Skip to main content
SpringerLink
Log in

MDR/PGP Auxin Transport Proteins and Endocytic Cycling

  • Chapter
  • First Online:
Plant Endocytosis

Part of the book series: Plant Cell Monographs ((CELLMONO,volume 1))

Abstract

Auxin is an essential regulator of plant growth and development. Polarized transport of auxin is responsible for apical dominance, tropic growth, and organ development. Previous studies have demonstrated that the polarized movement of auxin is dependent upon the action of polarly localized, endocytotically cycled PIN auxin efflux facilitator proteins. More recently, plant orthologs of mammalian multidrug-resistance (MDR)/P-glycoprotein (PGP) type ABC transporters have been shown to function in auxin transport. In this review, the PGP nomenclature/numbering system established by Martinoia et al., (Planta 214:345--355,2002) is used, as there is increasing evidence that in plants MDR/PGPs function as PGPs and not as multiple specificity MDR proteins. Defects in PGP1 and PGP19 (MDR1)genes result in decreased auxin transport and reduced growth phenotypes in Arabidopsis (pgp1, pgp19), maize (br2), and sorghum (dw3). Further, dwarf phenotypes are more severe in Arabidopsis double mutants, indicating that PGPs have overlapping functions. More recently, MDR/PGPs have been shown to function as ATP-activated hydrophobic anion transporters capable of auxin transport. Further, MDR/PGPs have been shown to stabilize PIN1 in detergent-resistant membrane microdomains, and synergistic MDR/PGP-PIN interactions have been shown to increase the rate and specificity of MDR/PGP-mediated auxin transport. Several lines of evidence indicate that, like their mammalian counterparts, Arabidopsis MDR/PGPs are regulated via endocytic cycling. Here we review the evidence for endocytic cycling of MDR/PGPs in planta and provide a model by which this cycling could occur.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Ambudkar S, Dey S, Hrycyna C, Ramachandra M, Pastan I, Gottesman M (1999) Biochemical, cellular, and pharmacological aspects of the multidrug transporter. Annu Rev Pharmacol Toxicol 39:361–398

    Article  Google Scholar 

  2. Baluška F, Hlavacka A, Šamaj J, Palme K, Robinson DG, Matoh T, McCurdy DW, Menzel D, Volkmann D (2002) F-actin-dependent endocytosis of cell wall pectins in meristematic root cells: insights from brefeldin A-induced compartments. Plant Physiol 130:422–431

    Article  PubMed  Google Scholar 

  3. Baumann CA, Saltiel AR (2001) Spatial compartmentalization of signal transduction in insulin action. Bioessays 23:215–222

    Article  PubMed  Google Scholar 

  4. Benkova E, Michniewicz M, Sauer M, Teichmann T, Seifertova D, Jurgens 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 

  5. Bernasconi P, Patel BC, Reagan JD, Subramanian MV (1996) The N-1-naphthylphthalamic acid-binding protein is an integral membrane protein. Plant Physiol 111:427–432

    PubMed  Google Scholar 

  6. Blakeslee JJ, Peer WA, Murphy A (2005) Auxin Transport. Curr Opin Plant Biol (in press)

    Google Scholar 

  7. Blancaflor EB, Masson PH (2003) Plant gravitropism. Unraveling the ups and downs of a complex process. Plant Physiol 133:1677–1690

    Article  PubMed  Google Scholar 

  8. 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  Google Scholar 

  9. Borner GHH, Sherrier DJ, Weimar T, Michaelson LV, Hawkins ND, MacAskill A, Napier JA, Beale MH, Lilley KS, Dupree P (2005) Analysis of detergent-resistant membranes in Arabidopsis. Evidence for plasma membrane lipid rafts. Plant Physiol 137:104–116

    Article  PubMed  Google Scholar 

  10. Borst P, Zelcer N, van Helvoort A (2000) ABC transporters in lipid transport. Biochim Biophys Acta Mol Cell Biol Lipids 1486:128–144

    PubMed  Google Scholar 

  11. Brown DA, London E (1998) Functions of lipid rafts in biological membranes. Annu Rev Cell Dev Biol 14:111–136

    Article  PubMed  Google Scholar 

  12. 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 126:524–535

    Article  PubMed  Google Scholar 

  13. Chen RJ, Hilson P, Sedbrook J, Rosen E, Caspar T, Masson PH (1998) The Arabidopsis thaliana AGRAVITROPIC 1 gene encodes a component of the polar-auxin-transport efflux carrier. Proc Natl Acad Sci USA 95:15112–15117

