Skip to main content

It Takes More Than Two to Tango: Regulation of Plant ABC Transporters

  • Chapter
  • First Online:
Book cover Plant ABC Transporters

Part of the book series: Signaling and Communication in Plants ((SIGCOMM,volume 22))

Abstract

ABC transporters require a tight regulation of their transport activity as they often distribute substrates that are either toxic or of metabolic or developmental function. Moreover in contrast to secondary active transporters or channels they represent in energetic terms rather inefficient ATP-consuming nano-machines.

The regulation of mammalian ABC transporters has been deeply investigated in the last three decades because malfunction of many ABC transporters is causing socially and economically relevant diseases. However, despite their striking over-representation and their emerging important developmental and physiological function, surprisingly few is so far known on the regulation of plant ABCs. Therefore, in this chapter we have compared our recent knowledge on plant and non-plant ABC transporters in respect to their post-transcriptional regulation. Despite the limited information on plant ABC regulation it becomes more and more clear that many—if not all—regulatory mechanisms found for mammalian ABC transporters are also found in plants. We highlight in more detail some interesting examples on Arabidopsis ABCB regulation where plant research provided a deep and integrated understanding of ABC regulation that might serve as a blueprint for clinical research.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Ambudkar SV, Kimchi-Sarfaty C, Sauna ZE, Gottesman MM (2003) P-glycoprotein: from genomics to mechanism. Oncogene 22:7468–7485

    CAS  PubMed  Google Scholar 

  • Bacso Z, Nagy H, Goda K, Bene L, Fenyvesi F, Matko J, Szabo G (2004) Raft and cytoskeleton associations of an ABC transporter: P-glycoprotein. Cytometry A 61:105–116

    PubMed  Google Scholar 

  • Bailly A, Yang H, Martinoia E, Geisler M, Murphy AS (2011) Plant lessons: exploring ABCB functionality through structural modeling. Front Plant Sci 2:108

    PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Bailly A, Wang B, Zwiewka M, Pollmann S, Schenck D, Luthen H, Schulz A, Friml J, Geisler M (2013) Expression of TWISTED DWARF1 lacking its in-plane membrane anchor leads to increased cell elongation and hypermorphic growth. Plant J 77:108–118

    PubMed  Google Scholar 

  • Banasavadi-Siddegowda YK, Mai J, Fan Y, Bhattacharya S, Giovannucci DR, Sanchez ER, Fischer G, Wang X (2011) FKBP38 peptidylprolyl isomerase promotes the folding of cystic fibrosis transmembrane conductance regulator in the endoplasmic reticulum. J Biol Chem 286:43071–43080

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • 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 6:1198–1214

    CAS  PubMed  Google Scholar 

  • Bessadok A, Garcia E, Jacquet H, Martin S, Garrigues A, Loiseau N, Andre F, Orlowski S, Vivaudou M (2011) Recognition of sulfonylurea receptor (ABCC8/9) ligands by the multidrug resistance transporter P-glycoprotein (ABCB1): functional similarities based on common structural features between two multispecific ABC proteins. J Biol Chem 286:3552–3569

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Borner GH, 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

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Bozoky Z, Krzeminski M, Chong PA, Forman-Kay JD (2013) Structural changes of CFTR R region upon phosphorylation: a plastic platform for intramolecular and intermolecular interactions. FEBS J 280:4407–4416

    CAS  PubMed  Google Scholar 

  • Breier A, Gibalova L, Seres M, Barancik M, Sulova Z (2013) New insight into p-glycoprotein as a drug target. Anticancer Agents Med Chem 13:159–170

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Buer CS, Djordjevic MA (2009) Architectural phenotypes in the transparent testa mutants of Arabidopsis thaliana. J Exp Bot 60:751–763

    CAS  PubMed Central  PubMed  Google Scholar 

  • Buer CS, Muday GK, Djordjevic MA (2007) Flavonoids are differentially taken up and transported long distances in Arabidopsis. Plant Physiol 145:478–490

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 6:185–188

    CAS  PubMed  Google Scholar 

  • Calcagno AM, Kim IW, Wu CP, Shukla S, Ambudkar SV (2007) ABC drug transporters as molecular targets for the prevention of multidrug resistance and drug-drug interactions. Curr Drug Deliv 4:324–333

    CAS  PubMed  Google Scholar 

  • Cameron AM, Steiner JP, Sabatini DM, Kaplin AI, Walensky LD, Snyder SH (1995) Immunophilin FK506 binding protein associated with inositol 1,4,5-trisphosphate receptor modulates calcium flux. Proc Natl Acad Sci U S A 92:1784–1788

