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Journey to the cell surface—the central role of the trans-Golgi network in plants

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Abstract

The secretion of proteins, lipids, and carbohydrates to the cell surface is essential for plant development and adaptation. Secreted substances synthesized at the endoplasmic reticulum pass through the Golgi apparatus and trans-Golgi network (TGN) en route to the plasma membrane via the conventional secretion pathway. The TGN is morphologically and functionally distinct from the Golgi apparatus. The TGN is located at the crossroads of many trafficking pathways and regulates a range of crucial processes including secretion to the cell surface, transport to the vacuole, and the reception of endocytic cargo. This review outlines the TGN’s central role in cargo secretion, showing that its behavior is more complex and controlled than the bulk-flow hypothesis suggests. Its formation, structure, and maintenance are discussed along with the formation and release of secretory vesicles.

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References

  • Asaoka R, Uemura T, Ito J, Fujimoto M, Ito E, Ueda T, Nakano A (2012) Arabidopsis RABA1 GTPases are involved in transport between the trans-Golgi network and the plasma membrane, and are required for salinity stress tolerance. Plant J

  • Aschenbrenner L, Naccache SN, Hasson T (2004) Uncoated endocytic vesicles require the unconventional myosin, Myo6, for rapid transport through actin barriers. Mol Biol Cell 15:2253–2263

    PubMed Central  CAS  PubMed  Google Scholar 

  • Assaad FF, Qiu JL, Youngs H, Ehrhardt D, Zimmerli L, Kalde M, Wanner G, Peck SC, Edwards H, Ramonell K, Somerville CR, Thordal-Christensen H (2004) The PEN1 syntaxin defines a novel cellular compartment upon fungal attack and is required for the timely assembly of papillae. Mol Biol Cell 15:5118–5129

    PubMed Central  CAS  PubMed  Google Scholar 

  • Baluska F, Liners F, Hlavacka A, Schlicht M, Van Cutsem P, McCurdy DW, Menzel D (2005) Cell wall pectins and xyloglucans are internalized into dividing root cells and accumulate within cell plates during cytokinesis. Protoplasma 225:141–155

    CAS  PubMed  Google Scholar 

  • Bard F, Malhotra V (2006) The formation of TGN-to-plasma-membrane transport carriers. Annu Rev Cell Dev Biol 22:439–455

    CAS  PubMed  Google Scholar 

  • Baron CL, Malhotra V (2002) Role of diacylglycerol in PKD recruitment to the TGN and protein transport to the plasma membrane. Science 295:325–328

    CAS  PubMed  Google Scholar 

  • Barr FA, Huttner WB (1996) A role for ADP-ribosylation factor 1, but not COP I, in secretory vesicle biogenesis from the trans-Golgi network. FEBS Lett 384:65–70

    CAS  PubMed  Google Scholar 

  • Barrowman J, Bhandari D, Reinisch K, Ferro-Novick S (2010) TRAPP complexes in membrane traffic: convergence through a common Rab. Nat Rev Mol Cell Biol 11:759–763

    CAS  PubMed  Google Scholar 

  • Bassham DC, Sanderfoot AA, Kovaleva V, Zheng H, Raikhel NV (2000) AtVPS45 complex formation at the trans-Golgi network. Mol Biol Cell 11:2251–2265

    PubMed Central  CAS  PubMed  Google Scholar 

  • Bottanelli F, Foresti O, Hanton S, Denecke J (2011) Vacuolar transport in tobacco leaf epidermis cells involves a single route for soluble cargo and multiple routes for membrane cargo. Plant Cell 23:3007–3025

    PubMed Central  CAS  PubMed  Google Scholar 

  • Boutte Y, Crosnier MT, Carraro N, Traas J, Satiat-Jeunemaitre B (2006) The plasma membrane recycling pathway and cell polarity in plants: studies on PIN proteins. J Cell Sci 119:1255–1265

    CAS  PubMed  Google Scholar 

  • Boutte Y, Jonsson K, McFarlane HE, Johnson E, Gendre D, Swarup R, Friml J, Samuels L, Robert S, Bhalerao RP (2013) ECHIDNA-mediated post-Golgi trafficking of auxin carriers for differential cell elongation. Proc Natl Acad Sci U S A 110:16259–16264

    PubMed Central  CAS  PubMed  Google Scholar 

  • Brandizzi F, Barlowe C (2013) Organization of the ER-Golgi interface for membrane traffic control. Nat Rev Mol Cell Biol 14:382–392

    PubMed Central  CAS  PubMed  Google Scholar 

  • Brownhill K, Wood L, Allan V (2009) Molecular motors and the Golgi complex: staying put and moving through. Semin Cell Dev Biol 20:784–792

