Delivery and final fusion of the secretory vesicles with the relevant target membrane are hierarchically organized and reciprocally interconnected multi-step processes involving not only specific protein-protein interactions, but also specific protein-phospholipid interactions. The exocyst was discovered as a tethering complex mediating initial encounter of arriving exocytic vesicles with the plasma membrane. The exocyst complex is regulated by Rab and Rho small GTPases, resulting in docking of exocytic vesicles to the plasma membrane (PM) and finally their fusion mediated by specific SNARE complexes. In model Opisthokont cells, the exocyst was shown to directly interact with both microtubule and microfilament cytoskeleton and related motor proteins as well as with the PM via phosphatidylinositol 4, 5-bisphosphate specific binding, which directly affects cortical cytoskeleton and PM dynamics. Here we summarize the current knowledge on exocyst-cytoskeleton-PM interactions in order to open a perspective for future research in this area in plant cells.

Laboratory of Cell Biology Institute of Experimental Botany Academy of Sciences of the Czech Republic Prague Czech Republic

Laboratory of Cell Biology Institute of Experimental Botany Academy of Sciences of the Czech Republic Prague Czech Republic ; Laboratory of Plant Cell Biology Department of Experimental Plant Biology Faculty of Science Charles University Prague Czech Republic

See more in PubMed

Adamo J. E., Rossi G., Brennwald P. (1999). The Rho GTPase Rho3 has a direct role in exocytosis that is distinct from its role in actin polarity. Mol. Biol. Cell 10 4121–4133 10.1091/mbc.10.12.4121 PubMed DOI PMC

Aronov S., Gerst J. E. (2004). Involvement of the late secretory pathway in actin regulation and mRNA transport in yeast. J. Biol. Chem. 279 36962–36971 10.1074/jbc.M402068200 PubMed DOI

Bendezú F. O., Martin S. G. (2011). Actin cables and the exocyst form two independent morphogenesis pathways in the fission yeast. Mol. Biol. Cell 22 44–53 10.1091/mbc.E10-08-0720 PubMed DOI PMC

Bendezú F. O., Martin S. G. (2013). Cdc42 explores the cell periphery for mate selection in fission yeast. Curr. Biol. 23 42–47 10.1016/j.cub.2012.10.042 PubMed DOI

Bendezú F. O., Vincenzetti V., Martin S. G. (2012). Fission yeast Sec3 and Exo70 are transported on actin cables and localize the exocyst complex to cell poles. PLoS ONE 7 e40248 10.1371/journal.pone.0040248 PubMed DOI PMC

Birkenfeld J., Nalbant P., Bohl B. P., Pertz O., Hahn K. M., Bokoch G. M. (2007). GEF-H1 modulates localized RhoA activation during cytokinesis under the control of mitotic kinases. Dev. Cell 12 699–712 10.1016/j.devcel.2007.03.014 PubMed DOI PMC

Boyd C., Hughes T., Pypaert M., Novick P. (2004). Vesicles carry most exocyst subunits to exocytic sites marked by the remaining two subunits, Sec3p and Exo70p. J. Cell Biol. 167 889–901 10.1083/jcb.200408124 PubMed DOI PMC

Brymora A., Valova V. A., Larsen M. R., Roufogalis B. D., Robinson P. J. (2001). The brain exocyst complex interacts with RalA in a GFP-dependent manner: identification of a novel mammalian Sec3 gene and a second Sec15 gene. J. Biol. Chem. 276 29792–29797 10.1074/jbc.C100320200 PubMed DOI

Chen X. W., Leto D., Chiang S. H., Wang Q., Saltiel A. R. (2007). Activation of RalA is required for insulin-stimulated Glut4 trafficking to the plasma membrane via the exocyst and the motor protein Myo1c. Dev. Cell 13 391–404 10.1016/j.devcel.2007.07.007 PubMed DOI

Cvrčková F. (2013). Formins and membranes: anchoring cortical actin to the cell wall and beyond. Front. Plant Sci. 4 436 PubMed PMC

