Auxin Transporters Controlling Plant Development

Chapter
Part of the Signaling and Communication in Plants book series (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.

Notes

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 ).

References

  1. 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 8:249–256PubMedCrossRefGoogle Scholar
  2. Badescu GO, Napier RM (2006) Receptors for auxin: will it all end in TIRs? Trends Plant Sci 11:217–223PubMedCrossRefGoogle Scholar
  3. 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 283:21817–21826PubMedCrossRefGoogle Scholar
  4. Bainbridge K, Guyomarc'h S, Bayer E, Swarup R, Bennett M, Mandel T, Kuhlemeier C (2008) Auxin influx carriers stabilize phyllotactic patterning. Genes Dev 22:810–823PubMedCrossRefGoogle Scholar
  5. 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 13:282–285PubMedCrossRefGoogle Scholar
  6. Baluška F, Schlicht M, Volkmann D, Mancuso S (2008) Vesicular secretion of auxin: evidences and implications. Plant Signal Behav 3:254–256PubMedCrossRefGoogle Scholar
  7. Becker P, Hakenbeck R, Henrich B (2009) An ABC transporter of Streptococcus pneumoniae involved in susceptibility to vancoresmycin and bacitracin. Antimicrob Agents Chemother 53:2034–2041PubMedCrossRefGoogle Scholar
  8. Benjamins R, Scheres B (2008) Auxin: the looping star in plant development. Annu Rev Plant Biol 59:443–465PubMedCrossRefGoogle Scholar
  9. 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 128:4057–4067PubMedGoogle Scholar
  10. 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 115:591–602PubMedCrossRefGoogle Scholar
  11. Bennett SRM, Alvarez J, Bossinger G, Smyth DR (1995) Morphogenesis in PINOID mutants of Arabidopsis thaliana. Plant J 8:505–520CrossRefGoogle Scholar
  12. 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 273:948–950PubMedCrossRefGoogle Scholar
  13. Bishopp A, Mahonen AP, Helariutta Y (2006) Signs of change: hormone receptors that regulate plant development. Development 133:1857–1869PubMedCrossRefGoogle Scholar
  14. 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 159–176CrossRefGoogle Scholar
  15. 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 19:131–147PubMedCrossRefGoogle Scholar
  16. 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 433:39–44PubMedCrossRefGoogle Scholar
  17. 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 281:30603–30612PubMedCrossRefGoogle Scholar
  18. 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 13:291–301PubMedCrossRefGoogle Scholar
  19. 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 142:254–264PubMedCrossRefGoogle Scholar
  20. Chawla R, DeMason D (2004) Molecular expression of PsPIN1, a putative auxin efflux carrier gene from pea (Pisum sativum L.). Plant Growth Regul 44:1–14CrossRefGoogle Scholar
  21. Chen LS, Ortiz-Lopez A, Jung A, Bush DR (2001) ANT1, an aromatic and neutral amino acid transporter in Arabidopsis. Plant Physiol 125:1813–1820PubMedCrossRefGoogle Scholar
  22. 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 21:1972–1991PubMedCrossRefGoogle Scholar
  23. 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 19:3930–3943PubMedCrossRefGoogle Scholar
  24. Christensen SK, Dagenais N, Chory J, Weigel D (2000) Regulation of auxin response by the protein kinase PINOID. Cell 100:469–478PubMedCrossRefGoogle Scholar
  25. 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 85–107Google Scholar
  26. Cox D, Muday G (1994) NPA binding activity is peripheral to the plasma membrane and is associated with the cytoskeleton. Plant Cell 6:1941–1953PubMedGoogle Scholar
  27. Darwin CR (1880) The power of movement in plants. John Murray, LondonGoogle Scholar
  28. Dawson R, Locher K (2006) Structure of a bacterial multidrug ABC transporter. Nature 443:180–185PubMedCrossRefGoogle Scholar
  29. 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 14:267–277PubMedCrossRefGoogle Scholar
  30. 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 322:1380–1384PubMedCrossRefGoogle Scholar
  31. 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 20:389–399PubMedCrossRefGoogle Scholar
  32. 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 9:109–119PubMedCrossRefGoogle Scholar
  33. 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 312:1218–1220PubMedCrossRefGoogle Scholar
