-helix, underwent significant expansion and diversification along metazoan and eumetazoan stems.
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MrBayes 3: Bayesian phylogenetic inference under mixed models
Ronquist, F., & Huelsenbeck, J. P. (2003) · Bioinformatics · doi:10.1093/bioinformatics/btg180 · Cited by 28,956 · see citing works
RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models
Stamatakis, A. (2006) · Bioinformatics · doi:10.1093/bioinformatics/btl446 · Cited by 15,582 · see citing works
Eddy, S. R. (1998) · Bioinformatics · doi:10.1093/bioinformatics/14.9.755 · Cited by 5,515 · see citing works
MAFFT version 5: improvement in accuracy of multiple sequence alignment
Katoh, K., Kuma, K., Toh, H., & Miyata, T. (2005) · Nucleic Acids Research · doi:10.1093/nar/gki198 · Cited by 5,063 · see citing works
Prediction of complete gene structures in human genomic DNA
Burge, C., & Karlin, S. (1997) · Journal of Molecular Biology · doi:10.1006/jmbi.1997.0951 · Cited by 4,211 · see citing works
Hayden, M. S., & Ghosh, S. (2004) · Genes & Development · doi:10.1101/gad.1228704 · Cited by 3,842 · see citing works
STATs: transcriptional control and biological impact
Levy, D. E., & Darnell, J. E. (2002) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm909 · Cited by 3,201 · see citing works
International Journal of Molecular Medicine
(2026) · International Journal of Molecular Medicine · doi:10.3892/ijmm · Cited by 2,247 · see citing works
CONSEL: for assessing the confidence of phylogenetic tree selection
Shimodaira, H., & Hasegawa, M. (2001) · Bioinformatics · doi:10.1093/bioinformatics/17.12.1246 · Cited by 2,051 · see citing works
CBP/p300 in cell growth, transformation, and development
Goodman, R. H., & Smolik, S. (2000) · Genes & Development · doi:10.1101/gad.14.13.1553 · Cited by 1,778 · see citing works
AUGUSTUS: a web server for gene prediction in eukaryotes that allows user-defined constraints
Stanke, M., & Morgenstern, B. (2005) · Nucleic Acids Research · doi:10.1093/nar/gki458 · Cited by 1,609 · see citing works
NFAT proteins: key regulators of T-cell development and function
Macián, F. (2005) · Nature reviews. Immunology · doi:10.1038/nri1632 · Cited by 1,575 · see citing works
Sea Anemone Genome Reveals Ancestral Eumetazoan Gene Repertoire and Genomic Organization
Putnam, N. H., Srivastava, M., Hellsten, U., Dirks, B., Chapman, J., Salamov, A., Terry, A., Shapiro, H., Lindquist, E., Kapitonov, V. V., et al. (2007) · Science · doi:10.1126/science.1139158 · Cited by 1,555 · see citing works
The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans
King, N., Westbrook, M. J., Young, S. L., Kuo, A., Abedin, M., Chapman, J., Fairclough, S., Hellsten, U., Isogai, Y., Letunic, I., et al. (2008) · Nature · doi:10.1038/nature06617 · Cited by 1,139 · see citing works
Phytophthora Genome Sequences Uncover Evolutionary Origins and Mechanisms of Pathogenesis
Tyler, B., Tripathy, S., Zhang, X.-M., Dehal, P., Jiang, R. H. Y., Aerts, A., Arredondo, F. D., Baxter, L., Bensasson, D., Beynon, J., et al. (2006) · Science · doi:10.1126/science.1128796 · Cited by 1,084 · see citing works
The Amphimedon queenslandica genome and the evolution of animal complexity
