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PMID: 25670713 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

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.

Plant & cell physiology ·Vol. 56 ·No. 4 ·2015-04-00 ·Pages 620-30

Shimotohno A, Sotta N, Sato T, De Ruvo M, Marée AF, Grieneisen VA, Fujiwara T

Abstract

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.

Keywords
Arabidopsis thaliana Boron LA-ICP-MS Mathematical modeling Polar localization Transporter
MeSH Terms
Arabidopsis/metabolism Arabidopsis Proteins/metabolism Biological Transport Boron/metabolism Computer Simulation Diffusion Lasers Meristem/metabolism Models, Biological Reproducibility of Results Solubility Spectrophotometry, Atomic
Chemicals
Arabidopsis Proteins Boron
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Shimotohno Akie
Graduate School of Agricultural and Life Sciences, the University of Tokyo, Yayoi, Bunkyo-ku, Tokyo, 113-8657 Japan These authors contributed equally to this work.
Sotta Naoyuki
Graduate School of Agricultural and Life Sciences, the University of Tokyo, Yayoi, Bunkyo-ku, Tokyo, 113-8657 Japan These authors contributed equally to this work.
Sato Takafumi
Graduate School of Agricultural and Life Sciences, the University of Tokyo, Yayoi, Bunkyo-ku, Tokyo, 113-8657 Japan.
De Ruvo Micol
Laboratory of Functional Genomics and Proteomics of Model Systems, Dipartimento di Genetica e Biologia Molecolare, Sapienza Università di Roma, Via dei Sardi 70, 00185 Rome, Italy Computational and Systems Biology, John Innes Centre, Norwich Research Park, Norwich NR4 7UH, UK.
Marée Athanasius F M
Computational and Systems Biology, John Innes Centre, Norwich Research Park, Norwich NR4 7UH, UK.
Grieneisen Verônica A
Computational and Systems Biology, John Innes Centre, Norwich Research Park, Norwich NR4 7UH, UK These authors contributed equally to this work. veronica.grieneisen@jic.ac.uk atorufu@mail.ecc.u-tokyo.ac.jp.
Fujiwara Toru
Graduate School of Agricultural and Life Sciences, the University of Tokyo, Yayoi, Bunkyo-ku, Tokyo, 113-8657 Japan These authors contributed equally to this work. veronica.grieneisen@jic.ac.uk atorufu@mail.ecc.u-tokyo.ac.jp.
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Article Info
Journal
Plant & cell physiology
Abbr.
Plant Cell Physiol
ISSN
1471-9053
Published
2015-04-00
Epub
2015-00-09
Pages
620-30
Language
English
Region
Japan
NLM ID
9430925
PMCID
PMC4387314
Subset
IM
Grants
Biotechnology and Biological Sciences Research Council · BBS/E/J/000C0645 · United Kingdom
Biotechnology and Biological Sciences Research Council · BBS/E/J/000C0646 · United Kingdom
Biotechnology and Biological Sciences Research Council · BB/J004553/1 · United Kingdom
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