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Endocytosis in Plants pp 165–183Cite as

Endocytic Trafficking of PIN Proteins and Auxin Transport

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Abstract

Plants display an amazing developmental plasticity which compensates for a sessile lifestyle and inability to move away from unfavorable conditions as in the case of animals. Many aspects of this adaptability inflict changing of cell fate, de novo organ formation, and rearrangement of the plant body plan. Coordination of those processes is facilitated by the hormone auxin, which through its directional flow and local accumulation patterns provides the spatial information linking cellular and developmental modifications. This tight control of auxin distribution is in a major extent facilitated by the activity of PIN-FORMED (PIN) auxin transporters mediating export of auxin from cells. Members of the PIN protein family can display polar localization at the plasma membrane which enables the directional auxin transit through cells. The local levels of PINs in the membrane are dynamically, controlled by subcellular vesicular trafficking events encompassing secretion, recycling, degradation, and most prominently endocytosis. This well-characterized process also provides entry points for different signals that engage the endocytic machinery forging PINs into different downstream trafficking pathways, in accordance with ontogenetic programs and environmental stimuli, thus facilitating plant development.

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References

  • Abas L, Benjamins R, Malenica N, Paciorek T, Wiśniewska 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. doi:10.1038/ncb1369

    Article  PubMed  CAS  Google Scholar 

  • Arighi CN, Hartnell LM, Aguilar RC, Haft CR, Bonifacino JS (2004) Role of the mammalian retromer in sorting of the cation-independent mannose 6-phosphate receptor. J Cell Biol 165:123–133. doi:10.1083/jcb200312055

    Article  PubMed  CAS  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. doi:10.1038/nature11001

    PubMed  Google Scholar 

  • Benjamins R, Ampudia CSG, Hooykaas PJJ, Offringa R (2003) PINOID-mediated signaling involves calcium-binding proteins. Plant Physiol 132:1623–1630. doi:10.1104/pp103.019943

    Article  PubMed  CAS  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

    PubMed  CAS  Google Scholar 

  • Benjamins R, Scheres B (2008) Auxin: the looping star in plant development. Annu Rev Plant Biol 59:443–465. doi:10.1146/annurev.arplant.58.032806.103805

    Article  PubMed  CAS  Google Scholar 

  • Benková E, Michniewicz M, Sauer M, Teichmann T, Seifertová D, Jürgens G, Friml J (2003) Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115:591–602. doi:10.1016/S0092-8674(03)00924-3

    Article  PubMed  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. doi:10.1126/science.273.5277.948

    Article  PubMed  CAS  Google Scholar 

  • Berleth T, Scarpella E, Prusinkiewicz P (2007) toward the systems biology of auxin-transport-mediated patterning. Trends Plant Sci 12:151–159. doi:10.1016/j.tplants.2007.03.005

    Article  PubMed  CAS  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. doi:10.1038/nature03184

    Article  PubMed  CAS  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. doi:10.1371/journal.pbio.1001076

    PubMed  Google Scholar 

  • Dettmer J, Hong-Hermesdorf A, Stierhof Y-D, Schumacher K (2006) Vacuolar H+-ATPase activity is required for endocytic and secretory trafficking in Arabidopsis. Plant Cell 18:715–730. doi:10.1105/tpc.105.037978

    Article  PubMed  CAS  Google Scholar 

  • Dhonukshe P, Aniento F, Hwang I, Robinson DG, Mravec J, Stierhof Y-D, Friml J (2007) Clathrin-mediated constitutive endocytosis of PIN auxin efflux carriers in Arabidopsis. Curr Biol 17:520–527. doi:10.1016/j.cub.2007.01.052

    Article  PubMed  CAS  Google Scholar 

  • Dhonukshe P, Tanaka H, Goh T, Ebine K, Mähönen 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. doi:10.1038/nature07409

    Article  PubMed  CAS  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. doi:10.1038/ncb2208

