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Bootstrapping and Pinning down the Root Meristem; the Auxin–PLT–ARR Network Unites Robustness and Sensitivity in Meristem Growth Control

After germination, the meristem of the embryonic plant root becomes activated, expands in size and subsequently stabilizes to support post-embryonic root growth. The plant hormones auxin and cytokinin, together with master transcription factors of the PLETHORA (PLT) family have been shown to form a...

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Autores principales: Rutten, Jacob P., Ten Tusscher, Kirsten H.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8125115/
https://www.ncbi.nlm.nih.gov/pubmed/33946960
http://dx.doi.org/10.3390/ijms22094731
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author Rutten, Jacob P.
Ten Tusscher, Kirsten H.
author_facet Rutten, Jacob P.
Ten Tusscher, Kirsten H.
author_sort Rutten, Jacob P.
collection PubMed
description After germination, the meristem of the embryonic plant root becomes activated, expands in size and subsequently stabilizes to support post-embryonic root growth. The plant hormones auxin and cytokinin, together with master transcription factors of the PLETHORA (PLT) family have been shown to form a regulatory network that governs the patterning of this root meristem. Still, which functional constraints contributed to shaping the dynamics and architecture of this network, has largely remained unanswered. Using a combination of modeling approaches we reveal how the interplay between auxin and PLTs enables meristem activation in response to above-threshold stimulation, while its embedding in a PIN-mediated auxin reflux loop ensures localized PLT transcription and thereby, a finite meristem size. We furthermore demonstrate how this constrained PLT transcriptional domain enables independent control of meristem size and division rates, further supporting a division of labor between auxin and PLT. We subsequently reveal how the weaker auxin antagonism of the earlier active Arabidopsis response regulator 12 (ARR12) may arise from the absence of a DELLA protein interaction domain. Our model indicates that this reduced strength is essential to prevent collapse in the early stages of meristem expansion while at later stages the enhanced strength of Arabidopsis response regulator 1 (ARR1) is required for sufficient meristem size control. Summarizing, our work indicates that functional constraints significantly contribute to shaping the auxin–cytokinin–PLT regulatory network.
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spelling pubmed-81251152021-05-17 Bootstrapping and Pinning down the Root Meristem; the Auxin–PLT–ARR Network Unites Robustness and Sensitivity in Meristem Growth Control Rutten, Jacob P. Ten Tusscher, Kirsten H. Int J Mol Sci Article After germination, the meristem of the embryonic plant root becomes activated, expands in size and subsequently stabilizes to support post-embryonic root growth. The plant hormones auxin and cytokinin, together with master transcription factors of the PLETHORA (PLT) family have been shown to form a regulatory network that governs the patterning of this root meristem. Still, which functional constraints contributed to shaping the dynamics and architecture of this network, has largely remained unanswered. Using a combination of modeling approaches we reveal how the interplay between auxin and PLTs enables meristem activation in response to above-threshold stimulation, while its embedding in a PIN-mediated auxin reflux loop ensures localized PLT transcription and thereby, a finite meristem size. We furthermore demonstrate how this constrained PLT transcriptional domain enables independent control of meristem size and division rates, further supporting a division of labor between auxin and PLT. We subsequently reveal how the weaker auxin antagonism of the earlier active Arabidopsis response regulator 12 (ARR12) may arise from the absence of a DELLA protein interaction domain. Our model indicates that this reduced strength is essential to prevent collapse in the early stages of meristem expansion while at later stages the enhanced strength of Arabidopsis response regulator 1 (ARR1) is required for sufficient meristem size control. Summarizing, our work indicates that functional constraints significantly contribute to shaping the auxin–cytokinin–PLT regulatory network. MDPI 2021-04-29 /pmc/articles/PMC8125115/ /pubmed/33946960 http://dx.doi.org/10.3390/ijms22094731 Text en © 2021 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Rutten, Jacob P.
Ten Tusscher, Kirsten H.
Bootstrapping and Pinning down the Root Meristem; the Auxin–PLT–ARR Network Unites Robustness and Sensitivity in Meristem Growth Control
title Bootstrapping and Pinning down the Root Meristem; the Auxin–PLT–ARR Network Unites Robustness and Sensitivity in Meristem Growth Control
title_full Bootstrapping and Pinning down the Root Meristem; the Auxin–PLT–ARR Network Unites Robustness and Sensitivity in Meristem Growth Control
title_fullStr Bootstrapping and Pinning down the Root Meristem; the Auxin–PLT–ARR Network Unites Robustness and Sensitivity in Meristem Growth Control
title_full_unstemmed Bootstrapping and Pinning down the Root Meristem; the Auxin–PLT–ARR Network Unites Robustness and Sensitivity in Meristem Growth Control
title_short Bootstrapping and Pinning down the Root Meristem; the Auxin–PLT–ARR Network Unites Robustness and Sensitivity in Meristem Growth Control
title_sort bootstrapping and pinning down the root meristem; the auxin–plt–arr network unites robustness and sensitivity in meristem growth control
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8125115/
https://www.ncbi.nlm.nih.gov/pubmed/33946960
http://dx.doi.org/10.3390/ijms22094731
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