DOI: 10.1105/tpc.110.081067. <i>Arabidopsis thaliana</i> High-Affinity Phosphate Transporters Exhibit Multiple Levels of Posttranslational Regulation

Arabidopsis thaliana High-Affinity Phosphate Transporters Exhibit Multiple Levels of Posttranslational Regulation

10.1105/tpc.110.081067

Crossref journal-article

Oxford University Press (OUP)

The Plant Cell (286)

Abstract

Abstract In Arabidopsis thaliana, the PHOSPHATE TRANSPORTER1 (PHT1) family encodes the high-affinity phosphate transporters. They are transcriptionally induced by phosphate starvation and require PHOSPHATE TRANSPORTER TRAFFIC FACILITATOR (PHF1) to exit the endoplasmic reticulum (ER), indicating intracellular traffic as an additional level of regulation of PHT1 activity. Our study revealed that PHF1 acts on PHT1, upstream of vesicle coat protein COPII formation, and that additional regulatory events occur during PHT1 trafficking and determine its ER exit and plasma membrane stability. Phosphoproteomic and mutagenesis analyses revealed modulation of PHT1;1 ER export by Ser-514 phosphorylation status. Confocal microscopy analysis of root tip cells showed that PHT1;1 is localized to the plasma membrane and is present in intracellular endocytic compartments. More precisely, PHT1;1 was localized to sorting endosomes associated with prevacuolar compartments. Kinetic analysis of PHT1;1 stability and targeting suggested a modulation of PHT1 internalization from the plasma membrane to the endosomes, followed by either subsequent recycling (in low Pi) or vacuolar degradation (in high Pi). For the latter condition, we identified a rapid mechanism that reduces the pool of PHT1 proteins present at the plasma membrane. This mechanism is regulated by the Pi concentration in the medium and appears to be independent of degradation mechanisms potentially regulated by the PHO2 ubiquitin conjugase. We propose a model for differential trafficking of PHT1 to the plasma membrane or vacuole as a function of phosphate concentration.

Authors 9

Vincent Bayle (first)
Jean-François Arrighi (additional)
Audrey Creff (additional)
Claude Nespoulous (additional)
Jérôme Vialaret (additional)
Michel Rossignol (additional)
Esperanza Gonzalez (additional)
Javier Paz-Ares (additional)
Laurent Nussaume (additional)

