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Auxin on the Road Navigated by Cellular PIN Polarity

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Auxin and Its Role in Plant Development

Abstract

The generation of asymmetry, at both cellular and tissue level, is one of the most essential capabilities of all eukaryotic organisms. It mediates basically all multicellular development ranging from embryogenesis and de novo organ formation till responses to various environmental stimuli. In plants, the awe-inspiring number of such processes is regulated by phytohormone auxin and its directional, cell-to-cell transport. The mediators of this transport, PIN auxin transporters, are asymmetrically localized at the plasma membrane, and this polar localization determines the directionality of intercellular auxin flow. Thus, auxin transport contributes crucially to the generation of local auxin gradients or maxima, which instruct given cell to change its developmental program. Here, we introduce and discuss the molecular components and cellular mechanisms regulating the generation and maintenance of cellular PIN polarity, as the general hallmarks of cell polarity in plants.

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References

  • Abas L, Benjamins R, Malenica N, Paciorek T, Wiśniewska J, Moulinier-Anzola JC, Sieberer T, Friml J, Luschnig C (2006) Intracellular trafficking and proteolysis of the Arabidopsis auxin-efflux facilitator PIN2 are involved in root gravitropism. Nat Cell Biol 8:249–256

    CAS  PubMed  Google Scholar 

  • Alberts B, Johnson A, Lewis J, Raff M, Roberts K, Walter P (2007) Molecular biology of the cell, 5th edn. Garland, New York

    Google Scholar 

  • Altschuler SJ, Angenent SB, Wang Y, Wu LF (2008) On the spontaneous emergence of cell polarity. Nature 454:886–889

    CAS  PubMed Central  PubMed  Google Scholar 

  • Arighi CN, Hartnell LM, Aguilar RC, Haft CR, Bonifacino JS (2004) Role of the mammalian retromer in sorting of the cation-independent mannose 6-phosphate receptor. J Cell Biol 165:123–133

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bach L, Michaelson LV, Haslam R, Bellec Y, Gissot L, Marion J, Da Costa M, Boutin JP, Miquel M, Tellier F, Domergue F, Markham JE, Beaudoin F, Napier JA, Faure JD (2008) The plant very long chain hydroxy fatty Acyl-CoA dehydratase PASTICCINO2 is essential and limiting for plant development. Proc Natl Acad Sci U S A 105:14727–14731

    CAS  PubMed Central  PubMed  Google Scholar 

  • Balla J, Kalousek P, Reinöhl V, Friml J, Procházka S (2011) Competitive canalization of PIN-dependent auxin flow from axillary buds controls pea bud outgrowth. Plant J 65:571–577

    CAS  PubMed  Google Scholar 

  • Ballesteros I, Domínguez T, Sauer M, Paredes P, Duprat A, Rojo E, Sanmartín M, Sánchez-Serrano JJ (2013) Specialized functions of the PP2A subfamily II catalytic subunits PP2A-C3 and PP2A-C4 in the distribution of auxin fluxes and development in Arabidopsis. Plant J 73:862–872

    CAS  PubMed  Google Scholar 

  • Baluška F, Samaj J, Menzel D (2003) Polar transport of auxin: carrier-mediated flux across the plasma membrane or neurotransmitter-like secretion? Trends Cell Biol 13:282–285

    PubMed  Google Scholar 

  • Bassham DC, Brandizzi F, Otegui MS, Sanderfoot AA (2008) The secretory system of Arabidopsis. Arabidopsis Book 6:e0116

    PubMed Central  PubMed  Google Scholar 

  • Baster P, Robert S, Kleine-Vehn J, Vanneste S, Kania U, Grunewald W, De Rybel B, Beeckman T, Friml J (2013) SCF(TIR1/AFB)-auxin signaling regulates PIN vacuolar trafficking and auxin fluxes during root gravitropism. EMBO J 32:260–274

    CAS  PubMed Central  PubMed  Google Scholar 

  • Benjamins R, Scheres B (2008) Auxin: the looping star in plant development. Annu Rev Plant Biol 59:443–465

    CAS  PubMed  Google Scholar 

  • Benjamins R, Quint A, Weijers D, Hooykaas P, Offringa R (2001) The PINOID protein kinase regulates organ development in Arabidopsis by enhancing polar auxin transport. Development 128:4057–4067

    CAS  PubMed  Google Scholar 

  • Benjamins R, Ampudia CSG, Hooykaas PJJ, Offringa R (2003) PINOID-mediated signaling involves calcium-binding proteins. Plant Physiol 132:1623–1630

    CAS  PubMed Central  PubMed  Google Scholar 

  • Benková E, Michniewicz M, Sauer M, Teichmann T, Seifertová D, Jürgens G, Friml J (2003) Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115:591–602

    PubMed  Google Scholar 

  • Bennett MJ, Marchant A, Green HG, May ST, Ward SP, Millner PA, Walker AR, Schulz B, Feldmann KA (1996) Arabidopsis AUX1 gene: a permease-like regulator of root gravitropism. Science 273:948–950

    CAS  PubMed  Google Scholar 

  • Berleth T, Sachs T (2001) Plant morphogenesis: long-distance coordination and local patterning. Curr Opin Plant Biol 4:57–62

    CAS  PubMed  Google Scholar 

  • Bishopp A, Help H, El-Showk S, Weijers D, Scheres B, Friml J, Benková E, Mähönen AP, Helariutta Y (2011) A mutually inhibitory interaction between auxin and cytokinin specifies vascular pattern in roots. Curr Biol 21:917–926

    CAS  PubMed  Google Scholar 

  • Blakeslee JJ, Bandyopadhyay A, Lee OR, Mravec J, Titapiwatanakun B, Sauer M, Makam SN, Cheng Y, Bouchard R, Adamec J, Geisler M, Nagashima A, Sakai T, Martinoia E, Friml J, Peer WA, Murphy AS (2007) Interactions among PIN-FORMED and P-glycoprotein auxin transporters in Arabidopsis. Plant Cell 19:131–147

    CAS  PubMed Central  PubMed  Google Scholar 

  • Blatt MR, Thiel G, Trentham DR (1990) Reversible inactivation of K+ channels of Vicia stomatal guard cells following the photolysis of caged inositol 1,4,5-trisphosphate. Nature 346:766–769

    CAS  PubMed  Google Scholar 

  • Blilou I, Xu J, Wildwater M, Willemsen V, Paponov I, Friml J, Heidstra R, Aida M, Palme K, Scheres B (2005) The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433:39–44

    CAS  PubMed  Google Scholar 

  • Bouchard R, Bailly A, Blakeslee JJ, Oehring SC, Vincenzetti V, Lee OR, Paponov I, Palme K, Mancuso S, Murphy AS, Schulz B, Geisler M (2006) Immunophilin-like TWISTED DWARF1 modulates auxin efflux activities of Arabidopsis P-glycoproteins. J Biol Chem 281:30603–30612

    CAS  PubMed  Google Scholar 

  • Boutté Y, Crosnier MT, Carraro N, Traas J, Satiat-Jeunemaitre B (2006) The plasma membrane recycling pathway and cell polarity in plants: studies on PIN proteins. J Cell Sci 119:1255–1265

    PubMed  Google Scholar 

  • Caño-Delgado A, Penfield S, Smith C, Catley M, Bevan M (2003) Reduced cellulose synthesis invokes lignification and defense responses in Arabidopsis thaliana. Plant J 34:351–362

    PubMed  Google Scholar 

  • Carland F, Fujioka S, Nelson T (2010) The sterol methyltransferases SMT1, SMT2, and SMT3 influence Arabidopsis development through nonbrassinosteroid products. Plant Physiol 153:741–756

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chapman EJ, Estelle M (2009) Mechanism of auxin-regulated gene expression in plants. Annu Rev Genet 43:265–285

    CAS  PubMed  Google Scholar 

  • Chen CL, Gajewski KM, Hamaratoglu F, Bossuyt W, Sansores-Garcia L, Tao C, Halder G (2010) The apical-basal cell polarity determinant Crumbs regulates Hippo signaling in Drosophila. Proc Natl Acad Sci U S A 107:15810–15815

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chen X, Irani NG, Friml J (2011) Clathrin-mediated endocytosis: the gateway into plant cells. Curr Opin Plant Biol 14:674–682

