Abstract
Auxin is an essential hormone that regulates both programmed and plastic plant development. The mechanisms that regulate auxin metabolism, transport and signal transduction are well characterized, although important unresolved questions remain. A unique feature of auxin-regulated plant development is that it involves a combination of cellular perception with polarized auxin gradients across groups of cells, tissues, and organs. Plants achieve these polarized auxin gradients via site-specific synthesis followed by directed and polar patterning of transport components in individual cells. These streams are primarily mediated by three functionally distinct plasma membrane transporter families. Apical–basal and organogenic patterning is largely defined by the polar efflux activities of full-length PIN-FORMED (PIN) facilitators. Dynamic auxin uptake into directed streams is mediated by the AUXIN RESISTANT 1 (AUX1) and LIKE AUX1 (LAX) symporters. Finally, long-distance transport streams are motivated by the ATP-BINDING CASSETTE subfamily B (ABCB) active transporters that continually pump across the plasma membrane and prevent reuptake of exported auxin. Multiple accessory proteins regulate auxin transporter activity and interactions with subcellular environments. The current understanding of cellular transport of auxin will be reviewed in this chapter.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Aller SG, Yu J, Ward A, Weng Y, Chittaboina S, Zhuo R, Harrell PM, Trinh YT, Zhang Q, Urbatsch IL, Chang G (2009) Structure of P-glycoprotein reveals a molecular basis for poly-specific drug binding. Science 323:1718–1722
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
Bailly A, Yang H, Martinoia E, Geisler M, Murphy AS (2012) Plant lessons: exploring ABCB functionality through structural modeling. Front Plant Sci 2:108
Bainbridge K, Guyomarch S, Bayer E, Swarup R, Bennett M, Mandel T, Kuhlemeier C (2008) Auxin influx carriers stabilize phyllotactic patterning. Genes Dev 22:810–823
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
Barbez E, Kubeš M, Rolčík J, Béziat C, Pěnčík A, Wang B, Rosquete MR, Zhu J, Dobrev PI, Lee Y, Zažímalová 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
Bayer EM, Smith RS, Mandel T, Nakayama N, Sauer M, Prusinkiewicz P, Kuhlemeier C (2009) Integration of transport-based models for phyllotaxis and midvein formation. Genes Dev 23:373–384
Bender RL, Fekete ML, Klinkenberg PM, Hampton M, Bauer B, Malecha M, Lindgren K, Maki JA, Perera MA, Nikolau BJ, Carter CJ (2013) PIN6 is required for nectary auxin response and short stamen development. Plant J 74:893–904
Benjamins R, Scheres B (2008) Auxin: the looping star in plant development. Annu Rev Plant Biol 59:443–465
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
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
Bhalerao RP, Eklof J, Ljung K, Marchant A, Bennett M, Sandberg G (2002) Shoot-derived auxin is essential for early lateral root emergence in Arabidopsis seedlings. Plant J 29:325–332
Blakeslee JJ, Peer WA, Murphy AS (2005) Auxin transport. Curr Opin Plant Biol 8:494–500
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
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
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
Carland FM, Fujioka S, Takatsuto S, Yoshida S, Nelson T (2002) The identification of CVP1 reveals a role for sterols in vascular patterning. Plant Cell 14:2045–2058
Chao DY, Gable K, Chen M, Baxter I, Dietrich CR, Cahoon EB, Guerinot ML, Lahner B, Lu S, Markham JE, Morrissey J, Han G, Gupta SD, Harmon JM, Jaworski JG, Dunn TM, Salt DE (2011) Sphingolipids in the root play an important role in regulating the leaf ionome in Arabidopsis thaliana. Plant Cell 23:1061–1081
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 95:15112–15117
Cheng Y, Dai X, Zhao Y (2006) Auxin biosynthesis by the YUCCA flavin monooxygenases controls the formation of floral organs and vascular tissues in Arabidopsis. Genes Dev 20:1790–1799