  34. 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 17:520–527PubMedCrossRefGoogle Scholar
  35. 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 105:4489–4494PubMedCrossRefGoogle Scholar
  36. Dixon MW, Jacobson JA, Cady CT, Muday GK (1996) Cytoplasmic orientation of the naphthylphthalamic acid-binding protein in Zucchini plasma membrane vesicles. Plant Physiol 112:421–432PubMedGoogle Scholar
  37. 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 105:8790–8794PubMedCrossRefGoogle Scholar
  38. 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 236:366–375PubMedCrossRefGoogle Scholar
  39. 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 29:717–731PubMedCrossRefGoogle Scholar
  40. 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 108:661–673PubMedCrossRefGoogle Scholar
  41. Friml J, Wiśniewska J, Benková E, Mendgen K, Palme K (2002b) Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature 415:806–809PubMedCrossRefGoogle Scholar
  42. 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 426:147–153PubMedCrossRefGoogle Scholar
  43. 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 306:862–865PubMedCrossRefGoogle Scholar
  44. 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 1773:1062–1072CrossRefGoogle Scholar
  45. 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 241:541–551PubMedCrossRefGoogle Scholar
  46. 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 131:5021–5030PubMedCrossRefGoogle Scholar
  47. Gallavotti A, Yang Y, Schmidt R, Jackson D (2008) The relationship between auxin transport and maize branching. Plant Physiol 147:1913–1923PubMedCrossRefGoogle Scholar
  48. 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 282:2226–2230PubMedCrossRefGoogle Scholar
  49. 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 15:2115–2124PubMedGoogle Scholar
  50. Geisler M, Murphy AS (2006) The ABC of auxin transport: the role of p-glycoproteins in plant development. FEBS Lett 580:1094–1102PubMedCrossRefGoogle Scholar
  51. 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 14:4238–4249PubMedCrossRefGoogle Scholar
  52. 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 44:179–194PubMedCrossRefGoogle Scholar
  53. Geldner N, Friml J, Stierhof YD, Jürgens G, Palme K (2001) Auxin transport inhibitors block PIN1 cycling and vesicle traficking. Nature 413:425–428PubMedCrossRefGoogle Scholar
  54. 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 112:219–230PubMedCrossRefGoogle Scholar
  55. 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 134:1555–1573PubMedCrossRefGoogle Scholar
  56. Goldsmith MHM (1977) Polar transport of auxin. Annu Rev Plant Physiol Plant Mol Biol 28:439–478Google Scholar
  57. Goto N, Starke M, Kranz A (1987) Effect of gibberellins on flower development of the pin-formed mutant of Arabidopsis thaliana. Arabidopsis Inf Serv 23:66–71Google Scholar
  58. 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 12:329–334PubMedCrossRefGoogle Scholar
  59. Guilfoyle TJ, Hagen G (2007) Auxin response factors. Curr Opin Plant Biol 10:453–460PubMedCrossRefGoogle Scholar
  60. 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 20:1330–1345PubMedCrossRefGoogle Scholar
  61. 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 16:1610–1615PubMedCrossRefGoogle Scholar
  62. Hardtke CS, Berleth T (1998) The Arabidopsis gene MONOPTEROS encodes a transcription factor mediating embryo axis formation and vascular development. EMBO J 17:1405–1411PubMedCrossRefGoogle Scholar
  63. 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):e1000282Google Scholar
  64. 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 15:1899–1911PubMedCrossRefGoogle Scholar
  65. Ho CH, Lin SH, Hu HC, Tsay YF (2009) CHL1 functions as a nitrate sensor in plants. Cell 138:1184–1194PubMedCrossRefGoogle Scholar
  66. Hochholdinger F, Wulff D, Reuter K, Park WJ, Feix G (2000) Tissue-specific expression of AUX1 in maize roots. J Plant Physiol 157:315–319CrossRefGoogle Scholar
  67. 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 17:175–176PubMedGoogle Scholar
  68. Hoshino T, Miyamoto K, Ueda J (2004) Automorphosis and auxin polar transport of etiolated pea seedlings under microgravity conditions. Biol Sci Space 18:94–95PubMedGoogle Scholar
  69. 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 146:1128–1141PubMedCrossRefGoogle Scholar