Srivastava, M., Simakov, O., Chapman, J., Fahey, B., Gauthier, M. E. A., Mitros, T., Richards, G. S., Conaco, C., Dacre, M., Hellsten, U., et al. (2010) · Nature · doi:10.1038/nature09201 · Cited by 1,049 · see citing works
Self-citationGehring, W. J., Affolter, M., & Bürglin, T. R. (1994) · Annual Review of Biochemistry · doi:10.1146/annurev.bi.63.070194.002415 · Cited by 861 · see citing works
Bromberg, J. (2002) · Journal of Clinical Investigation · doi:10.1172/jci15617 · Cited by 846 · see citing works
MEF2: a central regulator of diverse developmental programs
Potthoff, M. J., & Olson, E. N. (2007) · Development · doi:10.1242/dev.008367 · Cited by 834 · see citing works
Regulation of NF-κB by Cyclin-Dependent Kinases Associated with the p300 Coactivator
Perkins, N. D., Felzien, L. K., Betts, J. C., Leung, K., Beach, D., & Nabel, G. J. (1997) · Science · doi:10.1126/science.275.5299.523 · Cited by 722 · see citing works
Origin and Diversification of Basic-Helix-Loop-Helix Proteins in Plants
Pires, N. D., & Dolan, L. (2009) · Molecular Biology and Evolution · doi:10.1093/molbev/msp288 · Cited by 642 · see citing works
An ancestral MADS-box gene duplication occurred before the divergence of plants and animals
Alvarez-Buylla, E. R., Pelaz, S., Liljegren, S. J., Gold, S. E., Burgeff, C., Ditta, G. S., de Pouplana, L. R., Martínez-Castilla, L. P., & Yanofsky, M. F. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.10.5328 · Cited by 579 · see citing works
An overview of the basic helix-loop-helix proteins.
Jones, S. (2004) · Genome biology · doi:10.1186/gb-2004-5-6-226 · Cited by 501 · see citing works
A Comprehensive Classification and Evolutionary Analysis of Plant Homeobox Genes
Mukherjee, K., Brocchieri, L., & Bürglin, T. R. (2009) · Molecular Biology and Evolution · doi:10.1093/molbev/msp201 · Cited by 452 · see citing works
(1994) · PubMed · Cited by 381 · see citing works
Crystallographic structure of the T domain–DNA complex of the Brachyury transcription factor
Müller, C. W., & Herrmann, B. G. (1997) · Nature · doi:10.1038/39929 · Cited by 326 · see citing works
The HMG-box: a versatile protein domain occurring in a wide variety of DNA-binding proteins
Štros, M., Launholt, D., & Grasser, K. D. (2007) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-007-7162-3 · Cited by 312 · see citing works
The Origins of Multicellularity and the Early History of the Genetic Toolkit For Animal Development
Rokas, A. (2008) · Annual Review of Genetics · doi:10.1146/annurev.genet.42.110807.091513 · Cited by 312 · see citing works
Simionato, E., Ledent, V., Richards, G. S., Thomas‐Chollier, M., Kerner, P., Coornaert, D., Degnan, B. M., & Vervoort, M. (2007) · BMC Evolutionary Biology · doi:10.1186/1471-2148-7-33 · Cited by 289 · see citing works
Self-citationGenesis and Expansion of Metazoan Transcription Factor Gene Classes
Larroux, C., Luke, G. N., Koopman, P. A., Rokhsar, D. S., Shimeld, S. M., & Degnan, B. M. (2008) · Molecular Biology and Evolution · doi:10.1093/molbev/msn047 · Cited by 275 · see citing works
Self-citationA Phylogenomic Investigation into the Origin of Metazoa
Ruiz‐Trillo, I., Roger, A. J., Burger, G., Gray, M. W., & Lang, B. F. (2008) · Molecular Biology and Evolution · doi:10.1093/molbev/msn006 · Cited by 269 · see citing works
Self-citationp300/CBP/p53 interaction and regulation of the p53 response