    CAS  PubMed  Google Scholar 

  • Chen YG, Siddhanta A, Austin CD, Hammond SM, Sung TC, Frohman MA, Morris AJ, Shields D (1997) Phospholipase D stimulates release of nascent secretory vesicles from the trans-Golgi network. J Cell Biol 138:495–504

    PubMed Central  CAS  PubMed  Google Scholar 

  • Chen Y, Shin YK, Bassham DC (2005) YKT6 is a core constituent of membrane fusion machineries at the Arabidopsis trans-Golgi network. J Mol Biol 350:92–101

    CAS  PubMed  Google Scholar 

  • Chen Y, Chen T, Shen S, Zheng M, Guo Y, Lin J, Baluska F, Samaj J (2006) Differential display proteomic analysis of Picea meyeri pollen germination and pollen-tube growth after inhibition of actin polymerization by latrunculin B. Plant J 47:174–195

    CAS  PubMed  Google Scholar 

  • Chen X, Irani NG, Friml J (2011) Clathrin-mediated endocytosis: the gateway into plant cells. Curr Opin Plant Biol 14:674–682

    CAS  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

    PubMed Central  CAS  PubMed  Google Scholar 

  • Cole RA, Synek L, Zarsky V, Fowler JE (2005) SEC8, a subunit of the putative Arabidopsis exocyst complex, facilitates pollen germination and competitive pollen tube growth. Plant Physiol 138:2005–2018

    PubMed Central  CAS  PubMed  Google Scholar 

  • Crowell EF, Bischoff V, Desprez T, Rolland A, Stierhof YD, Schumacher K, Gonneau M, Hofte H, Vernhettes S (2009) Pausing of Golgi bodies on microtubules regulates secretion of cellulose synthase complexes in Arabidopsis. Plant Cell 21:1141–1154

    PubMed Central  CAS  PubMed  Google Scholar 

  • Damke H, Baba T, Warnock DE, Schmid SL (1994) Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. J Cell Biol 127:915–934

    CAS  PubMed  Google Scholar 

  • Danino D, Hinshaw JE (2001) Dynamin family of mechanoenzymes. Curr Opin Cell Biol 13:454–460

    CAS  PubMed  Google Scholar 

  • De Matteis MA, Godi A (2004) PI-loting membrane traffic. Nat Cell Biol 6:487–492

    PubMed  Google Scholar 

  • De Matteis MA, Luini A (2008) Exiting the Golgi complex. Nat Rev Mol Cell Biol 9:273–284

    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

    PubMed Central  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Ding Y, Robinson DG, Jiang L (2014a) Unconventional protein secretion (UPS) pathways in plants. Curr Opin Cell Biol 29C:107–115

    Google Scholar 

  • Ding Y, Wang J, Chun Lai JH, Ling Chan VH, Wang X, Cai Y, Tan X, Bao Y, Xia J, Robinson DG, Jiang L (2014b) Exo70E2 is essential for exocyst subunit recruitment and EXPO formation in both plants and animals. Mol Biol Cell 25:412–426

    PubMed Central  PubMed  Google Scholar 

  • Donohoe BS, Kang BH, Staehelin LA (2007) Identification and characterization of COPIa- and COPIb-type vesicle classes associated with plant and algal Golgi. Proc Natl Acad Sci U S A 104:163–168

    PubMed Central  CAS  PubMed  Google Scholar 

  • Drakakaki G, Dandekar A (2013) Protein secretion: how many secretory routes does a plant cell have? Plant Sci 203–204:74–78

    PubMed  Google Scholar 

  • Drakakaki G, van de Ven W, Pan S, Miao Y, Wang J, Keinath NF, Weatherly B, Jiang L, Schumacher K, Hicks G, Raikhel N (2012) Isolation and proteomic analysis of the SYP61 compartment reveal its role in exocytic trafficking in Arabidopsis. Cell Res 22:413–424

    PubMed Central  CAS  PubMed  Google Scholar 

  • El Kasmi F, Krause C, Hiller U, Stierhof YD, Mayer U, Conner L, Kong L, Reichardt I, Sanderfoot AA, Jurgens G (2013) SNARE complexes of different composition jointly mediate membrane fusion in Arabidopsis cytokinesis. Mol Biol Cell 24:1593–1601

    PubMed Central  PubMed  Google Scholar 

  • Enami K, Ichikawa M, Uemura T, Kutsuna N, Hasezawa S, Nakagawa T, Nakano A, Sato MH (2009) Differential expression control and polarized distribution of plasma membrane-resident SYP1 SNAREs in Arabidopsis thaliana. Plant Cell Physiol 50:280–289

