Skip to main content
Log in

Unique mechanism of plant endocytic/vacuolar transport pathways

  • Current Topics in Plant Research
  • Published:
Journal of Plant Research Aims and scope Submit manuscript

Abstract

The post-Golgi traffic network in plant cells is highly complex, which is correlated with the large number of genes related to this function. RABs and SNAREs are key regulators of tethering and fusion of transport vesicles to target membranes, and the numbers of these regulators have also expanded in plant lineages. In addition to this increase in the net number of genes, plants also seem to have evolved new gene families tailored to fulfill plant-unique functions. In this article, we summarize recent progress in studies on plant-unique RABs and SNAREs functioning in post-Golgi trafficking, with a special focus on the endocytic pathway.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Antonin W, Fasshauer D, Becker S, Jahn R, Schneider TR (2002) Crystal structure of the endosomal SNARE complex reveals common structural principles of all SNAREs. Nat Struct Biol 9:107–111

    Article  PubMed  CAS  Google Scholar 

  • Bassham DC (2007) Plant autophagy—more than a starvation response. Curr Opin Plant Biol 10:587–593

    Article  PubMed  CAS  Google Scholar 

  • Bassham DC, Blatt MR (2008) SNAREs: cogs and coordinators in signaling and development. Plant Physiol 147:1504–1515

    Article  PubMed  CAS  Google Scholar 

  • Becker B (2007) Function and evolution of the vacuolar compartment in green algae and land plants (Viridiplantae). Int Rev Cytol 264:1–24

    Article  PubMed  CAS  Google Scholar 

  • Benli M, Doring F, Robinson DG, Yang X, Gallwitz D (1996) Two GTPase isoforms, Ypt31p and Ypt32p, are essential for Golgi function in yeast. EMBO J 15:6460–6475

    PubMed  CAS  Google Scholar 

  • Bolte S, Brown S, Satiat-Jeunemaitre B (2004a) The N-myristoylated Rab-GTPase m-Rabmc is involved in post-Golgi trafficking events to the lytic vacuole in plant cells. J Cell Sci 117:943–954

    Article  PubMed  CAS  Google Scholar 

  • Bolte S, Talbot C, Boutte Y, Catrice O, Read ND, Satiat-Jeunemaitre B (2004b) FM-dyes as experimental probes for dissecting vesicle trafficking in living plant cells. J Microsc 214:159–173

    Article  PubMed  CAS  Google Scholar 

  • Borg S, Brandstrup B, Jensen TJ, Poulsen C (1997) Identification of new protein species among 33 different small GTP-binding proteins encoded by cDNAs from Lotus japonicus, and expression of corresponding mRNAs in developing root nodules. Plant J 11:237–250

    Article  PubMed  CAS  Google Scholar 

  • Bucci C, Parton RG, Mather IH, Stunnenberg H, Simons K, Hoflack B, Zerial M (1992) The small GTPase rab5 functions as a regulatory factor in the early endocytic pathway. Cell 70:715–728

    Article  PubMed  CAS  Google Scholar 

  • Burgoyne RD, Morgan A (2007) Membrane trafficking: three steps to fusion. Curr Biol 17:R255–258

    Article  PubMed  CAS  Google Scholar 

  • Busch M, Mayer U, Jurgens G (1996) Molecular analysis of the Arabidopsis pattern formation of gene GNOM: gene structure and intragenic complementation. Mol Gen Genet 250:681–691

    PubMed  CAS  Google Scholar 

  • Cai H, Reinisch K, Ferro-Novick S (2007) Coats, tethers, Rabs, and SNAREs work together to mediate the intracellular destination of a transport vesicle. Dev Cell 12:671–682

    Article  PubMed  CAS  Google Scholar 

  • Chavrier P, Gorvel JP, Stelzer E, Simons K, Gruenberg J, Zerial M (1991) Hypervariable C-terminal domain of rab proteins acts as a targeting signal. Nature 353:769–772

    Article  PubMed  CAS  Google Scholar 

  • Chen W, Feng Y, Chen D, Wandinger-Ness A (1998) Rab11 is required for trans-golgi network-to-plasma membrane transport and a preferential target for GDP dissociation inhibitor. Mol Biol Cell 9:3241–3257

