Advertisement

Regulation of Polar Auxin Transport by Protein–Protein Interactions

  • Markus GeislerEmail author
  • Sina Henrichs
Chapter
Part of the Signaling and Communication in Plants book series (SIGCOMM, volume 17)

Abstract

Work over the last years has uncovered that during the highly integrative process of polar auxin transport, dynamic interactions of membrane proteins with other membrane or soluble proteins or modulatory drugs are providing a high degree of flexibility. This overall concept is supported by the recent release of a first, partial Arabidopsis interactome by the Arabidopsis Interactome Mapping Consortium. In this context, we have summarized the current knowledge of posttranscriptional regulation of auxin transport with an emphasis on protein–protein interaction and protein phosphorylation. We suggest a novel protein–protein interaction feedback loop of auxin transport. Further, we summarize evidence that this interaction loop is tightly interconnected with a previously described PIN polarity loop via AGC3 kinases represented by PINOID. These data are compatible with the view of a putative multi-protein auxin efflux complex that is building the basis for a plastic and economic control of auxin streams during PAT.

Keywords

Auxin Transport Polar Auxin Transport Auxin Efflux Plasma Membrane Location PPIase Activity 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Bailly A, Sovero V, Geisler M (2006) The twisted dwarf's ABC: how immunophilins regulate auxin transport. Plant Signal Behav 1:277–280PubMedGoogle Scholar
  2. 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 283:21817–21826PubMedGoogle Scholar
  3. Bandyopadhyay A, Blakeslee JJ, Lee OR, Mravec J, Sauer M, Titapiwatanakun B, Makam SN, Bouchard R, Geisler M, Martinoia E, Friml J, Peer WA, Murphy AS (2007) Interactions of PIN and PGP auxin transport mechanisms. Biochem Soc Trans 35:137–141PubMedGoogle Scholar
  4. Barbez E, Kubes M, Rolcik J, Beziat C, Pencik A, Wang B, Rosquete MR, Zhu J, Dobrev PI, Lee Y, Zazimalova E, Petrasek J, Geisler M, Friml J, Kleine-Vehn J (2012) A novel putative auxin carrier family regulates intracellular auxin homeostasis in plants. Nature 485:119–122PubMedGoogle Scholar
  5. Barik S (2006) Immunophilins: for the love of proteins. Cell Mol Life Sci 63:2889–2900PubMedGoogle Scholar
  6. Benjamins R, Scheres B (2008) Auxin: the looping star in plant development. Annu Rev Plant Biol 59:443–465PubMedGoogle Scholar
  7. 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
  8. Bennett S, Alvarez J, Bossinger G, Smyth D (1995) Morphogenesis in pinoid mutants of Arabidopsis thaliana. Development 128:4057–4067Google Scholar
  9. Benschop JJ, Mohammed S, O'Flaherty M, Heck AJ, Slijper M, Menke FL (2007) Quantitative phosphoproteomics of early elicitor signaling in Arabidopsis. Mol Cell Proteomics 6:1198–1214PubMedGoogle Scholar
  10. Bernasconi P, Patel BC, Reagan JD, Subramanian MV (1996) The N-1-naphthylphthalamic acid-binding protein is an integral membrane protein. Plant Physiol 111:427–432PubMedGoogle Scholar
  11. 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 19:131–147PubMedGoogle Scholar
  12. Blecher O, Erel N, Callebaut I, Aviezer K, Breiman A (1996) A novel plant peptidyl-prolyl-cis-trans-isomerase (PPIase): cDNA cloning, structural analysis, enzymatic activity and expression. Plant Mol Biol 32:493–504PubMedGoogle Scholar