References 53 Referenced 208

10.1104/pp.106.078063 / Plant Physiol. / pho2, a phosphate overaccumulator, is caused by a nonsense mutation in a microRNA399 target gene by Aung (2006)
10.1021/jf60127a017 / J. Agric. Food Chem. / Mechanisms for movement of plant nutrients from soil and fertilizer to plant root by Barber (1963)
10.1104/pp.106.079707 / Plant Physiol. / PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants by Bari (2006)
10.1104/pp.108.117358 / Plant Physiol. / Combination of novel GFP mutant TSapphire and DsRed variant mOrange to set up a versatile in planta FRET-FLIM assay by Bayle (2008)
10.1111/j.1365-2818.2006.01706.x / J. Microsc. / A guided tour into subcellular colocalization analysis in light microscopy by Bolte (2006)
10.1105/tpc.001586 / Plant Cell / Membrane protein transport between the endoplasmic reticulum and the Golgi in tobacco leaves is energy dependent but cytoskeleton independent: Evidence from selective photobleaching by Brandizzi (2002)
10.1105/tpc.022673 / Plant Cell / Endoplasmic reticulum export sites and Golgi bodies behave as single mobile secretory units in plant cells by daSilva (2004)
10.1105/tpc.105.037978 / Plant Cell / Vacuolar H+-ATPase activity is required for endocytic and secretory trafficking in Arabidopsis by Dettmer (2006)
10.1105/tpc.105.033910 / Plant Cell / Arabidopsis SENESCENCE-ASSOCIATED GENE101 stabilizes and signals within an ENHANCED DISEASE SUSCEPTIBILITY1 complex in plant innate immunity by Feys (2005)
10.1038/nprot.2008.31 / Nat. Protoc. / Colocalization of fluorescent markers in confocal microscope images of plant cells by French (2008)
10.1016/j.pbi.2009.09.006 / Curr. Opin. Plant Biol. / The intracellular transport of transporters: Membrane trafficking of mineral transporters by Fuji (2009)
10.1016/S0092-8674(03)00003-5 / Cell / The Arabidopsis GNOM ARF-GEF mediates endosomal recycling, auxin transport, and auxin-dependent plant growth by Geldner (2003)
10.1038/35096571 / Nature / Auxin transport inhibitors block PIN1 cycling and vesicle trafficking by Geldner (2001)
10.1242/dev.00926 / Development / Partial loss-of-function alleles reveal a role for GNOM in auxin transport-related, post-embryonic development of Arabidopsis by Geldner (2004)
10.1046/j.1365-313X.2002.01268.x / Plant J / The water permeability of Arabidopsis plasma membrane is regulated by divalent cations and pH by Gerbeau (2002)
10.1105/tpc.105.036640 / Plant Cell / PHOSPHATE TRANSPORTER TRAFFIC FACILITATOR1 is a plant-specific SEC12-related protein that enables the endoplasmic reticulum exit of a high-affinity phosphate transporter in Arabidopsis by González (2005)
10.1016/S0960-9822(03)00538-4 / Curr. Biol. / Arabidopsis sterol endocytosis involves actin-mediated trafficking via ARA6-positive early endosomes by Grebe (2003)
10.1104/pp.106.094110 / Plant Physiol. / De novo formation of plant endoplasmic reticulum export sites is membrane cargo induced and signal mediated by Hanton (2007)
10.1186/1746-4811-2-19 / Plant Methods / A rapid and robust method of identifying transformed Arabidopsis thaliana seedlings following floral dip transformation by Harrison (2006)
10.1016/j.bbrc.2007.08.177 / Biochem. Biophys. Res. Commun. / Novel subsets of the Arabidopsis plasmalemma phosphoproteome identify phosphorylation sites in secondary active transporters by Hem (2007)
10.1016/j.biochi.2006.05.007 / Biochimie / Phosphate deficiency promotes modification of iron distribution in Arabidopsis plants by Hirsch (2006)
10.1111/j.1365-313X.2007.03338.x / Plant J. / Evidence for a sorting endosome in Arabidopsis root cells by Jaillais (2008)
10.1038/nature05046 / Nature / AtSNX1 defines an endosome for auxin-carrier trafficking in Arabidopsis by Jaillais (2006)
10.1016/j.cell.2007.08.040 / Cell / The retromer protein VPS29 links cell polarity and organ initiation in plants by Jaillais (2007)
10.1104/pp.020007 / Plant Physiol. / Regulated expression of Arabidopsis phosphate transporters by Karthikeyan (2002)
10.1073/pnas.0808073105 / Proc. Natl. Acad. Sci. USA / Differential degradation of PIN2 auxin efflux carrier by retromer-dependent vacuolar targeting by Kleine-Vehn (2008)
