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Signaling in Polar Auxin Transport

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Polar Auxin Transport

Part of the book series: Signaling and Communication in Plants ((SIGCOMM,volume 17))

Abstract

Polar auxin transport, directionally delivering auxin and generating local auxin gradients, is pivotal to fundamental developmental processes in plants. The directional auxin flow is attributable to polar-localized auxin transporters. In particular, over the past several years, the cytological and molecular mechanisms of how auxin transporters distribute asymmetrically in the plasma membrane have become greatly understood. The cellular polarity players for auxin transporters include intracellular trafficking components, cargo phosphorylation cues and corresponding kinases, membrane lipid composition, ubiquitylation, and extracellular auxin receptor-mediated modulation of cytoskeleton. In addition to these internal polarity regulators, other major plant hormones, signaling molecules, environmental stimuli, and nutrients have been implicated in regulation of auxin transporters, reflecting the communication between diverse developmental/environmental signals and auxin-mediated plant development. In this chapter, we review the recent studies that have elucidated the regulatory mechanisms of auxin transport.

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References

  • Abas L, Benjamins R, Malenica N, Paciorek T, Wisniewska J, Moulinier-Anzola JC, Sieberer T, Friml J, Luschnig C (2006) Intracellular trafficking and proteolysis of the Arabidopsis auxin-efflux facilitator PIN2 are involved in root gravitropism. Nat Cell Biol 8:249–256

    CAS  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 

  • 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 35:137–141

    CAS  PubMed  Google Scholar 

  • Barbez E, Kubeš M, Rolčík J, Béziat C, Pěnčík A, Wang B, Rosquete MR, Zhu J, Dobrev PI, Lee Y, Zažímalovà E, Petrášek J, Geisler M, Friml J, Kleine-Vehn J (2012) A novel putative auxin carrier family regulates intracellular auxin homeostasis in plants. Nature 485:119–122

    CAS  PubMed  Google Scholar 

  • Benjamins R, Quint A, Weijers D, Hooykaas P, Offringa R (2001) The PINOID protein kinase regulates organ development in Arabidopsis by enhancing polar auxin transport. Development 128:4057–4067

    CAS  PubMed  Google Scholar 

  • Benjamins R, Ampudia CS, Hooykaas PJ, Offringa R (2003) PINOID-mediated signaling involves calcium-binding proteins. Plant Physiol 132:1623–1630

    CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Bennett MJ, Marchant A, Green HG, May ST, Ward SP, Millner PA, Walker AR, Schulz B, Feldmann KA (1996) Arabidopsis AUX1 gene: a permease-like regulator of root gravitropism. Science 273:948–950

    CAS  PubMed  Google Scholar 

  • Bishopp A, Help H, El-Showk S, Weijers D, Scheres B, Friml J, Benkova E, Mahonen AP, Helariutta Y (2011) Mutually inhibitory interaction between auxin and cytokinin specifies vascular pattern in roots. Curr Biol 21:917–926

    CAS  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  Google Scholar 

  • Blilou I, Xu J, Wildwater M, Willemsen V, Paponov I, Friml J, Heidstra R, Aida M, Palme K, Scheres B (2005) The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433:39–44

    CAS  PubMed  Google Scholar 

  • Bögre L, Okrész L, Henriques R, Anthony RG (2003) Growth signalling pathways in Arabidopsis and the AGC protein kinases. Trends Plant Sci 8:424–431

    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  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 

  • Brown DA, London E (2000) Structure and function of sphingolipid-and cholesterol-rich membrane rafts. J Cell Biol 275:17221–17224

    CAS  Google Scholar 

  • Carland FM, Fujioka S, Nelson T (2010) The sterol methyltransferases SMT1, SMT2, and SMT3 influence Arabidopsis development through non-brassinosteroid products. Plant Physiol 153: 741–756

    CAS  PubMed  Google Scholar 

  • Chen R, 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

    CAS  PubMed  Google Scholar 

  • Cho M, Lee OR, Ganguly A, Cho H-T (2007a) Auxin-signaling: short and long. J Plant Biol 50: 79–89

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Cho M, Lee J, Cho H-T (2012) ATP-Binding cassette b4, an auxin-efflux transporter, stably associates with the plasma membrane and shows distinctive intracellular trafficking from that of PIN-FORMEDs. Plant Physiol 159:642–654

    CAS  PubMed  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  Google Scholar 