  13. Bosco CD, Dovzhenko A, Liu X, Woerner N, Rensch T, Eismann M, Eimer S, Hegermann J, Paponov IA, Ruperti B, Heberle-Bors E, Touraev A, Cohen JD, Palme K (2012) The endoplasmic reticulum localized PIN8 is a pollen specific auxin carrier involved in intracellular auxin homeostasis. Plant J 71:860–870Google Scholar
  14. 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 281:30603–30612PubMedGoogle Scholar
  15. Brown DE, Rashotte AM, Murphy AS, Normanly J, Tague BW, Peer WA, Taiz L, Muday GK (2001) Flavonoids act as negative regulators of auxin transport in vivo in arabidopsis. Plant Physiol 126:524–535PubMedGoogle Scholar
  16. Buer CS, Muday GK, Djordjevic MA (2007) Flavonoids are differentially taken up and transported long distances in Arabidopsis. Plant Physiol 145:478–490PubMedGoogle Scholar
  17. Burgardt NI, Linnert M, Weiwad M, Geisler M, Lucke C (2012) NMR assignments of the FKBP-type PPIase domain of FKBP42 from Arabidopsis thaliana. Biomol NMR Assign 6:185–188PubMedGoogle Scholar
  18. Chambers TC, McAvoy EM, Jacobs JW, Eilon G (1990) Protein kinase C phosphorylates P-glycoprotein in multidrug resistant human KB carcinoma cells. J Biol Chem 265:7679–7686PubMedGoogle Scholar
  19. Chen J, Lalonde S, Obrdlik P, Noorani Vatani A, Parsa SA, Vilarino C, Revuelta JL, Frommer WB, Rhee SY (2012) Uncovering Arabidopsis membrane protein interactome enriched in transporters using mating-based split ubiquitin assays and classification models. Front Plant Sci 3:124PubMedGoogle Scholar
  20. Cheng Y, Qin G, Dai X, Zhao Y (2008) NPY genes and AGC kinases define two key steps in auxin-mediated organogenesis in Arabidopsis. Proc Natl Acad Sci USA 105:21017–21022PubMedGoogle Scholar
  21. Christie JM, Yang H, Richter GL, Sullivan S, Thomson CE, Lin J, Titapiwatanakun B, Ennis M, Kaiserli E, Lee OR, Adamec J, Peer WA, Murphy AS (2011) phot1 inhibition of ABCB19 primes lateral auxin fluxes in the shoot apex required for phototropism. PLoS Biol 9:e1001076PubMedGoogle Scholar
  22. Conseil G, Baubichon-Cortay H, Dayan G, Jault JM, Barron D, Di Pietro A (1998) Flavonoids: a class of modulators with bifunctional interactions at vicinal ATP- and steroid-binding sites on mouse P-glycoprotein. Proc Natl Acad Sci USA 95:9831–9836PubMedGoogle Scholar
  23. Conseil G, Perez-Victoria JM, Jault JM, Gamarro F, Goffeau A, Hofmann J, Di Pietro A (2001) Protein kinase C effectors bind to multidrug ABC transporters and inhibit their activity. Biochemistry 40:2564–2571PubMedGoogle Scholar
  24. Consortium AIM (2011) Evidence for network evolution in an Arabidopsis interactome map. Science 333:601–607Google Scholar
  25. Cox DN, Muday GK (1994) NPA binding activity is peripheral to the plasma membrane and is associated with the cytoskeleton. Plant Cell 6:1941–1953PubMedGoogle Scholar
  26. De Bodt S, Hollunder J, Nelissen H, Meulemeester N, Inze D (2012) CORNET 2.0: integrating plant coexpression, protein-protein interactions, regulatory interactions, gene associations and functional annotations. New Phytol 195:707–720PubMedGoogle Scholar
  27. de la Fuente van Bentem S, Anrather D, Roitinger E, Djamei A, Hufnagl T, Barta A, Csaszar E, Dohnal I, Lecourieux D, Hirt H (2006) Phosphoproteomics reveals extensive in vivo phosphorylation of Arabidopsis proteins involved in RNA metabolism. Nucleic Acids Res 34:267–3278Google Scholar