    CAS  PubMed  Google Scholar 

  • Chen X, Naramoto S, Robert S, Tejos R, Löfke C, Lin D, Yang Z, Friml J (2012) ABP1 and ROP6 GTPase signaling regulate clathrin-mediated endocytosis in Arabidopsis roots. Curr Biol 22:1326–1332

    CAS  PubMed  Google Scholar 

  • Christensen SK, Dagenais N, Chory J, Weigel D (2000) Regulation of auxin response by the protein kinase PINOID. Cell 100:469–478

    CAS  PubMed  Google Scholar 

  • Christie JM, Yang H, Richter GL, Sullivan S, Thomson CE, Lin J, Titapiwatanakun B, Ennis M, Kaiserli E, Lee OR, Adamec J, Peer WA, Murphy AS (2011) phot1 inhibition of ABCB19 primes lateral auxin fluxes in the shoot apex required for phototropism. PLoS Biol 9(6):e1001076

    CAS  PubMed Central  PubMed  Google Scholar 

  • D’Souza-Schorey C, Chavrier P (2006) ARF proteins: roles in membrane traffic and beyond. Nat Rev Mol Cell Biol 7:347–358

    PubMed  Google Scholar 

  • Dai M, Zhang C, Kania U, Chen F, Xue Q, McCray T, Li G, Qin G, Wakeley M, Terzaghi W, Wan J, Zhao Y, Xu J, Friml J, Deng XW, Wang H (2012) A PP6-type phosphatase holoenzyme directly regulates PIN phosphorylation and auxin efflux in Arabidopsis. Plant Cell 24:2497–2514

    CAS  PubMed Central  PubMed  Google Scholar 

  • Davies PJ (2004) Plant hormones: biosynthesis, signal transduction, action! Kluwer Academic, London

    Google Scholar 

  • Dello Ioio R, Nakamura K, Moubayidin L, Perilli S, Taniguchi M, Morita MT, Aoyama T, Costantino P, Sabatini S (2008) A genetic framework for the control of cell division and differentiation in the root meristem. Science 322:1380–1384

    CAS  PubMed  Google Scholar 

  • Desprez T, Juraniec M, Crowell EF, Jouy H, Pochylova Z, Parcy F, Höfte H, Gonneau M, Vernhettes S (2007) Organization of cellulose synthase complexes involved in primary cell wall synthesis in Arabidopsis thaliana. Proc Natl Acad Sci U S A 104:15572–15577

    CAS  PubMed Central  PubMed  Google Scholar 

  • Dettmer J, Friml J (2011) Cell polarity in plants: when two do the same, it is not the same. Curr Opin Cell Biol 23:686–696

    CAS  PubMed  Google Scholar 

  • Dettmer J, Hong-Hermesdorf A, Stierhof Y-D, Schumacher K (2006) Vacuolar H+-ATPase activity is required for endocytic and secretory trafficking in Arabidopsis. Plant Cell 18:715–730

    CAS  PubMed Central  PubMed  Google Scholar 

  • Dharmasiri N, Estelle M (2004) Auxin signaling and regulated protein degradation. Trends Plant Sci 9:302–308

    CAS  PubMed  Google Scholar 

  • Dharmasiri N, Dharmasiri S, Estelle M (2005a) The F-box protein TIR1 is an auxin receptor. Nature 435:441–445

    CAS  PubMed  Google Scholar 

  • Dharmasiri N, Dharmasiri S, Weijers D, Lechner E, Yamada M, Hobbie L, Ehrismann JS, Jurgens G, Estelle M (2005b) Plant development is regulated by a family of auxin receptor F box proteins. Dev Cell 9:109–119

    CAS  PubMed  Google Scholar 

  • Dhonukshe P, Aniento F, Hwang I, Robinson DG, Mravec J, Stierhof YD, Friml J (2007) Clathrin-mediated constitutive endocytosis of PIN auxin efflux carriers in Arabidopsis. Curr Biol 17:520–527

    CAS  PubMed  Google Scholar 

  • Dhonukshe P, Tanaka H, Goh T, Ebine K, Mähönen AP, Prasad K, Blilou I, Geldner N, Xu J, Uemura T, Chory J, Ueda T, Nakano A, Scheres B, Friml J (2008a) Generation of cell polarity in plants links endocytosis, auxin distribution and cell fate decisions. Nature 456:962–966

    CAS  PubMed Central  PubMed  Google Scholar 

  • Dhonukshe P, Grigoriev I, Fischer R, Tominaga M, Robinson DG, Hasek J, Paciorek T, Petrásek J, Seifertová D, Tejos R, Meisel LA, Zazímalová E, Gadella TW Jr, Stierhof YD, Ueda T, Oiwa K, Akhmanova A, Brock R, Spang A, Friml J (2008b) Auxin transport inhibitors impair vesicle motility and actin cytoskeleton dynamics in diverse eukaryotes. Proc Natl Acad Sci U S A 105:4489–4494

    CAS  PubMed Central  PubMed  Google Scholar 

  • Dhonukshe P, Huang F, Galvan-Ampudia CS, Mähönen AP, Kleine-Vehn J, Xu J, Quint A, Prasad K, Friml J, Scheres B, Offringa R (2010) Plasma membrane-bound AGC3 kinases phosphorylate PIN auxin carriers at TPRXS(N/S) motifs to direct apical PIN recycling. Development 137:3245–3255

    CAS  PubMed  Google Scholar 

  • Dickson RC, Sumanasekera C, Lester RL (2006) Functions and metabolism of sphingolipids in Saccharomyces cerevisiae. Prog Lipid Res 45:447–465

    CAS  PubMed  Google Scholar 

  • Diener AC, Li H, Zhou W, Whoriskey WJ, Nes WD, Fink GR (2000) Sterol methyltransferase 1 controls the level of cholesterol in plants. Plant Cell 12:853–870

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ding Z, Friml J (2010) Auxin regulates distal stem cell differentiation in Arabidopsis roots. Proc Natl Acad Sci U S A 107:12046–12051

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ding Z, Galván-Ampudia CS, Demarsy E, Łangowski Ł, Kleine-Vehn J, Fan Y, Morita MT, Tasaka M, Fankhauser C, Offringa R, Friml J (2011) Light-mediated polarization of the PIN3 auxin transporter for the phototropic response in Arabidopsis. Nat Cell Biol 13:447–452

    CAS  PubMed  Google Scholar 

  • Drdová EJ, Synek L, Pečenková T, Hála M, Kulich I, Fowler JE, Murphy AS, Zárský V (2013) The exocyst complex contributes to PIN auxin efflux carrier recycling and polar auxin transport in Arabidopsis. Plant J 73:709–719

    PubMed  Google Scholar 

  • Du Y, Tejos R, Beck M, Himschoot E, Li H, Robatzek S, Vanneste S, Friml J (2013) Salicylic acid interferes with clathrin-mediated endocytic protein trafficking. Proc Natl Acad Sci U S A 110(19):7946–7951

    CAS  PubMed Central  PubMed  Google Scholar 

  • Dudu V, Pantazis P, Gonzalez-Gaitan M (2004) Membrane traffic during embryonic development: epithelial formation, cell fate decisions and differentiation. Curr Opin Cell Biol 16:407–414

    CAS  PubMed  Google Scholar 

  • Ellis C, Turner JG (2001) The Arabidopsis mutant cev1 has constitutively active jasmonate and ethylene signal pathways and enhanced resistance to pathogens. Plant Cell 13:1025–1033

    CAS  PubMed Central  PubMed  Google Scholar 

  • Feraru E, Paciorek T, Feraru MI, Zwiewka M, De Groodt R, De Rycke R, Kleine-Vehn J, Friml J (2010) The AP-3 B adaptin mediates the biogenesis and function of lytic vacuoles in Arabidopsis. Plant Cell 22:2812–2824

    CAS  PubMed Central  PubMed  Google Scholar 

  • Feraru E, Feraru MI, Kleine-Vehn J, Martinière A, Mouille G, Vanneste S, Vernhettes S, Runions J, Friml J (2011) PIN polarity maintenance by the cell wall in Arabidopsis. Curr Biol 21:338–343