    Article  PubMed  Google Scholar 

  14. Dixon M, Jacobson J, Cady C, Muday G (1996) Cytoplasmic orientation of the naphthylphthalamic acid-binding protein in zucchini plasma membrane vesicles. Plant Physiol 112:421–432

    PubMed  Google Scholar 

  15. Friml J (2003) Auxin transport–-shaping the plant. Curr Opin Plant Biol 6:7–12

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  20. Fruman D, Meyers R, Cantley L (1998) Phosphoinositide kinases. Annu Rev Biochem 67:481–507

    Article  PubMed  Google Scholar 

  21. Fu D, Bebawy M, Kable E, Roufogalis B (2004) Dynamic and intracellular trafficking of P-glycoprotein-EGFP fusion protein: Implications in multidrug resistance in cancer. Int J Cancer 109:174–181

    Article  PubMed  Google Scholar 

  22. Galweiler L, Guan CH, Muller 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  Google Scholar 

  23. Garrigues A, Escargueil A, Orlowski S (2002) The multidrug transporter, P-glycoprotein, actively mediates cholesterol redistribution in the cell membrane. Proc Natl Acad Sci USA 99:10347–10352

    Article  PubMed  Google Scholar 

  24. 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  Google Scholar 

  25. Geisler M, Blakeslee JJ, Bouchard R, Lee OR, Vincenzetti V, Bandyopadhyay A, Peer WA, Bailly A, Richards EL, Edjendal KF, Smith AP, Baroux C, Grossniklaus U, Muller A, Hrycyna CA, Dudler R, Murphy AS, Martinoia E (2005) Cellular export of auxin by MDR-type ATP-binding cassette transporters of Arabidopsis thaliana. Plant J 44:179–194

    Google Scholar 

  26. Geissler A, Pilet P, Katekar G (1985) Growth and gravireaction of maize roots treated with a phytotropin. J Plant Physiol 119:25–34

    PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  29. 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  Google Scholar 

  30. Hemenway C, Heitman J (1996) Immunosuppressant target protein FKBP12 is required for P-glycoprotein function in yeast. J Biol Chem 271:18527–18534

    Article  PubMed  Google Scholar 

  31. Higgins CF (1992) ABC transporters – from microorganisms to man. Annu Rev Cell Biol 8:67–113

    Article  PubMed  Google Scholar 

  32. Jacobs M, Rubery PH (1988) Naturally-occurring auxin transport regulators. Science 241:346–349

    Google Scholar 

  33. Jasinski M, Ducos E, Martinoia E, Boutry M (2003) The ATP-binding cassette transporters: Structure, function, and gene family comparison between rice and Arabidopsis. Plant Physiol 131:1169–1177

    Article  PubMed  Google Scholar 

  34. Kang BH, Busse JS, Bednarek SY (2003) Members of the Arabidopsis dynamin-like gene family, ADL1, are essential for plant cytokinesis and polarized cell growth. Plant Cell 15:899–913

    Article  PubMed  Google Scholar 

  35. Katekar GF, Geissler AE (1979) Evidence of a common-mode of action for a class of auxin transport inhibitors. Plant Physiol 63:22

    Google Scholar 

  36. Kim H, Barroso M, Samanta R, Greenberger L, Sztul E (1997) Experimentally induced changes in the endocytic traffic of P-glycoprotein alter drug resistance of cancer cells. Am J Physiol Cell Physiol 42:C687–C702

    Google Scholar 

  37. Kipp H, Arias I (2002) Trafficking of canalicular ABC transporters in hepatocytes. Annu Rev Physiol 64:595–608

    Google Scholar 

  38. Kipp H, Pichetshote N, Arias IM (2001) Transporters on demand–- intrahepatic pools of canalicular ATP binding cassette transporters in rat liver. J Biolo Chem 276:7218–7224

