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Auxin Transporters Controlling Plant Development

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Transporters and Pumps in Plant Signaling

Part of the book series: Signaling and Communication in Plants ((SIGCOMM,volume 7))

Abstract

The plant hormone auxin regulates many important aspects of plant development from the early embryogenesis to the seed production. On genomic and nongenomic levels, finely tuned auxin gradients form an important morphoregulatory trigger. In planta, auxin is transported to long distances using symplastic transport in the phloem. Besides, it is also a subject to the cell-to-cell transport, being able to move across the plasma membrane (PM) by diffusion and/or utilizing several types of auxin transporters. The role of the PM-localized auxin influx and efflux carriers lies mainly in the fast directional transport of auxin across the PM forming the basis for the establishment of developmentally significant auxin gradients. In addition to PM-localized auxin transporters, there is also a population of intracellular auxin transporters, which are probably involved in the regulation of auxin homeostasis and thus in the control of availability of free auxin molecules. This chapter summarizes recent knowledge on the types of auxin transporters, their functional characterization, and involvement in developmental processes in plants.

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References

  • Abas L, Benjamins R, Malenica N, Paciorek T, Wirniewska 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

    Article  PubMed  CAS  Google Scholar 

  • Badescu GO, Napier RM (2006) Receptors for auxin: will it all end in TIRs? Trends Plant Sci 11:217–223

    Article  PubMed  CAS  Google Scholar 

  • Bailly A, Sovero V, Vincenzetti V, Santelia D, Bartnik D, Koenig BW, Mancuso S, Martinoia E, Geisler M (2008) Modulation of P-glycoproteins by auxin transport inhibitors is mediated by interaction with immunophilins. J Biol Chem 283:21817–21826

    Article  PubMed  CAS  Google Scholar 

  • Bainbridge K, Guyomarc'h S, Bayer E, Swarup R, Bennett M, Mandel T, Kuhlemeier C (2008) Auxin influx carriers stabilize phyllotactic patterning. Genes Dev 22:810–823

    Article  PubMed  CAS  Google Scholar 

  • Baluška F, Šámaj 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

    Article  PubMed  CAS  Google Scholar 

  • Baluška F, Schlicht M, Volkmann D, Mancuso S (2008) Vesicular secretion of auxin: evidences and implications. Plant Signal Behav 3:254–256

    Article  PubMed  Google Scholar 

  • Becker P, Hakenbeck R, Henrich B (2009) An ABC transporter of Streptococcus pneumoniae involved in susceptibility to vancoresmycin and bacitracin. Antimicrob Agents Chemother 53:2034–2041

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  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

    PubMed  CAS  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

    Article  PubMed  Google Scholar 

  • Bennett SRM, Alvarez J, Bossinger G, Smyth DR (1995) Morphogenesis in PINOID mutants of Arabidopsis thaliana. Plant J 8:505–520

    Article  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Bishopp A, Mahonen AP, Helariutta Y (2006) Signs of change: hormone receptors that regulate plant development. Development 133:1857–1869

    Article  PubMed  CAS  Google Scholar 

  • Blakeslee J, Peer W, Murphy A (2005) MDR/PGP auxin transport proteins and andocytic cycling. In: Šamaj J, Baluška F, Menzel D (eds) Plant endocytosis. Springer, Berlin, pp 159–176

    Chapter  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

    Article  PubMed  CAS  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

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Butler JH, Hu S, Brady SR, Dixon MW, Muday GK (1998) In vitro and in vivo evidence for actin association of the naphthylphthalamic acid-binding protein from zucchini hypocotyls. Plant J 13:291–301

    Article  PubMed  CAS  Google Scholar 

  • Carraro N, Forestan C, Canova S, Traas J, Varotto S (2006) ZmPIN1a and ZmPIN1b encode two novel putative candidates for polar auxin transport and plant architecture determination of maize. Plant Physiol 142:254–264

    Article  PubMed  CAS  Google Scholar 

  • Chawla R, DeMason D (2004) Molecular expression of PsPIN1, a putative auxin efflux carrier gene from pea (Pisum sativum L.). Plant Growth Regul 44:1–14

    Article  CAS  Google Scholar 

  • Chen LS, Ortiz-Lopez A, Jung A, Bush DR (2001) ANT1, an aromatic and neutral amino acid transporter in Arabidopsis. Plant Physiol 125:1813–1820

    Article  PubMed  CAS  Google Scholar 

  • Chen Z, Noir S, Kwaaitaal M, Hartmann HA, Wu M-J, Mudgil Y, Sukumar P, Muday G, Panstruga R, Jones AM (2009) Two seven-transmembrane domain mildew resistance locus O proteins cofunction in Arabidopsis root thigmomorphogenesis. Plant Cell 21:1972–1991

    Article  PubMed  CAS  Google Scholar 

  • Cho M, Lee S, Cho H (2007) P-glycoprotein4 displays auxin efflux transporter-like action in Arabidopsis root hair cells and tobacco cells. Plant Cell 19:3930–3943

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Cook T, Poli D, Cohen J (2003) Did auxin play a crucial role in the evolution of novel body plans during the late silurian–early devonian radiation of land plants? In: Hemsley A, Poole I (eds) The evolution of plant physiology. Elsevier, Oxford, pp 85–107