    CAS  PubMed  Google Scholar 

  • Feraru E, Feraru MI, Asaoka R, Paciorek T, De Rycke R, Tanaka H, Nakano A, Friml J (2012) BEX5/RabA1b regulates trans-Golgi network-to-plasma membrane protein trafficking in Arabidopsis. Plant Cell 24:3074–3086

    CAS  PubMed Central  PubMed  Google Scholar 

  • Foti M, Moukil MA, Dudognon P, Carpentier JL (2004) Insulin and IGF-1 receptor trafficking and signaling. Novartis Found Symp 262:125–141

    CAS  PubMed  Google Scholar 

  • Friml J, Palme K (2002) Polar auxin transport – old questions and new concepts? Plant Mol Biol 49:273–284

    CAS  PubMed  Google Scholar 

  • Friml J, Benková E, Blilou I, Wisniewska J, Hamann T, Ljung K, Woody S, Sandberg G, Scheres B, Jürgens G, Palme K (2002a) AtPIN4 mediates sink-driven auxin gradients and root patterning in Arabidopsis. Cell 108:661–673

    CAS  PubMed  Google Scholar 

  • Friml J, Wiśniewska J, Benková E, Mendgen K, Palme K (2002b) Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature 415:806–809

    PubMed  Google Scholar 

  • Friml J, Vieten A, Sauer M, Weijers D, Schwarz H, Hamann T, Offringa R, Jürgens G (2003) Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 426:147–153

    CAS  PubMed  Google Scholar 

  • Friml J, Yang X, Michniewicz M, Weijers D, Quint A, Tietz O, Benjamins R, Ouwerkerk PB, Ljung K, Sandberg G, Hooykaas PJ, Palme K, Offringa R (2004) APINOID-dependent binary switch in apical-basal PIN polar targeting directs auxin efflux. Science 306:862–865

    CAS  PubMed  Google Scholar 

  • Fujimoto M, Arimura S, Ueda T, Takanashi H, Hayashi Y, Nakano A, Tsutsumi N (2010) Arabidopsis dynamin-related proteins DRP2B and DRP1A participate together in clathrin-coated vesicle formation during endocytosis. Proc Natl Acad Sci U S A 107:6094–6099

    CAS  PubMed Central  PubMed  Google Scholar 

  • Furutani M, Kajiwara T, Kato T, Treml BS, Stockum C, Torres-Ruiz RA, Tasaka M (2007) The gene MACCHI-BOU 4/ENHANCER OF PINOID encodes a NPH3-like protein and reveals similarities between organogenesis and phototropism at the molecular level. Development 134:3849–3859

    CAS  PubMed  Google Scholar 

  • Furutani M, Sakamoto N, Yoshida S, Kajiwara T, Robert HS, Friml J, Tasaka M (2011) Polarlocalized NPH3-like proteins regulate polarity and endocytosis of PIN-FORMED auxin efflux carriers. Development 138:2069–2078

    CAS  PubMed  Google Scholar 

  • Gälweiler L, Guan C, Müller A, Wisman E, Mendgen K, Yephremov A, Palme K (1998) Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 282:2226–2230

    PubMed  Google Scholar 

  • Geisler M, Blakeslee JJ, Bouchard R, Lee OR, Vincenzetti V, Bandyopadhyay A, Titapiwatanakun B, Peer WA, Bailly A, Richards EL, Ejendal KF, Smith AP, Baroux C, Grossniklaus U, Müller A, Hrycyna CA, Dudler R, Murphy AS, Martinoia E (2005) Cellular efflux of auxin catalyzed by the Arabidopsis MDR/PGP transporter AtPGP1. Plant J 44:179–194

    CAS  PubMed  Google Scholar 

  • Geldner N (2009) Cell polarity in plants: a PARspective on PINs. Curr Opin Plant Biol 12:42–48

    CAS  PubMed  Google Scholar 

  • Geldner N, Friml J, Stierhof YD, Jürgens G, Palme K (2001) Auxin transport inhibitors block PIN1 cycling and vesicle trafficking. Nature 413:425–428

    CAS  PubMed  Google Scholar 

  • Geldner N, Anders N, Wolters H, Keicher J, Kornberger W, Muller P, Delbarre A, Ueda T, Nakano A, Jürgens G (2003) The Arabidopsis GNOM ARF-GEF mediates endosomal recycling, auxin transport, and auxin-dependent plant growth. Cell 112:219–230

    CAS  PubMed  Google Scholar 

  • Giepmans BN, van Ijzendoorn SC (2009) Epithelial cell-cell junctions and plasma membrane domains. Biochim Biophys Acta 1788:820–831

    CAS  PubMed  Google Scholar 

  • Gilroy S, Read ND, Trewavas AJ (1990) Elevation of cytoplasmic calcium by caged calcium or caged inositol triphosphate initiates stomatal closure. Nature 346:769–771

    CAS  PubMed  Google Scholar 

  • Grebe M, Xu J, Mobius W, Ueda T, Nakano A, Geuze HJ, Rook MB, Scheres B (2003) Arabidopsis sterol endocytosis involves actin-mediated trafficking via ARA6-positive early endosomes. Curr Biol 13:1378–1387

    CAS  PubMed  Google Scholar 

  • Grieneisen VA, Xu J, Marée AF, Hogeweg P, Scheres B (2007) Auxin transport is sufficient to generate a maximum and gradient guiding root growth. Nature 449:1008–1013

    CAS  PubMed  Google Scholar 

  • Hazak O, Bloch D, Poraty L, Sternberg H, Zhang J, Friml J, Yalovsky S (2010) A rho scaffold integrates the secretory system with feedback mechanisms in regulation of auxin distribution. PLoS Biol 8(1):e1000282

    PubMed Central  PubMed  Google Scholar 

  • Heisler MG, Ohno C, Das P, Sieber P, Reddy GV, Long JA, Meyerowitz EM (2005) Patterns of auxin transport and gene expression during primordium development revealed by live imaging of the Arabidopsis inflorescence meristem. Curr Biol 15:1899–1911

    CAS  PubMed  Google Scholar 

  • Heisler MG, Hamant O, Krupinski P, Uyttewaal M, Ohno C, Jönsson H, Traas J, Meyerowitz EM (2010) Alignment between PIN1 polarity and microtubule orientation in the shoot apical meristem reveals a tight coupling between morphogenesis and auxin transport. PLoS Biol 8(10):e1000516

    PubMed Central  PubMed  Google Scholar 

  • Henrichs S, Wang B, Fukao Y, Zhu J, Charrier L, Bailly A, Oehring SC, Linnert M, Weiwad M, Endler A, Nanni P, Pollmann S, Mancuso S, Schulz A, Geisler M (2012) Regulation of ABCB1/PGP1-catalysed auxin transport by linker phosphorylation. EMBO J 31:2965–2980

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hertel R (1983) The mechanism of auxin transport as a model for auxin action. Z Pflanzenphysiol 112:53–67

    CAS  Google Scholar 

  • Heymann JAW, Hinshaw JE (2009) Dynamins at a glance. J Cell Sci 122:3427–3431

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hoekstra D, Maier O, van der Wouden JM, Slimane TA, van IJzendoorn SC (2003) Membrane dynamics and cell polarity: the role of sphingolipids. J Lipid Res 44:869–877

    CAS  PubMed  Google Scholar 

  • Holler D, Dikic I (2004) Receptor endocytosis via ubiquitin-dependent and -independent pathways. Biochem Pharmacol 67:1013–1017

    CAS  PubMed  Google Scholar 

  • Huang F, Zago MK, Abas L, van Marion A, Galván-Ampudia CS, Offringa R (2010) Phosphorylation of conserved PIN motifs directs Arabidopsis PIN1 polarity and auxin transport. Plant Cell 22:1129–1142

    CAS  PubMed Central  PubMed  Google Scholar 

  • Humbert PO, Dow LE, Russell SM (2006) The Scribble and Par complexes in polarity and migration: friends or foes? Trends Cell Biol 16:622–630

    CAS  PubMed  Google Scholar 

  • Irani NG, Russinova E (2009) Receptor endocytosis and signaling in plants. Curr Opin Plant Biol 12:653–659