    PubMed  CAS  Google Scholar 

  • Chinchilla D, Boller T, Robatzek S (2007) Flagellin signalling in plant immunity. Adv Exp Med Biol 598:358–371

    Article  PubMed  Google Scholar 

  • Chow CM, Neto H, Foucart C, Moore I (2008) Rab-A2 and Rab-A3 GTPases define a trans-golgi endosomal membrane domain in Arabidopsis that contributes substantially to the cell plate. Plant Cell 20:101–123

    Article  PubMed  CAS  Google Scholar 

  • Christoforidis S, Zerial M (2000) Purification and identification of novel Rab effectors using affinity chromatography. Methods 20:403–410

    Article  PubMed  CAS  Google Scholar 

  • Christoforidis S, McBride HM, Burgoyne RD, Zerial M (1999) The Rab5 effector EEA1 is a core component of endosome docking. Nature 397:621–625

    Article  PubMed  CAS  Google Scholar 

  • de Graaf BH, Cheung AY, Andreyeva T, Levasseur K, Kieliszewski M, Wu HM (2005) Rab11 GTPase-regulated membrane trafficking is crucial for tip-focused pollen tube growth in tobacco. Plant Cell 17:2564–2579

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Dirac-Svejstrup AB, Sumizawa T, Pfeffer SR (1997) Identification of a GDI displacement factor that releases endosomal Rab GTPases from Rab-GDI. EMBO J 16:465–472

    Article  PubMed  CAS  Google Scholar 

  • D’Souza-Schorey C, Chavrier P (2006) ARF proteins: roles in membrane traffic and beyond. Nat Rev 7:347–358

    Article  CAS  Google Scholar 

  • Dugani CB, Klip A (2005) Glucose transporter 4: cycling, compartments and controversies. EMBO Rep 6:1137–1142

    Article  PubMed  CAS  Google Scholar 

  • Ebine K, Okatani Y, Uemura T, Goh T, Shoda K, Niihama M, Morita MT, Spitzer C, Otegui MS, Nakano A, Ueda T (2008) A SNARE complex unique to seed plants is required for protein storage vacuole biogenesis and seed development of Arabidopsis thaliana. Plant Cell (in press) doi: 10.1105/tpc.107.057711

  • Echard A, el Marjou A, Goud B (2001) Expression, purification, and biochemical properties of rabkinesin-6 domains and their interactions with Rab6A. Methods Enzymol 329:157–165

    Article  PubMed  CAS  Google Scholar 

  • Fasshauer D, Sutton RB, Brunger AT, Jahn R (1998) Conserved structural features of the synaptic fusion complex: SNARE proteins reclassified as Q- and R-SNAREs. Proc Natl Acad Sci USA 95:15781–15786

    Article  PubMed  CAS  Google Scholar 

  • Foresti O, Denecke J (2008) Intermediate organelles of the plant secretory pathway: identity and function. Traffic 9(10):1599–1612

    Article  PubMed  CAS  Google Scholar 

  • Frigerio L, Hinz G, Robinson DG (2008) Multiple vacuoles in plant cells: rule or exception? Traffic 9(10):1564–1570

    Article  PubMed  CAS  Google Scholar 

  • Furutani M, Kajiwara T, Kato T, Treml BS, Stockum C, Torres-Ruiz RA, Tasaka M (2007) The gene MACCHI-BOU 4/ENHANCER OF PINOID encodes a NPH3-like protein and reveals similarities between organogenesis and phototropism at the molecular level. Development 134:3849–3859

    Article  PubMed  CAS  Google Scholar 

  • Geldner N, Robatzek S (2008) Plant receptors go endosomal: a moving view on signal transduction. Plant Physiol 147:1565–1574

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  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

    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

    Article  PubMed  CAS  Google Scholar 

  • Gillingham AK, Munro S (2007) The small G proteins of the Arf family and their regulators. Annu Rev Cell Dev Biol 23:579–611

    Article  PubMed  CAS  Google Scholar 

  • Goh T, Uchida W, Arakawa S, Ito E, Dainobu T, Ebine K, Takeuchi M, Sato K, Ueda T, Nakano A (2007) VPS9a, the common activator for two distinct types of Rab5 GTPases, is essential for the development of Arabidopsis thaliana. Plant Cell 19:3504–3515