  • Dal Bosco C, 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. doi:10.1111/j.1365-313X.2012.05037.x

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

    Google Scholar 

  • Delbarre A, Muller P, Guern J (1998) Short-lived and phosphorylated proteins contribute to carrier-mediated efflux. Plant Physiol 116:833–844

    CAS  PubMed  Google Scholar 

  • DelloIoio R, Linhares FS, Scacchi E, Casamitjana-Martinez E, Heidstra R, Costantino P, Sabatini S (2007) Cytokinins determine Arabidopsis root-meristem size by controlling cell differentiation. Curr Biol 17:678–682

    CAS  Google Scholar 

  • DelloIoio R, Nakamura K, Moubayidin L, Perilli S, Taniguchi M, Morita MT, Aoyama T, Costantino P, Sabatini S (2008) A genetic framework for the control of cell division and differentiation in the root meristem. Science 322:1380–1384

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Dhonukshe P, Baluska F, Schlicht M, Hlavacka A, Samaj J, Friml J, Gadella TW Jr (2006) Endocytosis of cell surface material mediates cell plate formation during plant cytokinesis. Dev Cell 10:137–150

    CAS  PubMed  Google Scholar 

  • Dhonukshe P, Tanaka H, Goh T, Ebine K, Mahonen AP, Prasad K, Blilou I, Geldner N, Xu J, Uemura T, Chory J, Ueda T, Nakano A, Scheres B, Friml J (2008) Generation of cell polarity in plants links endocytosis, auxin distribution and cell fate decisions. Nature 456:962–966

    CAS  PubMed  Google Scholar 

  • Dhonukshe P, Huang F, Galvan-Ampudia CS, Mähönen 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 137:3245–3255

    CAS  PubMed  Google Scholar 

  • Ding Z, Galván-Ampudia CS, Demarsy E, Łangowski Ł, 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 13:447–452

    CAS  PubMed  Google Scholar 

  • 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, Orellana A, Geisler M, Friml J (2012) ER-localized auxin transporter PIN8 regulates auxin homeostasis and male gametophyte development in Arabidopsis. Nat Commun 3:941. doi:10.1038/ncomms1941

    PubMed  Google Scholar 

  • Donaldson JG, Jackson CL (2000) Regulators and effectors of the ARF GTPases. Curr Opin Cell Biol 12:475–482

    CAS  PubMed  Google Scholar 

  • Ebine K, Fujimoto M, Okatani Y, Nishiyama T, Goh T, Ito E, Dainobu T, Nishitani A, Uemura T, Sato MH, Thordal-Christensen H, Tsutsumi N, Nakano A, Ueda T (2011) A membrane trafficking pathway regulated by the plant-specific RAB GTPase ARA6. Nat Cell Biol 13:853–860

    CAS  PubMed  Google Scholar 

  • Fernández-Marcos M, Sanz L, Lewis DR, Muday GK, Lorenzo O (2011) Nitric oxide causes root apical meristem defects and growth inhibition while reducing PIN-FORMED 1 (PIN1)-dependent acropetal auxin transport. Proc Natl Acad Sci USA 108:18506–18511

    PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • 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) APINOID-dependent binary switch in apical-basal PIN polar targeting directs auxin efflux. Science 306:862–865

    CAS  PubMed  Google Scholar 

  • Fu Y, Li H, Yang Z (2002) The ROP2 GTPase controls the formation of cortical fine F-actin and the early phase of directional cell expansion during Arabidopsis organogenesis. Plant Cell 14: 777–794

    CAS  PubMed  Google Scholar 

  • Fu Y, Gu Y, Zheng Z, Wasteneys G, Yang Z (2005) Arabidopsis interdigitating cell growth requires two antagonistic pathways with opposing action on cell morphogenesis. Cell 120: 687–700

    CAS  PubMed  Google Scholar 

  • Fu Y, Xu T, Zhu L, Wen M, Yang Z (2009) A ROP GTPase signaling pathway controls cortical microtubule ordering and cell expansion in Arabidopsis. Curr Biol 19:1827–1832

    CAS  PubMed  Google Scholar 

  • Gälweiler L, Guan C, Müller A, Wisman E, Mendgen K, Yephremov A, Palme K (1998) Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 282: 2226–2230

    PubMed  Google Scholar 

  • Ganguly A, Lee SH, Cho M, Lee OR, Ryu H, Cho H-T (2010) Differential auxin-transporting activities of PIN-FORMED proteins in Arabidopsis root hair cells. Plant Physiol 153: 1046–1061