    CAS  PubMed  Google Scholar 

  • Jaillais Y, Fobis-Loisy I, Miège C, Rollin C, Gaude T (2006) AtSNX1 defines an endosome for auxin-carrier trafficking in Arabidopsis. Nature 443:106–109

    CAS  PubMed  Google Scholar 

  • Jaillais Y, Santambrogio M, Rozier F, Fobis-Loisy I, Miège C, Gaude T (2007) The retromer protein VPS29 links cell polarity and organ initiation in plants. Cell 130:1057–1070

    CAS  PubMed  Google Scholar 

  • Kepinski S, Leyser O (2005) The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435:446–451

    CAS  PubMed  Google Scholar 

  • Kitakura S, Vanneste S, Robert S, Löfke C, Teichmann T, Tanaka H, Friml J (2011) Clathrin mediates endocytosis and polar distribution of PIN auxin transporters in Arabidopsis. Plant Cell 23:1920–1931

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kleine-Vehn J, Friml J (2008) Polar targeting and endocytic recycling in auxin-dependent plant development. Annu Rev Cell Dev Biol 24:447–473

    CAS  PubMed  Google Scholar 

  • Kleine-Vehn J, Dhonukshe P, Swarup R, Bennett M, Friml J (2006) Subcellular trafficking of the Arabidopsis auxin influx carrier AUX1 uses a novel pathway distinct from PIN1. Plant Cell 18:3171–3181

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kleine-Vehn J, Dhonukshe P, Sauer M, Brewer PB, Wiśniewska J, Paciorek T, Benková E, Friml J (2008a) ARF GEF-dependent transcytosis and polar delivery of PIN auxin carriers in Arabidopsis. Curr Biol 18:526–531

    CAS  PubMed  Google Scholar 

  • Kleine-Vehn J, Łangowski Ł, Wisniewska J, Dhonukshe P, Brewer PB, Friml J (2008b) Cellular and molecular requirements for polar PIN targeting and transcytosis in plants. Mol Plant 1:1056–1066

    CAS  PubMed  Google Scholar 

  • Kleine-Vehn J, Leitner J, Zwiewka M, Sauer M, Abas L, Luschnig C, Friml J (2008c) Differential degradation of PIN2 auxin efflux carrier by retromer-dependent vacuolar targeting. Proc Natl Acad Sci U S A 105:17812–17817

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kleine-Vehn J, Huang F, Naramoto S, Zhang J, Michniewicz M, Offringa R, Friml J (2009) PIN auxin efflux carrier polarity is regulated by PINOID kinase-mediated recruitment into GNOM-independent trafficking in Arabidopsis. Plant Cell 21:3839–3849

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kleine-Vehn J, Ding Z, Jones AR, Tasaka M, Morita MT, Friml J (2010) Gravity-induced PIN transcytosis for polarization of auxin fluxes in gravity-sensing root cells. Proc Natl Acad Sci U S A 107:22344–22349

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kleine-Vehn J, Wabnik K, Martinière A, Łangowski Ł, Willig K, Naramoto S, Leitner J, Tanaka H, Jakobs S, Robert S, Luschnig C, Govaerts W, Hell SW, Runions J, Friml J (2011) Recycling, clustering, and endocytosis jointly maintain PIN auxin carrier polarity at the plasma membrane. Mol Syst Biol 25:540

    Google Scholar 

  • Konopka CA, Backues SK, Bednarek SY (2008) Dynamics of Arabidopsis dynamin-related protein 1C and a clathrin light chain at the plasma membrane. Plant Cell 20:1363–1380

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kramer EM (2004) PIN and AUX/LAX proteins: their role in auxin accumulation. Trends Plant Sci 9:578–582

    CAS  PubMed  Google Scholar 

  • Krinke O, Novotná Z, Valentová O, Martinec J (2007) Inositol trisphosphate receptor in higher plants: is it real? J Exp Bot 58:361–376

    CAS  PubMed  Google Scholar 

  • Kubeš M, Yang H, Richter GL, Cheng Y, Młodzińska E, Wang X, Blakeslee JJ, Carraro N, Petrášek J, Zažímalová E, Hoyerová K, Peer WA, Murphy AS (2012) The Arabidopsis concentration-dependent influx/efflux transporter ABCB4 regulates cellular auxin levels in the root epidermis. Plant J 69:640–654

    PubMed  Google Scholar 

  • Lam SK, Siu CL, Hillmer S, Jang S, An G, Robinson DG, Jiang L (2007) Rice SCAMP1 defines clathrin-coated, trans-golgi-located tubular-vesicular structures as an early endosome in tobacco BY-2 cells. Plant Cell 19:296–319

    CAS  PubMed Central  PubMed  Google Scholar 

  • Langowski L, Růzicka K, Naramoto S, Kleine-Vehn J, Friml J (2010) Trafficking to the outer polar domain defines the root-soil interface. Curr Biol 20:904–908

    CAS  PubMed  Google Scholar 

  • Lavy M, Bloch D, Hazak O, Gutman I, Poraty L, Sorek N, Sternberg H, Yalovsky S (2007) A Novel ROP/RAC effector links cell polarity, root-meristem maintenance, and vesicle trafficking. Curr Biol 17:947–952

    CAS  PubMed  Google Scholar 

  • Laxmi A, Pan J, Morsy M, Chen R (2008) Light plays an essential role in intracellular distribution of auxin efflux carrier PIN2 in Arabidopsis thaliana. PLoS One 3(1):e1510

    PubMed Central  PubMed  Google Scholar 

  • Leitner J, Petrášek J, Tomanov K, Retzer K, Pařezová M, Korbei B, Bachmair A, Zažímalová E, Luschnig C (2012) Lysine63-linked ubiquitylation of PIN2 auxin carrier protein governs hormonally controlled adaptation of Arabidopsis root growth. Proc Natl Acad Sci U S A 109:8322–8327

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lemtiri-Chlieh F, MacRobbie EA, Webb AA, Manison NF, Brownlee C, Skepper JN, Chen J, Prestwich GD, Brearley CA (2003) Inositol hexakisphosphate mobilizes an endomembrane store of calcium in guard cells. Proc Natl Acad Sci U S A 100:10091–10095

    CAS  PubMed Central  PubMed  Google Scholar 

  • Leyser O (2011) Auxin, self-organisation, and the colonial nature of plants. Curr Biol 21:R331–R337

    CAS  PubMed  Google Scholar 

  • Li H, Lin D, Dhonukshe P, Nagawa S, Chen D, Friml J, Scheres B, Guo H, Yang Z (2011) Phosphorylation switch modulates the interdigitated pattern of PIN1 localization and cell expansion in Arabidopsis leaf epidermis. Cell Res 21:970–978

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lin D, Shingo N, Chen J, Chen X, Cao L, Xu T, Li H, Dhonukshe P, Friml J, Scheres B, Fu Y, Yang Z (2012) A ROP GTPase-dependent auxin signaling pathway inhibits PIN2 endocytosis in Arabidopsis roots. Curr Biol 22:1319–1325

    CAS  PubMed Central  PubMed  Google Scholar 

  • Liu T, Mirschberger C, Chooback L, Arana Q, Dal Sacco Z, MacWilliams H, Clarke M (2002) Altered expression of the 100 kDa subunit of the Dictyostelium vacuolar proton pump impairs enzyme assembly, endocytic function and cytosolic pH regulation. J Cell Sci 115:1907–1918

    CAS  PubMed  Google Scholar 

  • Liu J, Mehdi S, Topping J, Friml J, Lindsey K (2013) Interaction of PLS and PIN and hormonal crosstalk in Arabidopsis root development. Front Plant Sci 4:75

    PubMed Central  PubMed  Google Scholar 

  • Ljung K (2013) Auxin metabolism and homeostasis during plant development. Development 140:943–950

    CAS  PubMed  Google Scholar 

  • Löfke C, Zwiewka M, Heilmann I, Van Montagu MC, Teichmann T, Friml J (2013) Asymmetric gibberellin signaling regulates vacuolar trafficking of PIN auxin transporters during root gravitropism. Proc Natl Acad Sci U S A 110:3627–3632

    PubMed Central  PubMed  Google Scholar 

  • Ludwig-Müller J (2011) Auxin conjugates: their role for plant development and in the evolution of land plants. J Exp Bot 62:1757–1773