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cant N, Pollock N, Ford RC (2014) CFTR structure and cystic fibrosis. Int J Biochem Cell Biol. doi:10.1016/j.biocel.2014.02.004

    PubMed  Google Scholar 

  • Cho M, Cho HT (2012) The function of ABCB transporters in auxin transport. Plant Signal Behav 8

    Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 U S A 95:9831–9836

    CAS  PubMed Central  PubMed  Google Scholar 

  • Czar MJ, Galigniana MD, Silverstein AM, Pratt WB (1997) Geldanamycin, a heat shock protein 90-binding benzoquinone ansamycin, inhibits steroid-dependent translocation of the glucocorticoid receptor from the cytoplasm to the nucleus. Biochemistry 36:7776–7785

    CAS  PubMed  Google Scholar 

  • Dahan D, Evagelidis A, Hanrahan JW, Hinkson DA, Jia Y, Luo J, Zhu T (2001) Regulation of the CFTR channel by phosphorylation. Pflugers Archiv 443(Suppl 1):S92–96

    CAS  PubMed  Google Scholar 

  • Dawson RJ, Locher KP (2007) Structure of the multidrug ABC transporter Sav 1866 from Staphylococcus aureus in complex with AMP-PNP. FEBS Lett 581:935–938

    CAS  PubMed  Google Scholar 

  • 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 34:3267–3278

    CAS  PubMed  Google Scholar 

  • Diop NK, Hrycyna CA (2005) N-Linked glycosylation of the human ABC transporter ABCG2 on asparagine 596 is not essential for expression, transport activity, or trafficking to the plasma membrane. Biochemistry 44:5420–5429

    CAS  PubMed  Google Scholar 

  • Dos Santos SM, Weber CC, Franke C, Muller WE, Eckert GP (2007) Cholesterol: coupling between membrane microenvironment and ABC transporter activity. Biochem Biophys Res Commun 354:216–221

    Google Scholar 

  • Edlich F, Lucke C (2011) From cell death to viral replication: the diverse functions of the membrane-associated FKBP38. Curr Opin Pharmacol 11:1–6

    Google Scholar 

  • 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 24:2688–2699

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 282:36496–36504

    CAS  PubMed  Google Scholar 

  • Feraru E, Friml J (2008) PIN polar targeting. Plant Physiol 147:1553–1559

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gadsby DC, Vergani P, Csanady L (2006) The ABC protein turned chloride channel whose failure causes cystic fibrosis. Nature 440:477–483

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Geisler M, Bailly A (2007) Tete-a-tete: the function of FKBPs in plant development. Trends Plant Sci 12:465–473

    CAS  PubMed  Google Scholar 

  • Geisler M, Bailly A (2008) Tête-à-tête: FKBPs function as key players in plant development. Trends Plant Sci 12:465–73

    Google Scholar 

  • Geisler M, Henrichs S (2013) Regulation of polar auxin transport by protein-protein interactions. In: Chen R, Baluška F (eds) Signaling and communication in polar auxin transport. Springer, Berlin

    Google Scholar 

  • Geisler M, Wang B, Zhu J (2014) Auxin transport during root gravitropism: transporters and techniques. Plant Biol 16(Suppl 1):50–57

    PubMed  Google Scholar 

  • 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 15:3393–3405

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Geisler M, Blakeslee JJ, Bouchard R, Lee OR, Vincenzetti V, Bandyopadhyay A, Titapiwatanakun B, Peer WA, Bailly A, Richards EL, Ejendal KF, Smith AP, Baroux C, Grossniklaus U, 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 44:179–194

    CAS  PubMed  Google Scholar 

  • Geldner N, Richter S, Vieten A, Marquardt S, Torres-Ruiz RA, Mayer U, Jurgens G (2004) Partial loss-of-function alleles reveal a role for GNOM in auxin transport-related, post-embryonic development of Arabidopsis. Development 131:389–400

    CAS  PubMed  Google Scholar 

  • Giblin JP, Quinn K, Tinker A (2002) The cytoplasmic C-terminus of the sulfonylurea receptor is important for KATP channel function but is not key for complex assembly or trafficking. Eur J Biochem 269:5303–5313