    CAS  PubMed  Google Scholar 

  • Faso C, Boulaflous A, Brandizzi F (2009) The plant Golgi apparatus: last 10 years of answered and open questions. FEBS Lett 583:3752–3757

    CAS  PubMed  Google Scholar 

  • Fendrych M, Synek L, Pecenkova T, Drdova EJ, Sekeres J, de Rycke R, Nowack MK, Zarsky V (2013) Visualization of the exocyst complex dynamics at the plasma membrane of Arabidopsis thaliana. Mol Biol Cell 24:510–520

    PubMed Central  CAS  PubMed  Google Scholar 

  • Feraru E, Feraru MI, Asaoka R, Paciorek T, De Rycke R, Tanaka H, Nakano A, Friml J (2012) BEX5/RabA1b regulates trans-Golgi network-to-plasma membrane protein trafficking in Arabidopsis. Plant Cell 24:3074–3086

    PubMed Central  CAS  PubMed  Google Scholar 

  • Fischer von Mollard G, Stevens TH (1999) The Saccharomyces cerevisiae v-SNARE Vti1p is required for multiple membrane transport pathways to the vacuole. Mol Biol Cell 10:1719–1732

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Geelen D, Leyman B, Batoko H, Di Sansebastiano GP, Moore I, Blatt MR (2002) The abscisic acid-related SNARE homolog NtSyr1 contributes to secretion and growth: evidence from competition with its cytosolic domain. Plant Cell 14:387–406

    PubMed Central  CAS  PubMed  Google Scholar 

  • Gendre D, Oh J, Boutte Y, Best JG, Samuels L, Nilsson R, Uemura T, Marchant A, Bennett MJ, Grebe M, Bhalerao RP (2011) Conserved Arabidopsis ECHIDNA protein mediates trans-Golgi-network trafficking and cell elongation. Proc Natl Acad Sci U S A 108:8048–8053

    PubMed Central  CAS  PubMed  Google Scholar 

  • Gendre D, McFarlane HE, Johnson E, Mouille G, Sjodin A, Oh J, Levesque-Tremblay G, Watanabe Y, Samuels L, Bhalerao RP (2013) Trans-Golgi network localized ECHIDNA/Ypt interacting protein complex is required for the secretion of cell wall polysaccharides in Arabidopsis. Plant Cell 25:2633–2646

    PubMed Central  CAS  PubMed  Google Scholar 

  • Gu Y, Innes RW (2012) The KEEP ON GOING protein of Arabidopsis regulates intracellular protein trafficking and is degraded during fungal infection. Plant Cell 24:4717–4730

    PubMed Central  CAS  PubMed  Google Scholar 

  • Gu F, Crump CM, Thomas G (2001) Trans-Golgi network sorting. Cell Mol Life Sci 58:1067–1084

    PubMed Central  CAS  PubMed  Google Scholar 

  • Hala M, Cole R, Synek L, Drdova E, Pecenkova T, Nordheim A, Lamkemeyer T, Madlung J, Hochholdinger F, Fowler JE, Zarsky V (2008) An exocyst complex functions in plant cell growth in Arabidopsis and tobacco. Plant Cell 20:1330–1345

    PubMed Central  CAS  PubMed  Google Scholar 

  • Hawes C, Satiat-Jeunemaitre B (2005) The plant Golgi apparatus—going with the flow. Biochim Biophys Acta 1744:466–480

    PubMed  Google Scholar 

  • Hawes C, Schoberer J, Hummel E, Osterrieder A (2010) Biogenesis of the plant Golgi apparatus. Biochem Soc Trans 38:761–767

    CAS  PubMed  Google Scholar 

  • Hinz G, Colanesi S, Hillmer S, Rogers JC, Robinson DG (2007) Localization of vacuolar transport receptors and cargo proteins in the Golgi apparatus of developing Arabidopsis embryos. Traffic 8:1452–1464

    CAS  PubMed  Google Scholar 

  • Holthuis JC, Nichols BJ, Dhruvakumar S, Pelham HR (1998) Two syntaxin homologues in the TGN/endosomal system of yeast. EMBO J 17:113–126

    PubMed Central  CAS  PubMed  Google Scholar 

  • Holtzman E, Novikoff AB, Villaverde H (1967) Lysosomes and GERL in normal and chromatolytic neurons of the rat ganglion nodosum. J Cell Biol 33:419–435

    PubMed Central  CAS  PubMed  Google Scholar 

  • Hong Z, Bednarek SY, Blumwald E, Hwang I, Jurgens G, Menzel D, Osteryoung KW, Raikhel NV, Shinozaki K, Tsutsumi N, Verma DP (2003) A unified nomenclature for Arabidopsis dynamin-related large GTPases based on homology and possible functions. Plant Mol Biol 53:261–265