  70. Imhoff V, Müller P, Guern J, Delbarre A (2000) Inhibitors of the carrier-mediated influx of auxin in suspension-cultured tobacco cells. Planta 210:580–588PubMedCrossRefGoogle Scholar
  71. 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 142:63–74PubMedCrossRefGoogle Scholar
  72. 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 222:80–90PubMedCrossRefGoogle Scholar
  73. Jaillais Y, Fobis-Loisy I, Miege C, Rollin C, Gaude T (2006) AtSNX1 defines an endosome for auxin-carrier trafficking in Arabidopsis. Nature 443:106–109PubMedCrossRefGoogle Scholar
  74. Johri M (2008) Hormonal regulation in green plant lineage families. Physiol Mol Biol Plants 14:23–38CrossRefGoogle Scholar
  75. Jonsson H, Heisler M, Shapiro B, Meyerowitz E, Mjolsness E (2006) An auxin-driven polarized transport model for phyllotaxis. Proc Natl Acad Sci USA 103:1633–1638PubMedCrossRefGoogle Scholar
  76. 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 218:15–26PubMedCrossRefGoogle Scholar
  77. Kepinski S, Leyser O (2005) The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435:446–451PubMedCrossRefGoogle Scholar
  78. Kerr ID, Bennett MJ (2007) New insight into the biochemical mechanisms regulating auxin transport in plants. Biochem J 401:613–622PubMedCrossRefGoogle Scholar
  79. 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 18:3171–3181PubMedCrossRefGoogle Scholar
  80. 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 18:526–531PubMedCrossRefGoogle Scholar
  81. 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 105:17812–17817PubMedCrossRefGoogle Scholar
  82. 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 21:3839–3849PubMedCrossRefGoogle Scholar
  83. Koornneef M, Meinke D (2010) The development of Arabidopsis as a model plant. Plant J 61:909–921PubMedCrossRefGoogle Scholar
  84. Kramer EM (2004) PIN and AUX/LAX proteins: their role in auxin accumulation. Trends Plant Sci 9:578–582PubMedCrossRefGoogle Scholar
  85. Kramer E, Bennett M (2006) Auxin transport: a field in flux. Trends Plant Sci 11:382–386PubMedCrossRefGoogle Scholar
  86. 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 10:249PubMedCrossRefGoogle Scholar
  87. 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):927–937PubMedCrossRefGoogle Scholar
  88. Laskowski MJ, Williams ME, Nusbaum HC, Sussex IM (1995) Formation of lateral root-meristems is a 2-stage process. Development 121:3303–3310PubMedGoogle Scholar
  89. Lau S, Shao N, Bock R, Jürgens G, De Smet I (2009) Auxin signaling in algal lineages: fact or myth? Trends Plant Sci 14:182–188PubMedCrossRefGoogle Scholar
  90. 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:e1510PubMedCrossRefGoogle Scholar
  91. Lechner E, Achard P, Vansiri A, Potuschak T, Genschik P (2006) F-box proteins everywhere. Curr Opin Plant Biol 9:631–638PubMedCrossRefGoogle Scholar
  92. Lee SH, Cho HT (2006) PINOID positively regulates auxin efflux in Arabidopsis root hair cells and tobacco cells. Plant Cell 18:1604–1616PubMedCrossRefGoogle Scholar
  93. 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 10:1217–1223PubMedCrossRefGoogle Scholar
  94. 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 78:191–223PubMedCrossRefGoogle Scholar
  95. 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 19:1838–1850PubMedCrossRefGoogle Scholar
  96. 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: 91–101PubMedCrossRefGoogle Scholar
  97. Leyser O (2006) Dynamic integration of auxin transport and signalling. Curr Biol 16:R424–R433PubMedCrossRefGoogle Scholar
  98. Li G, Xue HW (2007) Arabidopsis PLDzeta2 regulates vesicle trafficking and is required for auxin response. Plant Cell 19:281–295PubMedCrossRefGoogle Scholar
  99. 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 310:121–125PubMedCrossRefGoogle Scholar
  100. 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 17:2738–2753PubMedCrossRefGoogle Scholar
  101. 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 138:949–964PubMedCrossRefGoogle Scholar
  102. Lomax T, Muday G, Rubery P (1995) Auxin transport. In: Davis PJ (ed) Plant hormones. Kluwer, Dordrecht, pp 509–530CrossRefGoogle Scholar
  103. 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 12:2175–2187PubMedCrossRefGoogle Scholar
  104. Maher E, Martindale S (1980) Mutants of Arabidopsis thaliana with altered responses to auxins and gravity. Biochem Genet 18:1041–1053PubMedCrossRefGoogle Scholar