    Google Scholar 

  • Cox D, Muday G (1994) NPA binding activity is peripheral to the plasma membrane and is associated with the cytoskeleton. Plant Cell 6:1941–1953

    PubMed  CAS  Google Scholar 

  • Darwin CR (1880) The power of movement in plants. John Murray, London

    Google Scholar 

  • Dawson R, Locher K (2006) Structure of a bacterial multidrug ABC transporter. Nature 443:180–185

    Article  PubMed  CAS  Google Scholar 

  • de Billy F, Grosjean C, May S, Bennett M, Cullimore JV (2001) Expression studies on AUX1-like genes in Medicago truncatula suggest that auxin is required at two steps in early nodule development. Mol Plant-Microbe Interact 14:267–277

    Article  PubMed  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

    Article  PubMed  CAS  Google Scholar 

  • Deruère J, Jackson K, Garbers C, Soll D, DeLong A (1999) The RCN1-encoded A subunit of protein phosphatase 2A increases phosphatase activity in vivo. Plant J 20:389–399

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Dharmasiri S, Swarup R, Mockaitis K, Dharmasiri N, Singh SK, Kowalchyk M, Marchant A, Mills S, Sandberg G, Bennett MJ, Estelle M (2006) AXR4 is required for localization of the auxin influx facilitator AUX1. Science 312:1218–1220

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Dixon MW, Jacobson JA, Cady CT, Muday GK (1996) Cytoplasmic orientation of the naphthylphthalamic acid-binding protein in Zucchini plasma membrane vesicles. Plant Physiol 112:421–432

    PubMed  CAS  Google Scholar 

  • Dubrovsky JG, Sauer M, Napsucialy-Mendivil S, Ivanchenko MG, Friml J, Shishkova S, Celenza J, Benková E (2008) Auxin acts as a local morphogenetic trigger to specify lateral root founder cells. Proc Natl Acad Sci USA 105:8790–8794

    Article  PubMed  CAS  Google Scholar 

  • Feugier F, Mochizuki A, Iwasa Y (2005) Self-organization of the vascular system in plant leaves: inter-dependent dynamics of auxin flux and carrier proteins. J Theor Biol 236:366–375

    Article  PubMed  CAS  Google Scholar 

  • Fischer W, Loo D, Koch W, Ludewig U, Boorer K, Tegeder M, Rentsch D, Wright E, Frommer W (2002) Low and high affinity amino acid H+-cotransporters for cellular import of neutral and charged amino acids. Plant J 29:717–731

    Article  PubMed  CAS  Google Scholar 

  • Friml J, Benková E, Blilou I, Wiśniewska 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

    Article  PubMed  CAS  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

    Article  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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Fu D, van Dam E, Brymora A, Duggin I, Robinson P, Roufogalis B (2007) The small GTPases Rab5 and Ra1A regulate intracellular traffic of P-glycoprotein. Biochim Biophys Acta Mol Cell Res 1773:1062–1072

    Article  CAS  Google Scholar 

  • Fujita H, Mochizuki A (2006) Pattern formation of leaf veins by the positive feedback regulation between auxin flow and auxin efflux carrier. J Theor Biol 241:541–551

    Article  PubMed  CAS  Google Scholar 

  • Furutani M, Vernoux T, Traas J, Kato T, Tasaka M, Aida M (2004) PIN-FORMED1 and PINOID regulate boundary formation and cotyledon development in Arabidopsis embryogenesis. Development 131:5021–5030

    Article  PubMed  CAS  Google Scholar 

  • Gallavotti A, Yang Y, Schmidt R, Jackson D (2008) The relationship between auxin transport and maize branching. Plant Physiol 147:1913–1923

    Article  PubMed  CAS  Google Scholar 

  • Gälweiler L, Guan CH, 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

    Article  PubMed  CAS  Google Scholar 

  • Garbers C, DeLong A, Deruère J, Bernasconi P, Soll D (1996) A mutation in protein phosphatase 2A regulatory subunit A affects auxin transport in Arabidopsis. EMBO J 15:2115–2124

    PubMed  CAS  Google Scholar 

  • Geisler M, Murphy AS (2006) The ABC of auxin transport: the role of p-glycoproteins in plant development. FEBS Lett 580:1094–1102

    Article  PubMed  CAS  Google Scholar 

  • Geisler M, Kolukisaoglu HU, Bouchard R, Billion K, Berger J, Saal B, Frangne N, Koncz-Kalman Z, Koncz C, Dudler R, Blakeslee JJ, Murphy AS, Martinoia E, Schulz B (2003) TWISTED DWARF1, a unique plasma membrane-anchored immunophilin-like protein, interacts with Arabidopsis multidrug resistance-like transporters AtPGP1 and AtPGP19. Mol Biol Cell 14:4238–4249

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Geldner N, Anders N, Wolters H, Keicher J, Kornberger W, Müller 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

    Article  PubMed  CAS  Google Scholar 

  • Goda H, Sawa S, Asami T, Fujioka S, Shimada Y, Yoshida S (2004) Comprehensive comparison of auxin-regulated and brassinosteroid-regulated genes in Arabidopsis. Plant Physiol 134:1555–1573

    Article  PubMed  CAS  Google Scholar 

  • Goldsmith MHM (1977) Polar transport of auxin. Annu Rev Plant Physiol Plant Mol Biol 28:439–478