  28. Dela Fuente RK, Leopold AC (1973) A role for calcium in auxin transport. Plant Physiol 51:845–847PubMedGoogle Scholar
  29. Dhonukshe P, Huang F, Galvan-Ampudia CS, Mahonen AP, Kleine-Vehn J, Xu J, Quint A, Prasad K, Friml J, Scheres B, Offringa R (2010) Plasma membrane-bound AGC3 kinases phosphorylate PIN auxin carriers at TPRXS(N/S) motifs to direct apical PIN recycling. Development 137:3245–3255PubMedGoogle Scholar
  30. Ding Z, Galvan-Ampudia CS, Demarsy E, Langowski L, Kleine-Vehn J, Fan Y, Morita MT, Tasaka M, Fankhauser C, Offringa R, Friml J (2011) Light-mediated polarization of the PIN3 auxin transporter for the phototropic response in Arabidopsis. Nat Cell Biol 13:447–452PubMedGoogle Scholar
  31. Ding Z, Wang B, Moreno I, Dupláková N, Simon S, Carraro N, Reemmer J, Pěnčík A, Chen X, Tejos R, Skůpa P, Pollmann S, Mravec J, Petrášek J, Zažímalová E, Honys D, Rolčík J, Murphy A, López AO, Geisler M, Friml J (2012) ER-localized auxin transporter PIN8 regulates auxin homoeostasis and male gametophyte development in Arabidopsis. Nat Commun 3:941. doi:  10.1038/ncomms.1941 PubMedGoogle Scholar
  32. Edlich F, Lucke C (2011) From cell death to viral replication: the diverse functions of the membrane-associated FKBP38. Curr Opin Pharmacol 11:1–6Google Scholar
  33. Edlich F, Weiwad M, Erdmann F, Fanghanel J, Jarczowski F, Rahfeld JU, Fischer G (2005) Bcl-2 regulator FKBP38 is activated by Ca2+/calmodulin. EMBO J 24:2688–2699PubMedGoogle Scholar
  34. Edlich F, Maestre-Martinez M, Jarczowski F, Weiwad M, Moutty MC, Malesevic M, Jahreis G, Fischer G, Lucke C (2007) A novel calmodulin-Ca2+ target recognition activates the Bcl-2 regulator FKBP38. J Biol Chem 282:36496–36504PubMedGoogle Scholar
  35. Feraru E, Friml J (2008) PIN polar targeting. Plant Physiol 147:1553–1559PubMedGoogle Scholar
  36. Friml J, Yang X, Michniewicz M, Weijers D, Quint A, Tietz O, Benjamins R, Ouwerkerk PB, Ljung K, Sandberg G, Hooykaas PJ, Palme K, Offringa R (2004) A PINOID-dependent binary switch in apical-basal PIN polar targeting directs auxin efflux. Science 306:862–865PubMedGoogle Scholar
  37. Furutani M, Kajiwara T, Kato T, Treml BS, Stockum C, Torres-Ruiz RA, Tasaka M (2007) The gene MACCHI-BOU 4/ENHANCER OF PINOID encodes a NPH3-like protein and reveals similarities between organogenesis and phototropism at the molecular level. Development 134:3849–3859PubMedGoogle Scholar
  38. Galvan-Ampudia CS, Offringa R (2007) Plant evolution: AGC kinases tell the auxin tale. Trends Plant Sci 12:541–547PubMedGoogle Scholar
  39. Geisler M, Bailly A (2007) Tête-à-tête: FKBPs function as key players in plant development. Trends Plant Sci 12:465–473PubMedGoogle Scholar
  40. Geisler M, Murphy AS (2006) The ABC of auxin transport: the role of p-glycoproteins in plant development. FEBS Lett 580:1094–1102PubMedGoogle Scholar
  41. 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 14:4238–4249PubMedGoogle Scholar
  42. Geisler M, Girin M, Brandt S, Vincenzetti V, Plaza S, Paris N, Kobae Y, Maeshima M, Billion K, Kolukisaoglu UH, Schulz B, Martinoia E (2004) Arabidopsis immunophilin-like TWD1 functionally interacts with vacuolar ABC transporters. Mol Biol Cell 15:3393–3405PubMedGoogle Scholar
  43. Geisler M, Blakeslee JJ, Bouchard R, Lee OR, Vincenzetti V, Bandyopadhyay A, Titapiwatanakun B, Peer WA, Bailly A, Richards EL, Ejendal KF, Smith AP, Baroux C, Grossniklaus U, Muller A, Hrycyna CA, Dudler R, Murphy AS, Martinoia E (2005) Cellular efflux of auxin catalyzed by the Arabidopsis MDR/PGP transporter AtPGP1. Plant J 44:179–194PubMedGoogle Scholar