    CAS  PubMed  Google Scholar 

  • Ichikawa M, Hirano T, Enami K, Fuselier T, Kato N, Kwon C, Voigt B, Schulze-Lefert P, Baluska F, Sato MH (2014) Syntaxin of plant proteins SYP123 and SYP132 mediate root hair tip growth in Arabidopsis thaliana. Plant Cell Physiol 55:790–800

    CAS  PubMed  Google Scholar 

  • Jaber E, Thiele K, Kindzierski V, Loderer C, Rybak K, Jurgens G, Mayer U, Sollner R, Wanner G, Assaad FF (2010) A putative TRAPPII tethering factor is required for cell plate assembly during cytokinesis in Arabidopsis. New Phytol 187:751–763

    CAS  PubMed  Google Scholar 

  • Jin JB, Kim YA, Kim SJ, Lee SH, Kim DH, Cheong GW, Hwang I (2001) A new dynamin-like protein, ADL6, is involved in trafficking from the trans-Golgi network to the central vacuole in Arabidopsis. Plant Cell 13:1511–1526

    PubMed Central  CAS  PubMed  Google Scholar 

  • Jones SM, Howell KE, Henley JR, Cao H, McNiven MA (1998) Role of dynamin in the formation of transport vesicles from the trans-Golgi network. Science 279:573–577

    CAS  PubMed  Google Scholar 

  • Kang BH (2011) Shrinkage and fragmentation of the trans-Golgi network in non-meristematic plant cells. Plant Signal Behav 6:884–886

    PubMed Central  CAS  PubMed  Google Scholar 

  • Kang BH, Staehelin LA (2008) ER-to-Golgi transport by COPII vesicles in Arabidopsis involves a ribosome-excluding scaffold that is transferred with the vesicles to the Golgi matrix. Protoplasma 234:51–64

    CAS  PubMed  Google Scholar 

  • Kang BH, Nielsen E, Preuss ML, Mastronarde D, Staehelin LA (2011) Electron tomography of RabA4b- and PI-4Kbeta1-labeled trans Golgi network compartments in Arabidopsis. Traffic 12:313–329

    CAS  PubMed  Google Scholar 

  • Kargul J, Gansel X, Tyrrell M, Sticher L, Blatt MR (2001) Protein-binding partners of the tobacco syntaxin NtSyr1. FEBS Lett 508:253–258

    CAS  PubMed  Google Scholar 

  • Kienzle C, von Blume J (2014) Secretory cargo sorting at the trans-Golgi network. Trends Cell Biol

  • Kim SJ, Bassham DC (2013) Functional redundancy between trans-Golgi network SNARE family members in Arabidopsis thaliana. BMC Biochem 14:22

    PubMed Central  CAS  PubMed  Google Scholar 

  • Klumperman J (2011) Architecture of the mammalian Golgi. Cold Spring Harb Perspect Biol 3

  • Krause C, Richter S, Knoll C, Jurgens G (2013) Plant secretome—from cellular process to biological activity. Biochim Biophys Acta 1834:2429–2441

    CAS  PubMed  Google Scholar 

  • Kulich I, Cole R, Drdova E, Cvrckova F, Soukup A, Fowler J, Zarsky V (2010) Arabidopsis exocyst subunits SEC8 and EXO70A1 and exocyst interactor ROH1 are involved in the localized deposition of seed coat pectin. New Phytol 188:615–625

    CAS  PubMed  Google Scholar 

  • Kulich I, Pecenkova T, Sekeres J, Smetana O, Fendrych M, Foissner I, Hoftberger M, Zarsky V (2013) Arabidopsis exocyst subcomplex containing subunit EXO70B1 is involved in autophagy-related transport to the vacuole. Traffic 14:1155–1165

    CAS  PubMed  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

    CAS  PubMed  Google Scholar 

  • Leucci MR, Di Sansebastiano GP, Gigante M, Dalessandro G, Piro G (2007) Secretion marker proteins and cell-wall polysaccharides move through different secretory pathways. Planta 225:1001–1017

    CAS  PubMed  Google Scholar 

  • Liljedahl M, Maeda Y, Colanzi A, Ayala I, Van Lint J, Malhotra V (2001) Protein kinase D regulates the fission of cell surface destined transport carriers from the trans-Golgi network. Cell 104:409–420

    CAS  PubMed  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

    CAS  PubMed  Google Scholar 

  • Loubery S, Coudrier E (2008) Myosins in the secretory pathway: tethers or transporters? Cell Mol Life Sci 65:2790–2800