    CAS  PubMed  Google Scholar 

  • Ganguly A, Sasayama D, Cho HT (2012a) Regulation of the polarity of protein trafficking by phosphorylation. Mol Cell 33:423–430

    CAS  Google Scholar 

  • Ganguly A, Lee SH, Cho HT (2012b) Functional identification of the phosphorylation sites of Arabidopsis PIN-FORMED3 for its subcellular localization and biological role. Plant J 71:810–823

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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Giehl RFH, Lima JE, Wiren N (2012) Localized iron supply triggers lateral root elongation in Arabidopsis by altering the AUX1-mediated auxin distribution. Plant Cell 24:33–49

    CAS  PubMed  Google Scholar 

  • Grebe M, Xu J, Mobius W, Ueda T, Nakano A, Geuze HJ, Rook MB, Scheres B (2003) Arabidopsis sterol endocytosis involves actin-mediated trafficking via ARA6-positive early endosomes. Curr Biol 13:1378–1387

    CAS  PubMed  Google Scholar 

  • Grunewald W, Friml J (2010) The march of the PINs: developmental plasticity by dynamic polar targeting in plant cells. EMBO J 29:2700–2714

    CAS  PubMed  Google Scholar 

  • Grunewald W, Cannoot B, Friml J, Gheysen G (2009) Parasitic nematodes modulate PIN-mediated auxin transport to facilitate infection. PLoS Pathog 5:e1000266

    PubMed  Google Scholar 

  • Haas TJ, Sliwinski MK, Martínez DE, Preuss M, Ebine K, Ueda T, Nielsen E, Odorizzi G, Otegui MS (2007) The Arabidopsis AAA ATPase SKD1 is involved in multivesicular endosome function and interacts with its positive regulator LYST-INTERACTING PROTEIN5. Plant Cell 19:1295–1312

    CAS  PubMed  Google Scholar 

  • Henderson J, Bauly JM, Ashford DA, Oliver SC, Hawes CR, Lazarus CM, Venis MA, Napier RM (1997) Retention of maize auxin-binding protein in the endoplasmic reticulum: quantifying escape and the role of auxin. Planta 202:313–323

    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 31:2965–2980

    CAS  PubMed  Google Scholar 

  • Huang F, Zago MK, Abas L, Van MA, Galvan-Ampudia CS, Offringa R (2010) Phosphorylation of conserved PIN motifs directs Arabidopsis PIN1 polarity and auxin transport. Plant Cell 22: 1129–1142

    CAS  PubMed  Google Scholar 

  • Jia DJ, Cao X, Wang W, Tan XY, Zhang XQ, Chen LQ, Ye D (2009) GNOM-LIKE 2, encoding an adenosine diphosphate-ribosylation factor-guanine nucleotide exchange factor protein homologous to GNOM and GNL1, is essential for pollen germination in Arabidopsis. J Integr Plant Biol 51:762–773

    CAS  PubMed  Google Scholar 

  • Jones AM, Herman EM (1993) KDEL-containing auxin-binding protein is secreted to the plasma membrane and cell wall. Plant Physiol 101:595–606

    CAS  PubMed  Google Scholar 

  • Jones AR, Kramer EM, Knox K, Swarup R, Bennett MJ, Lazarus CM, Leyser HM, Grierson CS (2009) Auxin transport through non-hair cells sustains root-hair development. Nat Cell Biol 11: 78–84

    CAS  PubMed  Google Scholar 

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

    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 

  • Kleine-Vehn J, Dhonukshe P, Swarup R, Bennett M, Friml J (2006) Subcellular trafficking of the Arabidopsis auxin influx carrier AUX1 uses a novel pathway distinct from PIN1. Plant Cell 18: 3171–3181

    CAS  PubMed  Google Scholar 

  • Kleine-Vehn J, Dhonukshe P, Sauer M, Brewer PB, Wisniewska J, Paciorek T, Benkova E, Friml J (2008a) ARF GEF-dependent transcytosis and polar delivery of PIN auxin carriers in Arabidopsis. Curr Biol 18:526–531

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Kleine-Vehn J, Huang F, Naramoto S, Zhang J, Michniewicz M, Offringa R, Friml J (2009) PIN auxin efflux carrier polarity is regulated by PINOID kinase-mediated recruitment into GNOM-independent trafficking in Arabidopsis. Plant Cell 21:3839–3849