    Article  PubMed  CAS  Google Scholar 

  • Golomb L, Abu-Abied M, Belausov E, Sadot E (2008) Different subcellular localizations and functions of Arabidopsis myosin VIII. BMC Plant Biol 8:3

    Article  PubMed  Google Scholar 

  • Gorvel JP, Chavrier P, Zerial M, Gruenberg J (1991) rab5 Controls early endosome fusion in vitro. Cell 64:915–925

    Article  PubMed  CAS  Google Scholar 

  • Griffing LR (2008) FRET analysis of transmembrane flipping of FM4-64 in plant cells: is FM4-64 a robust marker for endocytosis? J Microsc 231:291–298

    Article  PubMed  CAS  Google Scholar 

  • Grosshans BL, Ortiz D, Novick P (2006) Rabs and their effectors: achieving specificity in membrane traffic. Proc Natl Acad Sci USA 103:11821–11827

    Article  PubMed  CAS  Google Scholar 

  • Gruenberg J, Maxfield FR (1995) Membrane transport in the endocytic pathway. Curr Opin Cell Biol 7:552–563

    Article  PubMed  CAS  Google Scholar 

  • Gurkan C, Koulov AV, Balch WE (2007) An evolutionary perspective on eukaryotic membrane trafficking. Adv Exp Med Biol 607:73–83

    Article  PubMed  Google Scholar 

  • Haas TJ, Sliwinski MK, Martinez 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

    Article  PubMed  CAS  Google Scholar 

  • Hammer JA 3rd, Wu XS (2002) Rabs grab motors: defining the connections between Rab GTPases and motor proteins. Curr Opin Cell Biol 14:69–75

    Article  PubMed  CAS  Google Scholar 

  • Hoepfner S, Severin F, Cabezas A, Habermann B, Runge A, Gillooly D, Stenmark H, Zerial M (2005) Modulation of receptor recycling and degradation by the endosomal kinesin KIF16B. Cell 121:437–450

    Article  PubMed  CAS  Google Scholar 

  • Hong W (2005) SNAREs and traffic. Biochim Biophys Acta 1744:493–517

    PubMed  Google Scholar 

  • Inaba T, Nagano Y, Nagasaki T, Sasaki Y (2002) Distinct localization of two closely related Ypt3/Rab11 proteins on the trafficking pathway in higher plants. J Biol Chem 277:9183–9188

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Jaillais Y, Fobis-Loisy I, Miege C, Gaude T (2008) Evidence for a sorting endosome in Arabidopsis root cells. Plant J 53:237–247

    Article  PubMed  CAS  Google Scholar 

  • Jedd G, Mulholland J, Segev N (1997) Two new Ypt GTPases are required for exit from the yeast trans-Golgi compartment. J Cell Biol 137:563–580

    Article  PubMed  CAS  Google Scholar 

  • Jordens I, Fernandez-Borja M, Marsman M, Dusseljee S, Janssen L, Calafat J, Janssen H, Wubbolts R, Neefjes J (2001) The Rab7 effector protein RILP controls lysosomal transport by inducing the recruitment of dynein-dynactin motors. Curr Biol 11:1680–1685

    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

    Article  PubMed  CAS  Google Scholar 

  • Kotzer AM, Brandizzi F, Neumann U, Paris N, Moore I, Hawes C (2004) AtRabF2b (Ara7) acts on the vacuolar trafficking pathway in tobacco leaf epidermal cells. J Cell Sci 117:6377–6389

    Article  PubMed  CAS  Google Scholar 

  • Kwon C, Neu C, Pajonk S, Yun HS, Lipka U, Humphry M, Bau S, Straus M, Kwaaitaal M, Rampelt H, El Kasmi F, Jurgens G, Parker J, Panstruga R, Lipka V, Schulze-Lefert P (2008) Co-option of a default secretory pathway for plant immune responses. Nature 451:835–840

    Article  PubMed  CAS  Google Scholar 

  • Lipka V, Kwon C, Panstruga R (2007) SNARE-ware: the role of SNARE-domain proteins in plant biology. Annu Rev Cell Dev Biol 23:147–174

    Article  PubMed  CAS  Google Scholar 

  • Martinoia E, Maeshima M, Neuhaus HE (2007) Vacuolar transporters and their essential role in plant metabolism. J Exp Bot 58:83–102