    CAS  Google Scholar 

  • Goto N, Starke M, Kranz A (1987) Effect of gibberellins on flower development of the pin-formed mutant of Arabidopsis thaliana. Arabidopsis Inf Serv 23:66–71

    Google Scholar 

  • Grebe M, Friml J, Swarup R, Ljung K, Sandberg G, Terlou M, Palme K, Bennett MJ, Scheres B (2002) Cell polarity signaling in Arabidopsis involves a BFA-sensitive auxin influx pathway. Curr Biol 12:329–334

    Article  PubMed  CAS  Google Scholar 

  • Guilfoyle TJ, Hagen G (2007) Auxin response factors. Curr Opin Plant Biol 10:453–460

    Article  PubMed  CAS  Google Scholar 

  • Hála M, Cole R, Synek L, Drdová E, Pečenková T, Nordheim A, Lamkemeyer T, Madlung J, Hochholdinger F, Fowler J, Žárský V (2008) An exocyst complex functions in plant cell growth in Arabidopsis and tobacco. Plant Cell 20:1330–1345

    Article  PubMed  CAS  Google Scholar 

  • Hamann T, Benková E, Baurle I, Kientz M, Jürgens G (2002) The Arabidopsis BODENLOS gene encodes an auxin response protein inhibiting MONOPTEROS-mediated embryo patterning. Genes Dev 16:1610–1615

    Article  PubMed  CAS  Google Scholar 

  • Hardtke CS, Berleth T (1998) The Arabidopsis gene MONOPTEROS encodes a transcription factor mediating embryo axis formation and vascular development. EMBO J 17:1405–1411

    Article  PubMed  CAS  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

    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

    Article  PubMed  CAS  Google Scholar 

  • Ho CH, Lin SH, Hu HC, Tsay YF (2009) CHL1 functions as a nitrate sensor in plants. Cell 138:1184–1194

    Article  PubMed  CAS  Google Scholar 

  • Hochholdinger F, Wulff D, Reuter K, Park WJ, Feix G (2000) Tissue-specific expression of AUX1 in maize roots. J Plant Physiol 157:315–319

    Article  CAS  Google Scholar 

  • Hoshino T, Hitotsubashi R, Miyamoto K, Tanimoto E, Ueda J (2003) Expression of PIN and AUX1 genes encoding putative carrier proteins for auxin polar transport in etiolated pea epicotyls [correction of epicotyles] under simulated microgravity conditions on a three-dimensional clinostat. Biol Sci Space 17:175–176

    PubMed  Google Scholar 

  • Hoshino T, Miyamoto K, Ueda J (2004) Automorphosis and auxin polar transport of etiolated pea seedlings under microgravity conditions. Biol Sci Space 18:94–95

    PubMed  Google Scholar 

  • Hoyerová K, Perry L, Hand P, Laňková M, Kocábek T, May S, Kottová J, Pačes J, Napier R, Zažímalová E (2008) Functional characterization of PaLAX1, a putative auxin permease, in heterologous plant systems. Plant Physiol 146:1128–1141

    Article  PubMed  CAS  Google Scholar 

  • Imhoff V, Müller P, Guern J, Delbarre A (2000) Inhibitors of the carrier-mediated influx of auxin in suspension-cultured tobacco cells. Planta 210:580–588

    Article  PubMed  CAS  Google Scholar 

  • Ito H, Gray WM (2006) A gain-of-function mutation in the Arabidopsis pleiotropic drug resistance transporter PDR9 confers resistance to auxinic herbicides. Plant Physiol 142:63–74

    Article  PubMed  CAS  Google Scholar 

  • Jahrmann T, Bastida M, Pineda M, Gasol E, Ludevid M, Palacin M, Puigdomenech P (2005) Studies on the function of TM20, a transmembrane protein present in cereal embryos. Planta 222:80–90

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Johri M (2008) Hormonal regulation in green plant lineage families. Physiol Mol Biol Plants 14:23–38

    Article  CAS  Google Scholar 

  • Jonsson H, Heisler M, Shapiro B, Meyerowitz E, Mjolsness E (2006) An auxin-driven polarized transport model for phyllotaxis. Proc Natl Acad Sci USA 103:1633–1638

    Article  PubMed  CAS  Google Scholar 

  • Kamada M, Yamasaki S, Fujii N, Higashitani A, Takahashi H (2003) Gravity-induced modification of auxin transport and distribution for peg formation in cucumber seedlings: possible roles for CS-AUX1 and CS-PIN1. Planta 218:15–26

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Kerr ID, Bennett MJ (2007) New insight into the biochemical mechanisms regulating auxin transport in plants. Biochem J 401:613–622

    Article  PubMed  CAS  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

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Koornneef M, Meinke D (2010) The development of Arabidopsis as a model plant. Plant J 61:909–921

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Kramer E, Bennett M (2006) Auxin transport: a field in flux. Trends Plant Sci 11:382–386

    Article  PubMed  CAS  Google Scholar 

  • Křeček P, Skůpa P, Libus J, Naramoto S, Tejos R, Friml J, Zažímalová E (2009) The PIN-FORMED (PIN) protein family of auxin transporters. Genome Biol 10:249