    PubMed  Google Scholar 

  • Luschnig C, Gaxiola RA, Grisafi P, Fink GR (1998) EIR1, a root-specific protein involved in auxin transport, is required for gravitropism in Arabidopsis thaliana. Genes Dev 12:2175–2218

    CAS  PubMed Central  PubMed  Google Scholar 

  • Mancuso S, Marras AM, Mugnai S, Schlicht M, Zársky V, Li G, Song L, Xue HW, Baluska F (2007) Phospholipase Dζ2 drives vesicular secretion of auxin for its polar cell-cell transport in the transition zone of the root apex. Plant Signal Behav 2:240–244

    PubMed Central  PubMed  Google Scholar 

  • Mano Y, Nemoto K (2012) The pathway of auxin biosynthesis in plants. J Exp Bot 63:2853–2872

    CAS  PubMed  Google Scholar 

  • Marhavý P, Bielach A, Abas L, Abuzeineh A, Duclercq J, Tanaka H, Parezová M, Petrásek J, 917 Friml J, Kleine-Vehn J, Benková E (2011) Cytokinin modulates endocytic trafficking of PIN1 918 auxin efflux carrier to control plant organogenesis. Dev Cell 21:796–804

    Google Scholar 

  • Martinière A, Lavagi I, Nageswaran G, Rolfe DJ, Maneta-Peyret L, Luu DT, Botchway SW, Webb SEW, Mongrand S, Maurel C, Martin-Fernandez ML, Kleine-Vehn J, Friml J, Moreau P, Runions J (2012) The cell wall constrains lateral diffusion of plant plasma-membrane proteins. Proc Natl Acad Sci U S A 109:12805–12810

    PubMed Central  PubMed  Google Scholar 

  • Matheson LA, Hanton SL, Brandizzi F (2006) Traffic between the plant endoplasmic reticulum and Golgi apparatus: to the Golgi and beyond. Curr Opin Plant Biol 9:601–609

    CAS  PubMed  Google Scholar 

  • Matsuzaki Y, Ogawa-Ohnishi M, Mori A, Matsubayashi Y (2010) Secreted peptide signals required for maintenance of root stem cell niche in Arabidopsis. Science 329:1065–1067

    CAS  PubMed  Google Scholar 

  • McFarlane HE, Shin JJ, Bird DA, Samuels AL (2010) Arabidopsis ABCG transporters, which are required for export of diverse cuticular lipids, dimerize in different combinations. Plant Cell 22:3066–3075

    CAS  PubMed Central  PubMed  Google Scholar 

  • Men S, Boutté Y, Ikeda Y, Li X, Palme K, Stierhof Y-D, Hartmann M-A, Moritz T, Grebe M (2008) Sterol-dependent endocytosis mediates post-cytokinetic acquisition of PIN2 auxin efflux carrier polarity. Nat Cell Biol 10:237–244

    CAS  PubMed  Google Scholar 

  • Michell RH (2008) Inositol derivatives: evolution and functions. Nat Rev Mol Cell Biol 9:151–161

    CAS  PubMed  Google Scholar 

  • Michniewicz M, Brewer PB, Friml J (2007a) Polar auxin transport and asymmetric auxin distribution. Arabidopsis Book 5:e0108

    PubMed Central  PubMed  Google Scholar 

  • Michniewicz M, Zago MK, Abas L, Weijers D, Schweighofer A, Meskiene I, Heisler MG, Ohno C, Zhang J, Huang F, Schwab R, Weigel D, Meyerowitz EM, Luschnig C, Offringa R, Friml J (2007b) Antagonistic regulation of PIN phosphorylation by PP2A and PINOID directs auxin flux. Cell 130:1044–1056

    CAS  PubMed  Google Scholar 

  • Miwa K, Takano J, Omori H, Seki M, Shinozaki K, Fujiwara T (2007) Plants tolerant of high boron levels. Science 318:1417

    CAS  PubMed  Google Scholar 

  • Motchoulski A, Liscum E (1999) Arabidopsis NPH3: a NPH1 photoreceptor-interacting protein essential for phototropism. Science 286:961–964

    CAS  PubMed  Google Scholar 

  • Mouchel CF, Briggs GC, Hardtke CS (2004) Natural genetic variation in Arabidopsis identifies BREVIS RADIX, a novel regulator of cell proliferation and elongation in the root. Genes Dev 18:700–714

    CAS  PubMed Central  PubMed  Google Scholar 

  • Mravec J, Kubes M, Bielach A, Gaykova V, Petrásek J, Skůpa P, Chand S, Benková E, Zazímalová E, Friml J (2008) Interaction of PIN and PGP transport mechanisms in auxin distribution-dependent development. Development 135:3345–3354

    CAS  PubMed  Google Scholar 

  • Mravec J, Petrášek J, Li N, Boeren S, Karlova R, Kitakura S, Pařezová M, Naramoto S, Nodzyński T, Dhonukshe P, Bednarek SY, Zažímalová E, de Vries S, Friml J (2011) Cell plate restricted association of DRP1A and PIN proteins is required for cell polarity establishment in Arabidopsis. Curr Biol 21:1055–1060

    CAS  PubMed  Google Scholar 

  • Muday GK, DeLong A (2001) Polar auxin transport: controlling where and how much. Trends Plant Sci 6:535–542

    CAS  PubMed  Google Scholar 

  • Müller J, Mettbach U, Menzel D, Šamaj J (2007) Molecular dissection of endosomal compartments in plants. Plant Physiol 145:293–304

    PubMed Central  PubMed  Google Scholar 

  • Munnik T, Nielsen E (2011) Green light for polyphosphoinositide signals in plants. Curr Opin Plant Biol 14:489–497

    CAS  PubMed  Google Scholar 

  • Munnik T, Testerink C (2009) Plant phospholipid signaling: ‘in a nutshell’. J Lipid Res 50:260–265

    Google Scholar 

  • Nagawa S, Xu T, Lin D, Dhonukshe P, Zhang X, Friml J, Scheres B, Fu Y, Yang Z (2012) ROP GTPase-dependent actin microfilaments promote PIN1 polarization by localized inhibition of clathrin-dependent endocytosis. PLoS Biol 10(4):e1001299

    CAS  PubMed Central  PubMed  Google Scholar 

  • Naramoto S, Kleine-Vehn J, Robert S, Fujimoto M, Dainobu T, Paciorek T, Ueda T, Nakano A, Van Montagu MCE, Fukuda H, Friml J (2010) ADP-ribosylation factor machinery mediates endocytosis in plant cells. Proc Natl Acad Sci U S A 107:21890–21895

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nodzyński T, Feraru MI, Hirscha S, De Rycke R, Niculaesa C, Boerjana W, Van Leene J, De Jaeger G, Vanneste S, Friml J (2013) Retromer subunits VPS35A and VPS29 mediate prevacuolar compartment (PVC) function in Arabidopsis. Mol Plant 6:1849–1862

    PubMed  Google Scholar 

  • Noh B, Murphy AS, Spalding EP (2001) Multidrug resistance-like genes of Arabidopsis required for auxin transport and auxin-mediated development. Plant Cell 13:2441–2454

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nyasae LK, Hubbard AL, Tuma PL (2003) Transcytotic efflux from early endosomes is dependent on cholesterol and glycosphingolipids in polarized hepatic cells. Mol Biol Cell 14:2689–2705

    CAS  PubMed Central  PubMed  Google Scholar 

  • Okada K, Ueda J, Komaki MK, Bell CJ, Shimura Y (1991) Requirement of the auxin polar transport system in early stages of Arabidopsis floral bud formation. Plant Cell 3:677–684

    CAS  PubMed Central  PubMed  Google Scholar 

  • Paciorek T, Zažímalová E, Ruthardt N, Petrášek J, Stierhof YD, Kleine-Vehn J, Morris DA, Emans N, Jürgens G, Geldner N, Friml J (2005) Auxin inhibits endocytosis and promotes its own efflux from cells. Nature 435:1251–1256