    Article  PubMed  CAS  Google Scholar 

  • Mayer U, Ruiz RAT, Berleth T, Misera S, Jurgens G (1991) Mutations affecting body organization in the Arabidopsis embryo. Nature 353:402–407

    Article  Google Scholar 

  • Merchant SS, Prochnik SE, Vallon O, Harris EH, Karpowicz SJ, Witman GB, Terry A, Salamov A, Fritz-Laylin LK, Marechal-Drouard L, Marshall WF, Qu LH, Nelson DR, Sanderfoot AA, Spalding MH, Kapitonov VV, Ren Q, Ferris P, Lindquist E, Shapiro H, Lucas SM, Grimwood J, Schmutz J, Cardol P, Cerutti H, Chanfreau G, Chen CL, Cognat V, Croft MT, Dent R, Dutcher S, Fernandez E, Fukuzawa H, Gonzalez-Ballester D, Gonzalez-Halphen D, Hallmann A, Hanikenne M, Hippler M, Inwood W, Jabbari K, Kalanon M, Kuras R, Lefebvre PA, Lemaire SD, Lobanov AV, Lohr M, Manuell A, Meier I, Mets L, Mittag M, Mittelmeier T, Moroney JV, Moseley J, Napoli C, Nedelcu AM, Niyogi K, Novoselov SV, Paulsen IT, Pazour G, Purton S, Ral JP, Riano-Pachon DM, Riekhof W, Rymarquis L, Schroda M, Stern D, Umen J, Willows R, Wilson N, Zimmer SL, Allmer J, Balk J, Bisova K, Chen CJ, Elias M, Gendler K, Hauser C, Lamb MR, Ledford H, Long JC, Minagawa J, Page MD, Pan J, Pootakham W, Roje S, Rose A, Stahlberg E, Terauchi AM, Yang P, Ball S, Bowler C, Dieckmann CL, Gladyshev VN, Green P, Jorgensen R, Mayfield S, Mueller-Roeber B, Rajamani S, Sayre RT, Brokstein P, Dubchak I, Goodstein D, Hornick L, Huang YW, Jhaveri J, Luo Y, Martinez D, Ngau WC, Otillar B, Poliakov A, Porter A, Szajkowski L, Werner G, Zhou K, Grigoriev IV, Rokhsar DS, Grossman AR (2007) The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318:245–250

    Article  PubMed  CAS  Google Scholar 

  • Miaczynska M, Zerial M (2002) Mosaic organization of the endocytic pathway. Exp Cell Res 272:8–14

    Article  PubMed  CAS  Google Scholar 

  • Miaczynska M, Christoforidis S, Giner A, Shevchenko A, Uttenweiler-Joseph S, Habermann B, Wilm M, Parton RG, Zerial M (2004) APPL proteins link Rab5 to nuclear signal transduction via an endosomal compartment. Cell 116:445–456

    Article  PubMed  CAS  Google Scholar 

  • Mohrmann K, van der Sluijs P (1999) Regulation of membrane transport through the endocytic pathway by rabGTPases. Mol Membr Biol 16:81–87

    Article  PubMed  CAS  Google Scholar 

  • Nielsen E, Severin F, Backer JM, Hyman AA, Zerial M (1999) Rab5 regulates motility of early endosomes on microtubules. Nat Cell Biol 1:376–382

    Article  PubMed  CAS  Google Scholar 

  • Nielsen E, Cheung AY, Ueda T (2008) The regulatory RAB and ARF GTPases for vesicular trafficking. Plant Physiol 147:1516–1526

    Article  PubMed  CAS  Google Scholar 

  • Ohtomo I, Ueda H, Shimada T, Nishiyama C, Komoto Y, Hara-Nishimura I, Takahashi T (2005) Identification of an allele of VAM3/SYP22 that confers a semi-dwarf phenotype in Arabidopsis thaliana. Plant Cell Physiol 46:1358–1365

    Article  PubMed  CAS  Google Scholar 

  • Otegui MS, Spitzer C (2008) Endosomal functions in plants. Traffic 9(10):1589–1598

    Article  PubMed  CAS  Google Scholar 

  • Pereira-Leal JB, Seabra MC (2001) Evolution of the Rab family of small GTP-binding proteins. J Mol Biol 313:889–901