Grossman, S. R. (2001) · European Journal of Biochemistry · doi:10.1046/j.1432-1327.2001.02226.x · Cited by 264 · see citing works
Multigene Phylogeny of Choanozoa and the Origin of Animals
Shalchian‐Tabrizi, K., Minge, M. A., Espelund, M., Orr, R. J. S., Ruden, T. A., Jakobsen, K. S., & Cavalier‐Smith, T. (2008) · PLoS ONE · doi:10.1371/journal.pone.0002098 · Cited by 263 · see citing works
Phylogenomics reveals a new ‘megagroup’ including most photosynthetic eukaryotes
Burki, F., Shalchian‐Tabrizi, K., & Pawlowski, J. W. (2008) · Biology Letters · doi:10.1098/rsbl.2008.0224 · Cited by 256 · see citing works
Ancient origin of the integrin-mediated adhesion and signaling machinery
Sebé-Pedrós, A., Roger, A. J., Lang, B. F., King, N., & Ruiz‐Trillo, I. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1002257107 · Cited by 250 · see citing works
Self-citationConvergent Evolution of Chromosomal Sex-Determining Regions in the Animal and Fungal Kingdoms
Fraser, J. A., Diezmann, S., Subaran, R. L., Allen, A., Lengeler, K. B., Dietrich, F. S., & Heitman, J. (2004) · PLoS Biology · doi:10.1371/journal.pbio.0020384 · Cited by 249 · see citing works
The Premetazoan Ancestry of Cadherins
Sigg, M. A., & King, N. (2008) · Science · doi:10.1126/science.1151084 · Cited by 239 · see citing works
T-box genes: what they do and how they do it
Smith, J. (1999) · Trends in Genetics · doi:10.1016/s0168-9525(99)01693-5 · Cited by 238 · see citing works
Kawata, T., Shevchenko, A., Fukuzawa, M., Jermyn, K. A., Totty, N. F., Zhukovskaya, N. V., Sterling, A., Mann, M., & Williams, J. G. (1997) · Cell · doi:10.1016/s0092-8674(00)80276-7 · Cited by 231 · see citing works
Jin, Y.-H., Jeon, E.-J., Li, Q.-L., Lee, Y. H., Choi, J.-K., Kim, W.-J., Lee, K.-Y., & Bae, S.-C. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m313120200 · Cited by 211 · see citing works
Manning, G., Young, S. L., Miller, W. T., & Zhai, Y. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0801314105 · Cited by 211 · see citing works
Bray, S. J., & Kafatos, F. C. (1991) · Genes & Development · doi:10.1101/gad.5.9.1672 · Cited by 206 · see citing works
The origins of multicellularity: a multi-taxon genome initiative
Ruiz‐Trillo, I., Burger, G., Holland, P. W. H., King, N., Lang, B. F., Roger, A. J., & Gray, M. W. (2007) · Trends in Genetics · doi:10.1016/j.tig.2007.01.005 · Cited by 206 · see citing works
Self-citationCoffman, J. A. (2003) · Cell Biology International · doi:10.1016/s1065-6995(03)00018-0 · Cited by 204 · see citing works
Sheng, G., dos Reis, M., & Stern, C. D. (2003) · Cell · doi:10.1016/s0092-8674(03)00927-9 · Cited by 201 · see citing works
Structural basis for the diversity of DNA recognition by bZIP transcription factors
Fujii, Y., Shimizu, T., Toda, T., Yanagida, M., & Hakoshima, T. (2000) · Nature Structural Biology · doi:10.1038/82822 · Cited by 198 · see citing works
Dodou, E., & Treisman, R. (1997) · Molecular and Cellular Biology · doi:10.1128/mcb.17.4.1848 · Cited by 196 · see citing works
Evolution of homeobox genes: Q50 Paired-like genes founded the Paired class
Galliot, B., de Vargas, C., & Miller, D. J. (1999) · Development Genes and Evolution · doi:10.1007/s004270050243 · Cited by 188 · see citing works
Improvement in the accuracy of multiple sequence alignment program MAFFT.