    CAS  PubMed  Google Scholar 

  • Panikashvili D, Savaldi-Goldstein S, Mandel T, Yifhar T, Franke RB, Höfer R, Schreiber L, Chory J, Aharoni A (2007) The Arabidopsis DESPERADO/AtWBC11 transporter is required for cutin and wax secretion. Plant Physiol 145:1345–1360

    CAS  PubMed Central  PubMed  Google Scholar 

  • Paul MJ, Frigerio L (2007) Coated vesicles in plant cells. Semin Cell Dev Biol 18:471–478

    CAS  PubMed  Google Scholar 

  • Peer WA, Bandyopadhyay A, Blakeslee JJ, Makam SN, Chen RJ, Masson PH, Murphy AS (2004) Variation in expression and protein localization of the PIN family of auxin efflux facilitator proteins in flavonoid mutants with altered auxin transport in Arabidopsis thaliana. Plant Cell 16:1898–1911

    CAS  PubMed Central  PubMed  Google Scholar 

  • Petrášek J, Schwarzerová K (2009) Actin and microtubule cytoskeleton interactions. Curr Opin Plant Biol 12:728–734

    PubMed  Google Scholar 

  • Petrášek J, Mravec J, Bouchard R, Blakeslee JJ, Abas M, Seifertová D, Wiśniewska J, Tadele Z, Kubeš M, Čovanová M, Dhonukshe P, Skůpa P, Benková E, Perry L, Křeček P, Lee OR, Fink GR, Geisler M, Murphy AS, Luschnig C, Zažímalová E, Friml J (2006) PIN proteins perform a rate-limiting function in cellular auxin efflux. Science 312:914–918

    PubMed  Google Scholar 

  • Praefcke GJK, McMahon HT (2004) The dynamin superfamily: universal membrane tubulation and fission molecules? Nat Rev Mol Cell Biol 5:133–147

    CAS  PubMed  Google Scholar 

  • Rakusova H, Gallego-Bartolomé J, Vanstraelen M, Robert HS, Alabadí D, Blázquez MA, Benková E, Friml J (2011) Polarization of PIN3-dependent auxin transport for hypocotyl gravitropic response in Arabidopsis thaliana. Plant J 67:817–826

    CAS  PubMed  Google Scholar 

  • Raven JA (1975) Transport of indoleacetic acid in plant cells in relation to pH and electrical potential gradients, and its significance for polar IAA transport. New Phytol 74:163–172

    CAS  Google Scholar 

  • Reinhardt D, Pesce ER, Stieger P, Mandel T, Baltensperger K, Bennett M, Traas J, Friml J, Kuhlemeier C (2003) Regulation of phyllotaxis by polar auxin transport. Nature 426:255–260

    CAS  PubMed  Google Scholar 

  • Richmond TA, Somerville CR (2000) The cellulose synthase superfamily. Plant Physiol 124:495–498

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rigó G, Ayaydin F, Tietz O, Zsigmond L, Kovács H, Páy A, Salchert K, Darula Z, Medzihradszky KF, Szabados L, Palme K, Koncz C, Cséplo A (2013) Inactivation of plasma membrane-localized CDPK-RELATED KINASE5 decelerates PIN2 exocytosis and root gravitropic response in Arabidopsis. Plant Cell 25(5):1592–1608

    PubMed Central  PubMed  Google Scholar 

  • Robert S, Kleine-Vehn J, Barbez E, Sauer M, Paciorek T, Baster P, Vanneste S, Zhang J, Simon S, Čovanová M, Hayashi K, Dhonukshe P, Yang Z, Bednarek SY, Jones AM, Luschnig C, Aniento F, Zažímolová E, Friml J (2010) ABP1 mediates auxin inhibition of clathrin-dependent endocytosis in Arabidopsis. Cell 143:111–121

    CAS  PubMed Central  PubMed  Google Scholar 

  • Robinson DG, Jiang L, Schumacher K (2008) The endosomal system of plants: charting new and familiar territories. Plant Physiol 147:1482–1492

    CAS  PubMed Central  PubMed  Google Scholar 

  • Roppolo D, De Rybel B, Tendon VD, Pfister A, Alassimone J, Vermeer JE, Yamazaki M, Stierhof YD, Beeckman T, Geldner N (2011) A novel protein family mediates Casparian strip formation in the endodermis. Nature 473:380–383

    CAS  PubMed  Google Scholar 

  • Roudier F, Gissot L, Beaudoin F, Haslam R, Michaelson L, Marion J, Molino D, Lima A, Bach L, Morin H, Tellier F, Palauqui JC, Bellec Y, Renne C, Miquel M, Dacosta M, Vignard J, Rochat C, Markham JE, Moreau P, Napier J, Faure JD (2010) Very-long-chain fatty acids are involved in polar auxin transport and developmental patterning in Arabidopsis. Plant Cell 22:364–375

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rubery PH, Sheldrake AR (1974) Carrier-mediated auxin transport. Planta 118:101–121

    CAS  PubMed  Google Scholar 

  • Ruiz Rosquete M, Barbez E, Kleine-Vehn J (2012) Cellular auxin homeostasis: gatekeeping is housekeeping. Mol Plant 5:772–786

    CAS  Google Scholar 

  • Růžička K, Ljung K, Vanneste S, Podhorská R, Beeckman T, Friml J, Benková E (2007) Ethylene regulates root growth through effects on auxin biosynthesis and transport-dependent auxin distribution. Plant Cell 19:2197–2212

    PubMed Central  PubMed  Google Scholar 

  • Růžička K, Šimášková M, Duclercq J, Petrášek J, Zažímalová E, Simon S, Friml J, Van Montagu MC, Benková E (2009) Cytokinin regulates root meristem activity via modulation of the polar auxin transport. Proc Natl Acad Sci U S A 106:4284–4289

    PubMed Central  PubMed  Google Scholar 

  • Sabatini S, Beis D, Wolkenfelt H, Murfett J, Guilfoyle T, Malamy J, Benfey P, Leyser O, Bechtold N, Weisbeek P, Scheres B (1999) An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell 99:463–472

    CAS  PubMed  Google Scholar 

  • Sachs T (1981) The control of the patterned differentiation of vascular tissues. Adv Bot Res 9:151–262

    Google Scholar 

  • Sachs T (1991) Cell polarity and tissue patterning in plants. Development 113:83–93

    Google Scholar 

  • Santner AA, Watson JC (2006) The WAG1 and WAG2 protein kinases negatively regulate root waving in Arabidopsis. Plant J 45:752–764

    CAS  PubMed  Google Scholar 

  • Santuari L, Scacchi E, Rodriguez-Villalon A, Salinas P, Dohmann EM, Brunoud G, Vernoux T, Smith RS, Hardtke CS (2011) Positional information by differential endocytosis splits auxin response to drive Arabidopsis root meristem growth. Curr Biol 21:1918–1923

    CAS  PubMed  Google Scholar 

  • Sauer M, Friml J (2004) The matryoshka dolls of plant polarity. Development 131:5774–5775

    CAS  Google Scholar 

  • Sauer M, Balla J, Luschnig C, Wisniewska J, Reinöhl V, Friml J, Benková E (2006) Canalization of auxin flow by Aux/IAA-ARF-dependent feedback regulation of PIN polarity. Genes Dev 20:2902–2911

    CAS  PubMed Central  PubMed  Google Scholar 

  • Scarpella E, Marcos D, Friml J, Berleth T (2006) Control of leaf vascular patterning by polar auxin transport. Genes Dev 20:1015–1027

    CAS  PubMed Central  PubMed  Google Scholar 

  • Scheible WR, Eshed R, Richmond T, Delmer D, Somerville C (2001) Modifications of cellulose synthase confer resistance to isoxaben and thiazolidinone herbicides in Arabidopsis Ixr1 mutants. Proc Natl Acad Sci U S A 98:10079–10084

    CAS  PubMed Central  PubMed  Google Scholar 

  • Scheuring D, Viotti C, Krüger F, Künzl F, Sturm S, Bubeck J, Hillmer S, Frigerio L, Robinson DG, Pimpl P, Schumacher K (2011) Multivesicular bodies mature from the trans-Golgi network/early endosome in Arabidopsis. Plant Cell 23:3463–3481