    Article  PubMed  CAS  Google Scholar 

  • Dubrovsky JG, Sauer M, Napsucialy-Mendivil S, Ivanchenko MG, Friml J, Shishkova S, Celenza J, Benková E (2008) Auxin acts as a local morphogenetic trigger to specify lateral root founder cells. Proc Natl Acad Sci U S A 105:8790–8794. doi:10.1073/pnas.0712307105

    Article  PubMed  CAS  Google Scholar 

  • Feraru E, Paciorek T, Feraru MI, Zwiewka M, De Groodt R, De Rycke R, Kleine-Vehn J, Friml J (2010) The AP-3 Β adaptin mediates the biogenesis and function of lytic vacuoles in Arabidopsis. Plant Cell 22:2812–2824. doi:10.1105/tpc.110.075424

    Article  PubMed  CAS  Google Scholar 

  • 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. doi:10.1038/nature02085

    Article  PubMed  CAS  Google Scholar 

  • Friml J, Wiśniewska J, Benková E, Mendgen K, Palme K (2002) Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature 415:806–809. doi:10.1038/415806a

    Article  PubMed  Google Scholar 

  • Friml J, Yang X, Michniewicz M, Weijers D, Quint A, Tietz O, Benjamins R, Ouwerkerk PBF, Ljung K, Sandberg G, Hooykaas PJJ, Palme K, Offringa R (2004) A PINOID-dependent binary switch in apical-basal PIN polar targeting directs auxin efflux. Science 306:862–865. doi:10.1126/science.1100618

    Article  PubMed  CAS  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. doi:10.1126/science.282.5397.2226

    Article  PubMed  Google Scholar 

  • Geisler M, Blakeslee JJ, Bouchard R, Lee OR, Vincenzetti V, Bandyopadhyay A, Titapiwatanakun B, Peer WA, Bailly A, Richards EL, Ejendal KFK, 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. doi:10.1111/j.1365-313X.2005.02519.x

    Article  PubMed  CAS  Google Scholar 

  • Geldner N, Anders N, Wolters H, Keicher J, Kornberger W, Muller P, Delbarre A, Ueda T, Nakano A, Jürgens G (2003) The Arabidopsis GNOM ARF-GEF mediates endosomal recycling, auxin transport, and auxin-dependent plant growth. Cell 112:219–230. doi:10.1016/S0092-8674(03)00003-5

    Article  PubMed  CAS  Google Scholar 

  • Geldner N, Friml J, Stierhof Y-D, Jürgens G, Palme K (2001) Auxin transport inhibitors block PIN1 cycling and vesicle trafficking. Nature 413:425–428. doi:10.1038/35096571

    Article  PubMed  CAS  Google Scholar 

  • Geldner N, Hyman DL, Wang X, Schumacher K, Chory J (2007) Endosomal signaling of plant steroid receptor kinase BRI1. Genes Dev 21:1598–1602. doi:10.1101/gad.1561307

    Article  PubMed  CAS  Google Scholar 

  • Goldsmith MHM (1977) The polar transport of auxin. Annu Rev Plant Physiol 28:439–478. doi:10.1146/annurev.pp.28.060177.002255

    Article  CAS  Google Scholar 

  • Heisler MG, Hamant O, Krupinski P, Uyttewaal M, Ohno C, Jönsson H, Traas J, Meyerowitz EM (2010) Alignment between PIN1 polarity and microtubule orientation in the shoot apical meristem reveals a tight coupling between morphogenesis and auxin transport. PLoS Biol. doi:10.1371/journal.pbio.1000516

    PubMed  Google Scholar 

  • Holstein SE, Drucker M, Robinson DG (1994) Identification of a beta-type adaptin in plant clathrin-coated vesicles. J Cell Sci 107:945–953

    PubMed  CAS  Google Scholar 

  • Holstein SEH (2002) Clathrin and plant endocytosis. Traffic 3:614–620. doi:10.1034/j.1600-0854.2002.30903.x