Katoh, K., Kuma, K., Miyata, T., & Toh, H. (2005) · PubMed · Cited by 182 · see citing works
The Dictyostelium Kinome—Analysis of the Protein Kinases from a Simple Model Organism
Goldberg, J. M., Manning, G., Liu, A. P., Fey, P., Pilcher, K. E., Xu, Y., & Smith, J. L. (2006) · PLoS Genetics · doi:10.1371/journal.pgen.0020038 · Cited by 179 · see citing works
Larroux, C., Fahey, B., Liubicich, D., Hinman, V. F., Gauthier, M., Gongora, M., Green, K., Wörheide, G., Leys, S. P., & Degnan, B. M. (2006) · Evolution & Development · doi:10.1111/j.1525-142x.2006.00086.x · Cited by 173 · see citing works
Self-citationStructural basis for recruitment of CBP/p300 coactivators by STAT1 and STAT2 transactivation domains
Wojciak, J. M., Martinez‐Yamout, M. A., Dyson, H. J., & Wright, P. E. (2009) · The EMBO Journal · doi:10.1038/emboj.2009.30 · Cited by 172 · see citing works
CBP and p300 are cytoplasmic E4 polyubiquitin ligases for p53
Shi, D., Pop, M. S., Kulikov, R., Love, I. M., Kung, A. L., & Grossman, S. R. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0904305106 · Cited by 161 · see citing works
Brown, M. W., Spiegel, F. W., & Silberman, J. D. (2009) · Molecular Biology and Evolution · doi:10.1093/molbev/msp185 · Cited by 149 · see citing works
SnapShot:Forkhead Transcription Factors I
Tuteja, G., & Kaestner, K. H. (2007) · Cell · doi:10.1016/j.cell.2007.09.005 · Cited by 145 · see citing works
Scholz, C. B., & Technau, U. (2003) · Development Genes and Evolution · doi:10.1007/s00427-002-0272-x · Cited by 142 · see citing works
Redox Regulation of the DNA Binding Activity in Transcription Factor PEBP2
Akamatsu, Y., Ohno, T., Hirota, K., Kagoshima, H., Yodoi, J., & Shigesada, K. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.23.14497 · Cited by 141 · see citing works
Mukherjee, K., & Bürglin, T. R. (2007) · Journal of Molecular Evolution · doi:10.1007/s00239-006-0023-0 · Cited by 141 · see citing works
Liu, Y., Steenkamp, E. T., Brinkmann, H., Forget, L., Philippe, H., & Lang, B. F. (2009) · BMC Evolutionary Biology · doi:10.1186/1471-2148-9-272 · Cited by 140 · see citing works
Self-citationEarly evolution of metazoan transcription factors
Degnan, B. M., Vervoort, M., Larroux, C., & Richards, G. S. (2009) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2009.09.008 · Cited by 137 · see citing works
Self-citationDeppmann, C. D., Alvania, R. S., & Taparowsky, E. J. (2006) · Molecular Biology and Evolution · doi:10.1093/molbev/msl022 · Cited by 131 · see citing works
SnapShot: Forkhead Transcription Factors II
Tuteja, G., & Kaestner, K. H. (2007) · Cell · doi:10.1016/j.cell.2007.09.016 · Cited by 120 · see citing works
Mechanisms of regulatory diversity within the p53 transcriptional network
Espinosa, J. M. (2008) · Oncogene · doi:10.1038/onc.2008.37 · Cited by 114 · see citing works
Homeodomain proteins belong to the ancestral molecular toolkit of eukaryotes
Derelle, R., Lopez, P., Guyader, H. L., & Manuel, M. (2007) · Evolution & Development · doi:10.1111/j.1525-142x.2007.00153.x · Cited by 109 · see citing works
Evolution of the MAGUK protein gene family in premetazoan lineages
de Mendoza, A., Suga, H., & Ruiz‐Trillo, I. (2010) · BMC Evolutionary Biology · doi:10.1186/1471-2148-10-93 · Cited by 100 · see citing works
Self-citationRennert, J. L., Coffman, J. A., Mushegian, A. R., et al. (2003) · BMC Evolutionary Biology · doi:10.1186/1471-2148-3-4 · Cited by 96 · see citing works
