Recycling, clustering, and endocytosis jointly maintain PIN auxin carrier polarity at the plasma membrane

Kleine‐Vehn, Jürgen; Wabnik, Krzysztof; Martinière, Alexandre; Łangowski, Łukasz; Willig, Katrin I.; Naramoto, Satoshi; Leitner, Johannes; Tanaka, Hirokazu; Jakobs, Stefan; Robert, Stéphanie; Luschnig, Christian; Govaerts, W.; Hell, Stefan W.; Runions, John; Friml, Jiřı́

doi:10.1038/msb.2011.72

Cited by 237 publications

(238 citation statements)

References 60 publications

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“…4 C, I, and J and Movie S4) and high-ammonium treatment ( mutant. Indeed, a similar phenomenon was reported previously, showing that PIN protein clustering was linked to reduced dynamics of PIN proteins in the plasma membrane (27). However, the inactive analog of tyrA23, tyrA51 (28), had no effects on the behavior and fluorescence intensity of AMT1;3 ( Fig.…”

Section: Resultssupporting

confidence: 51%

Single-particle analysis reveals shutoff control of the Arabidopsis ammonium transporter AMT1;3 by clustering and internalization

Wang

Zhao

Luo

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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Ammonium is a preferred source of nitrogen for plants but is toxic at high levels. Plant ammonium transporters (AMTs) play an essential role in NH 4 + uptake, but the mechanism by which AMTs are regulated remains unclear. To study how AMTs are regulated in the presence of ammonium, we used variable-angle total internal reflection fluorescence microscopy and fluorescence crosscorrelation spectroscopy for single-particle fluorescence imaging of EGFP-tagged AMT1;3 on the plasma membrane of Arabidopsis root cells at various ammonium levels. We demonstrated that AMT1;3-EGFP dynamically appeared and disappeared on the plasma membrane as moving fluorescent spots in low oligomeric states under N-deprived and N-sufficient conditions. Under external high-ammonium stress, however, AMT1;3-EGFPs were found to amass into clusters, which were then internalized into the cytoplasm. A similar phenomenon also occurred in the glutamine synthetase mutant gln1;2 background. Single-particle analysis of AMT1;3-EGFPs in the clathrin heavy chain 2 mutant (chc2 mutant) and Flotllin1 artificial microRNA (Flot1 amiRNA) backgrounds, together with chemical inhibitor treatments, demonstrated that the endocytosis of AMT1;3 clusters induced by high-ammonium stress could occur mainly through clathrin-mediated endocytic pathways, but the contribution of microdomain-associated endocytic pathway cannot be excluded in the internalization. Our results revealed that the clustering and endocytosis of AMT1;3 provides an effective mechanism by which plant cells can avoid accumulation of toxic levels of ammonium by eliminating active AMT1;3 from the plasma membrane. VA-TIRFM | FCSA mmonium (NH 4 + ) and nitrate (NO 3 − ) are the primary sources of nitrogen (N) for most plants growing in agricultural soils. Ammonium assimilation requires less energy than nitrate assimilation, and, thus, ammonium is absorbed preferentially when plants are N-deficient. However, high concentrations of ammonium can be toxic (1); therefore, ammonia absorption and metabolism must be strictly controlled. Understanding the mechanisms by which plant cells regulate ammonium uptake and translocation is of critical importance for agricultural improvements in N-use efficiency and avoiding ammonium toxicity.Evidence suggests that membrane ammonium transporters (AMTs) act in NH 4 + uptake into plant cells, serving as the major transporters for high-affinity ammonium uptake (2). In Arabidopsis thaliana, the AMT family comprises six isoforms, of which three (AtAMT1;1, AtAMT1;2, and AtAMT1;3) are responsible for about 90% of the total high-affinity N uptake in roots (3). AMT gene expression in Arabidopsis roots is generally repressed by high N and induced by N deficiency (4). In addition to transcriptional mechanisms, regulation of membrane transporter activity is also involved in the plant's responses to changing nutrient supplies (1). Although posttranscriptional regulation of AMT appears to be N-dependent (5), the question of how ammonium regulates AMT transporter activity, particularly t...

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Section: Resultssupporting

confidence: 51%

Single-particle analysis reveals shutoff control of the Arabidopsis ammonium transporter AMT1;3 by clustering and internalization

Wang

Zhao

Luo

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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“…The polar localization of PIN proteins at the apico-basal domain of root cells requires clearance from the PM by endocytosis involving clathrin (37,38), retargeting to and retention at the polar domain (39,40). Similarly, possible tyrosine-based motifs have been involved in the lateral polarity of BOR1, suggesting a role for endocytosis that depends on clathrin in this process (27).…”

Section: Resultsmentioning

confidence: 99%

Polarization of IRON-REGULATED TRANSPORTER 1 (IRT1) to the plant-soil interface plays crucial role in metal homeostasis

Barberon

Dubeaux

Kolb

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

231

246

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In plants, the controlled absorption of soil nutrients by root epidermal cells is critical for growth and development. IRON-REGULATED TRANSPORTER 1 (IRT1) is the main root transporter taking up iron from the soil and is also the main entry route in plants for potentially toxic metals such as manganese, zinc, cobalt, and cadmium. Previous work demonstrated that the IRT1 protein localizes to early endosomes/trans-Golgi network (EE/TGN) and is constitutively endocytosed through a monoubiquitin-and clathrindependent mechanism. Here, we show that the availability of secondary non-iron metal substrates of IRT1 (Zn, Mn, and Co) controls the localization of IRT1 between the outer polar domain of the plasma membrane and EE/TGN in root epidermal cells. We also identify FYVE1, a phosphatidylinositol-3-phosphate-binding protein recruited to late endosomes, as an important regulator of IRT1-dependent metal transport and metal homeostasis in plants. FYVE1 controls IRT1 recycling to the plasma membrane and impacts the polar delivery of this transporter to the outer plasma membrane domain. This work establishes a functional link between the dynamics and the lateral polarity of IRT1 and the transport of its substrates, and identifies a molecular mechanism driving polar localization of a cell surface protein in plants.Arabidopsis | endocytosis | nutrition | radial transport | PI3P

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“…This process has been shown to regulate the abundance and polarity of various transporters, such as CHT1 in human embryonic kidney and neuroblastoma cells 39,[55][56][57][58] , aquaporins 59 and PIN-FORMED (PIN) auxin efflux carriers [60][61][62] in Arabidopsis. Our observation that CHER1 is rapidly endocytosed at forming cell plates suggests that a specific vesicle transport machinery is employed to continuously target CHER1 to the forming sieve plates.…”

Section: Discussionmentioning

confidence: 99%

CHOLINE TRANSPORTER-LIKE1 is required for sieve plate development to mediate long-distance cell-to-cell communication

et al. 2014

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Recycling, clustering, and endocytosis jointly maintain PIN auxin carrier polarity at the plasma membrane

Abstract: A combination of super-resolution microscopy in live cells and computational modeling provides new insights into the dynamic and interwoven mechanism that maintains the polar distribution of an important plant cargo.

Cited by 237 publications

References 60 publications

Single-particle analysis reveals shutoff control of the Arabidopsis ammonium transporter AMT1;3 by clustering and internalization

Single-particle analysis reveals shutoff control of the Arabidopsis ammonium transporter AMT1;3 by clustering and internalization

Polarization of IRON-REGULATED TRANSPORTER 1 (IRT1) to the plant-soil interface plays crucial role in metal homeostasis

CHOLINE TRANSPORTER-LIKE1 is required for sieve plate development to mediate long-distance cell-to-cell communication

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