10.1083/jcb.200408106 / J. Cell Biol. / Specialized membrane-localized chaperones prevent aggregation of polytopic proteins in the ER by Kota (2005)
10.1016/S0014-5793(02)03109-5 / FEBS Lett. / Mutagenic and functional analysis of the C-terminus of Saccharomyces cerevisiae Pho84 phosphate transporter by Lagerstedt (2002)
10.1006/anbo.1993.1102 / Ann. Bot. (Lond.) / Control of net uptake of nutrients by regulation of influx in barley plants recovering from nutrient deficiency by Lee (1993)
10.1038/74531 / Nat. Biotechnol. / Enhanced phosphorus uptake in transgenic tobacco plants that overproduce citrate by López-Bucio (2000)
10.1021/bi9001198 / Biochemistry / Molecular mechanisms controlling phosphate-induced downregulation of the yeast Pho84 phosphate transporter by Lundh (2009)
10.1007/s11103-008-9363-z / Plant Mol. Biol. / Functional characterization of the Arabidopsis thaliana nitrate transporter CHL1 in the yeast Hansenula polymorpha by Martín (2008)
10.1016/j.pbi.2009.09.020 / Curr. Opin. Plant Biol. / How do ER export motifs work on ion channel trafficking? by Mikosch (2009)
10.1104/pp.106.087064 / Plant Physiol. / Diacidic motif is required for efficient transport of the K+ channel KAT1 to the plasma membrane by Mikosch (2006)
10.1007/s11103-004-1965-5 / Plant Mol. Biol. / Transcriptional regulation and functional properties of Arabidopsis Pht1;4, a high affinity transporter contributing greatly to phosphate uptake in phosphate deprived plants by Misson (2004)
10.1073/pnas.0505266102 / Proc. Natl. Acad. Sci. USA / A genome-wide transcriptional analysis using Arabidopsis thaliana Affymetrix gene chips determined plant responses to phosphate deprivation by Misson (2005)
10.1073/pnas.93.19.10519 / Proc. Natl. Acad. Sci. USA / Phosphate transporters from the higher plant Arabidopsis thaliana by Muchhal (1996)
10.1073/pnas.96.10.5868 / Proc. Natl. Acad. Sci. USA / Transcriptional regulation of plant phosphate transporters by Muchhal (1999)
10.1046/j.1365-313X.2002.01356.x / Plant J. / Expression analysis suggests novel roles for members of the Pht1 family of phosphate transporters in Arabidopsis by Mudge (2002)
10.1263/jbb.104.34 / J. Biosci. Bioeng. / Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation by Nakagawa (2007)
10.1105/tpc.107.051896 / Plant Cell / Interaction between SGT1 and cytosolic/nuclear HSC70 chaperones regulates Arabidopsis immune responses by Noël (2007)
10.1105/tpc.104.023150 / Plant Cell / Phosphoproteomics of the Arabidopsis plasma membrane and a new phosphorylation site database by Nühse (2004)
10.1007/s00294-003-0400-9 / Curr. Genet. / Regulation of phosphate acquisition in Saccharomyces cerevisiae by Persson (2003)
10.1074/mcp.M700566-MCP200 / Mol. Cell. Proteomics / Multiple phosphorylations in the C-terminal tail of plant plasma membrane aquaporins: Role in subcellular trafficking of AtPIP2;1 in response to salt stress by Prak (2008)
10.1146/annurev.arplant.50.1.665 / Annu. Rev. Plant Physiol. Plant Mol. Biol. / Phosphate acquisition by Raghothama (1999)
10.1111/j.1600-0854.2009.01026.x / Traffic / New insights into the structural mechanisms of the COPII coat by Russell (2010)
10.1111/j.1365-313X.2004.02161.x / Plant J. / Phosphate transport in Arabidopsis: Pht1;1 and Pht1;4 play a major role in phosphate acquisition from both low- and high-phosphate environments by Shin (2004)
10.1046/j.1365-313X.1997.11010083.x / Plant J. / The cloning of two Arabidopsis genes belonging to a phosphate transporter family by Smith (1997)
10.1073/pnas.0502060102 / Proc. Natl. Acad. Sci. USA / Endocytosis and degradation of BOR1, a boron transporter of Arabidopsis thaliana, regulated by boron availability by Takano (2005)
10.1046/j.1365-313X.2003.01822.x / Plant J. / Why green fluorescent fusion proteins have not been observed in the vacuoles of higher plants by Tamura (2003)
10.1111/j.1365-313X.2010.04375.x / Plant J. / Dissection of local and systemic transcriptional responses to phosphate starvation in Arabidopsis by Thibaud (2010)
10.1074/mcp.T500041-MCP200 / Mol. Cell. Proteomics / Comprehensive identification of phosphorylation sites in postsynaptic density preparations by Trinidad (2006)
10.1038/nmeth.1322 / Nat. Methods / Universal sample preparation method for proteome analysis by Wiśniewski (2009)