    CAS  PubMed  Google Scholar 

  • Kleine-Vehn J, Ding Z, Jones AR, Tasaka M, Morita MT, Friml J (2010) Gravity-induced PIN transcytosis for polarization of auxin fluxes in gravity-sensing root cells. Proc Natl Acad Sci USA 107:22344–22349

    CAS  PubMed  Google Scholar 

  • Kleine-Vehn J, Wabnik K, Martinière A, Langowski L, Willig K, Naramoto S, Leitner J, Tanaka H, Jakobs S, Robert S, Luschnig C, Govaerts W, Hell S, Runions J, Friml J (2011) Recycling, clustering, and endocytosis jointly maintain PIN auxin carrier polarity at the plasma membrane. Mol Syst Biol 7:540. doi:10.1038/msb.2011.72

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Kubes M, Yang H, Richter GL, Cheng Y, Młodzinska E, Wang X, Blakeslee JJ, Carraro N, Petrasek J, Zazimalova E, Hoyerova K, Peer WA, Murphy AS (2012) The Arabidopsis concentration-dependent influx/efflux transporter ABCB4 regulates cellular auxin levels in the root epidermis. Plant J 69:640–654

    CAS  PubMed  Google Scholar 

  • Lanza M, Garcia-Ponce B, Castrillo G, Catarecha P, Sauer M, Rodriguez-Serrano M, Páez-García A, Sánchez-Bermejo E, Tc M, Leo Del Puerto Y, Sandalio LM, Paz-Ares J, Leyva A (2012) Role of actin cytoskeleton in brassinosteroid signaling and in its integration with the auxin response in plants. Dev Cell 22:1275–1285

    CAS  PubMed  Google Scholar 

  • Laplaze L, Benkova E, Casimiro I, Maes L, Vanneste S, Swarup R, Weijers D, Calvo V, Parizot B, Herrera-Rodriguez MB, Offringa R, Graham N, Doumas P, Friml J, Bogusz D, Beeckman T, Bennett M (2007) Cytokinins act directly on lateral root founder cells to inhibit root initiation. Plant Cell 19:3889–3900

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Laxmi A, Pan J, Morsy M, Chen R (2008) Light plays an essential role in intracellular distribution of auxin efflux carrier PIN2 in Arabidopsis thaliana. PLoS One 3:e1510

    PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Lee OR, Kim SJ, Kim HJ, Hong JK, Ryu SB, Lee SH, Ganguly A, Cho H-T (2010) Phospholipase A2 is required for PIN-FORMED protein trafficking to the plasma membrane in the Arabidopsis root. Plant Cell 22:812–825

    Google Scholar 

  • Leitner J, Petrásek J, Tomanov K, Retzer K, Parezová M, Korbei B, Bachmair A, Zazímalová E, Luschnig C (2012) Lysine63-linked ubiquitylation of PIN2 auxin carrier protein governs hormonally controlled adaptation of Arabidopsis root growth. Proc Natl Acad Sci USA 109: 8322–8327

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Li B, Li Q, Su Y, Chen H, Xiong L, Mi G, Kronzucker HJ, Shi W (2011) Shoot-supplied ammonium targets the root auxin influx carrier AUX1 and inhibits lateral root emergence in Arabidopsis. Plant Cell Environ 34:933–946

    CAS  PubMed  Google Scholar 

  • Luschnig C, Gaxiola RA, Grisafi P, Fink GR (1998) EIR1, a root specific protein involved in auxin transport, is required for gravitropism in Arabidopsis thaliana. Genes Dev 12:2175–2187

    CAS  PubMed  Google Scholar 

  • Marhavý P, Bielach A, Abas L, Abuzeineh A, Duclercq J, Tanaka H, Pařezová M, Petrášek J, Friml J, Kleine-Vehn J, Benková E (2011) Cytokinin modulates endocytic trafficking of PIN1 auxin efflux carrier to control plant organogenesis. Dev Cell 21:796–804

    PubMed  Google Scholar 

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

    CAS  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 

  • 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

    CAS  PubMed  Google Scholar 

  • 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 135:3345–3354

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Müller A, Guan C, 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

    PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Nagawa S, Xu T, Lin D, Dhonukshe P, Zhang X, Friml J, Scheres B, Fu Y, Yang Z (2012) ROP GTPase-dependent actin microfilaments promote PIN1 polarization by localized inhibition of clathrin-dependent endocytosis. PLoSBiol 10(4):e1001299. doi:10.1371/journal.pbio.1001299