Cheng Y, Dai X, Zhao Y (2007) Auxin synthesized by the YUCCA flavin monooxygenases is essential for embryogenesis and leaf formation in Arabidopsis. Plant Cell 19:2430–2439
Cho M, Lee SH, Cho HT (2007) P-Glycoprotein4 displays auxin efflux transporter like action in Arabidopsis root hair cells and tobacco cells. Plant Cell 19:3930–3943
Cholodny N (1927) Wuchshormone und Tropismen bei den Pflanzen. Biol Zent Bl 47:604–626
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
Dai X, Mashiguchi K, Chen Q, Kasahara H, Kamiya Y, Ojha S, DuBois J, Ballou D, Zhao Y (2013) The biochemical mechanism of auxin biosynthesis by an Arabidopsis YUCCA flavin-containing monooxygenase. J Biol Chem 288:1448–1457
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 71:860–870
Darwin C (1880) The power of movement in plants. John Murray, London, p 474
Dawson RJ, Locher KP (2006) Structure of a bacterial multidrug ABC transporter. Nature 443:180–185
Del Pozo JC, Boniotti MB, Gutierrez C (2002) Arabidopsis E2Fc functions in cell division and is degraded by the ubiquitin-SCF(AtSKP2) pathway in response to light. Plant Cell 14:3057–3071
Del Pozo JC, Diaz-Trivino S, Cisneros N, Gutierrez C (2006) The balance between cell division and endoreplication depends on E2FC- DPB, transcription factors regulated by the ubiquitin–SCFSKP2A pathway in Arabidopsis. Plant Cell 18:2224–2235
Dharmasiri N, Dharmasiri S, Estelle M (2005) The F-box protein TIR1 is an auxin receptor. Nature 435:441–445
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
Dhonukshe P, Huang F, Galvan-Ampudia CS, Mahonen AP, Kleine-Vehn J, Xu J, Quint A, Prasad K, Friml J, Scheres B, Offringa R (2010) Plasma membrane-bound AGC3 kinases phosphorylate PIN auxin carriers at TPRXS(N/S) motifs to direct apical PIN recycling. Development 137:3245–3255
Ding Z, Wang B, Moreno I, Duplakova N, Simon S, Carraro N, Reemmer J, Pencik A, Chen X, Tejos R, Skupa P, Pollmann S, Mravec J, Petrasek J, Zazimalova E, Honys D, Rolcik 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
Dudler R, Hertig C (1992) Structure of an mdr-like gene from Arabidopsis thaliana: evolutionary implications. J Biol Chem 267:5882–5888
Esmon CA, Tinsley AG, Ljung K, Sandberg G, Hearne LB, Liscum E (2006) A gradient of auxin and auxin-dependent transcription precedes tropic growth responses. Proc Natl Acad Sci USA 103:236–241
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
Friml J, Vieten A, Sauer M, Weijers D, Schwarz H, Hamann T, Offringa R, Jürgens G (2003) Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 426:147–153
Friml J, Yang X, Michniewicz M, Weijers D, Quint A, Tietz O, Benjamins R, Ouwerkerk PB, Ljung K, Sandberg G, Hooykaas PJ, Palme K, Offringa R (2004) A PINOID-dependent binary switch in apical-basal PIN polar targeting directs auxin efflux. Science 306:862–865
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
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
Galvan-Ampudia CS, Offringa R (2007) Plant evolution: AGC kinases tell the auxin tale. Trends Plant Sci 12:541–547
Ganguly A, Lee SH, Cho M, Lee OR, Yoo H, Cho HT (2010) Differential auxin-transporting activities of PIN-FORMED proteins in Arabidopsis root hair cells. Plant Physiol 153:1046–1061
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, inter- acts with Arabidopsis multidrug resistance-like transporters AtPGP1 and AtPGP19. Mol Biol Cell 14:4238–4249
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
Goto N, Starke M, Kranz AR (1987) Effect of gibberellins on flower development of the pin-formed mutant of Arabidopsis thaliana. Arabidopsis Inf Serv 23:66–71
Grunewald W, Friml J (2010) The march of the PINs: developmental plasticity by dynamic polar targeting in plant cells. EMBO J 29:2700–2714
Guilfoyle TJ, Suzich JA, Lindberg M (1986) Synthesis of 5S rRNA and putative tRNAs in nuclei isolated from wheat embryos. Plant Mol Biol 7:95–104
Hager A (2003) Role of the plasma membrane H+-ATPase in auxin-induced elongation growth: historical and new aspects. J Plant Res 116:483–505