    CAS  PubMed  Google Scholar 

  • 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 15:1985–1997

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 364:799–809

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Henrichs S, Wang B, Fukao Y, Zhu J, Charrier L, Bailly A, Oehring SC, Linnert M, Weiwad M, Endler A, Nanni P, Pollmann S, Mancuso S, Schulz A, Geisler M (2012) Regulation of ABCB1/PGP1-catalysed auxin transport by linker phosphorylation. EMBO J 31:2965–80. doi:10.1038/emboj.2012.120

    CAS  PubMed Central  PubMed  Google Scholar 

  • Higgins CF (2007) Multiple molecular mechanisms for multidrug resistance transporters. Nature 446:749–757

    CAS  PubMed  Google Scholar 

  • Ismair MG, Hausler S, Stuermer CA, Guyot C, Meier PJ, Roth J, Stieger B (2009) ABC-transporters are localized in caveolin-1-positive and reggie-1-negative and reggie-2-negative microdomains of the canalicular membrane in rat hepatocytes. Hepatology 49:1673–1682

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Jurgens G, Geldner N (2007) The high road and the low road: trafficking choices in plants. Cell 130:977–979

    PubMed  Google Scholar 

  • Kamimoto Y, Terasaka K, Hamamoto M, Takanashi K, Fukuda S, Shitan N, Sugiyama A, Suzuki H, Shibata D, Wang B, Pollmann S, Geisler M, Yazaki K (2012) Arabidopsis ABCB21 is a facultative auxin importer/exporter regulated by cytoplasmic auxin concentration. Plant Cell Physiol 53:2090–2100

    CAS  PubMed  Google Scholar 

  • 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 32:263–276

    CAS  PubMed  Google Scholar 

  • Kanelis V, Chong PA, Forman-Kay JD (2011) NMR spectroscopy to study the dynamics and interactions of CFTR. Methods Mol Biol 741:377–403

    CAS  PubMed  Google Scholar 

  • Kanelis V, Hudson RP, Thibodeau PH, Thomas PJ, Forman-Kay JD (2010) NMR evidence for differential phosphorylation-dependent interactions in WT and DeltaF508 CFTR. EMBO J 29:263–277

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kang J, Hwang JU, Lee M, Kim YY, Assmann SM, Martinoia E, Lee Y (2010) PDR-type ABC transporter mediates cellular uptake of the phytohormone abscisic acid. Proc Natl Acad Sci U S A 107:2355–2360

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kepinski S, Leyser O (2005) Plant development: auxin in loops. Curr Biol 15:R208–210

    CAS  PubMed  Google Scholar 

  • 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 285:23309–23317

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kipp H, Arias IM (2000) Intracellular trafficking and regulation of canalicular ATP-binding cassette transporters. Semin Liver Dis 20:339–351

    CAS  PubMed  Google Scholar 

  • Klappe K, Hummel I, Hoekstra D, Kok JW (2009) Lipid dependence of ABC transporter localization and function. Chem Phys Lipids 161:57–64

    CAS  PubMed  Google Scholar 

  • Klein M, Burla B, Martinoia E (2006) The multidrug resistance-associated protein (MRP/ABCC) subfamily of ATP-binding cassette transporters in plants. FEBS Lett 580:1112–1122

    CAS  PubMed  Google Scholar 

  • Klein M, Perfus-Barbeoch L, Frelet A, Gaedeke N, Reinhardt D, Mueller-Roeber B, Martinoia E, Forestier C (2003) The plant multidrug resistance ABC transporter AtMRP5 is involved in guard cell hormonal signalling and water use. Plant J 33:119–129

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Kretzschmar T, Kohlen W, Sasse J, Borghi L, Schlegel M, Bachelier JB, Reinhardt D, Bours R, Bouwmeester HJ, Martinoia E (2012) A petunia ABC protein controls strigolactone-dependent symbiotic signalling and branching. Nature 483:341–344

    CAS  PubMed  Google Scholar 

  • Kuromori T, Miyaji T, Yabuuchi H, Shimizu H, Sugimoto E, Kamiya A, Moriyama Y, Shinozaki K (2010) ABC transporter AtABCG25 is involved in abscisic acid transport and responses. Proc Natl Acad Sci U S A 107:2361–2366

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lalonde S, Ehrhardt DW, Loque D, Chen J, Rhee SY, Frommer WB (2008) Molecular and cellular approaches for the detection of protein-protein interactions: latest techniques and current limitations. Plant J 53:610–635

    CAS  PubMed  Google Scholar 

  • 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 1:24

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lam P, Xu S, Soroka CJ, Boyer JL (2012) A C-terminal tyrosine-based motif in the bile salt export pump directs clathrin-dependent endocytosis. Hepatology 55:1901–1911