    Article  Google Scholar 

  39. Kramer W, Girbig F, Corsiero D, Pfenninger A, Frick W, Jahne G, Rhein M, Wendler W, Lottspeich F, Hochleitner E, Orso E, Schmitz G (2005) Aminopeptidase N (CD13) is a molecular target of the cholesterol absorption inhibitor ezetimibe in the enterocyte brush border membrane. J Biol Chem 280:1306–1320

    Article  PubMed  Google Scholar 

  40. Lavie Y, Liscovitch M (2000) Changes in lipid and protein constituents of rafts and caveolae in multidrug resistant cancer cells and their functional consequences. Glycocon J 17:253–259

    Article  Google Scholar 

  41. Lavie Y, Fiucci G, Liscovitch M (1998) Up-regulation of caveolae and caveolar constituents in multidrug-resistant cancer cells. J Biol Chem 273:32380–32383

    Article  PubMed  Google Scholar 

  42. Locher K (2004) Structure and mechanism of ABC transporters. Curr Opin Struct Biol 14:426–431

    Article  PubMed  Google Scholar 

  43. Locher K, Lee A, Rees D (2002) The E-coli BtuCD structure: A framework for ABC transporter architecture and mechanism. Science 296:1091–1098

    Article  PubMed  Google Scholar 

  44. Lomax TL, Muday GK, Rubery PH (1995) Auxin transport. In: Davies PJ (ed) Plant hormones: physiology, biochemistry, and molecular biology. Kluwer, Dordrecht, The Netherlands, pp 509–530

    Google Scholar 

  45. Loo T, Bartlett M, Clarke D (2005) The dileucine motif at the COOH terminus of human multidrug resistance P-glycoprotein is important for folding but not activity. J Biol Chem 280:2522–2528

    Article  PubMed  Google Scholar 

  46. Luker G, Pica C, Kumar A, Covey D, Piwnica-Worms D (2000) Effects of cholesterol and enantiomeric cholesterol on P-glycoprotein localization and function in low-density membrane domains. Biochemistry 39:7651–7661

    Article  PubMed  Google Scholar 

  47. Martinoia E, Klein M, Geisler M, Bovet L, Forestier C, Kolukisaoglu U, Muller-Rober B, Schultz B (2002) Multifunctionality of plant ABC transporters–-more than just detoxifiers. Planta 214:345–355

    Article  PubMed  Google Scholar 

  48. Mealey K, Barhoumi R, Burghardt R, McIntyre B, Sylvester P, Hosick H, Kochevar D (1999) Immunosuppressant inhibition of P-glycoprotein function is independent of drug-induced suppression of peptide-prolyl isomerase and calcineurin activity. Cancer Chemother Pharmacal 44:152–158

    Google Scholar 

  49. Michalke W, Katekar GF, Geissler AE (1992) Phytotropin-binding sites and auxin transport in Cucurbita-pepo–-evidence for 2 recognition sites. Planta 187:254–260

    Article  Google Scholar 

  50. Mongrand S, Morel J, Laroche J, Claverol S, Carde JP, Hartmann MA, Bonneu M, Simon-Plas F, Lessire R, Bessoule JJ (2004) Lipid rafts in higher plant cells: purification and characterization of Triton X-100-insoluble microdomains from tobacco plasma membrane. J Biol Chem 279:36277–36286

    Article  PubMed  Google Scholar 

  51. Muday GK, Murphy AS (2002) An emerging model of auxin transport regulation. Plant Cell 14:293–299

    Article  PubMed  Google Scholar 

  52. Muday GK, Peer WA, Murphy AS (2003) Vesicular cycling mechanisms that control auxin transport polarity. Trends Plant Sci 8:301–304

    Article  PubMed  Google Scholar 

  53. Muller A, Guan CH, Galweiler 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 

  54. 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  Google Scholar 

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

    Article  PubMed  Google Scholar 

  56. Murphy A, Taiz L (1999) Naphthylphthalamic acid is enzymatically hydrolyzed at the hypocotyl-root transition zone and other tissues of Arabidopsis thaliana seedlings. Plant Physiol Biochem 37:413–430

    Article  Google Scholar 

  57. Murphy A, Taiz L (1999) Localization and characterization of soluble and plasma membrane aminopeptidase activities in Arabidopsis seedlings. Plant Physiol Biochem 37:431–443