    Article  PubMed  CAS  Google Scholar 

  • Huang F, Kemel Zago M, Abas L, van Marion A, Galván-Ampudia CS, Offringa R (2010) Phosphorylation of conserved PIN motifs directs Arabidopsis PIN1 polarity and auxin transport. Plant Cell 22:1129–1142. doi:10.1105/tpc.109.072678

    Article  PubMed  CAS  Google Scholar 

  • Jaillais Y, Fobis-Loisy I, Miège C, Rollin C, Gaude T (2006) AtSNX1 defines an endosome for auxin-carrier trafficking in Arabidopsis. Nature 443:106–109. doi:10.1038/nature05046

    Article  PubMed  CAS  Google Scholar 

  • Jaillais Y, Santambrogio M, Rozier F, Fobis-Loisy I, Miège C, Gaude T (2007) The retromer protein VPS29 links cell polarity and organ initiation in plants. Cell 130:1057–1070. doi:10.1016/j.cell.2007.08.040

    Article  PubMed  CAS  Google Scholar 

  • Keuskamp DH, Pollmann S, Voesenek LACJ, Peeters AJM, Pierik R (2010) Auxin transport through PIN-FORMED 3 (PIN3) controls shade avoidance and fitness during competition. PNAS 107(52):22740–22744. doi:10.1073/pnas.1013457108

    Article  PubMed  CAS  Google Scholar 

  • Kitakura S, Vanneste S, Robert S, Löfke C, Teichmann T, Tanaka H, Friml J (2011) Clathrin mediates endocytosis and polar distribution of PIN auxin transporters in Arabidopsis. Plant Cell 23:1920–1931. doi:10.1105/tpc.111.083030

    Article  PubMed  CAS  Google Scholar 

  • Kleine-Vehn J, Dhonukshe P, Sauer M, Brewer PB, Wiśniewska J, Paciorek T, Benková E, Friml J (2008a) ARF GEF-dependent transcytosis and polar delivery of PIN auxin carriers in Arabidopsis. Curr Biol 18:526–531. doi:10.1016/j.cub.2008.03.021

    Article  PubMed  CAS  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. doi:10.1105/tpc.106.042770

    Article  PubMed  CAS  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. PNAS 107:22344–22349. doi:10.1073/pnas.1013145107

    Article  PubMed  CAS  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. doi:10.1105/tpc.109.071639

    Article  PubMed  CAS  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. PNAS 105:17812–17817. doi:10.1073/pnas.0808073105

    Article  PubMed  CAS  Google Scholar 

  • Kleine-Vehn J, Wabnik K, Martinière A, Łangowski Ł, Willig K, Naramoto S, Leitner J, Tanaka H, Jakobs S, Robert S, Luschnig C, Govaerts W, Hell W, Runions S, 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

    Article  PubMed  CAS  Google Scholar 

  • Kramer EM (2004) PIN and AUX/LAX proteins: their role in auxin accumulation. Trends Plant Sci 9:578–582. doi:10.1016/j.tplants.2004.10.010

    Article  PubMed  CAS  Google Scholar 

  • Kubeš M, Yang H, Richter GL, Cheng Y, Młodzińska E, Wang X, Blakeslee JJ, Carraro N, Petrášek J, Zažímalová E, Hoyerová K, Peer WA, Murphy AS (2011) The Arabidopsis concentration-dependent influx/efflux transporter ABCB4 regulates cellular auxin levels in the root epidermis. Plant J 69:640–654. doi:10.1111/j.1365-313X.2011.04818.x

    Article  PubMed  CAS  Google Scholar 

  • Lam SK, Siu CL, Hillmer S, Jang S, An G, Robinson DG, Jiang L (2007) Rice SCAMP1 defines clathrin-coated, trans-golgi–located tubular-vesicular structures as an early endosome in tobacco BY-2 cells. Plant Cell 19:296–319. doi:10.1105/tpc.106.045708