Dates

Type	When
Created	14 years, 3 months ago (April 26, 2011, 9:54 p.m.)
Deposited	4 years, 4 months ago (April 6, 2021, 9:24 p.m.)
Indexed	2 weeks ago (Aug. 7, 2025, 4:26 p.m.)
Issued	14 years, 4 months ago (April 1, 2011)
Published	14 years, 4 months ago (April 1, 2011)
Published Online	14 years, 4 months ago (April 1, 2011)
Published Print	14 years, 4 months ago (April 1, 2011)

Funders 0

None

BibTeX

@article{Bayle_2011, title={Arabidopsis thaliana High-Affinity Phosphate Transporters Exhibit Multiple Levels of Posttranslational Regulation }, volume={23}, ISSN={1040-4651}, url={http://dx.doi.org/10.1105/tpc.110.081067}, DOI={10.1105/tpc.110.081067}, number={4}, journal={The Plant Cell}, publisher={Oxford University Press (OUP)}, author={Bayle, Vincent and Arrighi, Jean-François and Creff, Audrey and Nespoulous, Claude and Vialaret, Jérôme and Rossignol, Michel and Gonzalez, Esperanza and Paz-Ares, Javier and Nussaume, Laurent}, year={2011}, month=apr, pages={1523–1535} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        8,
        7
      ]
    ],
    "date-time": "2025-08-07T20:26:19Z",
    "timestamp": 1754598379290
  },
  "reference-count": 53,
  "publisher": "Oxford University Press (OUP)",
  "issue": "4",
  "license": [
    {
      "start": {
        "date-parts": [
          [
            2011,
            4,
            1
          ]
        ],
        "date-time": "2011-04-01T00:00:00Z",
        "timestamp": 1301616000000
      },
      "content-version": "vor",
      "delay-in-days": 0,
      "URL": "https://academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model"
    }
  ],
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        2011,
        4,
        1
      ]
    ]
  },
  "abstract": "<jats:title>Abstract</jats:title>\n               <jats:p>In Arabidopsis thaliana, the PHOSPHATE TRANSPORTER1 (PHT1) family encodes the high-affinity phosphate transporters. They are transcriptionally induced by phosphate starvation and require PHOSPHATE TRANSPORTER TRAFFIC FACILITATOR (PHF1) to exit the endoplasmic reticulum (ER), indicating intracellular traffic as an additional level of regulation of PHT1 activity. Our study revealed that PHF1 acts on PHT1, upstream of vesicle coat protein COPII formation, and that additional regulatory events occur during PHT1 trafficking and determine its ER exit and plasma membrane stability. Phosphoproteomic and mutagenesis analyses revealed modulation of PHT1;1 ER export by Ser-514 phosphorylation status. Confocal microscopy analysis of root tip cells showed that PHT1;1 is localized to the plasma membrane and is present in intracellular endocytic compartments. More precisely, PHT1;1 was localized to sorting endosomes associated with prevacuolar compartments. Kinetic analysis of PHT1;1 stability and targeting suggested a modulation of PHT1 internalization from the plasma membrane to the endosomes, followed by either subsequent recycling (in low Pi) or vacuolar degradation (in high Pi). For the latter condition, we identified a rapid mechanism that reduces the pool of PHT1 proteins present at the plasma membrane. This mechanism is regulated by the Pi concentration in the medium and appears to be independent of degradation mechanisms potentially regulated by the PHO2 ubiquitin conjugase. We propose a model for differential trafficking of PHT1 to the plasma membrane or vacuole as a function of phosphate concentration.</jats:p>",
  "DOI": "10.1105/tpc.110.081067",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2011,
        4,
        27
      ]
    ],
    "date-time": "2011-04-27T01:54:00Z",
    "timestamp": 1303869240000
  },
  "page": "1523-1535",
  "source": "Crossref",
  "is-referenced-by-count": 208,
  "title": "<i>Arabidopsis thaliana</i> High-Affinity Phosphate Transporters Exhibit Multiple Levels of Posttranslational Regulation\n\u00a0",
  "prefix": "10.1093",
  "volume": "23",
  "author": [
    {
      "given": "Vincent",
      "family": "Bayle",
      "sequence": "first",
      "affiliation": [
        {
          "name": "Commissariat \u00e0 l\u2019Energie Atomique Cadarache, Institut de Biologie Environnementale et Biotechnologie-Service de Biologie V\u00e9g\u00e9tale et de Microbiologie Environnementales, Laboratoire de Biologie du D\u00e9veloppement des Plantes, Unit\u00e9 Mixte de Recherche 6191 Centre National de la Recherche Scientifique\u2013Commissariat \u00e0 l\u2019Energie Atomique, Aix-Marseille II, F-13108 Saint-Paul-lez-Durance Cedex, France"
        }
      ]
    },
    {
      "given": "Jean-Fran\u00e7ois",
      "family": "Arrighi",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Commissariat \u00e0 l\u2019Energie Atomique Cadarache, Institut de Biologie Environnementale et Biotechnologie-Service de Biologie V\u00e9g\u00e9tale et de Microbiologie Environnementales, Laboratoire de Biologie du D\u00e9veloppement des Plantes, Unit\u00e9 Mixte de Recherche 6191 Centre National de la Recherche Scientifique\u2013Commissariat \u00e0 l\u2019Energie Atomique, Aix-Marseille II, F-13108 Saint-Paul-lez-Durance Cedex, France"
        }
      ]
    },
    {
      "given": "Audrey",
      "family": "Creff",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Commissariat \u00e0 l\u2019Energie Atomique Cadarache, Institut de Biologie Environnementale et Biotechnologie-Service de Biologie V\u00e9g\u00e9tale et de Microbiologie Environnementales, Laboratoire de Biologie du D\u00e9veloppement des Plantes, Unit\u00e9 Mixte de Recherche 6191 Centre National de la Recherche Scientifique\u2013Commissariat \u00e0 l\u2019Energie Atomique, Aix-Marseille II, F-13108 Saint-Paul-lez-Durance Cedex, France"
        }
      ]
    },
    {
      "given": "Claude",
      "family": "Nespoulous",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Laboratoire de Prot\u00e9omique Fonctionnelle, Institut National de la Recherche Agronomique UR1199, Place Viala, F-34060 Montpellier Cedex 1, France"
        }
      ]
    },
    {