    CAS  PubMed Central  PubMed  Google Scholar 

  • Schlereth A, Möller B, Liu W, Kientz M, Flipse J, Rademacher EH, Schmid M, Jürgens G, Weijers D (2010) MONOPTEROS controls embryonic root initiation by regulating a mobile transcription factor. Nature 464:913–916

    CAS  PubMed  Google Scholar 

  • Schlicht M, Strnad M, Scanlon MJ, Mancuso S, Hochholdinger F, Palme K, Volkmann D, Menzel D, Baluska F (2006) Auxin immunolocalization implicates vesicular neurotransmitter-like mode of polar auxin transport in root apices. Plant Signal Behav 1:122–133

    PubMed Central  PubMed  Google Scholar 

  • Seaman MNJ (2005) Recycle your receptors with retromer. Trends Cell Biol 15:68–75

    CAS  PubMed  Google Scholar 

  • Shimada T, Koumoto Y, Li L, Yamazaki M, Kondo M, Nishimura M, Hara-Nishimura I (2006) AtVPS29, a putative component of a retromer complex, is required for the efficient sorting of seed storage proteins. Plant Cell Physiol 47:1187–1194

    CAS  PubMed  Google Scholar 

  • Shirakawa M, Ueda H, Shimada T, Nishiyama C, Hara-Nishimura I (2009) Vacuolar SNAREs function in the formation of the leaf vascular network by regulating auxin distribution. Plant Cell Physiol 50:1319–1328

    CAS  PubMed  Google Scholar 

  • Shivas JM, Morrison HA, Bilder D, Skop AR (2010) Polarity and endocytosis: reciprocal regulation. Trends Cell Biol 20:445–452

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sieberer T, Seifert GJ, Hauser MT, Grisafi P, Fink GR, Luschnig C (2000) Post-transcriptional control of the Arabidopsis auxin efflux carrier EIR1 requires AXR1. Curr Biol 10:1595–1598

    CAS  PubMed  Google Scholar 

  • Sorefan K, Girin T, Liljegren SJ, Ljung K, Robles P, Galván-Ampudia CS, Offringa R, Friml J, Yanofsky MF, Østergaard L (2009) A regulated auxin minimum is required for seed dispersal in Arabidopsis. Nature 459:583–586

    CAS  PubMed  Google Scholar 

  • Spitzer C, Reyes FC, Buono R, Sliwinski MK, Haas TJ, Otegui MS (2009) The ESCRT-related CHMP1A and B proteins mediate multivesicular body sorting of auxin carriers in Arabidopsis and are required for plant development. Plant Cell 21:749–766

    CAS  PubMed Central  PubMed  Google Scholar 

  • Swarup R, Friml J, Marchant A, Ljung K, Sandberg G, Palme K, Bennett M (2001) Localization of the auxin permease AUX1 suggests two functionally distinct hormone transport pathways operate in the Arabidopsis root apex. Genes Dev 15:2648–2653

    CAS  PubMed Central  PubMed  Google Scholar 

  • Swarup R, Perry P, Hagenbeek D, Van Der Straeten D, Beemster GT, Sandberg G, Bhalerao R, Ljung K, Bennett MJ (2007) Ethylene upregulates auxin biosynthesis in Arabidopsis seedlings to enhance inhibition of root cell elongation. Plant Cell 19:2186–2196

    CAS  PubMed Central  PubMed  Google Scholar 

  • Swarup K, Benkova E, Swarup R, Casimiro I, Peret B, Yang Y, Parry G, Nielsen E, De Smet I, Vanneste S, Levesque MP, Carrier D, James N, Calvo V, Ljung K, Kramer E, Roberts R, Graham N, Marillonnet S, Patel K (2008) The auxin influx carrier LAX3 promotes lateral root emergence. Nat Cell Biol 10:946–954

    CAS  PubMed  Google Scholar 

  • Takano J, Tanaka M, Toyoda A, Miwa K, Kasai K, Fuji K, Onouchi H, Naito S, Fujiwara T (2010) Polar localization and degradation of Arabidopsis boron transporters through distinct trafficking pathways. Proc Natl Acad Sci U S A 107:5220–5225

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tanaka H, Dhonukshe P, Brewer PB, Friml J (2006) Spatiotemporal asymmetric auxin distribution: a means to coordinate plant development. Cell Mol Life Sci 63:2738–2754

    CAS  PubMed  Google Scholar 

  • Tanaka H, Kitakura S, De Rycke R, De Groodt R, Friml J (2009) Fluorescence imaging-based screen identifies ARF GEF component of early endosomal trafficking. Curr Biol 19:391–397

    CAS  PubMed  Google Scholar 

  • Tanaka H, Kitakura S, Rakusová R, Uemura T, Feraru MI, De Rycke R, Robert S, Kakimoto T, Friml J (2013) Cell polarity and patterning by PIN trafficking through early endosomal compartments in Arabidopsis. PLoS Genet 9(5):e1003540

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tang RH, Han S, Zheng H, Cook CW, Choi CS, Woerner TE, Jackson RB, Pei ZM (2007) Coupling diurnal cytosolic Ca2+ oscillations to the CAS-IP3 pathway in Arabidopsis. Science 315:1423–1426

    CAS  PubMed  Google Scholar 

  • Teh OK, Moore I (2007) An ARF-GEF acting at the golgi and in selective endocytosis in polarized plant cells. Nature 448:493–496

    CAS  PubMed  Google Scholar 

  • Tepass U, Tanentzapf G, Ward R, Fehon R (2001) Epithelial cell polarity and cell junctions in Drosophila. Annu Rev Genet 35:747–784

    CAS  PubMed  Google Scholar 

  • Testerink C, Munnik T (2011) Molecular, cellular and physiological responses to phosphatidic acid formation in plants. J Exp Bot 62:2349–2361

    CAS  PubMed  Google Scholar 

  • Titapiwatanakun B, Blakeslee JJ, Bandyopadhyay A, Yang H, Mravec J, Sauer M, Cheng Y, Adamec J, Nagashima A, Geisler M, Sakai T, Friml J, Peer WA, Murphy AS (2009) ABCB19/PGP19 stabilizes PIN1 in membrane microdomains in Arabidopsis. Plant J 57:27–44

    CAS  PubMed  Google Scholar 

  • Treml BS, Winderl S, Radykewicz R, Herz M, Schweizer G, Hutzler P, Glawischnig E, Ruiz RA (2005) The gene ENHANCER OF PINOID controls cotyledon development in the Arabidopsis embryo. Development 132:4063–4074

    CAS  PubMed  Google Scholar 

  • Tuma PL, Hubbard AL (2003) Transcytosis: crossing cellular barriers. Physiol Rev 83:871–932

    CAS  PubMed  Google Scholar 

  • Vanneste S, Friml J (2009) Auxin: a trigger for change in plant development. Cell 136:1005–1016

    CAS  PubMed  Google Scholar 

  • Verrier PJ, Bird D, Burla B, Dassa E, Forestier C, Geisler M, Klein M, Kolukisaoglu Ü, Lee Y, Martinoia E, Murphy A, Rea PA, Samuels L, Schulz B, Spalding EP, Yazaki K, Theodoulou FL (2008) Plant ABC proteins—a unified nomenclature and updated inventory. Trends Plant Sci 13:151–159

    CAS  PubMed  Google Scholar 

  • Vieten A, Vanneste S, Wiśniewska J, Benková E, Benjamins R, Beeckman T, Luschnig C, Friml J (2005) Functional redundancy of PIN proteins is accompanied by auxin-dependent cross-regulation of PIN expression. Development 132:4521–4531

    CAS  PubMed  Google Scholar 

  • Vieten A, Sauer M, Brewer PB, Friml J (2007) Molecular and cellular aspects of auxin transport-mediated development. Trends Plant Sci 12:160–168

    CAS  PubMed  Google Scholar 

  • Viotti C, Bubeck J, Stierhof YD, Krebs M, Langhans M, van den Berg W, van Dongen W, Richter S, Geldner N, Takano J, Jürgens G, de Vries SC, Robinson DG, Schumacher K (2010) Endocytic and secretory traffic in Arabidopsis merge in the trans-Golgi network/early endosome, an independent and highly dynamic organelle. Plant Cell 22:1344–1357