    Article  PubMed  CAS  Google Scholar 

  • Low PS, Chandra S (1994) Endocytosis in plants. Annu Rev Plant Physiol Plant Mol Biol 45:609–631. doi:10.1146/annurev.pp.45.060194.003141

    Article  CAS  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. doi:10.1016/j.devcel.2011.08.014

    Article  PubMed  CAS  Google Scholar 

  • Meckel T, Hurst AC, Thiel G, Homann U (2004) Endocytosis against high turgor: intact guard cells of Vicia faba constitutively endocytose fluorescently labelled plasma membrane and GFP-tagged K+-channel KAT1. Plant J 39:182–193. doi:10.1111/j.1365-313X.2004.02119.x

    Article  PubMed  CAS  Google Scholar 

  • Men S, Boutté Y, Ikeda Y, Li X, Palme K, Stierhof Y-D, Hartmann M-A, Moritz T, Grebe M (2008) Sterol-dependent endocytosis mediates post-cytokinetic acquisition of PIN2 auxin efflux carrier polarity. Nat Cell Biol 10:237–244. doi:10.1038/ncb1686

    Article  PubMed  CAS  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. doi:10.1016/j.cell.2007.07.033

    Article  PubMed  CAS  Google Scholar 

  • Morita MT (2010) Directional gravity sensing in gravitropism. Annu Rev Plant Biol 61:705–720. doi:10.1146/annurev.arplant.043008.092042

    Article  PubMed  CAS  Google Scholar 

  • Mravec J, Kubeš M, Bielach A, Gaykova V, Petrášek J, Skůpa P, Chand S, Benková E, Zažímalová E, Friml J (2008) Interaction of PIN and PGP transport mechanisms in auxin distribution-dependent development. Development 135:3345–3354. doi:10.1242/dev.021071

    Article  PubMed  CAS  Google Scholar 

  • Mravec J, Petrášek J, Li N, Boeren S, Karlova R, Kitakura S, Pařezová M, Naramoto S, Nodzyński T, Dhonukshe P, Bednarek SY, Zažímalová E, de Vries S, Friml J (2011) Cell plate restricted association of DRP1A and PIN proteins is required for cell polarity establishment in Arabidopsis. Curr Biol 21:1055–1060. doi:10.1016/j.cub.2011.05.018

    Article  PubMed  CAS  Google Scholar 

  • Mravec J, Skůpa P, Bailly A, Hoyerová K, Křeček P, Bielach A, Petrášek J, Zhang J, Gaykova V, Stierhof Y-D, Dobrev PI, Schwarzerová K, Rolčík J, Seifertová D, Luschnig C, Benková E, Zažímalovà E, Geisler M, Friml J (2009) Subcellular homeostasis of phytohormone auxin is mediated by the ER-localized PIN5 transporter. Nature 459:1136–1140. doi:10.1038/nature08066

    Article  PubMed  CAS  Google Scholar 

  • Muday GK, DeLong A (2001) Polar auxin transport: controlling where and how much. Trends Plant Sci 6:535–542. doi:10.1016/S1360-1385(01)02101-X

    Article  PubMed  CAS  Google Scholar 

  • Müller A, Guan C, Gälweiler L, Tänzler 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. doi:10.1093/emboj/17.23.6903

    Article  PubMed  Google Scholar 

  • Müller J, Mettbach U, Menzel D, Šamaj J (2007) Molecular dissection of endosomal compartments in plants. Plant Physiol 145:293–304. doi:10.1104/pp.107.102863

    Article  PubMed  CAS  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. PLoS Biol. doi:10.1371/journal.pbio.1001299