      "given": "J\u00e9r\u00f4me",
      "family": "Vialaret",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Laboratoire de Prot\u00e9omique Fonctionnelle, Institut National de la Recherche Agronomique UR1199, Place Viala, F-34060 Montpellier Cedex 1, France"
        }
      ]
    },
    {
      "given": "Michel",
      "family": "Rossignol",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Laboratoire de Prot\u00e9omique Fonctionnelle, Institut National de la Recherche Agronomique UR1199, Place Viala, F-34060 Montpellier Cedex 1, France"
        }
      ]
    },
    {
      "given": "Esperanza",
      "family": "Gonzalez",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Centro Nacional de Biotecnologia\u2013Consejo Superior de Investigaciones Cient\u00edficas, Campus de Cantoblanco, Madrid E-28049, Spain"
        }
      ]
    },
    {
      "given": "Javier",
      "family": "Paz-Ares",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Centro Nacional de Biotecnologia\u2013Consejo Superior de Investigaciones Cient\u00edficas, Campus de Cantoblanco, Madrid E-28049, Spain"
        }
      ]
    },
    {
      "given": "Laurent",
      "family": "Nussaume",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Commissariat \u00e0 l\u2019Energie Atomique Cadarache, Institut de Biologie Environnementale et Biotechnologie-Service de Biologie V\u00e9g\u00e9tale et de Microbiologie Environnementales, Laboratoire de Biologie du D\u00e9veloppement des Plantes, Unit\u00e9 Mixte de Recherche 6191 Centre National de la Recherche Scientifique\u2013Commissariat \u00e0 l\u2019Energie Atomique, Aix-Marseille II, F-13108 Saint-Paul-lez-Durance Cedex, France"
        }
      ]
    }
  ],
  "member": "286",
  "published-online": {
    "date-parts": [
      [
        2011,
        4,
        1
      ]
    ]
  },
  "reference": [
    {
      "key": "2021040622122175500_b1",
      "doi-asserted-by": "crossref",
      "first-page": "1000",
      "DOI": "10.1104/pp.106.078063",
      "article-title": "pho2, a phosphate overaccumulator, is caused by a nonsense mutation in a microRNA399 target gene",
      "volume": "141",
      "author": "Aung",
      "year": "2006",
      "journal-title": "Plant Physiol."
    },
    {
      "key": "2021040622122175500_b2",
      "doi-asserted-by": "crossref",
      "first-page": "204",
      "DOI": "10.1021/jf60127a017",
      "article-title": "Mechanisms for movement of plant nutrients from soil and fertilizer to plant root",
      "volume": "11",
      "author": "Barber",
      "year": "1963",
      "journal-title": "J. Agric. Food Chem."
    },
    {
      "key": "2021040622122175500_b3",
      "doi-asserted-by": "crossref",
      "first-page": "988",
      "DOI": "10.1104/pp.106.079707",
      "article-title": "PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants",
      "volume": "141",
      "author": "Bari",
      "year": "2006",
      "journal-title": "Plant Physiol."
    },
    {
      "key": "2021040622122175500_b4",
      "doi-asserted-by": "crossref",
      "first-page": "51",
      "DOI": "10.1104/pp.108.117358",
      "article-title": "Combination of novel GFP mutant TSapphire and DsRed variant mOrange to set up a versatile in planta FRET-FLIM assay",
      "volume": "148",
      "author": "Bayle",
      "year": "2008",
      "journal-title": "Plant Physiol."
    },
    {
      "key": "2021040622122175500_b5",
      "doi-asserted-by": "crossref",
      "first-page": "213",
      "DOI": "10.1111/j.1365-2818.2006.01706.x",
      "article-title": "A guided tour into subcellular colocalization analysis in light microscopy",
      "volume": "224",
      "author": "Bolte",
      "year": "2006",
      "journal-title": "J. Microsc."
    },
    {
      "key": "2021040622122175500_b6",
      "doi-asserted-by": "crossref",
      "first-page": "1293",
      "DOI": "10.1105/tpc.001586",
      "article-title": "Membrane protein transport between the endoplasmic reticulum and the Golgi in tobacco leaves is energy dependent but cytoskeleton independent: Evidence from selective photobleaching",
      "volume": "14",
      "author": "Brandizzi",
      "year": "2002",
      "journal-title": "Plant Cell"
    },
    {
      "key": "2021040622122175500_b7",
      "doi-asserted-by": "crossref",
      "first-page": "1753",
      "DOI": "10.1105/tpc.022673",
      "article-title": "Endoplasmic reticulum export sites and Golgi bodies behave as single mobile secretory units in plant cells",
      "volume": "16",
      "author": "daSilva",
      "year": "2004",
      "journal-title": "Plant Cell"
    },
    {
      "key": "2021040622122175500_b8",
      "doi-asserted-by": "crossref",
      "first-page": "715",
      "DOI": "10.1105/tpc.105.037978",
      "article-title": "Vacuolar H+-ATPase activity is required for endocytic and secretory trafficking in Arabidopsis",
      "volume": "18",
      "author": "Dettmer",
      "year": "2006",
      "journal-title": "Plant Cell"
    },
    {
      "key": "2021040622122175500_b9",
      "doi-asserted-by": "crossref",
      "first-page": "2601",
      "DOI": "10.1105/tpc.105.033910",
      "article-title": "Arabidopsis SENESCENCE-ASSOCIATED GENE101 stabilizes and signals within an ENHANCED DISEASE SUSCEPTIBILITY1 complex in plant innate immunity",
      "volume": "17",
      "author": "Feys",
      "year": "2005",
      "journal-title": "Plant Cell"
    },
    {
      "key": "2021040622122175500_b10",
      "doi-asserted-by": "crossref",
      "first-page": "619",
      "DOI": "10.1038/nprot.2008.31",
      "article-title": "Colocalization of fluorescent markers in confocal microscope images of plant cells",
      "volume": "3",
      "author": "French",
      "year": "2008",
      "journal-title": "Nat. Protoc."
    },
    {
      "key": "2021040622122175500_b11",
      "doi-asserted-by": "crossref",
      "first-page": "699",
      "DOI": "10.1016/j.pbi.2009.09.006",
      "article-title": "The intracellular transport of transporters: Membrane trafficking of mineral transporters",