    Article  PubMed  CAS  Google Scholar 

  • Krouk G, Lacombe B, Bielach A, Perrine-Walker F, Malinská K, Mounier E, Hoyerová K, Tillard P, Leon S, Ljung K, Zažímalová E, Benková E, Nacry P, Gojon A (2010) Nitrate-regulated auxin transport by NRT1.1 defines a mechanism for nutrient sensing in plants. Dev Cell 18(6):927–937

    Article  PubMed  CAS  Google Scholar 

  • Laskowski MJ, Williams ME, Nusbaum HC, Sussex IM (1995) Formation of lateral root-meristems is a 2-stage process. Development 121:3303–3310

    PubMed  CAS  Google Scholar 

  • Lau S, Shao N, Bock R, Jürgens G, De Smet I (2009) Auxin signaling in algal lineages: fact or myth? Trends Plant Sci 14:182–188

    Article  PubMed  CAS  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:e1510

    Article  PubMed  CAS  Google Scholar 

  • Lechner E, Achard P, Vansiri A, Potuschak T, Genschik P (2006) F-box proteins everywhere. Curr Opin Plant Biol 9:631–638

    Article  PubMed  CAS  Google Scholar 

  • Lee SH, Cho HT (2006) PINOID positively regulates auxin efflux in Arabidopsis root hair cells and tobacco cells. Plant Cell 18:1604–1616

    Article  PubMed  CAS  Google Scholar 

  • Lee M, Choi Y, Burla B, Kim Y, Jeon B, Maeshima M, Yoo J, Martinoia E, Lee Y (2008) The ABC transporter AtABCB14 is a malate importer and modulates stomatal response to CO2. Nat Cell Biol 10:1217–1223

    Article  PubMed  CAS  Google Scholar 

  • Levin M (2006) Is the early left-right axis like a plant, a kidney, or a neuron? The integration of physiological signals in embryonic asymmetry. Birth Defects Res C Embryo Today 78:191–223

    Article  PubMed  CAS  Google Scholar 

  • Lewis DR, Miller ND, Splitt BL, Wu GS, Spalding EP (2007) Separating the roles of acropetal and basipetal auxin transport on gravitropism with mutations in two Arabidopsis multidrug resistance-like ABC transporter genes. Plant Cell 19:1838–1850

    Article  PubMed  CAS  Google Scholar 

  • Lewis DR, Wu G, Ljung K, Spalding EP (2009) Auxin transport into cotyledons and cotyledon growth depend similarly on the ABCB19 Multidrug Resistance-like transporter. Plant J 60: 91–101

    Article  PubMed  CAS  Google Scholar 

  • Leyser O (2006) Dynamic integration of auxin transport and signalling. Curr Biol 16:R424–R433

    Article  PubMed  CAS  Google Scholar 

  • Li G, Xue HW (2007) Arabidopsis PLDzeta2 regulates vesicle trafficking and is required for auxin response. Plant Cell 19:281–295

    Article  PubMed  CAS  Google Scholar 

  • Li JS, Yang HB, Peer WA, Richter G, Blakeslee J, Bandyopadhyay A, Titapiwantakun B, Undurraga S, Khodakovskaya M, Richards EL, Krizek B, Murphy AS, Gilroy S, Gaxiola R (2005a) Arabidopsis H+-PPase AVP1 regulates auxin-mediated organ development. Science 310:121–125

    Article  PubMed  CAS  Google Scholar 

  • Li L, Xu J, Xu ZH, Xue HW (2005b) Brassinosteroids stimulate plant tropisms through modulation of polar auxin transport in Brassica and Arabidopsis. Plant Cell 17:2738–2753

    Article  PubMed  CAS  Google Scholar 

  • Lin R, Wang H (2005) Two homologous ATP-binding cassette transporter proteins, AtMDR1 and AtPGP1, regulate Arabidopsis photomorphogenesis and root development by mediating polar auxin transport. Plant Physiol 138:949–964

    Article  PubMed  CAS  Google Scholar 

  • Lomax T, Muday G, Rubery P (1995) Auxin transport. In: Davis PJ (ed) Plant hormones. Kluwer, Dordrecht, pp 509–530

    Chapter  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 12:2175–2187

    Article  PubMed  CAS  Google Scholar 

  • Maher E, Martindale S (1980) Mutants of Arabidopsis thaliana with altered responses to auxins and gravity. Biochem Genet 18:1041–1053

    Article  PubMed  CAS  Google Scholar 

  • Malenica N, Abas L, Benjamins R, Kitakura S, Sigmund HF, Jun KS, Hauser MT, Friml J, Luschnig C (2007) MODULATOR OF PIN genes control steady-state levels of Arabidopsis PIN proteins. Plant J 51:537–550

    Article  PubMed  CAS  Google Scholar 

  • Mancuso S, Marras A, Mugnai S, Schlicht M, Žárský V, Li G, Song L, Xue H, Baluška F (2007) Phospholipase dzeta2 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

    Article  PubMed  Google Scholar 

  • Marchant A, Bhalerao R, Casimiro I, Eklof J, Casero PJ, Bennett M, Sandberg G (2002) AUX1 promotes lateral root formation by facilitating indole-3-acetic acid distribution between sink and source tissues in the Arabidopsis seedling. Plant Cell 14:589–597