  105. 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 51:537–550PubMedCrossRefGoogle Scholar
  106. 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 2:240–244PubMedCrossRefGoogle Scholar
  107. 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 14:589–597PubMedCrossRefGoogle Scholar
  108. 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 10:237–244PubMedCrossRefGoogle Scholar
  109. Merks RMH, Van de Peer Y, Inze D, Beemster GTS (2007) Canalization without flux sensors: a traveling-wave hypothesis. Trends Plant Sci 12:384–390PubMedCrossRefGoogle Scholar
  110. 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 130:1044–1056PubMedCrossRefGoogle Scholar
  111. Mitchison G (1980) Model for vein formation in higher-plants. Proc R Soc Lond B 207:79–109CrossRefGoogle Scholar
  112. Mitchison G (1981) The polar transport of auxin and vein patterns in plants. Philos Trans R Soc Lond B Biol Sci 295:461–471CrossRefGoogle Scholar
  113. 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 149:835–840PubMedCrossRefGoogle Scholar
  114. Morris DA, Friml J, Zažímalová E (2004) The transport of auxins. In: Davies PJ (ed) Plant hormones: biosynthesis, signal transduction, action! Kluwer, Dordrecht, pp 437–470Google Scholar
  115. 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 135:3345–3354PubMedCrossRefGoogle Scholar
  116. 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 459:1136–1140PubMedCrossRefGoogle Scholar
  117. 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 17:6903–6911PubMedCrossRefGoogle Scholar
  118. 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 302:81–84PubMedCrossRefGoogle Scholar
  119. Murphy A, Peer WA, Taiz L (2000) Regulation of auxin transport by aminopeptidases and endogenous flavonoids. Planta 211:315–324PubMedCrossRefGoogle Scholar
  120. 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 128:935–950PubMedCrossRefGoogle Scholar
  121. 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 53:516–529PubMedCrossRefGoogle Scholar
  122. 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 49:1250–1255PubMedCrossRefGoogle Scholar
  123. Nemhauser JL, Mockler TC, Chory J (2004) Interdependency of brassinosteroid and auxin signaling in Arabidopsis. PLoS Biol 2:E258PubMedCrossRefGoogle Scholar
  124. 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 12:235–245PubMedCrossRefGoogle Scholar
  125. Nick P, Han M, An G (2009) Auxin stimulates its own transport by shaping actin filaments. Plant Physiol 151:155–167PubMedCrossRefGoogle Scholar
  126. Noh B, Murphy A, Spalding E (2001) Multidrug resistance-like genes of Arabidopsis required for auxin transport and auxin-mediated development. Plant Cell 13:2441–2454PubMedGoogle Scholar
  127. 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 423:999–1002PubMedCrossRefGoogle Scholar
  128. Ogawa M, Hanada A, Yamauchi Y, Kuwahara A, Kamiya Y, Yamaguchi S (2003) Gibberellin biosynthesis and response during Arabidopsis seed germination. Plant Cell 15:1591–1604PubMedCrossRefGoogle Scholar
  129. 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 269:1872–1875PubMedCrossRefGoogle Scholar
  130. 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 3:677–684PubMedGoogle Scholar
  131. 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 227:133–142PubMedCrossRefGoogle Scholar
  132. 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 435:1251–1256PubMedCrossRefGoogle Scholar
  133. Paponov IA, Teale WD, Trebar M, Blilou K, Palme K (2005) The PIN auxin efflux facilitators: evolutionary and functional perspectives. Trends Plant Sci 10:170–177PubMedCrossRefGoogle Scholar
  134. 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 1:321–337PubMedCrossRefGoogle Scholar
  135. 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 25:399–406PubMedCrossRefGoogle Scholar
  136. 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 12:381–385PubMedCrossRefGoogle Scholar
  137. Peer WA, Murphy AS (2007) Flavonoids and auxin transport: modulators or regulators? Trends Plant Sci 12:556–563PubMedCrossRefGoogle Scholar
  138. Petrášek J, Černá A, Schwarzerovà K, Elčkner M, Morris DA, Zažímalová E (2003) Do Phytotropins Inhibit Auxin Efflux by Impairing Vesicle Traffic? Plant Physiol 131:254–263Google Scholar
  139. 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 144:1852–1862PubMedCrossRefGoogle Scholar