    Article  PubMed  CAS  Google Scholar 

  • Preuss ML, Serna J, Falbel TG, Bednarek SY, Nielsen E (2004) The Arabidopsis Rab GTPase RabA4b localizes to the tips of growing root hair cells. Plant Cell 16:1589–1603

    Article  PubMed  CAS  Google Scholar 

  • Preuss ML, Schmitz AJ, Thole JM, Bonner HK, Otegui MS, Nielsen E (2006) A role for the RabA4b effector protein PI-4Kbeta1 in polarized expansion of root hair cells in Arabidopsis thaliana. J Cell Biol 172:991–998

    Article  PubMed  CAS  Google Scholar 

  • Rensing SA, Lang D, Zimmer AD, Terry A, Salamov A, Shapiro H, Nishiyama T, Perroud PF, Lindquist EA, Kamisugi Y, Tanahashi T, Sakakibara K, Fujita T, Oishi K, Shin IT, Kuroki Y, Toyoda A, Suzuki Y, Hashimoto S, Yamaguchi K, Sugano S, Kohara Y, Fujiyama A, Anterola A, Aoki S, Ashton N, Barbazuk WB, Barker E, Bennetzen JL, Blankenship R, Cho SH, Dutcher SK, Estelle M, Fawcett JA, Gundlach H, Hanada K, Heyl A, Hicks KA, Hughes J, Lohr M, Mayer K, Melkozernov A, Murata T, Nelson DR, Pils B, Prigge M, Reiss B, Renner T, Rombauts S, Rushton PJ, Sanderfoot A, Schween G, Shiu SH, Stueber K, Theodoulou FL, Tu H, Van de Peer Y, Verrier PJ, Waters E, Wood A, Yang L, Cove D, Cuming AC, Hasebe M, Lucas S, Mishler BD, Reski R, Grigoriev IV, Quatrano RS, Boore JL (2008) The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319:64–69

    Article  PubMed  CAS  Google Scholar 

  • Robatzek S, Chinchilla D, Boller T (2006) Ligand-induced endocytosis of the pattern recognition receptor FLS2 in Arabidopsis. Genes Dev 20:537–542

    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 USA 105:8464–8469

    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

    Article  PubMed  CAS  Google Scholar 

  • Sanderfoot A (2007) Increases in the number of SNARE genes parallels the rise of multicellularity among the green plants. Plant Physiol 144:6–17

    Article  PubMed  CAS  Google Scholar 

  • Seabra MC, Coudrier E (2004) Rab GTPases and myosin motors in organelle motility. Traffic 5:393–399

    Article  PubMed  CAS  Google Scholar 

  • Shevell DE, Leu WM, Gillmor CS, Xia G, Feldmann KA, Chua NH (1994) EMB30 is essential for normal cell division, cell expansion, and cell adhesion in Arabidopsis and encodes a protein that has similarity to Sec7. Cell 77:1051–1062

    Article  PubMed  CAS  Google Scholar 

  • Shin HW, Hayashi M, Christoforidis S, Lacas-Gervais S, Hoepfner S, Wenk MR, Modregger J, Uttenweiler-Joseph S, Wilm M, Nystuen A, Frankel WN, Solimena M, De Camilli P, Zerial M (2005) An enzymatic cascade of Rab5 effectors regulates phosphoinositide turnover in the endocytic pathway. J Cell Biol 170:607–618

    Article  PubMed  CAS  Google Scholar 

  • Sivars U, Aivazian D, Pfeffer SR (2003) Yip3 catalyses the dissociation of endosomal Rab-GDI complexes. Nature 425:856–859

    Article  PubMed  CAS  Google Scholar 

  • Sohn EJ, Kim ES, Zhao M, Kim SJ, Kim H, Kim YW, Lee YJ, Hillmer S, Sohn U, Jiang L, Hwang I (2003) Rha1, an Arabidopsis Rab5 homolog, plays a critical role in the vacuolar trafficking of soluble cargo proteins. Plant Cell 15:1057–1070

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Stenmark H, Olkkonen VM (2001) The Rab GTPase family. Genome Biol 2:reviews3007.1–3007.7

    Google Scholar 

  • Strickland LI, Burgess DR (2004) Pathways for membrane trafficking during cytokinesis. Trends Cell Biol 14:115–118