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Laude AJ, Prior IA (2004) Plasma membrane microdomains: organization, function and trafficking. Mol Membr Biol 21:193–205

    CAS  PubMed Central  PubMed  Google Scholar 

  • Leonhardt N, Vavasseur A, Forestier C (1999) ATP binding cassette modulators control abscisic acid-regulated slow anion channels in guard cells. Plant Cell 11:1141–1152

    CAS  PubMed Central  PubMed  Google Scholar 

  • Li C, Naren AP (2011) Analysis of CFTR interactome in the macromolecular complexes. Methods Mol Biol 741:255–270

    CAS  PubMed Central  PubMed  Google Scholar 

  • Li Y, Prinz WA (2004) ATP-binding cassette (ABC) transporters mediate nonvesicular, raft-modulated sterol movement from the plasma membrane to the endoplasmic reticulum. J Biol Chem 279:45226–45234

    CAS  PubMed  Google Scholar 

  • Lievens S, Eyckerman S, Lemmens I, Tavernier J (2010) Large-scale protein interactome mapping: strategies and opportunities. Expert Rev Proteomics 7:679–690

    CAS  PubMed  Google Scholar 

  • Linton KJ (2007) Structure and function of ABC transporters. Physiology (Bethesda) 22:122–130

    CAS  Google Scholar 

  • Loo TW, Clarke DM (1997) Identification of residues in the drug-binding site of human P-glycoprotein using a thiol-reactive substrate. J Biol Chem 272:31945–31948

    CAS  PubMed  Google Scholar 

  • Luschnig C (2001) Auxin transport: why plants like to think BIG. Curr Biol 11:R831–833

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Miller G (2006) Scientific publishing. A scientist’s nightmare: software problem leads to five retractions. Science 314:1856–1857

    CAS  PubMed  Google Scholar 

  • Modok S, Mellor HR, Callaghan R (2006) Modulation of multidrug resistance efflux pump activity to overcome chemoresistance in cancer. Curr Opin Pharmacol 6:350–354

    CAS  PubMed  Google Scholar 

  • Mohrmann K, van Eijndhoven MA, Schinkel AH, Schellens JH (2005) Absence of N-linked glycosylation does not affect plasma membrane localization of breast cancer resistance protein (BCRP/ABCG2). Cancer Chemother Pharmacol 56:344–350

    CAS  PubMed  Google Scholar 

  • Monterisi S, Casavola V, Zaccolo M (2013) Local modulation of cystic fibrosis conductance regulator: cytoskeleton and compartmentalized cAMP signalling. Br J Pharmacol 169:1–9

    CAS  PubMed Central  PubMed  Google Scholar 

  • Morita M, Imanaka T (2012) Peroxisomal ABC transporters: structure, function and role in disease. Biochim Biophys Acta 1822:1387–1396

    CAS  PubMed  Google Scholar 

  • Morris DA (2000) Transmembrane auxin carrier systems–dynamic regulators of polar auxin transport. Plant Growth Regul 32:161–172

    CAS  PubMed  Google Scholar 

  • Morris ME, Zhang S (2006) Flavonoid-drug interactions: effects of flavonoids on ABC transporters. Life Sci 78:2116–2130

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nuhse TS, Stensballe A, Jensen ON, Peck SC (2004) Phosphoproteomics of the Arabidopsis plasma membrane and a new phosphorylation site database. Plant Cell 16:2394–2405

    PubMed Central  PubMed  Google Scholar 

  • Odolczyk N, Fritsch J, Norez C, Servel N, da Cunha MF, Bitam S, Kupniewska A, Wiszniewski L, Colas J, Tarnowski K, Tondelier D, Roldan A, Saussereau EL, Melin-Heschel P, Wieczorek G, Lukacs GL, Dadlez M, Faure G, Herrmann H, Ollero M, Becq F, Zielenkiewicz P, Edelman A (2013) Discovery of novel potent DeltaF508-CFTR correctors that target the nucleotide binding domain. EMBO Mol Med 5:1484–1501

    CAS  PubMed Central  PubMed  Google Scholar 

  • Park J, Song WY, Ko D, Eom Y, Hansen TH, Schiller M, Lee TG, Martinoia E, Lee Y (2012) The phytochelatin transporters AtABCC1 and AtABCC2 mediate tolerance to cadmium and mercury. Plant J 69:278–288

