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Mathematical Modeling and Experimental Validation of the Spatial Distribution of Boron in the Root of Arabidopsis thaliana Identify High Boron Accumulation in the Tip and Predict a Distinct Root Tip Uptake Function

Boron, an essential micronutrient, is transported in roots of Arabidopsis thaliana mainly by two different types of transporters, BORs and NIPs (nodulin26-like intrinsic proteins). Both are plasma membrane localized, but have distinct transport properties and patterns of cell type-specific accumulat...

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Autores principales: Shimotohno, Akie, Sotta, Naoyuki, Sato, Takafumi, De Ruvo, Micol, Marée, Athanasius F.M., Grieneisen, Verônica A., Fujiwara, Toru
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4387314/
https://www.ncbi.nlm.nih.gov/pubmed/25670713
http://dx.doi.org/10.1093/pcp/pcv016
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author Shimotohno, Akie
Sotta, Naoyuki
Sato, Takafumi
De Ruvo, Micol
Marée, Athanasius F.M.
Grieneisen, Verônica A.
Fujiwara, Toru
author_facet Shimotohno, Akie
Sotta, Naoyuki
Sato, Takafumi
De Ruvo, Micol
Marée, Athanasius F.M.
Grieneisen, Verônica A.
Fujiwara, Toru
author_sort Shimotohno, Akie
collection PubMed
description Boron, an essential micronutrient, is transported in roots of Arabidopsis thaliana mainly by two different types of transporters, BORs and NIPs (nodulin26-like intrinsic proteins). Both are plasma membrane localized, but have distinct transport properties and patterns of cell type-specific accumulation with different polar localizations, which are likely to affect boron distribution. Here, we used mathematical modeling and an experimental determination to address boron distributions in the root. A computational model of the root is created at the cellular level, describing the boron transporters as observed experimentally. Boron is allowed to diffuse into roots, in cells and cell walls, and to be transported over plasma membranes, reflecting the properties of the different transporters. The model predicts that a region around the quiescent center has a higher concentration of soluble boron than other portions. To evaluate this prediction experimentally, we determined the boron distribution in roots using laser ablation-inductivity coupled plasma-mass spectrometry. The analysis indicated that the boron concentration is highest near the tip and is lower in the more proximal region of the meristem zone, similar to the pattern of soluble boron distribution predicted by the model. Our model also predicts that upward boron flux does not continuously increase from the root tip toward the mature region, indicating that boron taken up in the root tip is not efficiently transported to shoots. This suggests that root tip-absorbed boron is probably used for local root growth, and that instead it is the more mature root regions which have a greater role in transporting boron toward the shoots.
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spelling pubmed-43873142015-04-09 Mathematical Modeling and Experimental Validation of the Spatial Distribution of Boron in the Root of Arabidopsis thaliana Identify High Boron Accumulation in the Tip and Predict a Distinct Root Tip Uptake Function Shimotohno, Akie Sotta, Naoyuki Sato, Takafumi De Ruvo, Micol Marée, Athanasius F.M. Grieneisen, Verônica A. Fujiwara, Toru Plant Cell Physiol Special Focus Issue – Regular Papers Boron, an essential micronutrient, is transported in roots of Arabidopsis thaliana mainly by two different types of transporters, BORs and NIPs (nodulin26-like intrinsic proteins). Both are plasma membrane localized, but have distinct transport properties and patterns of cell type-specific accumulation with different polar localizations, which are likely to affect boron distribution. Here, we used mathematical modeling and an experimental determination to address boron distributions in the root. A computational model of the root is created at the cellular level, describing the boron transporters as observed experimentally. Boron is allowed to diffuse into roots, in cells and cell walls, and to be transported over plasma membranes, reflecting the properties of the different transporters. The model predicts that a region around the quiescent center has a higher concentration of soluble boron than other portions. To evaluate this prediction experimentally, we determined the boron distribution in roots using laser ablation-inductivity coupled plasma-mass spectrometry. The analysis indicated that the boron concentration is highest near the tip and is lower in the more proximal region of the meristem zone, similar to the pattern of soluble boron distribution predicted by the model. Our model also predicts that upward boron flux does not continuously increase from the root tip toward the mature region, indicating that boron taken up in the root tip is not efficiently transported to shoots. This suggests that root tip-absorbed boron is probably used for local root growth, and that instead it is the more mature root regions which have a greater role in transporting boron toward the shoots. Oxford University Press 2015-04 2015-02-09 /pmc/articles/PMC4387314/ /pubmed/25670713 http://dx.doi.org/10.1093/pcp/pcv016 Text en © The Author 2015. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists. 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 Special Focus Issue – Regular Papers
Shimotohno, Akie
Sotta, Naoyuki
Sato, Takafumi
De Ruvo, Micol
Marée, Athanasius F.M.
Grieneisen, Verônica A.
Fujiwara, Toru
Mathematical Modeling and Experimental Validation of the Spatial Distribution of Boron in the Root of Arabidopsis thaliana Identify High Boron Accumulation in the Tip and Predict a Distinct Root Tip Uptake Function
title Mathematical Modeling and Experimental Validation of the Spatial Distribution of Boron in the Root of Arabidopsis thaliana Identify High Boron Accumulation in the Tip and Predict a Distinct Root Tip Uptake Function
title_full Mathematical Modeling and Experimental Validation of the Spatial Distribution of Boron in the Root of Arabidopsis thaliana Identify High Boron Accumulation in the Tip and Predict a Distinct Root Tip Uptake Function
title_fullStr Mathematical Modeling and Experimental Validation of the Spatial Distribution of Boron in the Root of Arabidopsis thaliana Identify High Boron Accumulation in the Tip and Predict a Distinct Root Tip Uptake Function
title_full_unstemmed Mathematical Modeling and Experimental Validation of the Spatial Distribution of Boron in the Root of Arabidopsis thaliana Identify High Boron Accumulation in the Tip and Predict a Distinct Root Tip Uptake Function
title_short Mathematical Modeling and Experimental Validation of the Spatial Distribution of Boron in the Root of Arabidopsis thaliana Identify High Boron Accumulation in the Tip and Predict a Distinct Root Tip Uptake Function
title_sort mathematical modeling and experimental validation of the spatial distribution of boron in the root of arabidopsis thaliana identify high boron accumulation in the tip and predict a distinct root tip uptake function
topic Special Focus Issue – Regular Papers
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4387314/
https://www.ncbi.nlm.nih.gov/pubmed/25670713
http://dx.doi.org/10.1093/pcp/pcv016
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