      "volume": "12",
      "author": "Fuji",
      "year": "2009",
      "journal-title": "Curr. Opin. Plant Biol."
    },
    {
      "key": "2021040622122175500_b12",
      "doi-asserted-by": "crossref",
      "first-page": "219",
      "DOI": "10.1016/S0092-8674(03)00003-5",
      "article-title": "The Arabidopsis GNOM ARF-GEF mediates endosomal recycling, auxin transport, and auxin-dependent plant growth",
      "volume": "112",
      "author": "Geldner",
      "year": "2003",
      "journal-title": "Cell"
    },
    {
      "key": "2021040622122175500_b13",
      "doi-asserted-by": "crossref",
      "first-page": "425",
      "DOI": "10.1038/35096571",
      "article-title": "Auxin transport inhibitors block PIN1 cycling and vesicle trafficking",
      "volume": "413",
      "author": "Geldner",
      "year": "2001",
      "journal-title": "Nature"
    },
    {
      "key": "2021040622122175500_b14",
      "doi-asserted-by": "crossref",
      "first-page": "389",
      "DOI": "10.1242/dev.00926",
      "article-title": "Partial loss-of-function alleles reveal a role for GNOM in auxin transport-related, post-embryonic development of Arabidopsis",
      "volume": "131",
      "author": "Geldner",
      "year": "2004",
      "journal-title": "Development"
    },
    {
      "key": "2021040622122175500_b15",
      "doi-asserted-by": "crossref",
      "first-page": "71",
      "DOI": "10.1046/j.1365-313X.2002.01268.x",
      "article-title": "The water permeability of Arabidopsis plasma membrane is regulated by divalent cations and pH",
      "volume": "30",
      "author": "Gerbeau",
      "year": "2002",
      "journal-title": "Plant J"
    },
    {
      "key": "2021040622122175500_b16",
      "doi-asserted-by": "crossref",
      "first-page": "3500",
      "DOI": "10.1105/tpc.105.036640",
      "article-title": "PHOSPHATE TRANSPORTER TRAFFIC FACILITATOR1 is a plant-specific SEC12-related protein that enables the endoplasmic reticulum exit of a high-affinity phosphate transporter in Arabidopsis",
      "volume": "17",
      "author": "Gonz\u00e1lez",
      "year": "2005",
      "journal-title": "Plant Cell"
    },
    {
      "key": "2021040622122175500_b17",
      "doi-asserted-by": "crossref",
      "first-page": "1378",
      "DOI": "10.1016/S0960-9822(03)00538-4",
      "article-title": "Arabidopsis sterol endocytosis involves actin-mediated trafficking via ARA6-positive early endosomes",
      "volume": "13",
      "author": "Grebe",
      "year": "2003",
      "journal-title": "Curr. Biol."
    },
    {
      "key": "2021040622122175500_b18",
      "doi-asserted-by": "crossref",
      "first-page": "1640",
      "DOI": "10.1104/pp.106.094110",
      "article-title": "De novo formation of plant endoplasmic reticulum export sites is membrane cargo induced and signal mediated",
      "volume": "143",
      "author": "Hanton",
      "year": "2007",
      "journal-title": "Plant Physiol."
    },
    {
      "key": "2021040622122175500_b19",
      "doi-asserted-by": "crossref",
      "first-page": "19",
      "DOI": "10.1186/1746-4811-2-19",
      "article-title": "A rapid and robust method of identifying transformed Arabidopsis thaliana seedlings following floral dip transformation",
      "volume": "2",
      "author": "Harrison",
      "year": "2006",
      "journal-title": "Plant Methods"
    },
    {
      "key": "2021040622122175500_b20",
      "doi-asserted-by": "crossref",
      "first-page": "375",
      "DOI": "10.1016/j.bbrc.2007.08.177",
      "article-title": "Novel subsets of the Arabidopsis plasmalemma phosphoproteome identify phosphorylation sites in secondary active transporters",
      "volume": "363",
      "author": "Hem",
      "year": "2007",
      "journal-title": "Biochem. Biophys. Res. Commun."
    },
    {
      "key": "2021040622122175500_b21",
      "doi-asserted-by": "crossref",
      "first-page": "1767",
      "DOI": "10.1016/j.biochi.2006.05.007",
      "article-title": "Phosphate deficiency promotes modification of iron distribution in Arabidopsis plants",
      "volume": "88",
      "author": "Hirsch",
      "year": "2006",
      "journal-title": "Biochimie"
    },
    {
      "key": "2021040622122175500_b22",
      "doi-asserted-by": "crossref",
      "first-page": "237",
      "DOI": "10.1111/j.1365-313X.2007.03338.x",
      "article-title": "Evidence for a sorting endosome in Arabidopsis root cells",
      "volume": "53",
      "author": "Jaillais",
      "year": "2008",
      "journal-title": "Plant J."
    },
    {
      "key": "2021040622122175500_b23",
      "doi-asserted-by": "crossref",
      "first-page": "106",
      "DOI": "10.1038/nature05046",
      "article-title": "AtSNX1 defines an endosome for auxin-carrier trafficking in Arabidopsis",
      "volume": "443",
      "author": "Jaillais",
      "year": "2006",
      "journal-title": "Nature"
    },
    {
      "key": "2021040622122175500_b24",
      "doi-asserted-by": "crossref",
      "first-page": "1057",
      "DOI": "10.1016/j.cell.2007.08.040",
      "article-title": "The retromer protein VPS29 links cell polarity and organ initiation in plants",
      "volume": "130",
      "author": "Jaillais",
      "year": "2007",
      "journal-title": "Cell"
    },
    {
      "key": "2021040622122175500_b25",
      "doi-asserted-by": "crossref",
      "first-page": "221",
      "DOI": "10.1104/pp.020007",
      "article-title": "Regulated expression of Arabidopsis phosphate transporters",
      "volume": "130",
      "author": "Karthikeyan",
      "year": "2002",
      "journal-title": "Plant Physiol."
    },
    {
      "key": "2021040622122175500_b26",
      "doi-asserted-by": "crossref",
      "first-page": "17812",
      "DOI": "10.1073/pnas.0808073105",
      "article-title": "Differential degradation of PIN2 auxin efflux carrier by retromer-dependent vacuolar targeting",
      "volume": "105",
      "author": "Kleine-Vehn",