Evolutionary position of breviate amoebae and the primary eukaryote divergence
Minge, M. A., Silberman, J. D., Orr, R. J. S., Cavalier‐Smith, T., Shalchian‐Tabrizi, K., Burki, F., Skjæveland, Å., & Jakobsen, K. S. (2008) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2008.1358 · Cited by 91 · see citing works
Tissue-Specific Splicing and Functions of the Drosophila Transcription Factor Grainyhead
Uv, A., Harrison, E. J., & Bray, S. J. (1997) · Molecular and Cellular Biology · doi:10.1128/mcb.17.11.6727 · Cited by 87 · see citing works
Capsaspora owczarzaki is an independent opisthokont lineage
Ruiz‐Trillo, I., Inagaki, Y., Davis, L. A., Sperstad, S. V., Landfald, B., & Roger, A. J. (2004) · Current Biology · doi:10.1016/j.cub.2004.10.037 · Cited by 86 · see citing works
Self-citationFraser, J. A., & Heitman, J. (2003) · Current Biology · doi:10.1016/j.cub.2003.09.046 · Cited by 84 · see citing works
Giebler, H. A., Lemasson, I., & Nyborg, J. K. (2000) · Molecular and Cellular Biology · doi:10.1128/mcb.20.13.4849-4858.2000 · Cited by 82 · see citing works
Evolutionary genomics of the Fox genes: Origin of gene families and the ancestry of gene clusters
Shimeld, S. M., Degnan, B. M., & Luke, G. N. (2009) · Genomics · doi:10.1016/j.ygeno.2009.08.002 · Cited by 81 · see citing works
Self-citationMechanisms of transcriptional regulation by Runt domain proteins
Wheeler, J. C., Shigesada, K., Gergen, J. P., & Ito, Y. (2000) · Seminars in Cell and Developmental Biology · doi:10.1006/scdb.2000.0184 · Cited by 81 · see citing works
Bromberg, J. (2002) · Journal of Clinical Investigation · doi:10.1172/jci200215617 · Cited by 81 · see citing works
The p53 response: Emerging levels of co-factor complexity
Coutts, A. S., & La Thangue, N. B. (2005) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2005.03.150 · Cited by 72 · see citing works
Katoh, T., Nakaya, D., Tamura, K., & Aotsuka, T. (2007) · ZOOLOGICAL SCIENCE · doi:10.2108/zsj.24.913 · Cited by 69 · see citing works
Early diversification and complex evolutionary history of the p53 tumor suppressor gene family
Nedelcu, A. M., & Tan, C. A. (2007) · Development Genes and Evolution · doi:10.1007/s00427-007-0185-9 · Cited by 63 · see citing works
Lineage-specific and ubiquitous biological roles of the mammalian transcription factor LSF
Veljkovic, J., & Hansen, U. M. (2004) · Gene · doi:10.1016/j.gene.2004.08.010 · Cited by 62 · see citing works
Gauthier, M., & Degnan, B. M. (2008) · Development Genes and Evolution · doi:10.1007/s00427-007-0197-5 · Cited by 61 · see citing works
Self-citationAdell, T., Grebenjuk, V. A., Wiens, M., & M�ller, W. E. G. (2003) · Development Genes and Evolution · doi:10.1007/s00427-003-0345-5 · Cited by 61 · see citing works
Bielen, H., Oberleitner, S., Marcellini, S., Gee, L., Lemaire, P., Bode, H. R., Rupp, R., & Technau, U. (2007) · Development · doi:10.1242/dev.010173 · Cited by 61 · see citing works
Makita, N., Suzuki, M., Asami, S., Takahata, R., Kohzaki, D., Kobayashi, S., Hakamazuka, T., & Hozumi, N. (2008) · Gene · doi:10.1016/j.gene.2007.12.025 · Cited by 60 · see citing works
Marcellini, S., Technau, U., Smith, J. C., & Lemaire, P. (2003) · Developmental Biology · doi:10.1016/s0012-1606(03)00244-6 · Cited by 60 · see citing works
Manna, P. R., Dyson, M. T., & Stocco, D. M. (2008) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2008.12.009 · Cited by 56 · see citing works
