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, Jian Feng Ma, Satoshi Naito, Junpei Takano

Research output: Contribution to journalArticle

37 Citations (Scopus)

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 m 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.

Original languageEnglish
Pages (from-to)824-842
Number of pages19
JournalPlant Cell
Volume29
Issue number4
DOIs
Publication statusPublished - Apr 1 2017

Fingerprint

boric acid
Boron
endocytosis
Endocytosis
boron
Arabidopsis
clathrin
Proteins
phosphorylation
plasma membrane
nodulins
Vesicular Transport Adaptor Proteins
mutants
Phosphorylation
Cell Membrane
Xenopus laevis
Clathrin
complement
oocytes
Arabidopsis thaliana

ASJC Scopus subject areas

  • Plant Science
  • Cell Biology

Cite this

Polar localization of the NIP5;1 boric acid channel is maintained by endocytosis and facilitates boron transport in arabidopsis roots. / Wang, Sheliang; Yoshinari, Akira; Shimada, Tomoo; Hara-Nishimura, Ikuko; Mitani, Namiki; Ma, Jian Feng; Naito, Satoshi; Takano, Junpei.

In: Plant Cell, Vol. 29, No. 4, 01.04.2017, p. 824-842.

Research output: Contribution to journalArticle

Wang, Sheliang ; Yoshinari, Akira ; Shimada, Tomoo ; Hara-Nishimura, Ikuko ; Mitani, Namiki ; Ma, Jian Feng ; Naito, Satoshi ; Takano, Junpei. / Polar localization of the NIP5;1 boric acid channel is maintained by endocytosis and facilitates boron transport in arabidopsis roots. In: Plant Cell. 2017 ; Vol. 29, No. 4. pp. 824-842.
@article{e5f52e93bc8041be9f2d618b98b3f2bd,
title = "Polar localization of the NIP5;1 boric acid channel is maintained by endocytosis and facilitates boron transport in arabidopsis roots",
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 m 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.",
author = "Sheliang Wang and Akira Yoshinari and Tomoo Shimada and Ikuko Hara-Nishimura and Namiki Mitani and Ma, {Jian Feng} and Satoshi Naito and Junpei Takano",
year = "2017",
month = "4",
day = "1",
doi = "10.1105/tpc.16.00825",
language = "English",
volume = "29",
pages = "824--842",
journal = "Plant Cell",
issn = "1040-4651",
publisher = "American Society of Plant Biologists",
number = "4",

}

TY - JOUR

T1 - Polar localization of the NIP5;1 boric acid channel is maintained by endocytosis and facilitates boron transport in arabidopsis roots

AU - Wang, Sheliang

AU - Yoshinari, Akira

AU - Shimada, Tomoo

AU - Hara-Nishimura, Ikuko

AU - Mitani, Namiki

AU - Ma, Jian Feng

AU - Naito, Satoshi

AU - Takano, Junpei

PY - 2017/4/1

Y1 - 2017/4/1

N2 - 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 m 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.

AB - 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 m 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.

UR - http://www.scopus.com/inward/record.url?scp=85019042162&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85019042162&partnerID=8YFLogxK

U2 - 10.1105/tpc.16.00825

DO - 10.1105/tpc.16.00825

M3 - Article

C2 - 28341806

AN - SCOPUS:85019042162

VL - 29

SP - 824

EP - 842

JO - Plant Cell

JF - Plant Cell

SN - 1040-4651

IS - 4

ER -