    Article  Google Scholar 

  58. 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  Google Scholar 

  59. 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  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  62. Palme K, Galweiler L (1999) PIN-pointing the molecular basis of auxin transport. Curr Opin Plant Biol 2:375–381

    Article  PubMed  Google Scholar 

  63. Peer WA, Brown DE, Tague BW, Muday GK, Taiz L, Murphy AS (2001) Flavonoid accumulation patterns of transparent testa mutants of Arabidopsis. Plant Physiol 126:536–548

    Article  PubMed  Google Scholar 

  64. Peterman T, Ohol Y, McReynolds L, Luna E (2004) Patellin1, a novel Sec14-like protein, localizes to the cell plate and binds phosphoinositides. Plant Physiol 136:3080–3094

    Article  PubMed  Google Scholar 

  65. Petrasek J, Cerna A, Schwarzerova K, Elckner M, Morris DA, Zazimalova E (2003) Do phytotropins inhibit auxin efflux by impairing vesicle traffic? Plant Physiol 131:254–263

    Article  PubMed  Google Scholar 

  66. Šamaj J, Baluška F, Voigt B, Schlicht M, Volkmann D, Menzel D (2004) Endocytosis, actin cytoskeleton and signaling. Plant Physiol 135:1150–1161

    Article  PubMed  Google Scholar 

  67. Shogomori H, Brown D (2003) Use of detergents to study membrane rafts: The good, the bad, and the ugly. Biol Chem 384:1259–1263

    Article  PubMed  Google Scholar 

  68. 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

    Article  PubMed  Google Scholar 

  69. Swarup R, Bennett M (2003) Auxin transport: The fountain of life in plants? Dev Cell 5:824–826

    Article  PubMed  Google Scholar 

  70. 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. Gen Dev 15:2648–2653

    Article  Google Scholar 

  71. Terasaka K, Blakeslee JJ, Bandyopadhyay A, Peer WA, Murphy AS, Sato F, Yazaki K (2005) Involvement of AtPGP4, a P-glycoprotein-type ATP binding cassette protein, in the root basipetal auxin transport in Arabidopsis thaliana. Plant Cell (submitted)

    Google Scholar 

  72. Troost J, Lindenmaier H, Haefeli W, Weiss J (2004) Modulation of cellular cholesterol alters P-glycoprotein activity in multidrug-resistant cells. Mol Pharmacol 66:1332–1339

    Article  PubMed  Google Scholar 

  73. vanHelvoort A, Smith A, Sprong H, Fritzsche I, Schinkel A, Borst P, vanMeer G (1996) MDR1 P-glycoprotein is a lipid translocase of broad specificity, while MDR3 P-glycoprotein specifically translocates phosphatidylcholine. Cell 87:507–517

    Article  PubMed  Google Scholar 

  74. von Rozycki T, Schultzel M, Saier M (2004) Sequence analyses of cyanobacterial bicarbonate transporters and their homologues. J Mol Microbiol Biotech 7:102–108

    Article  Google Scholar 

  75. Wang E, Casciano C, Clement R, Johnson W (2000) Cholesterol interaction with the daunorubicin binding site of P-glycoprotein. Biochem Biophys Res Commun 276:909–916

    Article  PubMed  Google Scholar 

  76. Yazaki K, Shitan N, Takamatsu H, Ueda K, Sato F (2001) A novel Coptis japonica multidrug-resistant protein preferentially expressed in the alkaloid-accumulating rhizome. J Exp Bot 52:877–879

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Horticulture, Purdue University, IN 47907, West Lafayette, USA

    Joshua J. Blakeslee, Wendy Ann Peer & Angus S. Murphy

Authors
  1. Joshua J. Blakeslee
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wendy Ann Peer
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Angus S. Murphy
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Angus S. Murphy .

Editor information

Jozef Šamaj František Baluška Diedrik Menzel

Rights and permissions

Reprints and permissions

About this chapter

Cite this chapter

Blakeslee, J.J., Peer, W.A., Murphy, A.S. MDR/PGP Auxin Transport Proteins and Endocytic Cycling. In: Šamaj, J., Baluška, F., Menzel, D. (eds) Plant Endocytosis. Plant Cell Monographs, vol 1. Springer, Berlin, Heidelberg. https://doi.org/10.1007/7089_010

Download citation

Publish with us

Policies and ethics

Search

Navigation