    CAS  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  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Péret B, Swarup K, Ferguson A, Seth M, Yang Y, Dhondt S, James N, Casimiro I, Perry P, Syed A, Yang H, Reemmer J, Venison E, Howells C, Perez-Amador MA, Yun J, Alonso J, Beemster GT, Laplaze L, Murphy A, Bennett MJ, Nielsen E, Swarup R (2012) AUX/LAX genes encode a family of auxin influx transporters that perform distinct functions during Arabidopsis development. Plant Cell 24:2874–2885

    PubMed  Google Scholar 

  • Pernisová M, Klíma P, Horák J, Válková M, Malbeck J, Soucek P, Reichman P, Hoyerová K, Dubová J, Friml J, Zazímalová E, Hejátko J (2009) Cytokinins modulate auxin-induced organogenesis in plants via regulation of the auxin efflux. Proc Natl Acad Sci USA 106: 3609–3614

    PubMed  Google Scholar 

  • Prasad K, Grigg SP, Barkoulas M, Yadav RK, Sanchez-Perez GF, Pinon V, Blilou I, Hofhuis H, Dhonukshe P, Galinha C, Mähönen AP, Muller WH, Raman S, Verkleij AJ, Snel B, Reddy GV, Tsiantis M, Scheres B (2011) Arabidopsis PLETHORA transcription factors control phyllotaxis. Curr Biol 21:1123–1128

    CAS  PubMed  Google Scholar 

  • Rahman A, Takahashi M, Shibasaki K, Wu S, Inaba T, Tsurumi S, Baskin TI (2010) Gravitropism of Arabidopsis thaliana roots requires the polarization of PIN2 toward the root tip in meristematic cortical cells. Plant Cell 22:1762–1776

    CAS  PubMed  Google Scholar 

  • Rakusová H, Gallego-Bartolomé J, Vanstraelen M, Robert HS, Alabadí D, Blázquez MA, Benková E, Friml J (2011) Polarization of PIN3-dependent auxin transport for hypocotyl gravitropic response in Arabidopsis thaliana. Plant J 67:817–826

    PubMed  Google Scholar 

  • Rashotte AM, DeLong A, Muday GK (2011) Genetic and chemical reductions in protein phosphatase activity alter auxin transport, gravity response, and lateral root growth. Plant Cell 13: 1683–1697

    Google Scholar 

  • Reinhardt D, Pesce ER, Stieger P, Mandel T, Baltensperger K, Bennett M, Traas J, Friml J, Kuhlemeier C (2003) Regulation of phyllotaxis by polar auxin transport. Nature 426:255–260

    CAS  PubMed  Google Scholar 

  • Richter S, Geldner N, Schrader J, Wolters H, Stierhof YD, Rios G, Koncz C, Robinson DG, Jurgens G (2007) Functional diversification of closely related ARF-GEFs in protein secretion and recycling. Nature 448:488–492

    CAS  PubMed  Google Scholar 

  • Richter S, Müller LM, Stierhof YD, Mayer U, Takada N, Kost B, Vieten A, Geldner N, Koncz C, Jürgens G (2011) Polarized cell growth in Arabidopsis requires endosomal recycling mediated by GBF1-related ARF exchange factors. Nat Cell Biol 14:80–86

    PubMed  Google Scholar 

  • Robert S, Kleine-Vehn J, Barbez E, Sauer M, Paciorek T, Baster P, Vanneste S, Zhang J, Simon S, Covanová M, Hayashi K, Dhonukshe P, Yang Z, Bednarek SY, Jones AM, Luschnig C, Aniento F, Zažímalová E, Friml J (2010) ABP1 mediates auxin inhibition of clathrin-dependent endocytosis in Arabidopsis. Cell 143:111–121

    CAS  PubMed  Google Scholar 

  • Ruzicka K, Simásková M, Duclercq J, Petrásek J, Zazímalová E, Simon S, Friml J, Van Montagu MC, Benková E (2009) Cytokinin regulates root meristem activity via modulation of the polar auxin transport. Proc Natl Acad Sci USA 106:4284–4289

    CAS  PubMed  Google Scholar 

  • Sharma P, Sabharanjak S, Mayor S (2002) Endocytosis of lipid rafts: an identity crisis. Semin Cell Dev Biol 13:205–214