    Article  PubMed  CAS  Google Scholar 

  • Sutter JU, Sieben C, Hartel A, Eisenach C, Thiel G, Blatt MR (2007) Abscisic acid triggers the endocytosis of the arabidopsis KAT1K+ channel and its recycling to the plasma membrane. Curr Biol 17:1396–1402

    Article  PubMed  CAS  Google Scholar 

  • Takai Y, Sasaki T, Matozaki T (2001) Small GTP-binding proteins. Physiol Rev 81:153–208

    PubMed  CAS  Google Scholar 

  • Takano J, Miwa K, Yuan L, von Wiren N, Fujiwara T (2005) Endocytosis and degradation of BOR1, a boron transporter of Arabidopsis thaliana, regulated by boron availability. Proc Natl Acad Sci USA 102:12276–12281

    Article  PubMed  CAS  Google Scholar 

  • Tanaka H, Dhonukshe P, Brewer PB, Friml J (2006) Spatiotemporal asymmetric auxin distribution: a means to coordinate plant development. Cell Mol Life Sci 63:2738–2754

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Toonen RF, Verhage M (2007) Munc18-1 in secretion: lonely Munc joins SNARE team and takes control. Trends Neurosci 30:564–572

    PubMed  CAS  Google Scholar 

  • Ueda T, Yamaguchi M, Uchimiya H, Nakano A (2001) Ara6, a plant-unique novel type Rab GTPase, functions in the endocytic pathway of Arabidopsis thaliana. EMBO J 20:4730–4741

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Ueda H, Nishiyama C, Shimada T, Koumoto Y, Hayashi Y, Kondo M, Takahashi T, Ohtomo I, Nishimura M, Hara-Nishimura I (2006) AtVAM3 is required for normal specification of idioblasts, myrosin cells. Plant Cell Physiol 47:164–175

    Article  PubMed  CAS  Google Scholar 

  • Uemura T, Ueda T, Ohniwa RL, Nakano A, Takeyasu K, Sato MH (2004) Systematic analysis of SNARE molecules in Arabidopsis: dissection of the post-Golgi network in plant cells. Cell Struct Funct 29:49–65

    Article  PubMed  CAS  Google Scholar 

  • Uemura T, Sato MH, Takeyasu K (2005) The longin domain regulates subcellular targeting of VAMP7 in Arabidopsis thaliana. FEBS Lett 579:2842–2846

    Article  PubMed  CAS  Google Scholar 

  • Ullrich O, Reinsch S, Urbe S, Zerial M, Parton RG (1996) Rab11 regulates recycling through the pericentriolar recycling endosome. J Cell Biol 135:913–924

    Article  PubMed  CAS  Google Scholar 

  • Umebayashi K, Nakano A (2003) Ergosterol is required for targeting of tryptophan permease to the yeast plasma membrane. J Cell Biol 161:1117–1131

    Article  PubMed  CAS  Google Scholar 

  • van Gisbergen PAC, Esseling-Ozdoba A, Vos JW (2008) Microinjecting FM4-64 validates it as a marker of the endocytic pathway in plants. J Microsc 231:284–290

    Article  PubMed  Google Scholar 

  • Wickner W, Schekman R (2008) Membrane fusion. Nat Struct Mol Biol 15:658–664

    Article  CAS  Google Scholar 

  • Zazimalova E, Krecek P, Skupa P, Hoyerova K, Petrasek J (2007) Polar transport of the plant hormone auxin—the role of PIN-FORMED (PIN) proteins. Cell Mol Life Sci 64:1621–1637

    Article  PubMed  CAS  Google Scholar 

  • Zerial M, McBride H (2001) Rab proteins as membrane organizers. Nat Rev 2:107–117

    Article  CAS  Google Scholar 

  • Zhang J, Hill DR, Sylvester AW (2007) Diversification of the RAB guanosine triphosphatase family in dicots and monocots. J Integr Plant Biol 49:1129–1141

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Takashi Ueda.

Additional information

Takashi Ueda is the recipient of the BSJ Award for Young Scientist, 2007.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ebine, K., Ueda, T. Unique mechanism of plant endocytic/vacuolar transport pathways. J Plant Res 122, 21–30 (2009). https://doi.org/10.1007/s10265-008-0200-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10265-008-0200-x

Keywords

Navigation