Harper RM, Stowe-Evans EL, Luesse DR, Muto H, Tatematsu K, Watahiki MK, Yamamoto K, Liscum E (2000) The NPH4 locus encodes the auxin response factor ARF7, a conditional regulator of differential growth in aerial Arabidopsis tissue. Plant Cell 12:757–770
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
Hopfner KP, Karcher A, Shin DS, Craig L, Arthur LM, Carney JP, Tainer JA (2000) Structural biology of Rad50 ATPase: ATP-driven conformational control in DNA double-strand break repair and the ABC-ATPase superfamily. Cell 101:789–800
Hosek P, Kubes M, Lankova M, Dobrev PI, Klima P, Kohoutova M, Petrasek J, Hoyerova K, Jirina M, Zazimalova E (2012) Auxin transport at cellular level: new insights supported by mathematical modelling. J Exp Bot 63:3815–3827
Huang F, Zago MK, Abas L, van Marion A, Galvan-Ampudia CS, Offringa R (2010) Phosphorylation of conserved PIN motifs directs Arabidopsis PIN1 polarity and auxin transport. Plant Cell 22:1129–1142
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
Jonsson H, Heisler MG, Shapiro BE, Meyerowitz EM, Mjolsness E (2006) An auxin-driven polarized transport model for phyllotaxis. Proc Natl Acad Sci USA 103:1633–1638
Jurado S, Diaz-Trivino S, Abraham Z, Manzano C, Gutierrez C, del Pozo C (2008) SKP2A, an F-box protein that regulates cell division, is degraded via the ubiquitin pathway. Plant J 53:828–841
Jurado S, Abraham Z, Manzano C, Lopez-Torrejon G, Pacios LF, Del Pozo JC (2010) The Arabidopsis cell cycle F-box protein SKP2A binds to auxin. Plant Cell 22:3891–3904
Kai K, Horita J, Wakasa K, Miyagawa H (2007) Three oxidative metabolites of indole-3-acetic acid from Arabidopsis thaliana. Phytochemistry 68:1651–1663
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
Kamphausen T, Fanghänel 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
Katekar GK, Geissler AE (1977) Auxin transport inhibitors. III. Chemical requirements of a class of auxin transport inhibitors. Plant Physiol 60:826–829
Kepinski S, Leyser O (2005) The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435:446–451
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
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
Knöller AS, Blakeslee JJ, Richards EL, Peer WA, Murphy AS (2010) Brachytic2/ZmABCB1 functions in IAA export from intercalary meristems. J Exp Bot 61:3689–3696
Kögl F, Haagen-Smith AJ (1931) Über die Chemie des Wuchsstoffs K. Akad. Wetenschap. Amsterdam. Proc Sect Sci 34:1411–1416
Kramer EM (2004) PIN and AUX/LAX proteins: their role in auxin accumulation. Trends Plant Sci 9:578–582
Kubeš M, Yang H, Richter GL, Cheng Y, Mlodzinska 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
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
Lee M, Choi Y, Burla B, Kim YY, Jeon B, Maeshima M, Yoo JY, Martinoia E, Lee Y (2008) The ABC transporter AtABCB14 is a malate importer and modulates stomatal response to CO2. Nat Cell Biol 10:1217–1223
Leng ER, Vineyard ML (1951) Dwarf and short plants. Maize Genet Coop Newsl 25:31–32
Lewis DR, Miller ND, Splitt BL, Wu G, Spalding EP (2007) Separating the roles of acropetal and basipetal auxin transport on gravitropism with mutations in two Arabidopsis multidrug resistance-like ABC transporter genes. Plant Cell 19:1838–1850
Lin R, Wang H (2005) Two homologous ATP-binding cassette transporter proteins, AtMDR1 and AtPGP1, regulate Arabidopsis photomorphogenesis and root development by mediating polar auxin transport. Plant Physiol 138:949–964
Lin D, Cao L, Zhou Z, Zhu L, Ehrhardt D, Yang Z, Fu Y (2013) Rho GTPase signaling activates microtubule severing to promote microtubule ordering in Arabidopsis. Curr Biol 23:290–297
Liscum E, Briggs WR (1995) Mutations in the NPH1 locus of Arabidopsis disrupt the perception of phototropic stimuli. Plant Cell 7:473–485
Ljung K, Östin A, Lioussanne L, Sandberg G (2001) Developmental regulation of indole-3-acetic acid turnover in Scots pine seedlings. Plant Physiol 125:464–475
Ljung K, Hull AK, Celenza J, Yamada M, Estelle M, Normanly J, Sandberg G (2005) Sites and regulation of auxin biosynthesis in Arabidopsis roots. Plant Cell 17:1090–1104