    CAS  PubMed  Google Scholar 

  • Shi J-H, Yang Z (2011) Is ABP1 an auxin receptor yet? Mol Plant 4:635–640

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Sun J, Chen Q, Qi L, Jiang H, Li S, Xu Y, Liu F, Zhou W, Pan J, Li X, Palme K, Li C (2011) Jasmonate modulates endocytosis and plasma membrane accumulation of the Arabidopsis PIN2 protein. New Phytol 191:360–375

    CAS  PubMed  Google Scholar 

  • Swarup R, Friml J, Marchant A, Ljung K, Sandberg G, Palme K, Bennett M (2001) Localization of the auxin permease AUX1 suggests two functionally distinct hormone transport pathways operate in the Arabidopsis root apex. Genes Dev 15:2648–2653

    CAS  PubMed  Google Scholar 

  • Swarup R, Parry G, Graham N, Allen T, Bennett M (2002) Auxin cross-talk: integration of signalling pathways to control plant development. Plant Mol Biol 49:411–426

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Teh OK, Moore I (2007) An ARF-GEF acting at the Golgi and in selective endocytosis in polarized plant cells. Nature 448:493–496

    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  Google Scholar 

  • Tian H, Klämbt D, Jones AM (1995) Auxin-binding protein 1 does not bind auxin within the endoplasmic reticulum despite this being the predominant subcellular location for this hormone receptor. J Biol Chem 270:26962–26969

    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 (2008) ABCB19/PGP19 stabilises PIN1 in membrane microdomains in Arabidopsis. Plant J 57:27–44

    PubMed  Google Scholar 

  • Ueda T, Uemura T, Sato MH, Nakano A (2004) Functional differentiation of endosomes in Arabidopsis cells. Plant J 40:783–789

    CAS  PubMed  Google Scholar 

  • Utsuno K, Shikanai T, Yamada Y, Hashimoto T (1998) AGR, an agravitropic locus of Arabidopsis thaliana, encodes a novel membrane protein family member. Plant Cell Physiol 39:1111–1118

    CAS  PubMed  Google Scholar 

  • Went FW (1928) Wuchsstoff und Wachstum. Rec Trav Bot Neerland 25:1–116

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Willige BC, Isono E, Richter R, Zourelidou M, Schwechheimer C (2011) Gibberellin regulates PIN-FORMED abundance and is required for auxin transport-dependent growth and development in Arabidopsis thaliana. Plant Cell 23:2184–2195

    CAS  PubMed  Google Scholar 

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

    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  Google Scholar 

  • Xu T, Wen M, Nagawa S, Fu Y, Chen JG, Wu MJ, Perrot- Rechenmann C, Friml J, Jones AM, Yang Z (2010) Cell surface- and Rho GTPase-based auxin signaling controls cellular interdigitation in Arabidopsis. Cell 143:99–110

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Zhang J, Vanneste S, Brewer PB, Michniewicz M, Grones P, Kleine-Vehn J, Lofke C, Teichmann T, Bielach A, Cannoot B, Hoyerova K, Chen X, Xue H-W, Benkova E, Zazímalova E, Friml J (2011) Inositol triphosphate-induced Ca2+ signaling modulates auxin transport and PIN polarity. Dev Cell 20:855–866

    CAS  PubMed  Google Scholar 

  • Zourelidou M, Müller 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 136:627–636

    CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported by grants from the Mid-career Researcher Program (2011–0017242, NRF, MEST) and the Next-Generation BioGreen 21 programs (TAGC PJ00820701 and SSAC PJ00814102) of the Rural Development Administration.

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  1. Department of Biological Sciences and Plant Genomics and Breeding Institute, Seoul National University, Seoul, 151-742, South Korea

    Anindya Ganguly & Hyung-Taeg Cho

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  1. Anindya Ganguly
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  2. Hyung-Taeg Cho
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Correspondence to Hyung-Taeg Cho .

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  1. , Plant Biology Division, The Samuel Roberts Noble Foundation, Ardmore, 73401, Oklahoma, USA

    Rujin Chen

  2. University of Bonn, IZMB, Kirschallee 1, Bonn, 53115, Nordrhein-Westfalen, Germany

    František Baluška

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Ganguly, A., Cho, HT. (2013). Signaling in Polar Auxin Transport. In: Chen, R., Baluška, F. (eds) Polar Auxin Transport. Signaling and Communication in Plants, vol 17. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-35299-7_1

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