    CAS  PubMed  Google Scholar 

  • Luini A, Mironov AA, Polishchuk EV, Polishchuk RS (2008) Morphogenesis of post-Golgi transport carriers. Histochem Cell Biol 129:153–161

    PubMed Central  CAS  PubMed  Google Scholar 

  • Madison SL, Nebenfuhr A (2013) Understanding myosin functions in plants: are we there yet? Curr Opin Plant Biol 16:710–717

    CAS  PubMed  Google Scholar 

  • Malinovsky FG, Fangel JU, Willats WG (2014) The role of the cell wall in plant immunity. Front Plant Sci 5:178

    PubMed Central  PubMed  Google Scholar 

  • Malsam J, Kreye S, Sollner TH (2008) Membrane fusion: SNAREs and regulation. Cell Mol Life Sci 65:2814–2832

    CAS  PubMed  Google Scholar 

  • Marmiroli N, Maestri E (2014) Plant peptides in defense and signaling. Peptides 56C:30–44

    Google Scholar 

  • Marty F (1978) Cytochemical studies on GERL, provacuoles, and vacuoles in root meristematic cells of Euphorbia. Proc Natl Acad Sci U S A 75:852–856

    PubMed Central  CAS  PubMed  Google Scholar 

  • McFarlane HE, Young RE, Wasteneys GO, Samuels AL (2008) Cortical microtubules mark the mucilage secretion domain of the plasma membrane in Arabidopsis seed coat cells. Planta 227:1363–1375

    CAS  PubMed  Google Scholar 

  • McFarlane HE, Watanabe Y, Gendre D, Carruthers K, Levesque-Tremblay G, Haughn GW, Bhalerao RP, Samuels L (2013) Cell wall polysaccharides are mislocalized to the vacuole in echidna mutants. Plant Cell Physiol 54:1867–1880

    CAS  PubMed  Google Scholar 

  • McFarlane HE, Watanabe Y, Yang W, Huang Y, Ohlrogge J, Samuels AL (2014) Golgi- and trans-Golgi network-mediated vesicle trafficking is required for wax secretion from epidermal cells. Plant Physiol 164:1250–1260

    PubMed Central  CAS  PubMed  Google Scholar 

  • Mogelsvang S, Marsh BJ, Ladinsky MS, Howell KE (2004) Predicting function from structure: 3D structure studies of the mammalian Golgi complex. Traffic 5:338–345

    CAS  PubMed  Google Scholar 

  • Mollenhauer HH, Morre DJ (1966) Tubular connections between dictyosomes and forming secretory vesicles in plant Golgi apparatus. J Cell Biol 29:373–376

    PubMed Central  CAS  PubMed  Google Scholar 

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

    PubMed Central  CAS  PubMed  Google Scholar 

  • Novikoff PM, Novikoff AB, Quintana N, Hauw JJ (1971) Golgi apparatus, GERL, and lysosomes of neurons in rat dorsal root ganglia, studied by thick section and thin section cytochemistry. J Cell Biol 50:859–886

    PubMed Central  CAS  PubMed  Google Scholar 

  • Pappan K, Austin-Brown S, Chapman KD, Wang X (1998) Substrate selectivities and lipid modulation of plant phospholipase D alpha, -beta, and -gamma. Arch Biochem Biophys 353:131–140

    CAS  PubMed  Google Scholar 

  • Parton RM, Fischer-Parton S, Watahiki MK, Trewavas AJ (2001) Dynamics of the apical vesicle accumulation and the rate of growth are related in individual pollen tubes. J Cell Sci 114:2685–2695

    CAS  PubMed  Google Scholar 

  • Peremyslov VV, Prokhnevsky AI, Dolja VV (2010) Class XI myosins are required for development, cell expansion, and F-Actin organization in Arabidopsis. Plant Cell 22:1883–1897

    PubMed Central  CAS  PubMed  Google Scholar 

  • Pesacreta TC, Lucas WJ (1984) Plasma membrane coat and a coated vesicle-associated reticulum of membranes: their structure and possible interrelationship in Chara corallina. J Cell Biol 98:1537–1545

    CAS  PubMed  Google Scholar 

  • Picton JM, Steer MW (1981) Determination of secretory vesicle production rates by dictyosomes in pollen tubes of Tradescantia using cytochalasin D. J Cell Sci 49:261–272

    CAS  PubMed  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

    PubMed Central  CAS  PubMed  Google Scholar 

  • Preuss ML, Schmitz AJ, Thole JM, Bonner HK, Otegui MS, and 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

  • Qi X, Zheng H (2011) Arabidopsis TRAPPII is functionally linked to Rab-A, but not Rab-D in polar protein trafficking in trans-Golgi network. Plant Signal Behav 6:1679–1683