Löbler M, Klämbt D (1985) Auxin-binding protein from coleoptile membranes of corn (Zea mays L.). I. Purification by immunological methods and characterization. J Biol Chem 260:9848–9853
Luckie DB, Wilterding JH, Krha M, Krouse ME (2003) CFTR and MDR: ABC transporters with homologous structure but divergent function. Curr Genomics 4:225–235
Marchant A, Bhalerao R, Casimiro I, Eklöf J, Casero PJ, Bennett M, Sandberg G (2002) AUX1 promotes lateral root formation by facilitating indole-3-acetic acid distribution between sink and source tissues in the Arabidopsis seedling. Plant Cell 14:589–597
Markham JE, Molino D, Gissot L, Bellec Y, Hematy K, Marion J, Belcram K, Palauqui JC, Satiat-Jeunemaitre B, Faure JD (2011) Sphingolipids containing very-long-chain fatty acids define a secretory pathway for specific polar plasma membrane protein targeting in Arabidopsis. Plant Cell 23:2362–2378
Matsuda S, Kajizuka T, Kadota A, Nishimura T, Koshiba T (2011) NPH3- and PGP-like genes are exclusively expressed in the apical tip region essential for blue-light perception and lateral auxin transport in maize coleoptiles. J Exp Bot 62:3459–3466
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
Merks RMH, Van de Peer Y, Inzé D, Beemster GTS (2007) Canalization without flux sensors: a traveling-wave hypothesis. Trends Plant Sci 12:384–390
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
Mitchison GJ (1980) A model for vein formation in higher plants. Proc R Soc Lond B Boil Sci 207:79–109
Mravec J, Kubes M, Bielach A, Gaykova V, Petrasek J, Skupa P, Chand S, Benkova E, Zazımalova E, Friml J (2008) Interaction of PIN and PGP transport mechanisms in auxin distribution-dependent development. Development 135:3345–3354
Mravec J, Skůpa P, Bailly A, Hoyerová K, Křeček P, Bielach A, Petrášek J, Zhang J, Gaykova V, Stierhof YD, Dobrev PI, Schwarzerová K, Rolčík J, Seifertová D, Luschnig C, Benkova E, Zažímalová E, Geisler M, Friml J (2009) Subcellular homeostasis of phytohormone auxin is mediated by the ER-localized PIN5 transporter. Nature 459:1136–1140
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
Mullet JE, Klein RR, Klein PE (2002) Sorghum bicolor—an important species for comparative grass genomics and a source of beneficial genes for agriculture. Curr Opin Plant Biol 5:118–121
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
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
Nagashima A, Suzuki G, Uehara Y, Saji K, Furukawa T, Koshiba T, Sekimoto M, Fujioka S, Kuroha T, Kojima M, Sakakibara H, Fujisawa N, Okada K, Sakai T (2008) Phytochromes and cryptochromes regulate the differential growth of Arabidopsis hypocotyls in both a PGP19-dependent and a PGP19-independent manner. Plant J 53:516–529
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
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
Novák O, Hényková E, Sairanen I, Kowalczyk M, Pospíšil T, Ljung K (2012) Tissue-specific profiling of the Arabidopsis thaliana auxin metabolome. Plant J 72:523–536
Östin A, Kowalyczk M, Bhalerao RP, Sandberg G (1998) Metabolism of indole-3-acetic acid in Arabidopsis. Plant Physiol 118:285–296
Pan J, Fujioka S, Peng J, Chen J, Li G, Chen R (2009) The E3 ubiquitin ligase SCFTIR1/AFB and membrane sterols play key roles in auxin regulation of endocytosis, recycling, and plasma membrane accumulation of the auxin efflux transporter PIN2 in Arabidopsis thaliana. Plant Cell 21:568–580
Parry G, Delbarre A, Marchant A, Swarup R, Napier R, Perrot-Rechenmann C, Bennett MJ (2001) Novel auxin transport inhibitors phenocopy the auxin influx carrier mutation aux1. Plant J 25:399–406
Peer WA, Murphy AS (2007) Flavonoids and auxin transport: modulators or regulators? Trends Plant Sci 12:556–563
Peer WA, Blakeslee JJ, Yang H, Murphy AS (2011) Seven things we think we know about auxin transport. Mol Plant 4:487–504
Peer WA, Cheng Y, Murphy AS (2013) Evidence of oxidative attenuation of auxin signalling. J Exp Bot 64:2629–2639
Peret 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