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Merks RMH, Van de Peer Y, Inze D, Beemster GTS (2007) Canalization without flux sensors: a traveling-wave hypothesis. Trends Plant Sci 12:384–390

    Article  PubMed  CAS  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 (2007) Antagonistic regulation of PIN phosphorylation by PP2A and PINOID directs auxin flux. Cell 130:1044–1056

    Article  PubMed  CAS  Google Scholar 

  • Mitchison G (1980) Model for vein formation in higher-plants. Proc R Soc Lond B 207:79–109

    Article  Google Scholar 

  • Mitchison G (1981) The polar transport of auxin and vein patterns in plants. Philos Trans R Soc Lond B Biol Sci 295:461–471

    Article  CAS  Google Scholar 

  • Miyazawa Y, Takahashi A, Kobayashi A, Kaneyasu T, Fujii N, Takahashi H (2009) GNOM-mediated vesicular trafficking plays an essential role in hydrotropism of Arabidopsis roots. Plant Physiol 149:835–840

    Article  PubMed  CAS  Google Scholar 

  • Morris DA, Friml J, Zažímalová E (2004) The transport of auxins. In: Davies PJ (ed) Plant hormones: biosynthesis, signal transduction, action! Kluwer, Dordrecht, pp 437–470

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Mravec J, Skůpa P, Bailly A, Hoyerová K, Křeček P, Bielach A, Petrášek J, Zhang J, Gaykova V, Stierhof YD, Dobrev PI, Schwarzerová K, Rolčik J, Seifertová D, Luschnig C, Benková E, Zažímalová E, Geisler M, Friml J (2009) Subcellular homeostasis of phytohormone auxin is mediated by the ER-localized PIN5 transporter. Nature 459:1136–1140

    Article  PubMed  CAS  Google Scholar 

  • Müller A, Guan CH, Gälweiler L, Tanzler P, Huijser P, Marchant A, Parry G, Bennett M, Wisman E, Palme K (1998) AtPIN2 defines a locus of Arabidopsis for root gravitropism control. EMBO J 17:6903–6911

    Article  PubMed  Google Scholar 

  • Multani DS, Briggs SP, Chamberlin MA, Blakeslee JJ, Murphy AS, Johal GS (2003) Loss of an MDR transporter in compact stalks of maize br2 and sorghum dw3 mutants. Science 302:81–84

    Article  PubMed  CAS  Google Scholar 

  • Murphy A, Peer WA, Taiz L (2000) Regulation of auxin transport by aminopeptidases and endogenous flavonoids. Planta 211:315–324

    Article  PubMed  CAS  Google Scholar 

  • Murphy AS, Hoogner KR, Peer WA, Taiz L (2002) Identification, purification, and molecular cloning of N-1-naphthylphthalmic acid-binding plasma membrane-associated aminopeptidases from Arabidopsis. Plant Physiol 128:935–950

    Article  PubMed  CAS  Google Scholar 

  • Nagashima A, Suzuki G, Uehara Y, Saji K, Furukawa T, Koshiba T, Sekimoto M, Fujioka S, Kuroha T, Kojima M, Sakakibara H, Fujisawa N, Okada K, Sakai T (2008a) Phytochromes and cryptochromes regulate the differential growth of Arabidopsis hypocotyls in both a PGP19-dependent and a PGP19-independent manner. Plant J 53:516–529

    Article  PubMed  CAS  Google Scholar 

  • Nagashima A, Uehara Y, Sakai T (2008b) The ABC subfamily B auxin transporter AtABCB19 is involved in the inhibitory effects of N-1-Naphthyphthalamic acid on the phototropic and gravitropic responses of Arabidopsis hypocotyls. Plant Cell Physiol 49:1250–1255

    Article  PubMed  CAS  Google Scholar 

  • Nemhauser JL, Mockler TC, Chory J (2004) Interdependency of brassinosteroid and auxin signaling in Arabidopsis. PLoS Biol 2:E258

    Article  PubMed  CAS  Google Scholar 

  • Ni WM, Chen XY, Xu ZH, Xue HW (2002) Isolation and functional analysis of a Brassica juncea gene encoding a component of auxin efflux carrier. Cell Res 12:235–245

    Article  PubMed  Google Scholar 

  • Nick P, Han M, An G (2009) Auxin stimulates its own transport by shaping actin filaments. Plant Physiol 151:155–167

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Noh B, Bandyopadhyay A, Peer WA, Spalding EP, Murphy AS (2003) Enhanced gravi- and phototropism in plant mdr mutants mislocalizing the auxin efflux protein PIN1. Nature 423:999–1002

    Article  PubMed  CAS  Google Scholar 

  • Ogawa M, Hanada A, Yamauchi Y, Kuwahara A, Kamiya Y, Yamaguchi S (2003) Gibberellin biosynthesis and response during Arabidopsis seed germination. Plant Cell 15:1591–1604

    Article  PubMed  CAS  Google Scholar 

  • Ohno H, Stewart J, Fournier M, Bosshart H, Rhee I, Miyatake S, Saito T, Gallusser A, Kirchhausen T, Bonifacino J (1995) Interaction of tyrosine-based sorting signals with clathrin-associated proteins. Science 269:1872–1875

