Student or educator? Sign up with your school email and get 6 months of Pro free.
CoChat
Sign Up
Cited by 240

The DOI matches its Crossref record; 9 of the 9 references it cites were found in a registry or an index.

Transcription factor evolution in eukaryotes and the assembly of the regulatory toolkit in multicellular lineages

Open access
de Mendoza, Alex, Sebé-Pedrós, Arnau, Šestak, Martin Sebastijan, Matejčić, Marija, Torruella, Guifré, Domazet-Lošo, Tomislav, Ruiz-Trillo, Iñaki·2013·Proceedings of the National Academy of Sciences
DOI 10.1073/pnas.1311818110
Open this paper in CoChat — free account

Abstract

Significance: Independent transitions to multicellularity in eukaryotes involved the evolution of complex transcriptional regulation toolkits to control cell differentiation. By using comparative genomics, we show that plants and animals required richer transcriptional machineries compared with other eukaryotic multicellular lineages. We suggest this is due to their orchestrated embryonic development. Moreover, our analysis of transcription factor (TF) expression patterns during the development of animals reveal links between TF evolution, species ontogeny, and the phylotypic stage.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1073/pnas.1311818110

Cites

9 of 9 references verified0 citation errors · 0 not checkable

Statistics

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

Show all 9 references

Research works printed but not linked: 65

  1. Z Wunderlich, LA Mirny, Different gene regulation strategies revealed by analysis of binding motifs. Trends Genet 25, 434–440 (2009). · DOI · Paper page
  2. DS Latchman, Transcription factors: An overview. Int J Biochem Cell Biol 29, 1305–1312 (1997). · DOI · Paper page
  3. DS Latchman Eukaryotic Transcription Factors (Elsevier/Academic Press, 5th Ed, Amsterdam, 2008).
  4. A Papavassiliou Transcription Factors in Eukaryotes (Landes Bioscience, Austin, TX, 1997).
  5. V Charoensawan, D Wilson, SA Teichmann, Genomic repertoires of DNA-binding transcription factors across the tree of life. Nucleic Acids Res 38, 7364–7377 (2010). · DOI
  6. EM Meyerowitz, Plants compared to animals: The broadest comparative study of development. Science 295, 1482–1485 (2002). · DOI · Paper page
  7. T Domazet-Lošo, D Tautz, A phylogenetically based transcriptome age index mirrors ontogenetic divergence patterns. Nature 468, 815–818 (2010). · DOI · Paper page
  8. AT Kalinka, et al., Gene expression divergence recapitulates the developmental hourglass model. Nature 468, 811–814 (2010). · DOI · Paper page
  9. N Irie, S Kuratani, Comparative transcriptome analysis reveals vertebrate phylotypic period during organogenesis. Nat Commun 2, 248 (2011). · DOI · Paper page
  10. M Quint, et al., A transcriptomic hourglass in plant embryogenesis. Nature 490, 98–101 (2012). · DOI
  11. M Levin, T Hashimshony, F Wagner, I Yanai, Developmental milestones punctuate gene expression in the Caenorhabditis embryo. Dev Cell 22, 1101–1108 (2012). · DOI · Paper page
  12. V Charoensawan, D Wilson, SA Teichmann, Lineage-specific expansion of DNA-binding transcription factor families. Trends Genet 26, 388–393 (2010). · DOI
  13. MT Weirauch, TR Hughes A Handbook of Transcription Factors, ed TR Hughes (Springer Netherlands, Dordrecht), pp. 25–73 (2011). · DOI
  14. D Lang, et al., Genome-wide phylogenetic comparative analysis of plant transcriptional regulation: A timeline of loss, gain, expansion, and correlation with complexity. Genome Biol Evol 2, 488–503 (2010). · DOI · Paper page
  15. E Shelest, Transcription factors in fungi. FEMS Microbiol Lett 286, 145–151 (2008). · DOI · Paper page
  16. A Sebé-Pedrós, A de Mendoza, BF Lang, BM Degnan, I Ruiz-Trillo, Unexpected repertoire of metazoan transcription factors in the unicellular holozoan Capsaspora owczarzaki. Mol Biol Evol 28, 1241–1254 (2011). · DOI · Paper page
  17. BM Degnan, M Vervoort, C Larroux, GS Richards, Early evolution of metazoan transcription factors. Curr Opin Genet Dev 19, 591–599 (2009). · DOI
  18. E Rayko, F Maumus, U Maheswari, K Jabbari, C Bowler, Transcription factor families inferred from genome sequences of photosynthetic stramenopiles. New Phytol 188, 52–66 (2010). · DOI
  19. SH Shiu, MC Shih, WH Li, Transcription factor families have much higher expansion rates in plants than in animals. Plant Physiol 139, 18–26 (2005). · DOI · Paper page
  20. TR Bürglin A Handbook of Transcription Factors, ed TR Hughes (Springer, Dordrecht, The Netherlands), pp. 95–122 (2011). · DOI
  21. I Ruiz-Trillo, et al., The origins of multicellularity: A multi-taxon genome initiative. Trends Genet 23, 113–118 (2007). · DOI · Paper page
  22. SL Glockling, WL Marshall, FH Gleason, Phylogenetic interpretations and ecological potentials of the Mesomycetozoea (Ichthyosporea). Fungal Ecol 6, 237–247 (2013). · DOI
  23. J-M Aury, et al., Global trends of whole-genome duplications revealed by the ciliate Paramecium tetraurelia. Nature 444, 171–178 (2006). · DOI · Paper page
  24. W Albertin, P Marullo, Polyploidy in fungi: Evolution after whole-genome duplication. Proc R Soc B Biol Sci 279, 2497–509 (2012). · DOI · Paper page
  25. R De Smet, et al., Convergent gene loss following gene and genome duplications creates single-copy families in flowering plants. Proc Natl Acad Sci USA 110, 2898–2903 (2013). · DOI · Paper page
  26. KS Pick, et al., Improved phylogenomic taxon sampling noticeably affects nonbilaterian relationships. Mol Biol Evol 27, 1983–1987 (2010). · DOI · Paper page
  27. H Philippe, et al., Phylogenomics revives traditional views on deep animal relationships. Curr Biol 19, 706–712 (2009). · DOI · Paper page
  28. A Sebé-Pedrós, Y Zheng, I Ruiz-Trillo, D Pan, Premetazoan origin of the hippo signaling pathway. Cell Rep 1, 13–20 (2012). · DOI
  29. M Clarke, et al., Genome of Acanthamoeba castellanii highlights extensive lateral gene transfer and early evolution of tyrosine kinase signaling. Genome Biol 14, R11 (2013). · DOI · Paper page