Petersson SV, Johansson AI, Kowalczyk M, Makoveychuk A, Wang JY, Moritz T, Grebe M, Benfey PN, Sandberg G, Ljung K (2009) An auxin gradient and maximum in the Arabidopsis root apex shown by high-resolution cell-specific analysis of IAA distribution and synthesis. Plant Cell 21:1659–1668
Procko E, O’Mara ML, Bennett WFD, Tieleman DP, Gaudet R (2009) The mechanism of ABC transporters: general lessons from structural and functional studies of an antigenic peptide transporter. FASEB J 23:1287–1302
Radwanski ER, Last RL (1995) Tryptophan biosynthesis and metabolism: biochemical and molecular genetics. Plant Cell 7:921–934
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
Raven JA (1975) Transport of indoleacetic acid in plant cells in relation to pH and electrical potential gradients, and its significance for polar IAA transport. New Phytol 74:163–172
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
Robert S, Kleine-Vehn J, Barbez E, Sauer M, Paciorek T, Baster P, Vanneste S, Zhang J, Simon S, Čovanová M, Hayashi K, Dhonukshe P, Yang Z, Bednarek SY, Jones AM, Luschnig C, Aniento F, Zažimalová E, Friml J (2010) ABP1 mediates auxin inhibition of clathrin-dependent endocytosis in Arabidopsis. Cell 143:111–121
Roudier F, Gissot L, Beaudoin F, Haslam R, Michaelson L, Marion J, Molino D, Lima A, Bach L, Morin H, Tellier F, Palauqui JC, Bellec Y, Renne C, Miquel M, Dacosta M, Vignard J, Rochat C, Markham JE, Moreau P, Napier J, Faure JD (2010) Very-long-chain fatty acids are involved in polar auxin transport and developmental patterning in Arabidopsis. Plant Cell 22:364–375
Rubery PH, Sheldrake AR (1974) Carrier-mediated auxin transport. Planta 118:101–121
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 the auxinic compounds including the auxin precursor indole-3-butyric acid. Proc Natl Acad Sci USA 107:10749–10753
Sachs T (1969) Polarity and the induction of organized vascular tissues. Ann Bot Lond 33:263
Sakai T, Kagawa T, Kasahara M, Swartz TE, Christie JM, Briggs WR, Wada M, Okada K (2001) Arabidopsis nph1 and npl1: Blue light receptors that mediate both phototropism and chloroplast relocation. Proc Natl Acad Sci USA 98:6969–6974
Santelia D, Vincenzetti V, Azzarello E, Bovet L, Fukao Y, Duchtig P, Mancuso S, Martinoia E, Geisler M (2005) MDR-like ABC transporter AtPGP4 is involved in auxin-mediated lateral root and root hair development. FEBS Lett 579:5399–5406
Santner AA, Watson JC (2006) The WAG1 and WAG2 protein kinases negatively regulate root waving in Arabidopsis. Plant J 45:752–764
Sauer M, Balla J, Luschnig C, Wisniewska J, Reinohl V, Friml J, Benkova E (2006) Canalization of auxin flow by Aux/IAA-ARF-dependent feedback regulation of PIN polarity. Genes Dev 20:2902–2911
Sawchuk MG, Edgar A, Scarpella E (2013) Patterning of leaf vein networks by convergent auxin transport pathways. PLoS Genet 9:e1003294
Scarpella E, Marcos D, Friml J, Berleth T (2006) Control of leaf vascular patterning by polar auxin transport. Genes Dev 20:1015–1027
Shitan N, Bazin I, Dan K, Obata K, Kigawa K, Ueda K, Sato F, Forestier C, Yazaki K (2003) Involvement of CjMDR1, a plant multidrug-resistance-type ATP-binding cassette protein, in alkaloid transport in Coptis japonica. Proc Natl Acad Sci USA 100:751–756
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
Smith RS, Guyomarch S, Mendel T, Reinhardt D, Kuhlemeier C (2006) A plausible model of phyllotaxis. Proc Natl Acad Sci 103:1301–1306
Stein OL (1955) Rates of leaf initiation in two mutants of Zea mays, dwarf1 and brachytic2. Am J Bot 42:885–892
Stepanova AN, Robertson-Hoyt J, Yun J, Benavente LM, Xie DY, Dolezal K, Schlereth A, Jurgens G, Alonso JM (2008) TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development. Cell 133:177–191
Stoma S, Lucas M, Chopard J, Schaedel M, Traas J, Godin C (2008) Flux-based transport enhancement as a plausible unifying mechanism for auxin transport in meristem development. PLoS Comput Biol 4:e1000207
Sugawara S, Hishiyama S, Jikumaru Y, Hanada A, Nishimura T, Koshiba T, Zhao Y, Kamiya Y, Kasahara H (2009) Biochemical analyses of indole-3-acetaldoxime-dependent auxin biosynthesis in Arabidopsis. Proc Natl Acad Sci USA 106:5430–5435