    PubMed  Google Scholar 

  • Naramoto S, Kleine-Vehn J, Robert S, Fujimoto M, Dainobu T, Paciorek T, Ueda T, Nakano A, Van Montagu MCE, Fukuda H, Friml J (2010) ADP-ribosylation factor machinery mediates endocytosis in plant cells. Proc Natl Acad Sci U S A 107:21890–21895. doi:10.1073/pnas.1016260107

    Article  PubMed  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. doi:10.1105/tpc.010350

    PubMed  CAS  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. doi:10.1105/tpc.3.7.677

    PubMed  CAS  Google Scholar 

  • Paciorek T, Zazímalová E, Ruthardt N, Petrásek J, Stierhof Y-D, 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. doi:10.1038/nature03633

    Article  PubMed  CAS  Google Scholar 

  • Petrášek J, Friml J (2009) Auxin transport routes in plant development. Development 136:2675–2688. doi:10.1242/dev.030353

    Article  PubMed  CAS  Google Scholar 

  • Petrášek J, Mravec J, Bouchard R, Blakeslee JJ, Abas M, Seifertová D, Wiśniewska J, Tadele Z, Kubeš M, Čovanová M, Dhonukshe P, Skůpa P, Benková E, Perry L, Křeček P, Lee OR, Fink GR, Geisler M, Murphy AS, Luschnig C, Zažímalová E, Friml J (2006) PIN proteins perform a rate-limiting function in cellular auxin efflux. Science 312:914–918. doi:10.1126/science.1123542

    Article  PubMed  CAS  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. doi:10.1111/j.1365-313X.2011.04636.x

    Article  PubMed  CAS  Google Scholar 

  • Reinhardt D, Pesce E-R, 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. doi:10.1038/nature02081

    Article  PubMed  CAS  Google Scholar 

  • Reyes FC, Buono R, Otegui MS (2011) Plant endosomal trafficking pathways. Curr Opin Plant Biol 14:666–673. doi:10.1016/j.pbi.2011.07.009

    Article  PubMed  CAS  Google Scholar 

  • Robert S, Chary SN, Drakakaki G, Li S, Yang Z, Raikhel NV, Hicks GR (2008) Endosidin1 defines a compartment involved in endocytosis of the brassinosteroid receptor BRI1 and the auxin transporters PIN2 and AUX1. Proc Natl Acad Sci U S A 105:8464–8469. doi:10.1073/pnas.0711650105

    Article  PubMed  CAS  Google Scholar 

  • 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, Zažímalová E, Friml J (2010) ABP1 mediates auxin inhibition of clathrin-dependent endocytosis in Arabidopsis. Cell 143:111–121. doi:10.1016/j.cell.2010.09.027

    Article  PubMed  CAS  Google Scholar 

  • Robinson DG, Jiang L, Schumacher K (2008) The endosomal system of plants: charting new and familiar territories. Plant Physiol 147:1482–1492. doi:10.1104/pp.108.120105

    Article  PubMed  CAS  Google Scholar 

  • Robinson DG, Pimpl P, Scheuring D, Stierhof Y-D, Sturm S, Viotti C (2012) Trying to make sense of retromer. Trends Plant Sci. doi:10.1016/j.tplants.2012.03.005

    Google Scholar 

  • Roudier F, Gissot L, Beaudoin F, Haslam R, Michaelson L, Marion J, Molino D, Lima A, Bach L, Morin H, Tellier F, Palauqui J-C, Bellec Y, Renne C, Miquel M, DaCosta M, Vignard J, Rochat C, Markham JE, Moreau P, Napier J, Faure J-D (2010) Very-long-chain fatty acids are involved in polar auxin transport and developmental patterning in Arabidopsis. Plant Cell 22:364–375. doi:10.1105/tpc.109.071209

    Article  PubMed  CAS  Google Scholar 

  • Rubery PH, Sheldrake AR (1974) Carrier-mediated auxin transport. Planta 118:101–121. doi:10.1007/BF00388387