    PubMed Central  CAS  PubMed  Google Scholar 

  • Qi X, Kaneda M, Chen J, Geitmann A, Zheng H (2011) A specific role for Arabidopsis TRAPPII in post-Golgi trafficking that is crucial for cytokinesis and cell polarity. Plant J 68:234–248

    CAS  PubMed  Google Scholar 

  • Reichardt I, Stierhof YD, Mayer U, Richter S, Schwarz H, Schumacher K, Jurgens G (2007) Plant cytokinesis requires de novo secretory trafficking but not endocytosis. Curr Biol 17:2047–2053

    CAS  PubMed  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

    PubMed Central  CAS  PubMed  Google Scholar 

  • Robinson MS, Bonifacino JS (2001) Adaptor-related proteins. Curr Opin Cell Biol 13:444–453

    CAS  PubMed  Google Scholar 

  • Robinson DG, Pimpl P (2014) Clathrin and post-Golgi trafficking: a very complicated issue. Trends Plant Sci 19:134–139

    CAS  PubMed  Google Scholar 

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

    PubMed Central  CAS  PubMed  Google Scholar 

  • Rosen WG, Gawlik SR, Dashek WV, Siegesmund KA (1964) Fine structure and cytochemistry of Lilium pollen tubes. Am J Bot 51:61–71

    CAS  Google Scholar 

  • Rutherford S, Moore I (2002) The Arabidopsis Rab GTPase family: another enigma variation. Curr Opin Plant Biol 5:518–528

    CAS  PubMed  Google Scholar 

  • Rybak K, Steiner A, Synek L, Klaeger S, Kulich I, Facher E, Wanner G, Kuster B, Zarsky V, Persson S, Assaad FF (2014) Plant cytokinesis is orchestrated by the sequential action of the TRAPPII and exocyst tethering complexes. Dev Cell 29:607–620

    CAS  PubMed  Google Scholar 

  • Sacher M, Kim YG, Lavie A, Oh BH, Segev N (2008) The TRAPP complex: insights into its architecture and function. Traffic 9:2032–2042

    PubMed Central  CAS  PubMed  Google Scholar 

  • Salim K, Bottomley MJ, Querfurth E, Zvelebil MJ, Gout I, Scaife R, Margolis RL, Gigg R, Smith CI, Driscoll PC, Waterfield MD, Panayotou G (1996) Distinct specificity in the recognition of phosphoinositides by the pleckstrin homology domains of dynamin and Bruton’s tyrosine kinase. EMBO J 15:6241–6250

    PubMed Central  CAS  PubMed  Google Scholar 

  • Sanderfoot AA, Ahmed SU, Marty-Mazars D, Rapoport I, Kirchhausen T, Marty F, Raikhel NV (1998) A putative vacuolar cargo receptor partially colocalizes with AtPEP12p on a prevacuolar compartment in Arabidopsis roots. Proc Natl Acad Sci U S A 95:9920–9925

    PubMed Central  CAS  PubMed  Google Scholar 

  • Sanderfoot AA, Kovaleva V, Bassham DC, Raikhel NV (2001) Interactions between syntaxins identify at least five SNARE complexes within the Golgi/prevacuolar system of the Arabidopsis cell. Mol Biol Cell 12:3733–3743

    PubMed Central  CAS  PubMed  Google Scholar 

  • Sauer M, Delgadillo MO, Zouhar J, Reynolds GD, Pennington JG, Jiang L, Liljegren SJ, Stierhof YD, De Jaeger G, Otegui MS, Bednarek SY, Rojo E (2013) MTV1 and MTV4 encode plant-specific ENTH and ARF GAP proteins that mediate clathrin-dependent trafficking of vacuolar cargo from the trans-Golgi network. Plant Cell 25:2217–2235

    PubMed Central  CAS  PubMed  Google Scholar 

  • Scheuring D, Viotti C, Kruger F, Kunzl 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • Staehelin LA, Kang BH (2008) Nanoscale architecture of endoplasmic reticulum export sites and of Golgi membranes as determined by electron tomography. Plant Physiol 147:1454–1468

    PubMed Central  CAS  PubMed  Google Scholar 

  • Stierhof YD, El Kasmi F (2010) Strategies to improve the antigenicity, ultrastructure preservation and visibility of trafficking compartments in Arabidopsis tissue. Eur J Cell Biol 89:285–297

    CAS  PubMed  Google Scholar 

  • Stierhof YD, Viotti C, Scheuring D, Sturm S, Robinson DG (2013) Sorting nexins 1 and 2a locate mainly to the TGN. Protoplasma 250:235–240