  30. DC Price, et al., Cyanophora paradoxa genome elucidates origin of photosynthesis in algae and plants. Science 335, 843–847 (2012). · DOI · Paper page
  31. JM Cock, et al., The Ectocarpus genome and the independent evolution of multicellularity in brown algae. Nature 465, 617–621 (2010). · DOI · Paper page
  32. R Radakovits, et al., Draft genome sequence and genetic transformation of the oleaginous alga Nannochloropis gaditana. Nat Commun 3, 686 (2012). · DOI · Paper page
  33. AF Peters, et al., Life-cycle-generation-specific developmental processes are modified in the immediate upright mutant of the brown alga Ectocarpus siliculosus. Development 135, 1503–1512 (2008). · DOI
  34. SM Coelho, et al., OUROBOROS is a master regulator of the gametophyte to sporophyte life cycle transition in the brown alga Ectocarpus. Proc Natl Acad Sci USA 108, 11518–11523 (2011). · DOI
  35. FY Bouget, F Berger, C Brownlee, Position dependent control of cell fate in the Fucus embryo: Role of intercellular communication. Development 125, 1999–2008 (1998). · DOI
  36. N King, The unicellular ancestry of animal development. Dev Cell 7, 313–325 (2004). · DOI · Paper page
  37. A Rokas, The origins of multicellularity and the early history of the genetic toolkit for animal development. Annu Rev Genet 42, 235–251 (2008). · DOI · Paper page
  38. MN Arbeitman, et al., Gene expression during the life cycle of Drosophila melanogaster. Science 297, 2270–2275 (2002). · DOI · Paper page
  39. D Xiang, et al., Genome-wide analysis reveals gene expression and metabolic network dynamics during embryo development in Arabidopsis. Plant Physiol 156, 346–356 (2011). · DOI
  40. MF Belmonte, et al., Comprehensive developmental profiles of gene activity in regions and subregions of the Arabidopsis seed. Proc Natl Acad Sci USA 110, E435–E444 (2013). · DOI · Paper page
  41. JW Valentine, BH Tiffney, JJ Sepkoski, Evolutionary dynamics of plants and animals: A comparative approach. Palaios 6, 81–88 (1991). · DOI
  42. LM Turner, HE Hoekstra, Causes and consequences of the evolution of reproductive proteins. Int J Dev Biol 52, 769–780 (2008). · DOI
  43. DB Burt, Evolutionary stasis, constraint and other terminology describing evolutionary patterns. Biol J Linn Soc Lond 72, 509–517 (2001). · doi:10.1111/j.1095-8312.2001.tb01334.x
  44. CG Kurland, LJ Collins, D Penny, Genomics and the irreducible nature of eukaryote cells. Science 312, 1011–1014 (2006). · DOI · Paper page
  45. J Collén, et al., Genome structure and metabolic features in the red seaweed Chondrus crispus shed light on evolution of the Archaeplastida. Proc Natl Acad Sci USA 110, 5247–5252 (2013). · DOI · Paper page
  46. MB Lohse, et al., Identification and characterization of a previously undescribed family of sequence-specific DNA-binding domains. Proc Natl Acad Sci USA 110, 7660–7665 (2013). · DOI
  47. MG Grabherr, et al., Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29, 644–652 (2011). · DOI · Paper page
  48. M Punta, et al., The Pfam protein families database. Nucleic Acids Res 40, D290–D301 (2012). · DOI · Paper page
  49. D Wilson, V Charoensawan, SK Kummerfeld, SA Teichmann, DBD—taxonomically broad transcription factor predictions: New content and functionality. Nucleic Acids Res 36, D88–D92 (2008). · DOI · Paper page
  50. T Domazet-Loso, J Brajković, D Tautz, A phylostratigraphy approach to uncover the genomic history of major adaptations in metazoan lineages. Trends Genet 23, 533–539 (2007). · DOI · Paper page
  51. T Domazet-Loso, D Tautz, Phylostratigraphic tracking of cancer genes suggests a link to the emergence of multicellularity in metazoa. BMC Biol 8, 66 (2010). · DOI · Paper page
  52. A-R Carvunis, et al., Proto-genes and de novo gene birth. Nature 487, 370–374 (2012). · DOI · Paper page
  53. P Flicek, et al., Ensembl 2011. Nucleic Acids Res 39, D800–D806 (2011). · DOI · Paper page
  54. SF Altschul, et al., Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res 25, 3389–3402 (1997). · DOI · Paper page
  55. JE Blair, SB Hedges, Molecular phylogeny and divergence times of deuterostome animals. Mol Biol Evol 22, 2275–2284 (2005). · DOI · Paper page
  56. F Delsuc, H Brinkmann, D Chourrout, H Philippe, Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature 439, 965–968 (2006). · DOI · Paper page
  57. F Delsuc, G Tsagkogeorga, N Lartillot, H Philippe, Additional molecular support for the new chordate phylogeny. Genesis 46, 592–604 (2008). · DOI · Paper page
  58. MJ Telford, SJ Bourlat, A Economou, D Papillon, O Rota-Stabelli, The evolution of the Ecdysozoa. Philos Trans R Soc Lond B Biol Sci 363, 1529–1537 (2008). · DOI · Paper page
  59. GE Budd, MJ Telford, The origin and evolution of arthropods. Nature 457, 812–817 (2009). · DOI · Paper page
  60. AM Heimberg, R Cowper-Sal-lari, M Sémon, PC Donoghue, KJ Peterson, microRNAs reveal the interrelationships of hagfish, lampreys, and gnathostomes and the nature of the ancestral vertebrate. Proc Natl Acad Sci USA 107, 19379–19383 (2010). · DOI · Paper page
  61. I Rivals, L Personnaz, L Taing, MC Potier, Enrichment or depletion of a GO category within a class of genes: Which test? Bioinformatics 23, 401–407 (2007). · DOI · Paper page
  62. Y Benjamini, Y Hochberg, Controlling the false discovery rate: A practical and powerful approach to multiple testing. J R Stat Soc B 57, 289–300 (1995). · DOI · Paper page
  63. V Hampl, et al., Phylogenomic analyses support the monophyly of Excavata and resolve relationships among eukaryotic “supergroups”. Proc Natl Acad Sci USA 106, 3859–3864 (2009). · DOI · Paper page
  64. R Derelle, BF Lang, Rooting the eukaryotic tree with mitochondrial and bacterial proteins. Mol Biol Evol 29, 1277–1289 (2012). · DOI
  65. MW Brown, M Kolisko, JD Silberman, AJ Roger, Aggregative multicellularity evolved independently in the eukaryotic supergroup Rhizaria. Curr Biol 22, 1123–1127 (2012). · DOI