  44. Geisler-Lee J, O'Toole N, Ammar R, Provart NJ, Millar AH, Geisler M (2007) A predicted interactome for Arabidopsis. Plant Physiol 145:317–329PubMedGoogle Scholar
  45. Gil P, Dewey E, Friml J, Zhao Y, Snowden KC, Putterill J, Palme K, Estelle M, Chory J (2001) BIG: a calossin-like protein required for polar auxin transport in Arabidopsis. Genes Dev 15:1985–1997PubMedGoogle Scholar
  46. Granzin J, Eckhoff A, Weiergraber OH (2006) Crystal structure of a multi-domain immunophilin from Arabidopsis thaliana: a paradigm for regulation of plant ABC transporters. J Mol Biol 364:799–809PubMedGoogle Scholar
  47. Harrar Y, Bellec Y, Bellini C, Faure JD (2003) Hormonal control of cell proliferation requires PASTICCINO genes. Plant Physiol 132:1217–1227PubMedGoogle Scholar
  48. Hemenway CS, Heitman J (1996) Immunosuppressant target protein FKBP12 is required for P-glycoprotein function in yeast. J Biol Chem 271:18527–18534PubMedGoogle Scholar
  49. Henrichs S, Wang B, Fukao Y, Zhu J, Charrier L, Bailly A, Oehring SC, Linnert M, Weiwad M, Endler A, Nanni P, Pollmann S, Mancuso S, Schulz A, Geisler M (2012) Regulation of ABCB1/PGP1-catalysed auxin transport by linker phosphorylation. EMBO J 31:2965–2980PubMedGoogle Scholar
  50. Huang F, Zago MK, Abas L, van Marion A, Galvan-Ampudia CS, Offringa R (2010) Phosphorylation of conserved PIN motifs directs Arabidopsis PIN1 polarity and auxin transport. Plant Cell 22:1129–1142PubMedGoogle Scholar
  51. Jacobs M, Rubery PH (1988) Naturally-occurring auxin transport regulators. Science 241:346–349PubMedGoogle Scholar
  52. Jurgens G, Geldner N (2007) The high road and the low road: trafficking choices in plants. Cell 130:977–979PubMedGoogle Scholar
  53. Kamphausen T, Fanghanel J, Neumann D, Schulz B, Rahfeld JU (2002) Characterization of Arabidopsis thaliana AtFKBP42 that is membrane-bound and interacts with Hsp90. Plant J 32:263–276PubMedGoogle Scholar
  54. Kim JY, Henrichs S, Bailly A, Vincenzetti V, Sovero V, Mancuso S, Pollmann S, Kim D, Geisler M, Nam HG (2010) Identification of an ABCB/P-glycoprotein-specific inhibitor of auxin transport by chemical genomics. J Biol Chem 285:23309–23317PubMedGoogle Scholar
  55. Kleine-Vehn J, Friml J (2008) Polar targeting and endocytic recycling in auxin-dependent plant development. Annu Rev Cell Dev Biol 24:447–473PubMedGoogle Scholar
  56. 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 21:3839–3849PubMedGoogle Scholar
  57. Lalonde S, Sero A, Pratelli R, Pilot G, Chen J, Sardi MI, Parsa SA, Kim DY, Acharya BR, Stein EV, Hu HC, Villiers F, Takeda K, Yang Y, Han YS, Schwacke R, Chiang W, Kato N, Loque D, Assmann SM, Kwak JM, Schroeder JI, Rhee SY, Frommer WB (2010) A membrane protein/signaling protein interaction network for Arabidopsis version AMPv2. Front Physiol 1:24PubMedGoogle Scholar
  58. Lee SH, Cho HT (2006) PINOID positively regulates auxin efflux in Arabidopsis root hair cells and tobacco cells. Plant Cell 18:1604–1616PubMedGoogle Scholar
  59. Lee K, Thorneycroft D, Achuthan P, Hermjakob H, Ideker T (2010) Mapping plant interactomes using literature curated and predicted protein-protein interaction data sets. Plant Cell 22:997–1005PubMedGoogle Scholar