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 trans- port pathways operate in the Arabidopsis root apex. Genes Dev 15:2648–2653
Swarup K, Benkova E, Swarup R, Casimiro I, Peret B, Yang Y, Parry G, Nielsen E, De Smet I, Vanneste S, Levesque MP, Carrier D, James N, Calvo V, Ljung K, Kramer E, Roberts R, Graham N, Marillonnet S, Patel K, Jones 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
Tanaka K, Fujimura-Kamada K, Yamamoto T (2011) Functions of phospholipid flippases. J Biochem 149:131–143
Tao Y, Ferrer JL, Ljung K, Pojer F, Hong F, Long JA, Li L, Moreno JE, Bowman ME, Ivans LJ, Cheng Y, Lim J, Zhao Y, Ballare CL, Sandberg G, Noel JP, Chory J (2008) Rapid synthesis of auxin via a new tryptophan-dependent pathway is required for shade avoidance in plants. Cell 133:164–176
Tarling EJ, Edwards PA (2011) ATP binding cassette transporter G1 (ABCG1) is an intracellular sterol transporter. Proc Natl Acad Sci USA 108:19719–19724
Teale WD, Paponov IA, Palme K (2006) Auxin in action: signalling, transport and the control of plant growth and development. Nat Rev Mol Cell Biol 7:847–859
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
Theologis A, Huynh TV, Davis RW (1985) Rapid induction of specific mRNAs by auxin in pea epicotyl tissue. J Mol Biol 183:53–68
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
Vernoux T, Besnard F, Traas J (2010) Auxin at the shoot apical meristem. Cold Spring Harb Perspect Biol 2:a001487
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-unified nomenclature and updated inventory. Trends Plant Sci 13:151–159
Vieten A, Vanneste S, Wisniewska J, Benková E, Benjamins R, Beeckman T, Luschnig C, Friml J (2005) Functional redundancy of PIN proteins is accompanied by auxin-dependent cross-regulation of PIN expression. Development 132:4521–4531
Wang B, Bailly A, Zwiewka M, Henrichs S, Azzarello E, Mancuso S, Maeshima M, Friml J, Schulz A, Geisler M (2013) Arabidopsis TWISTED DWARF1 functionally interacts with auxin exporter ABCB1 on the root plasma membrane. Plant Cell 25:202–214
Went FW, Thimann KV (1937) Phytohormones. MacMillan, New York
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
Willige BC, Ahlers S, Zourelidou M, Barbosa ICR, Demarsy E, Trevisan M, Davis PA, Roelfsema MRG, Hangarter R, Fankhauser C, Schwechheimer C (2013) D6PK AGCVIII kinases are required for auxin transport and phototropic hypocotyl bending in Arabidopsis. Plant Cell 25:1674–1688
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
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
Yamada M, Greenham K, Prigge MJ, Jensen PJ, Estelle M (2009) The TRANSPORT INHIBITOR RESPONSE2 gene is required for auxin synthesis and diverse aspects of plant development. Plant Physiol 151:168–179
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
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
Yang H, Richter GL, Wang X, Młodzińska E, Carraro N, Ma G, Jenness M, Chao D, Peer WA, Murphy AS (2013) Sterols and sphingolipids differentially function in trafficking of the Arabidopsis ABCB19 auxin transporter. Plant J 74:37–47
Zažímalová E, Murphy AS, Yang H, Hoyerová K, Hošek P (2010) Auxin transporters-why so many? Cold Spring Harb Perspect Biol 2:a001552
Zourelidou M, Müller I, Willige BC, Nill C, Jikumaru Y, Li H, Schwechheimer C (2009) The polarly localised D6 PROTEIN KINASE is required for efficient auxin transport in Arabidopsis thaliana. Development 136:627–636
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2014 Springer-Verlag Wien
About this chapter
Cite this chapter
Reemmer, J., Murphy, A. (2014). Intercellular Transport of Auxin. In: Zažímalová, E., Petrášek, J., Benková, E. (eds) Auxin and Its Role in Plant Development. Springer, Vienna. https://doi.org/10.1007/978-3-7091-1526-8_5
Download citation
DOI: https://doi.org/10.1007/978-3-7091-1526-8_5
Published:
Publisher Name: Springer, Vienna
Print ISBN: 978-3-7091-1525-1
Online ISBN: 978-3-7091-1526-8
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)