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Evidence for a Strong Correlation Between Transcription Factor Protein Disorder and Organismic Complexity

Studies of diverse phylogenetic lineages reveal that protein disorder increases in concert with organismic complexity but that differences nevertheless exist among lineages. To gain insight into this phenomenology, we analyzed all of the transcription factor (TF) families for which sequences are kno...

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Autores principales: Yruela, Inmaculada, Oldfield, Christopher J., Niklas, Karl J., Dunker, A. Keith
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5434936/
https://www.ncbi.nlm.nih.gov/pubmed/28430951
http://dx.doi.org/10.1093/gbe/evx073
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author Yruela, Inmaculada
Oldfield, Christopher J.
Niklas, Karl J.
Dunker, A. Keith
author_facet Yruela, Inmaculada
Oldfield, Christopher J.
Niklas, Karl J.
Dunker, A. Keith
author_sort Yruela, Inmaculada
collection PubMed
description Studies of diverse phylogenetic lineages reveal that protein disorder increases in concert with organismic complexity but that differences nevertheless exist among lineages. To gain insight into this phenomenology, we analyzed all of the transcription factor (TF) families for which sequences are known for 17 species spanning bacteria, yeast, algae, land plants, and animals and for which the number of different cell types has been reported in the primary literature. Although the fraction of disordered residues in TF sequences is often moderately or poorly correlated with organismic complexity as gauged by cell-type number (r(2) < 0.5), an unbiased and phylogenetically broad analysis shows that organismic complexity is positively and strongly correlated with the total number of TFs, the number of their spliced variants and their total disordered residues content (r(2) > 0.8). Furthermore, the correlation between the fraction of disordered residues and cell-type number becomes stronger when confined to the TF families participating in cell cycle, cell size, cell division, cell differentiation, or cell proliferation, and other important developmental processes. The data also indicate that evolutionarily simpler organisms allow for the detection of subtle differences in the conserved IDRs of TFs as well as changes in variable IDRs, which can influence the DNA recognition and multifunctionality of TFs through direct or indirect mechanisms. Although strong correlations cannot be taken as evidence for cause-and-effect relationships, we interpret our data to indicate that increasing TF disorder likely was an important factor contributing to the evolution of organismic complexity and not merely a concurrent unrelated effect of increasing organismic complexity.
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spelling pubmed-54349362017-05-22 Evidence for a Strong Correlation Between Transcription Factor Protein Disorder and Organismic Complexity Yruela, Inmaculada Oldfield, Christopher J. Niklas, Karl J. Dunker, A. Keith Genome Biol Evol Research Article Studies of diverse phylogenetic lineages reveal that protein disorder increases in concert with organismic complexity but that differences nevertheless exist among lineages. To gain insight into this phenomenology, we analyzed all of the transcription factor (TF) families for which sequences are known for 17 species spanning bacteria, yeast, algae, land plants, and animals and for which the number of different cell types has been reported in the primary literature. Although the fraction of disordered residues in TF sequences is often moderately or poorly correlated with organismic complexity as gauged by cell-type number (r(2) < 0.5), an unbiased and phylogenetically broad analysis shows that organismic complexity is positively and strongly correlated with the total number of TFs, the number of their spliced variants and their total disordered residues content (r(2) > 0.8). Furthermore, the correlation between the fraction of disordered residues and cell-type number becomes stronger when confined to the TF families participating in cell cycle, cell size, cell division, cell differentiation, or cell proliferation, and other important developmental processes. The data also indicate that evolutionarily simpler organisms allow for the detection of subtle differences in the conserved IDRs of TFs as well as changes in variable IDRs, which can influence the DNA recognition and multifunctionality of TFs through direct or indirect mechanisms. Although strong correlations cannot be taken as evidence for cause-and-effect relationships, we interpret our data to indicate that increasing TF disorder likely was an important factor contributing to the evolution of organismic complexity and not merely a concurrent unrelated effect of increasing organismic complexity. Oxford University Press 2017-05-01 /pmc/articles/PMC5434936/ /pubmed/28430951 http://dx.doi.org/10.1093/gbe/evx073 Text en © The Author 2017. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. http://creativecommons.org/licenses/by-nc/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Research Article
Yruela, Inmaculada
Oldfield, Christopher J.
Niklas, Karl J.
Dunker, A. Keith
Evidence for a Strong Correlation Between Transcription Factor Protein Disorder and Organismic Complexity
title Evidence for a Strong Correlation Between Transcription Factor Protein Disorder and Organismic Complexity
title_full Evidence for a Strong Correlation Between Transcription Factor Protein Disorder and Organismic Complexity
title_fullStr Evidence for a Strong Correlation Between Transcription Factor Protein Disorder and Organismic Complexity
title_full_unstemmed Evidence for a Strong Correlation Between Transcription Factor Protein Disorder and Organismic Complexity
title_short Evidence for a Strong Correlation Between Transcription Factor Protein Disorder and Organismic Complexity
title_sort evidence for a strong correlation between transcription factor protein disorder and organismic complexity
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5434936/
https://www.ncbi.nlm.nih.gov/pubmed/28430951
http://dx.doi.org/10.1093/gbe/evx073
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