  60. Li JF, Bush J, Xiong Y, Li L, McCormack M (2011) Large-scale protein-protein interaction analysis in Arabidopsis mesophyll protoplasts by split firefly luciferase complementation. PLoS One 6:e27364PubMedGoogle Scholar
  61. Lomax TL, Muday GK, Rubery PH (1995) Auxin transport. In: Davies PJ (ed) Plant hormones: physiology, biochemistry and molecular biology. Kluwer, Dordrecht, pp 509–530Google Scholar
  62. Luschnig C (2001) Auxin transport: why plants like to think BIG. Curr Biol 11:R831–R833PubMedGoogle Scholar
  63. Merks RM, Van de Peer Y, Inze D, Beemster GT (2007) Canalization without flux sensors: a traveling-wave hypothesis. Trends Plant Sci 12:384–390PubMedGoogle Scholar
  64. Michalke W, Gerard FK, Art EG (1992) Phytotropin-binding sites and auxin transport in Cucurbita pepo: evidence for two recognition sites. Planta 187:254–260Google Scholar
  65. 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 130:1044–1056PubMedGoogle Scholar
  66. Morel J, Claverol S, Mongrand S, Furt F, Fromentin J, Bessoule JJ, Blein JP, Simon-Plas F (2006) Proteomics of plant detergent-resistant membranes. Mol Cell Proteomics 5:1396–1411PubMedGoogle Scholar
  67. Morris DA (2000) Transmembrane auxin carrier systems–dynamic regulators of polar auxin transport. Plant Growth Regul 32:161–172PubMedGoogle Scholar
  68. Morris ME, Zhang S (2006) Flavonoid-drug interactions: effects of flavonoids on ABC transporters. Life Sci 78:2116–2130PubMedGoogle Scholar
  69. Mravec J, Kubes M, Bielach A, Gaykova V, Petrasek J, Skupa P, Chand S, Benkova E, Zazimalova E, Friml J (2008) Interaction of PIN and PGP transport mechanisms in auxin distribution-dependent development. Development 135:3345–3354PubMedGoogle Scholar
  70. Mravec J, Skupa P, Bailly A, Hoyerova K, Krecek P, Bielach A, Petrasek J, Zhang J, Gaykova V, Stierhof YD, Dobrev PI, Schwarzerova K, Rolcik J, Seifertova D, Luschnig C, Benkova E, Zazimalova E, Geisler M, Friml J (2009) Subcellular homeostasis of phytohormone auxin is mediated by the ER-localized PIN5 transporter. Nature 459:1136–1140PubMedGoogle Scholar
  71. 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 128:935–950PubMedGoogle Scholar
  72. Noh B, Murphy AS, Spalding EP (2001) Multidrug resistance-like genes of Arabidopsis required for auxin transport and auxin-mediated development. Plant Cell 13:2441–2454PubMedGoogle Scholar
  73. Nuhse TS, Stensballe A, Jensen ON, Peck SC (2004) Phosphoproteomics of the Arabidopsis plasma membrane and a new phosphorylation site database. Plant Cell 16:2394–2405PubMedGoogle Scholar
  74. Orr GA, Han EK, Browne PC, Nieves E, O'Connor BM, Yang CP, Horwitz SB (1993) Identification of the major phosphorylation domain of murine mdr1b P-glycoprotein. Analysis of the protein kinase A and protein kinase C phosphorylation sites. J Biol Chem 268:25054–25062PubMedGoogle Scholar
  75. Palme K, Galweiler L (1999) PIN-pointing the molecular basis of auxin transport. Curr Opin Plant Biol 2:375–381PubMedGoogle Scholar
  76. Peck SC (2006) Phosphoproteomics in Arabidopsis: moving from empirical to predictive science. J Exp Bot 57:1523–1527PubMedGoogle Scholar
  77. Peer WA, Murphy AS (2006) Flavonoids as signal molecules targets of flavonoid action. In: Grotewold E (ed) The science of flavonoids. Springer, Berlin, pp 239–268Google Scholar
  78. Peer WA, Murphy AS (2007) Flavonoids and auxin transport: modulators or regulators? Trends Plant Sci 12:556–563PubMedGoogle Scholar