Shirra, M., & Hansen, U. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.30.19260 · Cited by 53 · see citing works
Sullivan, J. C., Sher, D., Eisenstein, M., Shigesada, K., Reitzel, A. M., Marlow, H. Q., Levanon, D., Groner, Y., Finnerty, J. R., & Gat, U. (2008) · BMC Evolutionary Biology · doi:10.1186/1471-2148-8-228 · Cited by 52 · see citing works
Traylor‐Knowles, N., Hansen, U. M., DuBuc, T. Q., et al. (2010) · BMC Evolutionary Biology · doi:10.1186/1471-2148-10-101 · Cited by 48 · see citing works
The longevity assurance homologue of yeast lag1 (Lass) gene family (Review)
Teufel (1998) · International Journal of Molecular Medicine · doi:10.3892/ijmm_00000110 · Cited by 42 · see citing works
The Evolutionary History of Lysine Biosynthesis Pathways Within Eukaryotes
Torruella, G., Suga, H., Riutort, M., Peretó, J. G., & Ruiz‐Trillo, I. (2009) · Journal of Molecular Evolution · doi:10.1007/s00239-009-9266-x · Cited by 38 · see citing works
Self-citationSuga, H., Sasaki, G., Kuma, K.-I., Nishiyori, H., Hirose, N., Su, Z.-H., Iwabe, N., & Miyata, T. (2008) · FEBS Letters · doi:10.1016/j.febslet.2008.02.002 · Cited by 29 · see citing works
A new family of transcription factors
Yamada, Y., Wang, H. Y., Fukuzawa, M., Barton, G. J., & Williams, J. G. (2008) · Development · doi:10.1242/dev.026377 · Cited by 21 · see citing works
Expression pattern of the Brachyury and Tbx2 homologues from the sponge Suberites domuncula
Adell, T., & Müller, W. E. G. (2005) · Biology of the Cell · doi:10.1042/bc20040135 · Cited by 21 · see citing works
Clues to the evolution of complex signaling machinery
Mayer, B. J. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0804669105 · Cited by 19 · see citing works
Dual regulation of a Dictyostelium STAT by cGMP and Ca2+ signalling
Araki, T., van Egmond, W. N., Haastert, P. J. M. V., & Williams, J. G. (2010) · Journal of Cell Science · doi:10.1242/jcs.064436 · Cited by 16 · see citing works
Robertson, A., Larroux, C., Degnan, B. M., & Coffman, J. A. (2009) · BMC Research Notes · doi:10.1186/1756-0500-2-59 · Cited by 16 · see citing works
Self-citationChurchill regulates cell movement and mesoderm specification by repressing Nodal signaling
Londin, E. R., Mentzer, L., & Sirotkin, H. I. (2007) · BMC Developmental Biology · doi:10.1186/1471-213x-7-120 · Cited by 14 · see citing works
Dictyostelium kinase DPYK3 negatively regulates STATc signaling in cell fate decision
Lee, N., Rodriguez, M., Kim, B., & Kim, L. (2008) · Development Growth & Differentiation · doi:10.1111/j.1440-169x.2008.01058.x · Cited by 8 · see citing works
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Erwin, D. H., Laflamme, M., Tweedt, S. M., Sperling, E. A., Pisani, D., & Peterson, K. J. (2011) · Science · doi:10.1126/science.1206375 · Cited by 1,336 · see citing works
Uncertainty in the Timing of Origin of Animals and the Limits of Precision in Molecular Timescales
dos Reis, M., Thawornwattana, Y., Angelis, K., Telford, M. J., Donoghue, P. C. J., & Yang, Z. (2015) · Current Biology · doi:10.1016/j.cub.2015.09.066 · Cited by 471 · see citing works
The Capsaspora genome reveals a complex unicellular prehistory of animals
Suga, H., Chen, Z., de Mendoza, A., Sebé-Pedrós, A., Brown, M. W., Kramer, E., Carr, M., Kerner, P., Vervoort, M., Sánchez-Pons, N., et al. (2013) · Nature Communications · doi:10.1038/ncomms3325 · Cited by 317 · see citing works
Self-citationThe Genomic and Cellular Foundations of Animal Origins