    Article  CAS  Google Scholar 

  • Ruiz Rosquete M, Barbez E, Kleine-Vehn J (2011) Cellular auxin homeostasis: gatekeeping is housekeeping. Mol Plant. doi:10.1093/mp/ssr109

    Google Scholar 

  • Sachs T (1981) The control of the patterned differentiation of vascular tissues. Adv Botanical Res 9:151–262

    Article  Google Scholar 

  • Sachs T (1991) Cell polarity and tissue patterning in plants. Development 113:83–93

    Google Scholar 

  • Šamaj J, Read ND, Volkmann D, Menzel D, Baluška F (2005) The endocytic network in plants. Trends Cell Biol 15:425–433. doi:10.1016/j.tcb.2005.06.006

    Article  PubMed  CAS  Google Scholar 

  • Sauer M, Balla J, Luschnig C, Wiśniewska J, Reinöhl V, Friml J, Benková E (2006) Canalization of auxin flow by Aux/IAA-ARF-dependent feedback regulation of PIN polarity. Genes Dev 20:2902–2911. doi:10.1101/gad.390806

    Article  PubMed  CAS  Google Scholar 

  • Scarpella E, Marcos D, Friml J, Berleth T (2006) Control of leaf vascular patterning by polar auxin transport. Genes Dev 20:1015–1027. doi:10.1101/gad.1402406

    Article  PubMed  CAS  Google Scholar 

  • Scheuring D, Viotti C, Krüger F, Künzl F, Sturm S, Bubeck J, Hillmer S, Frigerio L, Robinson DG, Pimpl P, Schumacher K (2011) Multivesicular bodies mature from the trans-Golgi network/early endosome in Arabidopsis. Plant Cell 23:3463–3481. doi:10.1105/tpc.111.086918

    Article  PubMed  CAS  Google Scholar 

  • Schlereth A, Möller B, Liu W, Kientz M, Flipse J, Rademacher EH, Schmid M, Jürgens G, Weijers D (2010) MONOPTEROS controls embryonic root initiation by regulating a mobile transcription factor. Nature 464:913–916. doi:10.1038/nature08836

    Article  PubMed  CAS  Google Scholar 

  • Schlicht M, Strnad M, Scanlon MJ, Mancuso S, Hochholdinger F, Palme K, Volkmann D, Menzel D, Baluška F (2006) Auxin immunolocalization implicates vesicular neurotransmitter-like mode of polar auxin transport in root apices. Plant Signal Behav 1:122–133

    Article  PubMed  Google Scholar 

  • Seaman MNJ (2005) Recycle your receptors with retromer. Trends Cell Biol 15:68–75. doi:10.1016/j.tcb.2004.12.004

    Article  PubMed  CAS  Google Scholar 

  • Shimada T, Koumoto Y, Li L, Yamazaki M, Kondo M, Nishimura M, Hara-Nishimura I (2006) AtVPS29, a putative component of a retromer complex, is required for the efficient sorting of seed storage proteins. Plant Cell Physiol 47:1187–1194. doi:10.1093/pcp/pcj103

    Article  PubMed  CAS  Google Scholar 

  • Spitzer C, Reyes FC, Buono R, Sliwinski MK, Haas TJ, Otegui MS (2009) The ESCRT-related CHMP1A and B proteins mediate multivesicular body sorting of auxin carriers in Arabidopsis and are required for plant development. Plant Cell 21:749–766. doi:10.1105/tpc.108.064865

    Article  PubMed  CAS  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 JDG, 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. doi:10.1038/ncb1754

    Article  PubMed  CAS  Google Scholar 

  • Takáč T, Pechan T, Šamajová O, Ovečka M, Richter H, Eck C, Niehaus K, Šamaj J (2012) Wortmannin treatment induces changes in Arabidopsis root proteome and post-Golgi compartments. J Proteome Res. doi:10.1021/pr201111n