    CAS  PubMed Central  PubMed  Google Scholar 

  • Vitale A, Denecke J (1999) The endoplasmic reticulum – gateway of the secretory pathway. Plant Cell 11:615–628

    CAS  PubMed Central  PubMed  Google Scholar 

  • Voigt B, Timmers AC, Šamaj J, Müller J, Baluška F, Menzel D (2005) GFP-FABD2 fusion construct allows in vivo visualization of the dynamic actin cytoskeleton in all cells of Arabidopsis seedlings. Eur J Cell Biol 84:595–608

    CAS  PubMed  Google Scholar 

  • Wabnik K, Kleine-Vehn J, Balla J, Sauer M, Naramoto S, Reinöhl V, Merks RMH, Govaerts W, Friml J (2010) Emergence of tissue polarization from synergy of intracellular and extracellular auxin signaling. Mol Syst Biol 6:447

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wabnik K, Govaerts W, Friml J, Kleine-Vehn J (2011) Feedback models for polarized auxin transport: an emerging trend. Mol Biosyst 7:2352

    CAS  PubMed  Google Scholar 

  • Wan Y, Jasik J, Wang L, Hao H, Volkmann D, Menzel D, Mancuso S, Baluška F, Lin J (2012) The signal transducer NPH3 integrates the phototropin1 photosensor with PIN2-based polar auxin transport in Arabidopsis root phototropism. Plant Cell 24:551–565

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wang B, Henrichs S, Geisler M (2012) The AGC kinase, PINOID, blocks interactive ABCB/PIN auxin transport. Plant Signal Behav 7(12):1515–1517 (Epub ahead of print)

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wang B, Bailly A, Zwiewka M, Henrichs S, Azzarello E, Mancuso S, Maeshima M, Friml J, Schulz A, Geisler M (2013) Arabidopsis TWISTED DWARF1 functionally interacts with auxin exporter ABCB1 on the root plasma membrane. Plant Cell 25:202–214

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wells CD, Fawcett JP, Traweger A, Yamanaka Y, Goudreault M, Elder K, Kulkarni S, Gish G, Virag C, Lim C, Colwill K, Starostine A, Metalnikov P, Pawson T (2006) A Rich1/Amot complex regulates the Cdc42 GTPase and apical-polarity proteins in epithelial cells. Cell 125:535–548

    CAS  PubMed  Google Scholar 

  • Whitford R, Fernandez A, Tejos R, Pérez AC, Kleine-Vehn J, Vanneste S, Drozdzecki A, Leitner J, Abas L, Aerts M, Hoogewijs K, Baster P, De Groodt R, Lin Y-C, Storme V, Van de Peer Y, Beeckman T, Madder A, Devreese B, Luschnig C, Friml J, Hilson P (2012) GOLVEN secretory peptides regulate auxin carrier turnover during plant gravitropic responses. Dev Cell 22:678–685

    CAS  PubMed  Google Scholar 

  • Willemsen V, Friml J, Grebe M, van den Toorn A, Palme K, Scheres B (2003) Cell polarity and PIN protein positioning in Arabidopsis require STEROL METHYLTRANSFERASE1 function. Plant Cell 15:612–625

    CAS  PubMed Central  PubMed  Google Scholar 

  • Willige BC, Isono E, Richter R, Zourelidou M, Schwechheimer C (2011) Gibberellin regulates PIN-FORMED abundance and is required for auxin transport-dependent growth and development in Arabidopsis thaliana. Plant Cell 23:2184–2195

    CAS  PubMed Central  PubMed  Google Scholar 

  • Winter V, Hauser MT (2006) Exploring the ESCRTing machinery in eukaryotes. Trends Plant Sci 11:115–123

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wiśniewska J, Xu J, Seifertová D, Brewer PB, Růžička K, Blilou I, Rouquié D, Benková E, Scheres B, Friml J (2006) Polar PIN localization directs auxin flow in plants. Science 312:883

    PubMed  Google Scholar 

  • Wollert T, Wunder C, Lippincott-Schwartz J, Hurley JH (2009) Membrane scission by the ESCRT-III complex. Nature 458:172–177

    CAS  PubMed Central  PubMed  Google Scholar 

  • Xu T, Wen M, Nagawa S, Fu Y, Chen JG, Wu MJ, Perrot-Rechenmann C, Friml J, Jones AM, Yang Z (2010) Cell surface- and rho GTPase-based auxin signaling controls cellular interdigitationin Arabidopsis. Cell 143:99–110

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yang Y, Hammes UZ, Taylor CG, Schachtman DP, Nielsen E (2006) High-affinity auxin transport by the AUX1 influx carrier protein. Curr Biol 16:1123–1127

    CAS  PubMed  Google Scholar 

  • Žárský V, Cvrčková F, Potocký M, Hála M (2009) Exocytosis and cell polarity in plants – exocyst and recycling domains. New Phytol 183:255–272

    PubMed  Google Scholar 

  • Zažímalová E, Krecek P, Skůpa P, Hoyerová K, Petrásek J (2007) Polar transport of the plant hormone auxin—the role of PIN-FORMED (PIN) proteins. Cell Mol Life Sci 64:1621–1637

    PubMed  Google Scholar 

  • Zegzouti H, Anthony RG, Jahchan N, Bögre L, Christensen SK (2006) Phosphorylation and activation of PINOID by the phospholipid signaling kinase 3-phosphoinositide-dependent protein kinase 1 (PDK1) in Arabidopsis. Proc Natl Acad Sci U S A 103:6404–6409

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang J, Nodzynski T, Pencík A, Rolcík J, Friml J (2010) PIN phosphorylation is sufficient to mediate PIN polarity and direct auxin transport. Proc Natl Acad Sci U S A 107:918–922

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang J, Vanneste S, Brewer PB, Michniewicz M, Grones P, Kleine-Vehn J, Löfke C, Teichmann T, Bielach A, Cannoot B, Hoyerová K, Chen X, Xue HW, Benková E, Zažímalová E, Friml J (2011a) Inositol trisphosphate-induced Ca2+ signaling modulates auxin transport and PIN polarity. Dev Cell 20:855–866

    CAS  PubMed  Google Scholar 

  • Zhang W, To JP, Cheng CY, Eric Schaller G, Kieber JJ (2011b) Type-A response regulators are required for proper root apical meristem function through post-transcriptional regulation of PIN auxin efflux carriers. Plant J 68:1–10

    CAS  PubMed  Google Scholar 

  • Zourelidou M, Müller I, Willige BC, Nill C, Jikumaru Y, Li H, Schwechheimer C (2009) The polarly localized D6 PROTEIN KINASE is required for efficient auxin transport in Arabidopsis thaliana. Development 136:627–636

    CAS  PubMed  Google Scholar 

  • Zwiewka M, Feraru E, Müller B, Hwang I, Feraru MI, Kleine-Vehn J, Weijers D, Friml J (2011) The AP-3 adaptor complex is required for vacuolar function in Arabidopsis. Cell Res 21:1711–1722

    CAS  PubMed Central  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Plant Systems Biology, VIB, 9052, Gent, Belgium

    Pawel Baster & Jiří Friml

  2. Department of Plant Biotechnology and Genetics, Ghent University, 9052, Gent, Belgium

    Pawel Baster & Jiří Friml

  3. Institute of Science and Technology Austria (IST Austria), 3400, Klosterneuburg, Austria

    Pawel Baster & Jiří Friml

Authors
  1. Pawel Baster
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  2. Jiří Friml
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Correspondence to Jiří Friml .

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Editors and Affiliations

  1. Laboratory of Hormonal Regulations in Plants, Institute of Experimental Botany AS CR, Prague 6, Czech Republic

    Eva Zažímalová

  2. Laboratory of Hormonal Regulations in Plants, Institute of Experimental Botany AS CR, Prague 6, Czech Republic

    Jan Petrášek

  3. Hormonal Cross-talk Group, Institute of Science and Technology (IST), Austria, Klosterneuburg, Austria

    Eva Benková

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Baster, P., Friml, J. (2014). Auxin on the Road Navigated by Cellular PIN Polarity. In: Zažímalová, E., Petrášek, J., Benková, E. (eds) Auxin and Its Role in Plant Development. Springer, Vienna. https://doi.org/10.1007/978-3-7091-1526-8_8

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