    CAS  PubMed  Google Scholar 

  • Paumi CM, Chuk M, Snider J, Stagljar I, Michaelis S (2009) ABC transporters in Saccharomyces cerevisiae and their interactors: new technology advances the biology of the ABCC (MRP) subfamily. Microbiol Mol Biol Rev 73:577–593

    CAS  PubMed Central  PubMed  Google Scholar 

  • Paumi CM, Menendez J, Arnoldo A, Engels K, Iyer KR, Thaminy S, Georgiev O, Barral Y, Michaelis S, Stagljar I (2007) Mapping protein-protein interactions for the yeast ABC transporter Ycf1p by integrated split-ubiquitin membrane yeast two-hybrid analysis. Mol Cell 26:15–25

    CAS  PubMed  Google Scholar 

  • Peck SC (2006) Phosphoproteomics in Arabidopsis: moving from empirical to predictive science. J Exp Bot 57:1523–1527

    CAS  PubMed  Google Scholar 

  • Peer WA, Murphy AS (2006) Flavonoids as signal molecules. Targets of flavonoid action. In: Grotewold E (ed) The science of flavonoids. Springer, Berlin, pp 239–268

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Peterson LB, Eskew JD, Vielhauer GA, Blagg BS (2012) The hERG channel is dependent upon the Hsp90alpha isoform for maturation and trafficking. Mol Pharm 9:1841–1846

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 312:914–918

    CAS  PubMed  Google Scholar 

  • Quazi F, Molday RS (2011) Lipid transport by mammalian ABC proteins. Essays Biochem 50:265–290

    CAS  PubMed  Google Scholar 

  • Radeva G, Perabo J, Sharom FJ (2005) P-Glycoprotein is localized in intermediate-density membrane microdomains distinct from classical lipid rafts and caveolar domains. FEBS J 272:4924–4937

    CAS  PubMed  Google Scholar 

  • Ranocha P, Dima O, Nagy R, Felten J, Corratge-Faillie C, Novak O, Morreel K, Lacombe B, Martinez Y, Pfrunder S, Jin X, Renou JP, Thibaud JB, Ljung K, Fischer U, Martinoia E, Boerjan W, Goffner D (2013) Arabidopsis WAT1 is a vacuolar auxin transport facilitator required for auxin homoeostasis. Nat Commun 4:2625

    PubMed Central  PubMed  Google Scholar 

  • Rea PA (2007) Plant ATP-binding cassette transporters. Annu Rev Plant Biol 58:347–375

    CAS  PubMed  Google Scholar 

  • 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 14:1366–1376

    CAS  PubMed  Google Scholar 

  • Rumsby MG, Drew L, Warr JR (1998) Protein kinases and multidrug resistance. Cytotechnology 27:203–224

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ruzicka K, Strader LC, Bailly A, Yang H, Blakeslee J, Langowski L, Nejedla E, Fujita H, Itoh H, Syono K, Hejatko J, Gray WM, Martinoia E, Geisler M, Bartel B, Murphy AS, Friml J (2010) Arabidopsis PIS1 encodes the ABCG37 transporter of auxinic compounds including the auxin precursor indole-3-butyric acid. Proc Natl Acad Sci U S A 107:10749–10753

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sanchez-Fernandez R, Davies TGE, Coleman JOD, Rea PA (2001) The Arabidopsis thaliana ABC protein superfamily, a complete inventory. J Biol Chem 276:30231–30244

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sauna ZE, Kim IW, Ambudkar SV (2007) Genomics and the mechanism of P-glycoprotein (ABCB1). J Bioenerg Biomembr 39:481–487

    CAS  PubMed  Google Scholar 

  • 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 36:393–404

    CAS  PubMed  Google Scholar 

  • Seino S, Takahashi H, Takahashi T, Shibasaki T (2012) Treating diabetes today: a matter of selectivity of sulphonylureas. Diabetes Obes Metab 14(Suppl 1):9–13

    CAS  PubMed  Google Scholar 

  • Shapiro AB, Ling V (1995) Reconstitution of drug transport by purified P-glycoprotein. J Biol Chem 270:16167–16175

    CAS  PubMed  Google Scholar 

  • Shirane M, Nakayama KI (2003) Inherent calcineurin inhibitor FKBP38 targets Bcl-2 to mitochondria and inhibits apoptosis. Nat Cell Biol 5:28–37