    PubMed  Google Scholar 

  • Takano J, Tanaka M, Toyoda A, Miwa K, Kasai K, Fuji K, Onouchi H, Naito S, Fujiwara T (2010) Polar localization and degradation of Arabidopsis boron transporters through distinct trafficking pathways. PNAS. doi:10.1073/pnas.0910744107

    Google Scholar 

  • Tanaka H, Kitakura S, De Rycke R, De Groodt R, Friml J (2009) Fluorescence imaging-based screen identifies ARF GEF component of early endosomal trafficking. Curr Biol 19:391–397. doi:10.1016/j.cub.2009.01.057

    Article  PubMed  CAS  Google Scholar 

  • Teh O-K, Moore I (2007) An ARF-GEF acting at the golgi and in selective endocytosis in polarized plant cells. Nature 448:493–496. doi:10.1038/nature06023

    Article  PubMed  CAS  Google Scholar 

  • Tse YC, Mo B, Hillmer S, Zhao M, Lo SW, Robinson DG, Jiang L (2004) Identification of multivesicular bodies as prevacuolar compartments in Nicotiana tabacum BY-2 cells. Plant Cell 16:672–693. doi:10.1105/tpc.019703

    Article  PubMed  CAS  Google Scholar 

  • Vanneste S, Friml J (2009) Auxin: a trigger for change in plant development. Cell 136:1005–1016. doi:10.1016/j.cell.2009.03.001

    Article  PubMed  CAS  Google Scholar 

  • Verrier PJ, Bird D, Burla B, Dassa E, Forestier C, Geisler M, Klein M, Kolukisaoglu Ü, Lee Y, Martinoia E, Murphy A, Rea PA, Samuels L, Schulz B, Spalding EP, Yazaki K, Theodoulou FL (2008) Plant ABC proteins—a unified nomenclature and updated inventory. Trends Plant Sci 13:151–159. doi:10.1016/j.tplants.2008.02.001

    Article  PubMed  CAS  Google Scholar 

  • Vieten A, Sauer M, Brewer PB, Friml J (2007) Molecular and cellular aspects of auxin-transport-mediated development. Trends Plant Sci 12:160–168. doi:10.1016/j.tplants.2007.03.006

    Article  PubMed  CAS  Google Scholar 

  • Wabnik K, Govaerts W, Friml J, Kleine-Vehn J (2011a) Feedback models for polarized auxin transport: an emerging trend. Mol BioSyst 7:2352. doi:10.1039/c1mb05109a

    Article  PubMed  CAS  Google Scholar 

  • Wabnik K, Kleine-Vehn J, Govaerts W, Friml J (2011b) Prototype cell-to-cell auxin transport mechanism by intracellular auxin compartmentalization. Trends Plant Sci 16:468–475. doi:10.1016/j.tplants.2011.05.002

    Article  PubMed  CAS  Google Scholar 

  • Wan Y, Jasik J, Wang L, Hao H, Volkmann D, Menzel D, Mancuso S, Baluška F, Lin J (2012) The signal transducer NPH3 integrates the phototropin1 photosensor with PIN2-based polar auxin transport in Arabidopsis root phototropism. Plant Cell 24:551–565. doi:10.1105/tpc.111.094284

    Article  PubMed  CAS  Google Scholar 

  • Whitford R, Fernandez A, Tejos R, Pérez AC, Kleine-Vehn J, Vanneste S, Drozdzecki A, Leitner J, Abas L, Aerts M, Hoogewijs K, Baster P, De Groodt R, Lin Y-C, Storme V, Van de Peer Y, Beeckman T, Madder A, Devreese B, Luschnig C, Friml J, Hilson P (2012) GOLVEN secretory peptides regulate auxin carrier turnover during plant gravitropic responses. Dev Cell 22:678–685. doi:10.1016/j.devcel.2012.02.002

    Article  PubMed  CAS  Google Scholar 

  • Winter V, Hauser M-T (2006) Exploring the ESCRTing machinery in eukaryotes. Trends Plant Sci 11:115–123. doi:10.1016/j.tplants.2006.01.008