Richter, D. J., & King, N. (2013) · Annual Review of Genetics · doi:10.1146/annurev-genet-111212-133456 · Cited by 196 · see citing works
Torruella, G., Derelle, R., Paps, J., Lang, B. F., Roger, A. J., Shalchian-Tabrizi, K., & Ruiz-Trillo, I. (2012) · Molecular Biology and Evolution · doi:10.1093/molbev/msr185 · Cited by 169 · see citing works
Self-citationEvolution of voltage-gated ion channels at the emergence of Metazoa
Moran, Y., Barzilai, M. G., Liebeskind, B. J., & Zakon, H. H. (2015) · Journal of Experimental Biology · doi:10.1242/jeb.110270 · Cited by 139 · see citing works
Diversity as opportunity: Insights from 600 million years of AHR evolution
Hahn, M. E., Karchner, S. I., & Merson, R. R. (2017) · Current Opinion in Toxicology · doi:10.1016/j.cotox.2017.02.003 · Cited by 134 · see citing works
Gastric pouches and the mucociliary sole: setting the stage for nervous system evolution
Arendt, D., Benito-Gutierrez, E., Brunet, T., & Marlow, H. (2015) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2015.0286 · Cited by 112 · see citing works
Vij, S., Rink, J. C., Ho, H. K., Babu, D., Eitel, M., Narasimhan, V., Tiku, V., Westbrook, J., Schierwater, B., & Roy, S. (2012) · PLoS Genetics · doi:10.1371/journal.pgen.1003019 · Cited by 65 · see citing works
The Origin of Metazoan Multicellularity: A Potential Microbial Black Swan Event
Ruiz-Trillo, I., Kin, K., & Casacuberta, E. (2023) · Annual Review of Microbiology · doi:10.1146/annurev-micro-032421-120023 · Cited by 36 · see citing works
Self-citationFerrier, D. E. K. (2016) · Briefings in Functional Genomics · doi:10.1093/bfgp/elv056 · Cited by 28 · see citing works
Origin of Metazoan Developmental Toolkits and Their Expression in the Fossil Record
Tweedt, S. M., & Erwin, D. H. (2015) · Advances in Marine Genomics · doi:10.1007/978-94-017-9642-2_3 · Cited by 27 · see citing works
- Authors
- Sebe-Pedros, A., de Mendoza, A., Lang, B. F., Degnan, B. M., & Ruiz-Trillo, I.
- Affiliations
- Université de Montréal (CA)
- The University of Queensland (AU)
- Venue
- Molecular Biology and Evolution
- Publisher
- Oxford University Press (OUP)
- Published
- 2010-11-17
- Volume
- 28
- Issue
- 3
- Pages
- 1241-1254
- ISSN
- 0737-4038 (ISSN-L)
- 1537-1719
- PMC
- PMC4342549
- OpenAlex
- W2108650715
- Cited by
- 195
- References
- 97
- Citations by year
- 2026: 5 · 2025: 6 · 2024: 8 · 2023: 7 · 2022: 9 · 2021: 8 · 2020: 6 · 2019: 11 · 2018: 12 · 2017: 16 · 2016: 20 · 2015: 27 · 2014: 12 · 2013: 19 · 2012: 19
- FWCI
- 10.79
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Molecular Biology and Evolution (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Harvard University
- Broad Institute
- Institució Catalana de Recerca i Estudis Avançats
- Ministerio de Ciencia e Innovación (ERC-2007-StG-206883)
- Topics
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Marine Invertebrate Physiology and Ecology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protist diversity and phylogeny
- Keywords
- Capsaspora owczarzaki, transcription factors, metazoan origin, T-box, RUNX, homeodomain, bHLH, transcription factor evolution, gene family expansion, choanoflagellates, transcriptional regulation
- MeSH terms
- Amino Acid Sequence, Animals, DNA-Binding Proteins, Molecular Sequence Data, Phylogeny, Transcription Factors, Evolution, Molecular, Genomics, Choanoflagellata
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