Cited by

See all 240

Metadata

Authors
de Mendoza, A., Sebé-Pedrós, A., Šestak, M. S., Matejčić, M., Torruella, G., Domazet-Lošo, T., & Ruiz-Trillo, I.
Venue
Proceedings of the National Academy of Sciences
Publisher
Proceedings of the National Academy of Sciences
Published
2013-11-25
Volume
110
Issue
50
Pages
E4858-66
ISSN
  • 0027-8424 (ISSN-L)
  • 1091-6490
DOI
10.1073/pnas.1311818110
OpenAlex
W1981842195
Cited by
240
References
9
FWCI
5.24
Type
journal article
Language
en
Open access
bronze

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

How to cite

Cite CoChat for the checks on this page, and the paper for its own findings.

This page
CoChat. (2026). Citation check: Transcription factor evolution in eukaryotes and the assembly of the regulatory toolkit in multicellular lineages. https://app.cochat.ai/papers/10.1073/pnas.1311818110
The paper
de Mendoza, A., Sebé-Pedrós, A., Šestak, M. S., Matejčić, M., Torruella, G., Domazet-Lošo, T., & Ruiz-Trillo, I. (2013). Transcription factor evolution in eukaryotes and the assembly of the regulatory toolkit in multicellular lineages. Proceedings of the National Academy of Sciences. https://doi.org/10.1073/pnas.1311818110

Data sources

Bibliographic data: Semantic Scholar, OpenAlex, Crossref.

Contains information from the Semantic Scholar Academic Graph Datasets, made available under the ODC Attribution License (ODC-BY 1.0).

Semantic Scholar’s data is described in: Kinney, R., et al. (2023). The Semantic Scholar Open Data Platform. arXiv:2301.10140.