      "year": "2008",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "2021040622122175500_b27",
      "doi-asserted-by": "crossref",
      "first-page": "79",
      "DOI": "10.1083/jcb.200408106",
      "article-title": "Specialized membrane-localized chaperones prevent aggregation of polytopic proteins in the ER",
      "volume": "168",
      "author": "Kota",
      "year": "2005",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2021040622122175500_b28",
      "doi-asserted-by": "crossref",
      "first-page": "31",
      "DOI": "10.1016/S0014-5793(02)03109-5",
      "article-title": "Mutagenic and functional analysis of the C-terminus of Saccharomyces cerevisiae Pho84 phosphate transporter",
      "volume": "526",
      "author": "Lagerstedt",
      "year": "2002",
      "journal-title": "FEBS Lett."
    },
    {
      "key": "2021040622122175500_b29",
      "doi-asserted-by": "crossref",
      "first-page": "223",
      "DOI": "10.1006/anbo.1993.1102",
      "article-title": "Control of net uptake of nutrients by regulation of influx in barley plants recovering from nutrient deficiency",
      "volume": "72",
      "author": "Lee",
      "year": "1993",
      "journal-title": "Ann. Bot. (Lond.)"
    },
    {
      "key": "2021040622122175500_b30",
      "doi-asserted-by": "crossref",
      "first-page": "450",
      "DOI": "10.1038/74531",
      "article-title": "Enhanced phosphorus uptake in transgenic tobacco plants that overproduce citrate",
      "volume": "18",
      "author": "L\u00f3pez-Bucio",
      "year": "2000",
      "journal-title": "Nat. Biotechnol."
    },
    {
      "key": "2021040622122175500_b31",
      "doi-asserted-by": "crossref",
      "first-page": "4497",
      "DOI": "10.1021/bi9001198",
      "article-title": "Molecular mechanisms controlling phosphate-induced downregulation of the yeast Pho84 phosphate transporter",
      "volume": "48",
      "author": "Lundh",
      "year": "2009",
      "journal-title": "Biochemistry"
    },
    {
      "key": "2021040622122175500_b32",
      "doi-asserted-by": "crossref",
      "first-page": "215",
      "DOI": "10.1007/s11103-008-9363-z",
      "article-title": "Functional characterization of the Arabidopsis thaliana nitrate transporter CHL1 in the yeast Hansenula polymorpha",
      "volume": "68",
      "author": "Mart\u00edn",
      "year": "2008",
      "journal-title": "Plant Mol. Biol."
    },
    {
      "key": "2021040622122175500_b33",
      "doi-asserted-by": "crossref",
      "first-page": "685",
      "DOI": "10.1016/j.pbi.2009.09.020",
      "article-title": "How do ER export motifs work on ion channel trafficking?",
      "volume": "12",
      "author": "Mikosch",
      "year": "2009",
      "journal-title": "Curr. Opin. Plant Biol."
    },
    {
      "key": "2021040622122175500_b34",
      "doi-asserted-by": "crossref",
      "first-page": "923",
      "DOI": "10.1104/pp.106.087064",
      "article-title": "Diacidic motif is required for efficient transport of the K+ channel KAT1 to the plasma membrane",
      "volume": "142",
      "author": "Mikosch",
      "year": "2006",
      "journal-title": "Plant Physiol."
    },
    {
      "key": "2021040622122175500_b35",
      "doi-asserted-by": "crossref",
      "first-page": "727",
      "DOI": "10.1007/s11103-004-1965-5",
      "article-title": "Transcriptional regulation and functional properties of Arabidopsis Pht1;4, a high affinity transporter contributing greatly to phosphate uptake in phosphate deprived plants",
      "volume": "55",
      "author": "Misson",
      "year": "2004",
      "journal-title": "Plant Mol. Biol."
    },
    {
      "key": "2021040622122175500_b36",
      "doi-asserted-by": "crossref",
      "first-page": "11934",
      "DOI": "10.1073/pnas.0505266102",
      "article-title": "A genome-wide transcriptional analysis using Arabidopsis thaliana Affymetrix gene chips determined plant responses to phosphate deprivation",
      "volume": "102",
      "author": "Misson",
      "year": "2005",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "2021040622122175500_b37",
      "doi-asserted-by": "crossref",
      "first-page": "10519",
      "DOI": "10.1073/pnas.93.19.10519",
      "article-title": "Phosphate transporters from the higher plant Arabidopsis thaliana",
      "volume": "93",
      "author": "Muchhal",
      "year": "1996",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "2021040622122175500_b38",
      "doi-asserted-by": "crossref",
      "first-page": "5868",
      "DOI": "10.1073/pnas.96.10.5868",
      "article-title": "Transcriptional regulation of plant phosphate transporters",
      "volume": "96",
      "author": "Muchhal",
      "year": "1999",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "2021040622122175500_b39",
      "doi-asserted-by": "crossref",
      "first-page": "341",
      "DOI": "10.1046/j.1365-313X.2002.01356.x",
      "article-title": "Expression analysis suggests novel roles for members of the Pht1 family of phosphate transporters in Arabidopsis",
      "volume": "31",
      "author": "Mudge",
      "year": "2002",
      "journal-title": "Plant J."
    },
    {
      "key": "2021040622122175500_b40",
      "doi-asserted-by": "crossref",
      "first-page": "34",
      "DOI": "10.1263/jbb.104.34",
      "article-title": "Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation",
      "volume": "104",
      "author": "Nakagawa",
      "year": "2007",
      "journal-title": "J. Biosci. Bioeng."
    },
    {
      "key": "2021040622122175500_b41",
      "doi-asserted-by": "crossref",
      "first-page": "4061",
      "DOI": "10.1105/tpc.107.051896",
      "article-title": "Interaction between SGT1 and cytosolic/nuclear HSC70 chaperones regulates Arabidopsis immune responses",
      "volume": "19",
      "author": "No\u00ebl",
      "year": "2007",
      "journal-title": "Plant Cell"
    },
    {
      "key": "2021040622122175500_b42",
      "doi-asserted-by": "crossref",
      "first-page": "2394",