    CAS  PubMed  Google Scholar 

  • Suda Y, Nakano A (2012) The yeast Golgi apparatus. Traffic 13:505–510

    CAS  PubMed  Google Scholar 

  • Surma MA, Klose C, Simons K (2012) Lipid-dependent protein sorting at the trans-Golgi network. Biochim Biophys Acta 1821:1059–1067

    CAS  PubMed  Google Scholar 

  • Synek L, Schlager N, Elias M, Quentin M, Hauser MT, Zarsky V (2006) AtEXO70A1, a member of a family of putative exocyst subunits specifically expanded in land plants, is important for polar growth and plant development. Plant J 48:54–72

    PubMed Central  CAS  PubMed  Google Scholar 

  • Tanchak MA, Griffing LR, Mersey BG, Fowke LC (1984) Endocytosis of cationized ferritin by coated vesicles of soybean protoplasts. Planta 162:481–486

    CAS  PubMed  Google Scholar 

  • Thomas PD, Poznansky MJ (1989) Curvature and composition-dependent lipid asymmetry in phosphatidylcholine vesicles containing phosphatidylethanolamine and gangliosides. Biochim Biophys Acta 978:85–90

    CAS  PubMed  Google Scholar 

  • Toyooka K, Goto Y, Asatsuma S, Koizumi M, Mitsui T, Matsuoka K (2009) A mobile secretory vesicle cluster involved in mass transport from the Golgi to the plant cell exterior. Plant Cell 21:1212–1229

    PubMed Central  CAS  PubMed  Google Scholar 

  • Ueda H, Yokota E, Kutsuna N, Shimada T, Tamura K, Shimmen T, Hasezawa S, Dolja VV, Hara-Nishimura I (2010) Myosin-dependent endoplasmic reticulum motility and F-actin organization in plant cells. Proc Natl Acad Sci U S A 107:6894–6899

    PubMed Central  CAS  PubMed  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

    CAS  PubMed  Google Scholar 

  • Uemura T, Kim H, Saito C, Ebine K, Ueda T, Schulze-Lefert P, Nakano A (2012) Qa-SNAREs localized to the trans-Golgi network regulate multiple transport pathways and extracellular disease resistance in plants. Proc Natl Acad Sci U S A 109:1784–1789

    PubMed Central  CAS  PubMed  Google Scholar 

  • Uemura T, Suda Y, Ueda T, Nakano A (2014) Dynamic behavior of the trans-Golgi network in root tissues of Arabidopsis revealed by super-resolution live imaging. Plant Cell Physiol 55:694–703

    CAS  PubMed  Google Scholar 

  • van Dam EM, Stoorvogel W (2002) Dynamin-dependent transferrin receptor recycling by endosome-derived clathrin-coated vesicles. Mol Biol Cell 13:169–182

    PubMed Central  PubMed  Google Scholar 

  • van Meer G, Voelker DR, Feigenson GW (2008) Membrane lipids: where they are and how they behave. Nat Rev Mol Cell Biol 9:112–124

    PubMed Central  PubMed  Google Scholar 

  • van Weering JR, Verkade P, Cullen PJ (2010) SNX-BAR proteins in phosphoinositide-mediated, tubular-based endosomal sorting. Semin Cell Dev Biol 21:371–380

    PubMed Central  PubMed  Google Scholar 

  • VanDerWoude WJ, Morre DJ, Bracker CE (1971) Isolation and characterization of secretory vesicles in germinated pollen of Lilium longiflorum. J Cell Sci 8:331–351

    CAS  PubMed  Google Scholar 

  • Vicré M, Jauneau A, Knox JP, Driouich A (1998) Immunolocalization of beta (1–4) and beta-(1–6)-D-galactan epitopes in the cell wall and Golgi stacks of developing flax root tissues. Protoplasma 203:26–34

    Google Scholar 

  • Viotti C, Bubeck J, Stierhof YD, Krebs M, Langhans M, van den Berg W, van Dongen W, Richter S, Geldner N, Takano J, Jurgens G, de Vries SC, Robinson DG, Schumacher K (2010) Endocytic and secretory traffic in Arabidopsis merge in the trans-Golgi network/early endosome, an independent and highly dynamic organelle. Plant Cell 22:1344–1357

    PubMed Central  CAS  PubMed  Google Scholar 

  • von Blume J, Duran JM, Forlanelli E, Alleaume AM, Egorov M, Polishchuk R, Molina H, Malhotra V (2009) Actin remodeling by ADF/cofilin is required for cargo sorting at the trans-Golgi network. J Cell Biol 187:1055–1069