    Article  PubMed  CAS  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

    PubMed  CAS  Google Scholar 

  • Oliveros-Valenzuela MR, Reyes D, Sanchez-Bravo J, Acosta M, Nicolas C (2007) The expression of genes coding for auxin carriers in different tissues and along the organ can explain variations in auxin transport and the growth pattern in etiolated lupin hypocotyls. Planta 227:133–142

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Paponov IA, Teale WD, Trebar M, Blilou K, Palme K (2005) The PIN auxin efflux facilitators: evolutionary and functional perspectives. Trends Plant Sci 10:170–177

    Article  PubMed  CAS  Google Scholar 

  • Paponov IA, Paponov M, Teale W, Menges M, Chakrabortee S, Murray JA, Palme K (2008) Comprehensive transcriptome analysis of auxin responses in Arabidopsis. Mol Plant 1:321–337

    Article  PubMed  CAS  Google Scholar 

  • Parry G, Delbarre A, Marchant A, Swarup R, Napier R, Perrot-Rechenmann C, Bennett MJ (2001) Novel auxin transport inhibitors phenocopy the auxin influx carrier mutation aux1. Plant J 25:399–406

    Article  PubMed  CAS  Google Scholar 

  • Pasquier C, Promponas V, Palaios G, Hamodrakas J, Hamodrakas S (1999) A novel method for predicting transmembrane segments in proteins based on a statistical analysis of the SwissProt database: the PRED-TMR algorithm. Protein Eng 12:381–385

    Article  PubMed  CAS  Google Scholar 

  • Peer WA, Murphy AS (2007) Flavonoids and auxin transport: modulators or regulators? Trends Plant Sci 12:556–563

    Article  PubMed  CAS  Google Scholar 

  • Petrášek J, Černá A, Schwarzerovà K, Elčkner M, Morris DA, Zažímalová E (2003) Do Phytotropins Inhibit Auxin Efflux by Impairing Vesicle Traffic? Plant Physiol 131:254–263

    Google Scholar 

  • Peret B, Swarup R, Jansen L, Devos G, Auguy F, Collin M, Santi C, Hocher V, Franche C, Bogusz D, Bennett M, Laplaze L (2007) Auxin influx activity is associated with Frankia infection during actinorhizal nodule formation in Casuarina glauca. Plant Physiol 144:1852–1862

    Article  PubMed  CAS  Google Scholar 

  • Petrášek J, Friml J (2009) Auxin transport routes in plant development. Development 136:2675–2688

    Article  PubMed  CAS  Google Scholar 

  • Pernisová M, Klíma P, Horák J, Válková M, Malbeck J, Souček P, Reichman P, Hoyerová K, Dubová J, Friml J, Zažímalová E, Hejátko J (2009) Cytokinins modulate auxin-induced organogenesis in plants via regulation of the auxin efflux. Proc Natl Acad Sci USA 106:609–3614

    Article  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

    Article  PubMed  CAS  Google Scholar 

  • Prusinkiewicz P, Rolland-Lagan A (2006) Modeling plant morphogenesis. Curr Opin Plant Biol 9:83–88

    Article  PubMed  CAS  Google Scholar 

  • Quint M, Gray WM (2006) Auxin signaling. Curr Opin Plant Biol 9:448–453

    Article  PubMed  CAS  Google Scholar 

  • Rahman A, Ahamed A, Amakawa T, Goto N, Tsurumi S (2001) Chromosaponin I specifically interacts with AUX1 protein in regulating the gravitropic response of arabidopsis roots. Plant Physiol 125:990–1000

    Article  PubMed  CAS  Google Scholar 

  • Rahman A, Bannigan A, Sulaman W, Pechter P, Blancaflor E, Bascin T (2007) Auxin, actin and growth of the Arabidopsis thalian. Plant J 50:514–528

    Article  PubMed  CAS  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

    Article  CAS  Google Scholar 

  • Reinhardt D, Mandel T, Kuhlemeier C (2000) Auxin regulates the initiation and radial position of plant lateral organs. Plant Cell 12:507–518

    PubMed  CAS  Google Scholar 

  • Ren Q, Chen K, Paulsen I (2007) TransportDB: a comprehensive database resource for cytoplasmic membrane transport systems and outer membrane channels. Nucleic Acids Res 35:D274–D279

    Article  PubMed  CAS  Google Scholar 

  • Robinson JS, Albert AC, Morris DA (1999) Differential effects of brefeldin A and cycloheximide on the activity of auxin efflux carriers in Cucurbita pepo L. J Plant Physiol 155:678–684

    Article  CAS  Google Scholar 

  • Rojas-Pierce M, Titapiwatanakun B, Sohn EJ, Fang F, Larive CK, Blakeslee J, Cheng Y, Cuttler S, Peer WA, Murphy AS, Raikhel NV (2007) Arabidopsis P-glycoprotein19 participates in the inhibition of gravitropism by gravacin. Chem Biol 14:1366–1376

    Article  PubMed  CAS  Google Scholar 

  • Rubery PH (1990) Phytotropins-receptors and endogenous ligands. Hormone perception and signal transduction in animals and plants. Symp Soc Exp Biol 44:119–146

