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Polar Localization of the NIP5;1 Boric Acid Channel Is Maintained by Endocytosis and Facilitates Boron Transport in Arabidopsis Roots

Sheliang Wang, Akira Yoshinari, Tomoo Shimada, Ikuko Hara-Nishimura, Namiki Mitani-Ueno, Jian Feng Ma, Satoshi Naito, Junpei Takano
Sheliang Wang
aGraduate School of Life and Environmental Sciences, Osaka Prefecture University, Sakai 599-8531, Japan
bGraduate School of Agriculture, Hokkaido University, Sapporo 060-8589, Japan
cResearch Faculty of Agriculture, Hokkaido University, Sapporo 060-8589, Japan
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  • ORCID record for Sheliang Wang
Akira Yoshinari
aGraduate School of Life and Environmental Sciences, Osaka Prefecture University, Sakai 599-8531, Japan
bGraduate School of Agriculture, Hokkaido University, Sapporo 060-8589, Japan
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Tomoo Shimada
dGraduate School of Science, Kyoto University, Kyoto 608-8502, Japan
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Ikuko Hara-Nishimura
dGraduate School of Science, Kyoto University, Kyoto 608-8502, Japan
eFaculty of Science and Engineering, Konan University, Kobe 658-0072, Japan
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Namiki Mitani-Ueno
fInstitute of Plant Science and Resources, Okayama University, Kurashiki 710-0046, Japan
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Jian Feng Ma
fInstitute of Plant Science and Resources, Okayama University, Kurashiki 710-0046, Japan
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Satoshi Naito
cResearch Faculty of Agriculture, Hokkaido University, Sapporo 060-8589, Japan
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  • ORCID record for Satoshi Naito
Junpei Takano
aGraduate School of Life and Environmental Sciences, Osaka Prefecture University, Sakai 599-8531, Japan
cResearch Faculty of Agriculture, Hokkaido University, Sapporo 060-8589, Japan
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  • For correspondence: jtakano@plant.osakafu-u.ac.jp

Published April 2017. DOI: https://doi.org/10.1105/tpc.16.00825

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  • © 2017 American Society of Plant Biologists. All rights reserved.

Abstract

Boron uptake in Arabidopsis thaliana is mediated by nodulin 26-like intrinsic protein 5;1 (NIP5;1), a boric acid channel that is located preferentially on the soil side of the plasma membrane in root cells. However, the mechanism underlying this polar localization is poorly understood. Here, we show that the polar localization of NIP5;1 in epidermal and endodermal root cells is mediated by the phosphorylation of Thr residues in the conserved TPG (ThrProGly) repeat in the N-terminal region of NIP5;1. Although substitutions of Ala for three Thr residues in the TPG repeat did not affect lateral diffusion in the plasma membrane, these substitutions inhibited endocytosis and strongly compromised the polar localization of GFP-NIP5;1. Consistent with this, the polar localization was compromised in µ subunit mutants of the clathrin adaptor AP2. The Thr-to-Ala substitutions did not affect the boron transport activity of GFP-NIP5;1 in Xenopus laevis oocytes but did inhibit the ability to complement boron translocation to shoots and rescue growth defects in nip5;1-1 mutant plants under boron-limited conditions. These results demonstrate that the polar localization of NIP5;1 is maintained by clathrin-mediated endocytosis, is dependent on phosphorylation in the TPG repeat, and is necessary for the efficient transport of boron in roots.

  • Glossary

    PM
    plasma membrane
    UTR
    untranslated region
    BFA
    brefeldin A
    PI
    polarity index
    TMD
    transmembrane domain
    Nt
    N-terminal region
    CHX
    cycloheximide
    FRAP
    fluorescence recovery after photobleaching
    ICP-MS
    inductively coupled plasma-mass spectrometry
    ORF
    open reading frame
    ROI
    region of interest
    IP
    immunoprecipitation
    HRP
    horseradish peroxidase
    • Received November 2, 2016.
    • Revised January 26, 2017.
    • Accepted March 23, 2017.
    • Published March 24, 2017.
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    Polar Localization of the NIP5;1 Boric Acid Channel Is Maintained by Endocytosis and Facilitates Boron Transport in Arabidopsis Roots
    Sheliang Wang, Akira Yoshinari, Tomoo Shimada, Ikuko Hara-Nishimura, Namiki Mitani-Ueno, Jian Feng Ma, Satoshi Naito, Junpei Takano
    The Plant Cell Apr 2017, 29 (4) 824-842; DOI: 10.1105/tpc.16.00825

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    Polar Localization of the NIP5;1 Boric Acid Channel Is Maintained by Endocytosis and Facilitates Boron Transport in Arabidopsis Roots
    Sheliang Wang, Akira Yoshinari, Tomoo Shimada, Ikuko Hara-Nishimura, Namiki Mitani-Ueno, Jian Feng Ma, Satoshi Naito, Junpei Takano
    The Plant Cell Apr 2017, 29 (4) 824-842; DOI: 10.1105/tpc.16.00825
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    The Plant Cell: 29 (4)
    The Plant Cell
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    Apr 2017
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