    CAS  PubMed  Google Scholar 

  • Sinko E, Ilias A, Ujhelly O, Homolya L, Scheffer GL, Bergen AA, Sarkadi B, Varadi A (2003) Subcellular localization and N-glycosylation of human ABCC6, expressed in MDCKII cells. Biochem Biophys Res Commun 308:263–269

    CAS  PubMed  Google Scholar 

  • Skach WR (2006) CFTR: new members join the fold. Cell 127:673–675

    CAS  PubMed  Google Scholar 

  • Snider J, Hanif A, Lee ME, Jin K, Yu AR, Graham C, Chuk M, Damjanovic D, Wierzbicka M, Tang P, Balderes D, Wong V, Jessulat M, Darowski KD, San Luis BJ, Shevelev I, Sturley SL, Boone C, Greenblatt JF, Zhang Z, Paumi CM, Babu M, Park HO, Michaelis S, Stagljar I (2013) Mapping the functional yeast ABC transporter interactome. Nat Chem Biol 9:565–572

    CAS  PubMed  Google Scholar 

  • Stolarczyk EI, Reiling CJ, Paumi CM (2011) Regulation of ABC transporter function via phosphorylation by protein kinases. Curr Pharm Biotechnol 12:621–635

    CAS  PubMed Central  PubMed  Google Scholar 

  • Storch CH, Ehehalt R, Haefeli WE, Weiss J (2007) Localization of the human breast cancer resistance protein (BCRP/ABCG2) in lipid rafts/caveolae and modulation of its activity by cholesterol in vitro. J Pharmacol Exp Therap 323:257–264

    CAS  Google Scholar 

  • Storer CL, Dickey CA, Galigniana MD, Rein T, Cox MB (2011) FKBP51 and FKBP52 in signaling and disease. Trend Endocrinol Metabol 22:481–490

    CAS  Google Scholar 

  • Strader LC, Bartel B (2009) The Arabidopsis PLEIOTROPIC DRUG RESISTANCE8/ABCG36 ATP binding cassette transporter modulates sensitivity to the auxin precursor indole-3-butyric acid. Plant Cell 21:1992–2007

    CAS  PubMed Central  PubMed  Google Scholar 

  • Strader LC, Bartel B (2011) Transport and metabolism of the endogenous auxin precursor indole-3-butyric acid. Mol Plant 4:477–486

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 272:23165–23171

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Theodoulou FL (2000) Plant ABC transporters. Biochimica Et Biophysica Acta-Biomembranes 1465:79–103

    CAS  Google Scholar 

  • Timerman AP, Wiederrecht G, Marcy A, Fleischer S (1995) Characterization of an exchange reaction between soluble FKBP-12 and the FKBP.ryanodine receptor complex. Modulation by FKBP mutants deficient in peptidyl-prolyl isomerase activity. J Biol Chem 270:2451–2459

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Walker VE, Atanasiu R, Lam H, Shrier A (2007) Co-chaperone FKBP38 promotes HERG trafficking. J Biol Chem 282:23509–23516

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Weiergraber OH, Eckhoff A, Granzin J (2006) Crystal structure of a plant immunophilin domain involved in regulation of MDR-type ABC transporters. FEBS Lett 580:251–255

    PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Williams RJ, Spencer JPE, Rice-Evans C (2004) Flavonoids: antioxidants or signalling molecules? Free Rad Biol Med 36:838–849

    CAS  PubMed  Google Scholar 

  • 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 22:3295–3304

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Yang H, Richter GL, Wang X, Mlodzinska E, Carraro N, Ma G, Jenness M, Chao DY, Peer WA, Murphy AS (2013) Sterols and sphingolipids differentially function in trafficking of the Arabidopsis ABCB19 auxin transporter. Plant J 74:37–47

    CAS  PubMed  Google Scholar 

  • Yun UJ, Lee JH, Koo KH, Ye SK, Kim SY, Lee CH, Kim YN (2013) Lipid raft modulation by Rp1 reverses multidrug resistance via inactivating MDR-1 and Src inhibition. Biochem Pharmacol 85:1441–1453

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The geislerLab is supported by funds of the University of Fribourg (Pool de Recherche), of the Novartis Foundation and the SNF. The author thanks Martin di Donato for critically reading the text.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Markus Geisler .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Geisler, M. (2014). It Takes More Than Two to Tango: Regulation of Plant ABC Transporters. In: Geisler, M. (eds) Plant ABC Transporters. Signaling and Communication in Plants, vol 22. Springer, Cham. https://doi.org/10.1007/978-3-319-06511-3_13

Download citation

Publish with us

Policies and ethics