    PubMed  CAS  Google Scholar 

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

    Article  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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Růžička K, Strader L, Bailly A, Blakeslee J, Nejedlá E, Langowski L, Yang H, Fujika H, Ito H, Syono K, Gray W, Hejátko J, Martinoia E, Geisler M, Murphy A, Bartel B, Friml J (2010) Arabidopsis PIS1encodes the ABCG37 transporter of the auxin precursor indole-3-butyric acid. Proc Natl Acad Sci USA 107:10749–10753

    Article  PubMed  Google Scholar 

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

    Google Scholar 

  • Sachs T (1991) Pattern formation in plant tissues. Cambridge University Press, New York

    Book  Google Scholar 

  • Santelia D, Vincenzetti V, Azzarello E, Bovet L, Fukao Y, Düchtig P, Mancuso S, Martinoia E, Geisler M (2005) MDR-like ABC transporter AtPGP4 is involved in auxin-mediated lateral root and root hair development. FEBS Lett 579:5399–5406

    Article  PubMed  CAS  Google Scholar 

  • Santelia D, Henrichs S, Vincenzetti V, Sauer M, Bigler L, Klein M, Bailly A, Lee Y, Friml J, Geisler M, Martinoia E (2008) Flavonoids redirect PIN-mediated polar auxin fluxes during root gravitropic responses. J Biol Chem 283:31218–31226

    Article  PubMed  CAS  Google Scholar 

  • Santner A, Estelle M (2009) Recent advances and emerging trends in plant hormone signalling. Nature 459:1071–1078

    Article  PubMed  CAS  Google Scholar 

  • Sauer M, Balla J, Luschnig C, Wiśniewska 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

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Schnabel EL, Frugoli JF (2004) The PIN and LAX families of auxin transport genes in Medicago truncatula. Mol Genet Genomics 272:420–432

    Article  PubMed  CAS  Google Scholar 

  • Schrader J, Baba K, May ST, Palme K, Bennett M, Bhalerao RP, Sandberg G (2003) Polar auxin transport in the wood-forming tissues of hybrid aspen is under simultaneous control of developmental and environmental signals. Proc Natl Acad Sci USA 100:10096–10101

    Article  PubMed  CAS  Google Scholar 

  • Sidler M, Hassa P, Hasan S, Ringli C, Dudler R (1998) Involvement of an ABC transporter in a developmental pathway regulating hypocotyl cell elongation in the light. Plant Cell 10:1623–1636

    PubMed  CAS  Google Scholar 

  • Smith R, Guyomarc'h S, Mandel T, Reinhardt D, Kuhlemeier C, Prusinkiewicz P (2006) A plausible model of phyllotaxis. Proc Natl Acad Sci USA 103:1301–1306

    Article  PubMed  CAS  Google Scholar 

  • Steinmann T, Geldner N, Grebe M, Mangold S, Jackson C, Paris S, Gälweiler L, Palme K, Jürgens G (1999) Coordinated polar localization of auxin efflux carrier PIN1 by GNOM ARF GEF. Science 286:316–318

    Article  PubMed  CAS  Google Scholar 

  • Stone BB, Stowe-Evans EL, Harper RM, Celaya RB, Ljung K, Sandberg R, Liscum E (2008) Disruptions in AUX1-dependent auxin influx alter hypocotyl phototropism in Arabidopsis. Mol Plant 1:129–144

    Article  PubMed  CAS  Google Scholar 

  • Sussman MR, Gardner G (1980) Solubilization of the receptor for N-1-naphthylphthalamic acid. Plant Physiol 66:1074–1078

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Swarup R, Kargul J, Marchant A, Zadik D, Rahman A, Mills R, Yemm A, May S, Williams L, Millner P, Tsurumi S, Moore I, Napier R, Kerr ID, Bennett MJ (2004) Structure-function analysis of the presumptive Arabidopsis auxin permease AUX1. Plant Cell 16:3069–3083

    Article  PubMed  CAS  Google Scholar 

  • Swarup R, Kramer EM, Perry P, Knox K, Leyser HMO, Haseloff J, Beemster GTS, Bhalerao R, Bennett MJ (2005) Root gravitropism requires lateral root cap and epidermal cells for transport and response to a mobile auxin signal. Nat Cell Biol 7:1057–1065

    Article  PubMed  CAS  Google Scholar 

  • Swarup K, Benková 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, Jones JDG, Taylor CG, Schachtman DP, May S, Sandberg G, Benfey P, Friml J, Kerr I, Beeckman T, Laplaze L, Bennett MJ (2008) The auxin influx carrier LAX3 promotes lateral root emergence. Nat Cell Biol 10:946–954

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Terasaka K, Blakeslee JJ, Titapiwatanakun B, Peer WA, Bandyopadhyay A, Makam SN, Lee OR, Richards EL, Murphy AS, Sato F, Yazaki K (2005) PGP4, an ATP binding cassette P-glycoprotein, catalyzes auxin transport in Arabidopsis thaliana roots. Plant Cell 17:2922–2939

    Article  PubMed  CAS  Google Scholar 

  • Titapiwatanakun B, Murphy AS (2009) Post-transcriptional regulation of auxin transport proteins: cellular trafficking, protein phosphorylation, protein maturation, ubiquitination, and membrane composition. J Exp Bot 60:1093–1107

    Article  PubMed  CAS  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 stabilises PIN1 in membrane microdomains in Arabidopsis. Plant J 57:27–44

