A dynamic genetic-hormonal regulatory network model explains multiple cellular behaviors of the root apical meristem of Arabidopsis thaliana.

The study of the concerted action of hormones and transcription factors is fundamental to understand cell differentiation and pattern formation during organ development. The root apical meristem of Arabidopsis thaliana is a useful model to address this. It has a stem cell niche near its tip conforme...

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Main Authors: Mónica L García-Gómez, Eugenio Azpeitia, Elena R Álvarez-Buylla
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2017-04-01
Series:PLoS Computational Biology
Online Access:http://europepmc.org/articles/PMC5417714?pdf=render
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spelling doaj-62fd64b1632546619c7a0989769b95c82020-11-24T22:04:01ZengPublic Library of Science (PLoS)PLoS Computational Biology1553-734X1553-73582017-04-01134e100548810.1371/journal.pcbi.1005488A dynamic genetic-hormonal regulatory network model explains multiple cellular behaviors of the root apical meristem of Arabidopsis thaliana.Mónica L García-GómezEugenio AzpeitiaElena R Álvarez-BuyllaThe study of the concerted action of hormones and transcription factors is fundamental to understand cell differentiation and pattern formation during organ development. The root apical meristem of Arabidopsis thaliana is a useful model to address this. It has a stem cell niche near its tip conformed of a quiescent organizer and stem or initial cells around it, then a proliferation domain followed by a transition domain, where cells diminish division rate before transiting to the elongation zone; here, cells grow anisotropically prior to their final differentiation towards the plant base. A minimal model of the gene regulatory network that underlies cell-fate specification and patterning at the root stem cell niche was proposed before. In this study, we update and couple such network with both the auxin and cytokinin hormone signaling pathways to address how they collectively give rise to attractors that correspond to the genetic and hormonal activity profiles that are characteristic of different cell types along A. thaliana root apical meristem. We used a Boolean model of the genetic-hormonal regulatory network to integrate known and predicted regulatory interactions into alternative models. Our analyses show that, after adding some putative missing interactions, the model includes the necessary and sufficient components and regulatory interactions to recover attractors characteristic of the root cell types, including the auxin and cytokinin activity profiles that correlate with different cellular behaviors along the root apical meristem. Furthermore, the model predicts the existence of activity configurations that could correspond to the transition domain. The model also provides a possible explanation for apparently paradoxical cellular behaviors in the root meristem. For example, how auxin may induce and at the same time inhibit WOX5 expression. According to the model proposed here the hormonal regulation of WOX5 might depend on the cell type. Our results illustrate how non-linear multi-stable qualitative network models can aid at understanding how transcriptional regulators and hormonal signaling pathways are dynamically coupled and may underlie both the acquisition of cell fate and the emergence of hormonal activity profiles that arise during complex organ development.http://europepmc.org/articles/PMC5417714?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Mónica L García-Gómez
Eugenio Azpeitia
Elena R Álvarez-Buylla
spellingShingle Mónica L García-Gómez
Eugenio Azpeitia
Elena R Álvarez-Buylla
A dynamic genetic-hormonal regulatory network model explains multiple cellular behaviors of the root apical meristem of Arabidopsis thaliana.
PLoS Computational Biology
author_facet Mónica L García-Gómez
Eugenio Azpeitia
Elena R Álvarez-Buylla
author_sort Mónica L García-Gómez
title A dynamic genetic-hormonal regulatory network model explains multiple cellular behaviors of the root apical meristem of Arabidopsis thaliana.
title_short A dynamic genetic-hormonal regulatory network model explains multiple cellular behaviors of the root apical meristem of Arabidopsis thaliana.
title_full A dynamic genetic-hormonal regulatory network model explains multiple cellular behaviors of the root apical meristem of Arabidopsis thaliana.
title_fullStr A dynamic genetic-hormonal regulatory network model explains multiple cellular behaviors of the root apical meristem of Arabidopsis thaliana.
title_full_unstemmed A dynamic genetic-hormonal regulatory network model explains multiple cellular behaviors of the root apical meristem of Arabidopsis thaliana.
title_sort dynamic genetic-hormonal regulatory network model explains multiple cellular behaviors of the root apical meristem of arabidopsis thaliana.
publisher Public Library of Science (PLoS)
series PLoS Computational Biology
issn 1553-734X
1553-7358
publishDate 2017-04-01
description The study of the concerted action of hormones and transcription factors is fundamental to understand cell differentiation and pattern formation during organ development. The root apical meristem of Arabidopsis thaliana is a useful model to address this. It has a stem cell niche near its tip conformed of a quiescent organizer and stem or initial cells around it, then a proliferation domain followed by a transition domain, where cells diminish division rate before transiting to the elongation zone; here, cells grow anisotropically prior to their final differentiation towards the plant base. A minimal model of the gene regulatory network that underlies cell-fate specification and patterning at the root stem cell niche was proposed before. In this study, we update and couple such network with both the auxin and cytokinin hormone signaling pathways to address how they collectively give rise to attractors that correspond to the genetic and hormonal activity profiles that are characteristic of different cell types along A. thaliana root apical meristem. We used a Boolean model of the genetic-hormonal regulatory network to integrate known and predicted regulatory interactions into alternative models. Our analyses show that, after adding some putative missing interactions, the model includes the necessary and sufficient components and regulatory interactions to recover attractors characteristic of the root cell types, including the auxin and cytokinin activity profiles that correlate with different cellular behaviors along the root apical meristem. Furthermore, the model predicts the existence of activity configurations that could correspond to the transition domain. The model also provides a possible explanation for apparently paradoxical cellular behaviors in the root meristem. For example, how auxin may induce and at the same time inhibit WOX5 expression. According to the model proposed here the hormonal regulation of WOX5 might depend on the cell type. Our results illustrate how non-linear multi-stable qualitative network models can aid at understanding how transcriptional regulators and hormonal signaling pathways are dynamically coupled and may underlie both the acquisition of cell fate and the emergence of hormonal activity profiles that arise during complex organ development.
url http://europepmc.org/articles/PMC5417714?pdf=render
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