  140. Petrášek J, Friml J (2009) Auxin transport routes in plant development. Development 136:2675–2688PubMedCrossRefGoogle Scholar
  141. 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 106:609–3614CrossRefGoogle Scholar
  142. 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 312:914–918PubMedCrossRefGoogle Scholar
  143. Prusinkiewicz P, Rolland-Lagan A (2006) Modeling plant morphogenesis. Curr Opin Plant Biol 9:83–88PubMedCrossRefGoogle Scholar
  144. Quint M, Gray WM (2006) Auxin signaling. Curr Opin Plant Biol 9:448–453PubMedCrossRefGoogle Scholar
  145. 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 125:990–1000PubMedCrossRefGoogle Scholar
  146. Rahman A, Bannigan A, Sulaman W, Pechter P, Blancaflor E, Bascin T (2007) Auxin, actin and growth of the Arabidopsis thalian. Plant J 50:514–528PubMedCrossRefGoogle Scholar
  147. 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 74:163–172CrossRefGoogle Scholar
  148. Reinhardt D, Mandel T, Kuhlemeier C (2000) Auxin regulates the initiation and radial position of plant lateral organs. Plant Cell 12:507–518PubMedGoogle Scholar
  149. 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–D279PubMedCrossRefGoogle Scholar
  150. 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 155:678–684CrossRefGoogle Scholar
  151. 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 14:1366–1376PubMedCrossRefGoogle Scholar
  152. Rubery PH (1990) Phytotropins-receptors and endogenous ligands. Hormone perception and signal transduction in animals and plants. Symp Soc Exp Biol 44:119–146PubMedGoogle Scholar
  153. Rubery PH, Sheldrake AR (1974) Carrier-mediated auxin auxin transport. Planta 118:101–121CrossRefGoogle Scholar
  154. 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 19:2197–2212PubMedCrossRefGoogle Scholar
  155. 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 106:4284–4289PubMedCrossRefGoogle Scholar
  156. 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 107:10749–10753PubMedCrossRefGoogle Scholar
  157. Sachs T (1981) The control of the patterned differentiation of vascular tissues. Adv Bot Res Inc Adv Plant Pathol 9:151–262Google Scholar
  158. Sachs T (1991) Pattern formation in plant tissues. Cambridge University Press, New YorkCrossRefGoogle Scholar
  159. 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 579:5399–5406PubMedCrossRefGoogle Scholar
  160. 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 283:31218–31226PubMedCrossRefGoogle Scholar
  161. Santner A, Estelle M (2009) Recent advances and emerging trends in plant hormone signalling. Nature 459:1071–1078PubMedCrossRefGoogle Scholar
  162. 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 20:2902–2911PubMedCrossRefGoogle Scholar
  163. Scarpella E, Marcos D, Friml J, Berleth T (2006) Control of leaf vascular patterning by polar auxin transport. Genes Dev 20:1015–1027PubMedCrossRefGoogle Scholar
  164. 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 1:122–133PubMedCrossRefGoogle Scholar
  165. Schnabel EL, Frugoli JF (2004) The PIN and LAX families of auxin transport genes in Medicago truncatula. Mol Genet Genomics 272:420–432PubMedCrossRefGoogle Scholar
  166. 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 100:10096–10101PubMedCrossRefGoogle Scholar
  167. 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 10:1623–1636PubMedGoogle Scholar
  168. Smith R, Guyomarc'h S, Mandel T, Reinhardt D, Kuhlemeier C, Prusinkiewicz P (2006) A plausible model of phyllotaxis. Proc Natl Acad Sci USA 103:1301–1306PubMedCrossRefGoogle Scholar
  169. 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 286:316–318PubMedCrossRefGoogle Scholar
  170. 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 1:129–144PubMedCrossRefGoogle Scholar
  171. Sussman MR, Gardner G (1980) Solubilization of the receptor for N-1-naphthylphthalamic acid. Plant Physiol 66:1074–1078PubMedCrossRefGoogle Scholar
  172. 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 15:2648–2653PubMedCrossRefGoogle Scholar
  173. 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 16:3069–3083PubMedCrossRefGoogle Scholar
  174. 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 7:1057–1065PubMedCrossRefGoogle Scholar
  175. 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 10:946–954PubMedCrossRefGoogle Scholar