    Article  PubMed  CAS  Google Scholar 

  • Wiśniewska J, Xu J, Seifertová D, Brewer PB, Růžička K, Blilou I, Rouquié D, Benková E, Scheres B, Friml J (2006) Polar PIN localization directs auxin flow in plants. Science 312:883–884. doi:10.1126/science.1121356

    Article  PubMed  Google Scholar 

  • Wollert T, Wunder C, Lippincott-Schwartz J, Hurley JH (2009) Membrane scission by the ESCRT-III complex. Nature 458:172–177. doi:10.1038/nature07836

    Article  PubMed  CAS  Google Scholar 

  • Xu T, Wen M, Nagawa S, Fu Y, Chen J-G, Wu M-J, 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. doi:10.1016/j.cell.2010.09.003

    Article  PubMed  CAS  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. doi:10.1111/j.1365-313X.2009.03856.x

    Article  PubMed  CAS  Google Scholar 

  • Zažímalová E, Krecek P, Skůpa P, Hoyerová K, Petrášek J (2007) Polar transport of the plant hormone auxin—the role of PIN-FORMED (PIN) proteins. Cell Mol Life Sci 64:1621–1637. doi:10.1007/s00018-007-6566-4

    Article  PubMed  CAS  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. PNAS 103:6404–6409. doi:10.1073/pnas.0510283103

    Article  PubMed  CAS  Google Scholar 

  • Zhang J, Nodzyński T, Pěnčík A, Rolčík J, Friml J (2010) PIN phosphorylation is sufficient to mediate PIN polarity and direct auxin transport. PNAS 107:918–922. doi:10.1073/pnas.0909460107

    Article  PubMed  CAS  Google Scholar 

  • Zhang J, Vanneste S, Brewer PB, Michniewicz M, Grones P, Kleine-Vehn J, Löfke C, Teichmann T, Bielach A, Cannoot B, Hoyerová K, Chen X, Xue H-W, Benková E, Zažímalová E, Friml J (2011) Inositol trisphosphate-induced Ca2+ signaling modulates auxin transport and PIN polarity. Dev Cell 20:855–866. doi:10.1016/j.devcel.2011.05.013

    Article  PubMed  CAS  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. doi:10.1242/dev.028365

    Article  PubMed  CAS  Google Scholar 

  • Zwiewka M, Feraru E, Müller B, Hwang I, Feraru MI, Kleine-Vehn J, Weijers D, Friml J (2011) The AP-3 adaptor complex is required for vacuolar function in Arabidopsis. Cell Res 21:1711–1722. doi:10.1038/cr.2011.99

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This work was supported by the Odysseus Programme of the Research Foundation-Flanders. SV is a postdoctoral fellow of the Research Foundation-Flanders (FWO09/PDO/196); TN is a predoctoral fellow of Jiří Friml’s research group which is supported by the Odysseus Program of the Research Foundation-Flanders (Grant no. G091608).

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Authors and Affiliations

  1. Department of Plant Systems Biology, VIB, 9052, Ghent, Belgium

    Tomasz Nodzyński, Steffen Vanneste & Jiří Friml

  2. Department of Plant Biotechnology and Bioinformatics, Ghent University, 9052, Ghent, Belgium

    Tomasz Nodzyński, Steffen Vanneste & Jiří Friml

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  1. Tomasz Nodzyński
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  2. Steffen Vanneste
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  3. Jiří Friml
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Correspondence to Jiří Friml .

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  1. , Faculty of Science, Palacky University in Olomouc, Slechtitelu 11, Olomouc, 78371, Czech Republic

    Jozef Šamaj

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Nodzyński, T., Vanneste, S., Friml, J. (2012). Endocytic Trafficking of PIN Proteins and Auxin Transport. In: Šamaj, J. (eds) Endocytosis in Plants. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-32463-5_8

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