    Article  PubMed  CAS  Google Scholar 

  • Tusnady G, Simon I (1998) Principles governing amino acid composition of integral membrane proteins: Application to topology prediction. J Mol Biol 283:489–506

    Article  PubMed  CAS  Google Scholar 

  • Ugartechea-Chirino Y, Swarup R, Swarup K, Peret B, Whitworth M, Bennett M, Bougourd S (2010) The AUX1 LAX family of auxin influx carriers is required for the establishment of embryonic root cell organization in Arabidopsis thaliana. Ann Bot 105:277–289

    Article  PubMed  CAS  Google Scholar 

  • Vandenbussche F, Petrášek J, Žádníková P, Hoyerová K, Pešek B, Raz V, Swarup R, Bennett M, Zažímalová E, Benková E, Van Der Straeten D (2010) The auxin influx carriers AUX1 and LAX3 are involved in auxin-ethylene interactions during apical hook development in Arabidopsis thaliana seedlings. Development 137:597–606

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Vanneste S, Maes L, De Smet I, Himanen K, Naudts M, Inze D, Beeckman T (2005) Auxin regulation of cell cycle and its role during lateral root initiation. Physiol Plant 123:139–146

    Article  CAS  Google Scholar 

  • Verrier PJ, Bird D, Buria B, Dassa E, Forestier C, Geisler M, Klein M, Kolukisaoglu U, 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

    Article  PubMed  CAS  Google Scholar 

  • Vicente-Agullo F, Rigas S, Desbrosses G, Dolan L, Hatzopoulos P, Grabov A (2004) Potassium carrier TRH1 is required for auxin transport in Arabidopsis roots. Plant J 40:523–535

    Article  PubMed  CAS  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 auxindependent cross-regulation of PIN expression. Development 132:4521–4531

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Walch-Liu P, Forde BG (2008) Nitrate signalling mediated by the NRT1.1 nitrate transporter antagonises L-glutamate-induced changes in root architecture. Plant J 54:820–828

    Article  PubMed  CAS  Google Scholar 

  • Wang J, Hu H, Wang G, Li J, Chen J, Wu P (2009) Expression of PIN genes in rice (Oryza sativa L.): tissue specificity and regulation by hormones. Mol Plant 2:823–831

    Article  PubMed  CAS  Google Scholar 

  • Weijers D, Sauer M, Meurette O, Friml J, Ljung K, Sandberg G, Hooykaas P, Offringa R (2005) Maintenance of embryonic auxin distribution for apical-basal patterning by PIN-FORMED-dependent auxin transport in Arabidopsis. Plant Cell 17:2517–2526

    Article  PubMed  CAS  Google Scholar 

  • Went FW (1974) Reflections and speculations. Annu Rev Plant Physiol Plant Mol Biol 25:1–26

    CAS  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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Wu GS, Lewis DR, Spalding EP (2007) Mutations in Arabidopsis multidrug resistance-like ABC transporters separate the roles of acropetal and basipetal auxin transport in lateral root development. Plant Cell 19:1826–1837

    Article  PubMed  CAS  Google Scholar 

  • Wu G, Cameron JN, Ljung K, Spalding EP (2010) A role for ABCB19-mediated polar auxin transport in seedling photomorphogenesis mediated by cryptochrome 1 and phytochrome B. Plant J 62(2):179–191

    Article  PubMed  CAS  Google Scholar 

  • Xu J, Scheres B (2005) Dissection of Arabidopsis ADP-RIBOSYLATION FACTOR 1 function in epidermal cell polarity. Plant Cell 17:525–536

    Article  PubMed  CAS  Google Scholar 

  • Xu M, Zhu L, Shou HX, Wu P (2005) A PIN1 family gene, OsPIN1, involved in auxin-dependent adventitious root emergence and tillering in rice. Plant Cell Physiol 46:1674–1681

    Article  PubMed  CAS  Google Scholar 

  • Yang HB, Murphy AS (2009) Functional expression and characterization of Arabidopsis ABCB, AUX 1 and PIN auxin transporters in Schizosaccharomyces pombe. Plant J 59:179–191

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Young G, Jack D, Smith D, Saier M (1999) The amino acid/auxin: proton symport permease family. Biochim Biophys Acta Biomembr 1415:306–322

    Article  CAS  Google Scholar 

  • Žádníková P, Petrášek J, Marhavý P, Raz V, Vandenbussche F, Ding Z, Schwarzerová K, Morita M, Tasaka M, Hejátko J, Van Der Straeten D, Friml J, Benková E (2010) Role of PIN-mediated auxin efflux in apical hook development of Arabidopsis thaliana. Development 137:607–617

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Zažímalová E, Murphy A, Yang H, Hoyerová K, Hošek P (2010) Auxin transporters-why so many? Cold Spring Harb Perspect Biol 2:a001552

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

The authors acknowledge the support for their work from the Ministry of Education, Youth and Sports of the Czech Republic, project LN06034. Figures were drawn by G. Rzewuski (http://www.bioartworks.com ).

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Petrášek, J., Malínská, K., Zažímalová, E. (2011). Auxin Transporters Controlling Plant Development. In: Geisler, M., Venema, K. (eds) Transporters and Pumps in Plant Signaling. Signaling and Communication in Plants, vol 7. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-14369-4_9

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