      "DOI": "10.1105/tpc.104.023150",
      "article-title": "Phosphoproteomics of the Arabidopsis plasma membrane and a new phosphorylation site database",
      "volume": "16",
      "author": "N\u00fchse",
      "year": "2004",
      "journal-title": "Plant Cell"
    },
    {
      "key": "2021040622122175500_b43",
      "doi-asserted-by": "crossref",
      "first-page": "225",
      "DOI": "10.1007/s00294-003-0400-9",
      "article-title": "Regulation of phosphate acquisition in Saccharomyces cerevisiae",
      "volume": "43",
      "author": "Persson",
      "year": "2003",
      "journal-title": "Curr. Genet."
    },
    {
      "key": "2021040622122175500_b44",
      "doi-asserted-by": "crossref",
      "first-page": "1019",
      "DOI": "10.1074/mcp.M700566-MCP200",
      "article-title": "Multiple phosphorylations in the C-terminal tail of plant plasma membrane aquaporins: Role in subcellular trafficking of AtPIP2;1 in response to salt stress",
      "volume": "7",
      "author": "Prak",
      "year": "2008",
      "journal-title": "Mol. Cell. Proteomics"
    },
    {
      "key": "2021040622122175500_b45",
      "doi-asserted-by": "crossref",
      "first-page": "665",
      "DOI": "10.1146/annurev.arplant.50.1.665",
      "article-title": "Phosphate acquisition",
      "volume": "50",
      "author": "Raghothama",
      "year": "1999",
      "journal-title": "Annu. Rev. Plant Physiol. Plant Mol. Biol."
    },
    {
      "key": "2021040622122175500_b46",
      "doi-asserted-by": "crossref",
      "first-page": "303",
      "DOI": "10.1111/j.1600-0854.2009.01026.x",
      "article-title": "New insights into the structural mechanisms of the COPII coat",
      "volume": "11",
      "author": "Russell",
      "year": "2010",
      "journal-title": "Traffic"
    },
    {
      "key": "2021040622122175500_b47",
      "doi-asserted-by": "crossref",
      "first-page": "629",
      "DOI": "10.1111/j.1365-313X.2004.02161.x",
      "article-title": "Phosphate transport in Arabidopsis: Pht1;1 and Pht1;4 play a major role in phosphate acquisition from both low- and high-phosphate environments",
      "volume": "39",
      "author": "Shin",
      "year": "2004",
      "journal-title": "Plant J."
    },
    {
      "key": "2021040622122175500_b48",
      "doi-asserted-by": "crossref",
      "first-page": "83",
      "DOI": "10.1046/j.1365-313X.1997.11010083.x",
      "article-title": "The cloning of two Arabidopsis genes belonging to a phosphate transporter family",
      "volume": "11",
      "author": "Smith",
      "year": "1997",
      "journal-title": "Plant J."
    },
    {
      "key": "2021040622122175500_b49",
      "doi-asserted-by": "crossref",
      "first-page": "12276",
      "DOI": "10.1073/pnas.0502060102",
      "article-title": "Endocytosis and degradation of BOR1, a boron transporter of Arabidopsis thaliana, regulated by boron availability",
      "volume": "102",
      "author": "Takano",
      "year": "2005",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "2021040622122175500_b50",
      "doi-asserted-by": "crossref",
      "first-page": "545",
      "DOI": "10.1046/j.1365-313X.2003.01822.x",
      "article-title": "Why green fluorescent fusion proteins have not been observed in the vacuoles of higher plants",
      "volume": "35",
      "author": "Tamura",
      "year": "2003",
      "journal-title": "Plant J."
    },
    {
      "key": "2021040622122175500_b51",
      "doi-asserted-by": "crossref",
      "first-page": "775",
      "DOI": "10.1111/j.1365-313X.2010.04375.x",
      "article-title": "Dissection of local and systemic transcriptional responses to phosphate starvation in Arabidopsis",
      "volume": "64",
      "author": "Thibaud",
      "year": "2010",
      "journal-title": "Plant J."
    },
    {
      "key": "2021040622122175500_b52",
      "doi-asserted-by": "crossref",
      "first-page": "914",
      "DOI": "10.1074/mcp.T500041-MCP200",
      "article-title": "Comprehensive identification of phosphorylation sites in postsynaptic density preparations",
      "volume": "5",
      "author": "Trinidad",
      "year": "2006",
      "journal-title": "Mol. Cell. Proteomics"
    },
    {
      "key": "2021040622122175500_b53",
      "doi-asserted-by": "crossref",
      "first-page": "359",
      "DOI": "10.1038/nmeth.1322",
      "article-title": "Universal sample preparation method for proteome analysis",
      "volume": "6",
      "author": "Wi\u015bniewski",
      "year": "2009",
      "journal-title": "Nat. Methods"
    }
  ],
  "container-title": "The Plant Cell",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "http://academic.oup.com/plcell/article-pdf/23/4/1523/36935205/plcell_v23_4_1523.pdf",
      "content-type": "application/pdf",
      "content-version": "vor",
      "intended-application": "syndication"
    },
    {
      "URL": "http://academic.oup.com/plcell/article-pdf/23/4/1523/36935205/plcell_v23_4_1523.pdf",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2021,
        4,
        7
      ]
    ],
    "date-time": "2021-04-07T01:24:08Z",
    "timestamp": 1617758648000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://academic.oup.com/plcell/article/23/4/1523/6097550"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        2011,
        4,
        1
      ]
    ]
  },
  "references-count": 53,
  "journal-issue": {
    "issue": "4",
    "published-online": {
      "date-parts": [
        [
          2011,
          4,
          1
        ]
      ]
    },
    "published-print": {
      "date-parts": [
        [
          2011,
          4,
          1
        ]
      ]
    }
  },
  "URL": "http://dx.doi.org/10.1105/tpc.110.081067",
  "relation": {},
  "ISSN": [
    "1532-298X",
    "1040-4651"
  ],
  "subject": [],
  "published-other": {
    "date-parts": [
      [
        2011,
        4,
        1
      ]
    ]
  },
  "published": {
    "date-parts": [
      [
        2011,
        4,
        1
      ]
    ]
  }
}