  79. Peer WA, Brown DE, Tague BW, Muday GK, Taiz L, Murphy AS (2001) Flavonoid accumulation patterns of transparent testa mutants of arabidopsis. Plant Physiol 126:536–548PubMedGoogle Scholar
  80. Perez-Perez JM, Ponce MR, Micol JL (2004) The ULTRACURVATA2 gene of Arabidopsis encodes an FK506-binding protein involved in auxin and brassinosteroid signaling. Plant Physiol 134:101–117PubMedGoogle Scholar
  81. Petrasek J, Cerna A, Schwarzerova K, Elckner M, Morris DA, Zazimalova E (2003) Do phytotropins inhibit auxin efflux by impairing vesicle traffic? Plant Physiol 131:254–263PubMedGoogle Scholar
  82. Petrasek J, Mravec J, Bouchard R, Blakeslee JJ, Abas M, Seifertova D, Wisniewska J, Tadele Z, Kubes M, Covanova M, Dhonukshe P, Skupa P, Benkova E, Perry L, Krecek P, Lee OR, Fink GR, Geisler M, Murphy AS, Luschnig C, Zazimalova E, Friml J (2006) PIN proteins perform a rate-limiting function in cellular auxin efflux. Science 312:914–918PubMedGoogle Scholar
  83. Rakusova H, Gallego-Bartolome J, Vanstraelen M, Robert HS, Alabadi D, Blazquez MA, Benkova E, Friml J (2011) Polarization of PIN3-dependent auxin transport for hypocotyl gravitropic response in Arabidopsis thaliana. Plant J 67:817–826PubMedGoogle Scholar
  84. Robert HS, Friml J (2009) Auxin and other signals on the move in plants. Nat Chem Biol 5:325–332PubMedGoogle Scholar
  85. Robert HS, Offringa R (2008) Regulation of auxin transport polarity by AGC kinases. Curr Opin Plant Biol 11:495–502PubMedGoogle Scholar
  86. Rojas-Pierce M, Titapiwatanakun B, Sohn EJ, Fang F, Larive CK, Blakeslee J, Cheng Y, Cutler SR, Peer WA, Murphy AS, Raikhel NV (2007) Arabidopsis P-glycoprotein19 participates in the inhibition of gravitropism by gravacin. Chem Biol 14:1366–1376PubMedGoogle Scholar
  87. Ruegger M, Dewey E, Hobbie L, Brown D, Bernasconi P, Turner J, Muday G, Estelle M (1997) Reduced naphthylphthalamic acid binding in the tir3 mutant of Arabidopsis is associated with a reduction in polar auxin transport and diverse morphological defects. Plant Cell 9:745–757PubMedGoogle Scholar
  88. Sachs T (1969) Polarity and the induction of organized vascular tissues. Ann Bot 33:263–272Google Scholar
  89. 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 283:31218–31226PubMedGoogle Scholar
  90. Santner AA, Watson JC (2006) The WAG1 and WAG2 protein kinases negatively regulate root waving in Arabidopsis. Plant J 45:752–764PubMedGoogle Scholar
  91. Scheidt HA, Vogel A, Eckhoff A, Koenig BW, Huster D (2007) Solid-state NMR characterization of the putative membrane anchor of TWD1 from Arabidopsis thaliana. Eur Biophys J 36:393–404PubMedGoogle Scholar
  92. 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 1:122–133PubMedGoogle Scholar
  93. Shirane M, Nakayama KI (2003) Inherent calcineurin inhibitor FKBP38 targets Bcl-2 to mitochondria and inhibits apoptosis. Nat Cell Biol 5:28–37PubMedGoogle Scholar
  94. Sistrunk ML, Antosiewicz DM, Purugganan MM, Braam J (1994) Arabidopsis TCH3 encodes a novel Ca2+ binding protein and shows environmentally induced and tissue-specific regulation. Plant Cell 6:1553–1565PubMedGoogle Scholar
  95. Stoma S, Lucas M, Chopard J, Schaedel M, Traas J, Godin C (2008) Flux-based transport enhancement as a plausible unifying mechanism for auxin transport in meristem development. PLoS Comput Biol 4:e1000207PubMedGoogle Scholar