  176. Tanaka H, Dhonukshe P, Brewer PB, Friml J (2006) Spatiotemporal asymmetric auxin distribution: a means to coordinate plant development. Cell Mol Life Sci 63:2738–2754PubMedCrossRefGoogle Scholar
  177. 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 17:2922–2939PubMedCrossRefGoogle Scholar
  178. 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 60:1093–1107PubMedCrossRefGoogle Scholar
  179. 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 57:27–44PubMedCrossRefGoogle Scholar
  180. Tusnady G, Simon I (1998) Principles governing amino acid composition of integral membrane proteins: Application to topology prediction. J Mol Biol 283:489–506PubMedCrossRefGoogle Scholar
  181. 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 105:277–289PubMedCrossRefGoogle Scholar
  182. 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 137:597–606PubMedCrossRefGoogle Scholar
  183. Vanneste S, Friml J (2009) Auxin: a trigger for change in plant development. Cell 136:1005–1016PubMedCrossRefGoogle Scholar
  184. 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 123:139–146CrossRefGoogle Scholar
  185. 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 13:151–159PubMedCrossRefGoogle Scholar
  186. 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 40:523–535PubMedCrossRefGoogle Scholar
  187. 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 132:4521–4531PubMedCrossRefGoogle Scholar
  188. Vieten A, Sauer M, Brewer PB, Friml J (2007) Molecular and cellular aspects of auxin-transport-mediated development. Trends Plant Sci 12:160–168PubMedCrossRefGoogle Scholar
  189. 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 54:820–828PubMedCrossRefGoogle Scholar
  190. 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 2:823–831PubMedCrossRefGoogle Scholar
  191. 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 17:2517–2526PubMedCrossRefGoogle Scholar
  192. Went FW (1974) Reflections and speculations. Annu Rev Plant Physiol Plant Mol Biol 25:1–26Google Scholar
  193. 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 15:612–625PubMedCrossRefGoogle Scholar
  194. 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 312:883PubMedCrossRefGoogle Scholar
  195. 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 19:1826–1837PubMedCrossRefGoogle Scholar
  196. 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):179–191PubMedCrossRefGoogle Scholar
  197. Xu J, Scheres B (2005) Dissection of Arabidopsis ADP-RIBOSYLATION FACTOR 1 function in epidermal cell polarity. Plant Cell 17:525–536PubMedCrossRefGoogle Scholar
  198. 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 46:1674–1681PubMedCrossRefGoogle Scholar
  199. Yang HB, Murphy AS (2009) Functional expression and characterization of Arabidopsis ABCB, AUX 1 and PIN auxin transporters in Schizosaccharomyces pombe. Plant J 59:179–191PubMedCrossRefGoogle Scholar
  200. Yang Y, Hammes U, Taylor C, Schachtman D, Nielsen E (2006) High-affinity auxin transport by the AUX1 influx carrier protein. Curr Biol 16:1123–1127PubMedCrossRefGoogle Scholar
  201. Young G, Jack D, Smith D, Saier M (1999) The amino acid/auxin: proton symport permease family. Biochim Biophys Acta Biomembr 1415:306–322CrossRefGoogle Scholar
  202. 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 137:607–617PubMedCrossRefGoogle Scholar
  203. Žárský V, Cvrčková F, Potocký M, Hála M (2009) Exocytosis and cell polarity in plants – exocyst and recycling domains. New Phytol 183:255–272PubMedCrossRefGoogle Scholar
  204. 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 64:1621–1637PubMedCrossRefGoogle Scholar
  205. Zažímalová E, Murphy A, Yang H, Hoyerová K, Hošek P (2010) Auxin transporters-why so many? Cold Spring Harb Perspect Biol 2:a001552PubMedCrossRefGoogle Scholar
  206. 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 103:6404–6409PubMedCrossRefGoogle Scholar
  207. 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 107:918–922PubMedCrossRefGoogle Scholar
  208. 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 136:627–636PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2011

Authors and Affiliations

  • J. Petrášek
    • 1
  • K. Malínská
    • 1
  • E. Zažímalová
    • 1
  1. 1.Institute of Experimental BotanyThe Academy of Sciences of the Czech RepublicPrague 6Czech Republic

Personalised recommendations