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Expression and regulatory asymmetry of retained Arabidopsis thaliana transcription factor genes derived from whole genome duplication

BACKGROUND: Transcription factors (TFs) play a key role in regulating plant development and response to environmental stimuli. While most genes revert to single copy after whole genome duplication (WGD) event, transcription factors are retained at a significantly higher rate. Little is known about h...

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Autores principales: Panchy, Nicholas L., Azodi, Christina B., Winship, Eamon F., O’Malley, Ronan C., Shiu, Shin-Han
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6416927/
https://www.ncbi.nlm.nih.gov/pubmed/30866803
http://dx.doi.org/10.1186/s12862-019-1398-z
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author Panchy, Nicholas L.
Azodi, Christina B.
Winship, Eamon F.
O’Malley, Ronan C.
Shiu, Shin-Han
author_facet Panchy, Nicholas L.
Azodi, Christina B.
Winship, Eamon F.
O’Malley, Ronan C.
Shiu, Shin-Han
author_sort Panchy, Nicholas L.
collection PubMed
description BACKGROUND: Transcription factors (TFs) play a key role in regulating plant development and response to environmental stimuli. While most genes revert to single copy after whole genome duplication (WGD) event, transcription factors are retained at a significantly higher rate. Little is known about how TF duplicates have diverged in their expression and regulation, the answer to which may contribute to a better understanding of the elevated retention rate among TFs. RESULTS: Here we assessed what features may explain differences in the retention of TF duplicates and other genes using Arabidopsis thaliana as a model. We integrated 34 expression, sequence, and conservation features to build a linear model for predicting the extent of duplicate retention following WGD events among TFs and 19 groups of genes with other functions. We found that TFs was the least well predicted, demonstrating the features of TFs are substantially deviated from duplicate genes in other function groups. Consistent with this, the evolution of TF expression patterns and cis-regulatory cites favors the partitioning of ancestral states among the resulting duplicates: one “ancestral” TF duplicate retains most ancestral expression and cis-regulatory sites, while the “non-ancestral” duplicate is enriched for novel regulatory sites. By modeling the retention of ancestral expression and cis-regulatory states in duplicate pairs using a system of differential equations, we found that TF duplicate pairs in a partitioned state are preferentially maintained. CONCLUSIONS: These TF duplicates with asymmetrically partitioned ancestral states are likely maintained because one copy retains ancestral functions while the other, at least in some cases, acquires novel cis-regulatory sites that may be important for novel, adaptive traits. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12862-019-1398-z) contains supplementary material, which is available to authorized users.
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spelling pubmed-64169272019-03-25 Expression and regulatory asymmetry of retained Arabidopsis thaliana transcription factor genes derived from whole genome duplication Panchy, Nicholas L. Azodi, Christina B. Winship, Eamon F. O’Malley, Ronan C. Shiu, Shin-Han BMC Evol Biol Research Article BACKGROUND: Transcription factors (TFs) play a key role in regulating plant development and response to environmental stimuli. While most genes revert to single copy after whole genome duplication (WGD) event, transcription factors are retained at a significantly higher rate. Little is known about how TF duplicates have diverged in their expression and regulation, the answer to which may contribute to a better understanding of the elevated retention rate among TFs. RESULTS: Here we assessed what features may explain differences in the retention of TF duplicates and other genes using Arabidopsis thaliana as a model. We integrated 34 expression, sequence, and conservation features to build a linear model for predicting the extent of duplicate retention following WGD events among TFs and 19 groups of genes with other functions. We found that TFs was the least well predicted, demonstrating the features of TFs are substantially deviated from duplicate genes in other function groups. Consistent with this, the evolution of TF expression patterns and cis-regulatory cites favors the partitioning of ancestral states among the resulting duplicates: one “ancestral” TF duplicate retains most ancestral expression and cis-regulatory sites, while the “non-ancestral” duplicate is enriched for novel regulatory sites. By modeling the retention of ancestral expression and cis-regulatory states in duplicate pairs using a system of differential equations, we found that TF duplicate pairs in a partitioned state are preferentially maintained. CONCLUSIONS: These TF duplicates with asymmetrically partitioned ancestral states are likely maintained because one copy retains ancestral functions while the other, at least in some cases, acquires novel cis-regulatory sites that may be important for novel, adaptive traits. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12862-019-1398-z) contains supplementary material, which is available to authorized users. BioMed Central 2019-03-13 /pmc/articles/PMC6416927/ /pubmed/30866803 http://dx.doi.org/10.1186/s12862-019-1398-z Text en © The Author(s). 2019 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Panchy, Nicholas L.
Azodi, Christina B.
Winship, Eamon F.
O’Malley, Ronan C.
Shiu, Shin-Han
Expression and regulatory asymmetry of retained Arabidopsis thaliana transcription factor genes derived from whole genome duplication
title Expression and regulatory asymmetry of retained Arabidopsis thaliana transcription factor genes derived from whole genome duplication
title_full Expression and regulatory asymmetry of retained Arabidopsis thaliana transcription factor genes derived from whole genome duplication
title_fullStr Expression and regulatory asymmetry of retained Arabidopsis thaliana transcription factor genes derived from whole genome duplication
title_full_unstemmed Expression and regulatory asymmetry of retained Arabidopsis thaliana transcription factor genes derived from whole genome duplication
title_short Expression and regulatory asymmetry of retained Arabidopsis thaliana transcription factor genes derived from whole genome duplication
title_sort expression and regulatory asymmetry of retained arabidopsis thaliana transcription factor genes derived from whole genome duplication
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6416927/
https://www.ncbi.nlm.nih.gov/pubmed/30866803
http://dx.doi.org/10.1186/s12862-019-1398-z
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