  96. Sukumar P, Edwards KS, Rahman A, Delong A, Muday GK (2009) PINOID kinase regulates root gravitropism through modulation of PIN2-dependent basipetal auxin transport in Arabidopsis. Plant Physiol 150:722–735PubMedGoogle Scholar
  97. Sussman MR, Gardner G (1980) Solubilization of the receptor for N-1-naphthylphthalamic acid. Plant Physiol 66:1074–1078PubMedGoogle Scholar
  98. Szabo K, Bakos E, Welker E, Muller M, Goodfellow HR, Higgins CF, Varadi A, Sarkadi B (1997) Phosphorylation site mutations in the human multidrug transporter modulate its drug-stimulated ATPase activity. J Biol Chem 272:23165–23171PubMedGoogle Scholar
  99. Taylor LP, Grotewold E (2005) Flavonoids as developmental regulators. Curr Opin Plant Biol 8:317–323PubMedGoogle Scholar
  100. 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 17:2922–2939PubMedGoogle Scholar
  101. 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 60:1093–1107PubMedGoogle Scholar
  102. 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 57:27–44PubMedGoogle Scholar
  103. Toyota M, Furuichi T, Tatsumi H, Sokabe M (2008a) Critical consideration on the relationship between auxin transport and calcium transients in gravity perception of Arabidopsis seedlings. Plant Signal Behav 3:521–524PubMedGoogle Scholar
  104. Toyota M, Furuichi T, Tatsumi H, Sokabe M (2008b) Cytoplasmic calcium increases in response to changes in the gravity vector in hypocotyls and petioles of Arabidopsis seedlings. Plant Physiol 146:505–514PubMedGoogle Scholar
  105. Vanneste S, Friml J (2009) Auxin: a trigger for change in plant development. Cell 136:1005–1016PubMedGoogle Scholar
  106. Vieten A, Sauer M, Brewer PB, Friml J (2007) Molecular and cellular aspects of auxin-transport-mediated development. Trends Plant Sci 12:160–168PubMedGoogle Scholar
  107. Wang B, Bailly A, Zwiewka M, Henrichs S, Azzarello E, Mancuso S, Maeshima M, Friml J, Schulz A, Geisler M (2013) Arabidopsis TWISTED DWARF1 functionally interacts with auxin exporter ABCB1 on the root plasma membrane. Plant Cell (in press)Google Scholar
  108. Weiergraber OH, Eckhoff A, Granzin J (2006) Crystal structure of a plant immunophilin domain involved in regulation of MDR-type ABC transporters. FEBS Lett 580:251–255PubMedGoogle Scholar
  109. Wisniewska J, Xu J, Seifertova D, Brewer PB, Ruzicka K, Blilou I, Rouquie D, Benkova E, Scheres B, Friml J (2006) Polar PIN localization directs auxin flow in plants. Science 312:883PubMedGoogle Scholar
  110. Wu G, Otegui MS, Spalding EP (2010) The ER-localized TWD1 immunophilin is necessary for localization of multidrug resistance-like proteins required for polar auxin transport in Arabidopsis roots. Plant Cell 22:3295–3304PubMedGoogle Scholar
  111. Zhang J, Nodzynski T, Pencik A, Rolcik J, Friml J (2010) PIN phosphorylation is sufficient to mediate PIN polarity and direct auxin transport. Proc Natl Acad Sci USA 107:918–922PubMedGoogle Scholar
  112. Zourelidou M, Muller I, Willige BC, Nill C, Jikumaru Y, Li H, Schwechheimer C (2009) The polarly localized D6 PROTEIN KINASE is required for efficient auxin transport in Arabidopsis thaliana. Development 136:627–636PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.Department of Biology—Plant BiologyUniversity of FribourgFribourgSwitzerland
  2. 2.Institute of Plant Biology, Basel-Zurich Plant Science CenterUniversity of ZurichZurichSwitzerland
  3. 3.Medical Parasitology & Infection BiologySwiss Tropical and Public Health InstituteBaselSwitzerland

Personalised recommendations