    Google Scholar 

  • von Blume J, Alleaume AM, Kienzle C, Carreras-Sureda A, Valverde M, Malhotra V (2012) Cab45 is required for Ca(2+)-dependent secretory cargo sorting at the trans-Golgi network. J Cell Biol 199:1057–1066

    Google Scholar 

  • Wang X, Teng Y, Wang Q, Li X, Sheng X, Zheng M, Samaj J, Baluska F, Lin J (2006) Imaging of dynamic secretory vesicles in living pollen tubes of Picea meyeri using evanescent wave microscopy. Plant Physiol 141:1591–1603

    PubMed Central  CAS  PubMed  Google Scholar 

  • Wang J, Ding Y, Hillmer S, Miao Y, Lo SW, Wang X, Robinson DG, Jiang L (2010) EXPO, an exocyst-positive organelle distinct from multivesicular endosomes and autophagosomes, mediates cytosol to cell wall exocytosis in Arabidopsis and tobacco cells. Plant Cell 22:4009–4030

    PubMed Central  CAS  PubMed  Google Scholar 

  • Wei L, Zhang W, Liu Z, Li Y (2009) AtKinesin-13A is located on Golgi-associated vesicle and involved in vesicle formation/budding in Arabidopsis root-cap peripheral cells. BMC Plant Biol 9:138

    PubMed Central  PubMed  Google Scholar 

  • Wolf S, Hematy K, Hofte H (2012) Growth control and cell wall signaling in plants. Annu Rev Plant Biol 63:381–407

    CAS  PubMed  Google Scholar 

  • Xiang L, Etxeberria E, Van den Ende W (2013) Vacuolar protein sorting mechanisms in plants. FEBS J 280:979–993

    CAS  PubMed  Google Scholar 

  • Young RE, McFarlane HE, Hahn MG, Western TL, Haughn GW, Samuels AL (2008) Analysis of the Golgi apparatus in Arabidopsis seed coat cells during polarized secretion of pectin-rich mucilage. Plant Cell 20:1623–1638

    PubMed Central  CAS  PubMed  Google Scholar 

  • Zarsky V, Cvrckova F, Potocky M, Hala M (2009) Exocytosis and cell polarity in plants—exocyst and recycling domains. New Phytol 183:255–272

    CAS  PubMed  Google Scholar 

  • Zarsky V, Kulich I, Fendrych M, Pecenkova T (2013) Exocyst complexes multiple functions in plant cells secretory pathways. Curr Opin Plant Biol 16:726–733

    CAS  PubMed  Google Scholar 

  • Zhang L, Zhang H, Liu P, Hao H, Jin JB, Lin J (2011) Arabidopsis R-SNARE proteins VAMP721 and VAMP722 are required for cell plate formation. PLoS One 6:e26129

    PubMed Central  CAS  PubMed  Google Scholar 

  • Zheng H, Bednarek SY, Sanderfoot AA, Alonso J, Ecker JR, Raikhel NV (2002) NPSN11 is a cell plate-associated SNARE protein that interacts with the syntaxin KNOLLE. Plant Physiol 129:530–539

    PubMed Central  CAS  PubMed  Google Scholar 

  • Zouhar J, Rojo E, Bassham DC (2009) AtVPS45 is a positive regulator of the SYP41/SYP61/VTI12 SNARE complex involved in trafficking of vacuolar cargo. Plant Physiol 149:1668–1678

    PubMed Central  CAS  PubMed  Google Scholar 

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Acknowledgments

RPB thanks the Knut and Alice Wallenberg foundation for financial support. We thank Heather McFarlane for the careful reading of the manuscript and helpful insights.

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Authors and Affiliations

  1. Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, SE-901 83, Umeå, Sweden

    Delphine Gendre, Kristoffer Jonsson & Rishikesh P. Bhalerao

  2. Membrane Biogenesis Laboratory, UMR 5200 CNRS, Université Bordeaux Segalen, Bâtiment A3, INRA Bordeaux Aquitaine BP 81, 71 Avenue Edouard Bourlaux, 33883 Villenave d’Ornon Cedex, Bordeaux, France

    Yohann Boutté

  3. College of Science, King Saud University, Riyadh, 11451, Kingdom of Saudi Arabia

    Rishikesh P. Bhalerao

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  1. Delphine Gendre
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  2. Kristoffer Jonsson
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  4. Rishikesh P. Bhalerao
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Correspondence to Delphine Gendre or Rishikesh P. Bhalerao.

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Gendre, D., Jonsson, K., Boutté, Y. et al. Journey to the cell surface—the central role of the trans-Golgi network in plants. Protoplasma 252, 385–398 (2015). https://doi.org/10.1007/s00709-014-0693-1

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