Cvrčková F., Grunt M., Bezvoda R., Hála M., Kulich I., Rawat A., et al. (2012). Evolution of the land plant exocyst complexes. Front. Plant Sci. 3 159 10.3389/fpls.2012.00159 PubMed DOI PMC

de Curtis I., Meldolesi J. (2012). Cell surface dynamics – how Rho GTPases orchestrate the interplay between the plasma membrane and the cortical cytoskeleton. J. Cell Sci. 125 4435–4444 10.1242/jcs.108266 PubMed DOI

Donovan K. W., Bretscher A. (2012). Myosin-V is activated by binding secretory cargo and released in coordination with Rab/exocyst function. Dev. Cell 23 769–781 10.1016/j.devcel.2012.09.001 PubMed DOI PMC

Estravïs M., Rincón S. A., Santos B, Pérez P. (2011). Cdc42 regulates multiple membrane traffic events in fission yeast. Traffic 12 1744–1758 10.1111/j.1600-0854.2011.01275.xd PubMed DOI

Feig L. A., Urano T., Cantor S. (1996). Evidence for a Ras/Ral signaling cascade. Trends Biochem. Sci. 21 438–441 10.1016/S0968-0004(96)10058-X PubMed DOI

Fendrych M., Synek L., Pecenková T., Drdová E. J., Sekeres J., de Rycke R., et al. (2013). Visualization of the exocyst complex dynamics at the plasma membrane of Arabidopsis thaliana. Mol. Biol. Cell 24 510–520 10.1091/mbc.E12-06-0492 PubMed DOI PMC

Fendrych M., Synek L., Pecenkova T., Toupalova H., Cole R., Drdova E., et al. (2010). The Arabidopsis exocyst complex is involved in cytokinesis and cell plate maturation. Plant Cell 22 3053–3065 10.1105/tpc.110.074351 PubMed DOI PMC

Finger F. P., Hughes T. E., Novick P. (1998). Sec3p is a spatial landmark for polarized secretion in budding yeast. Cell 92 559–571 10.1016/S0092-8674(00)80948-4 PubMed DOI

Fukai S., Matern H. T., Jagath J. R., Scheller R. H., Brunger A. T. (2003). Structural basis of the interaction between RalA and Sec5, a subunit of the sec6/8 complex. EMBO J. 22 3267–3278 10.1093/emboj/cdg329 PubMed DOI PMC

Fu Y., Wu G., Yang Z. (2001). Rop GTPase-dependent dynamics of tip-localized F-actin controls tip growth in pollen tubes. J. Cell Biol. 152 1019–1032 10.1083/jcb.152.5.1019 PubMed DOI PMC

Guo W., Roth D., Walch-Solimena C., Novick P. (1999). The exocyst is an effector for Sec4p, targeting secretory vesicles to sites of exocytosis. EMBO J. 4 71–80 PubMed PMC

Hála M., Cole R., Synek L., Drdová E., Pecenková T., Nordheim A., et al. (2008). An exocyst complex functions in plant cell growth in Arabidopsis and tobacco. Plant Cell 20 1330–1345 10.1105/tpc.108.059105 PubMed DOI PMC

Hammer J. A., Sellers J. R. (2012). Walking to work: roles for class V myosins as cargo transporters. Nat. Rev. Mol. Cell. Biol. 13 13–26 10.1038/nrm3248 PubMed DOI

Hazak O., Bloch D., Poraty L., Sternberg H., Zhang J., Friml J., et al. (2010). A RHO scaffold integrates the secretory system with feedback mechanisms in regulation of auxin distribution. PLoS Biol. 8 e1000282 10.1371/journal.pbio.1000282 PubMed DOI PMC

Hazelett C. C., Yeaman C. (2012). Sec5 and Exo84 mediate distinct aspects of RalA-dependent cell polarization. PLoS ONE 7 e39602 10.1371/journal.pone.0039602 PubMed DOI PMC

He B., Xi F., Zhang X., Zhang J., Guo W. (2007). Exo70 interacts with phospholipids and mediates the targeting of the exocyst to the plasma membrane. EMBO J. 26 4053–4065 10.1038/sj.emboj.7601834 PubMed DOI PMC

Heider M. R., Munson M. (2012). Exorcising the exocyst complex. Traffic 13 898–907 10.1111/j.1600-0854.2012.01353.x PubMed DOI PMC

Holubcová Z., Howard G., Schuh M. (2013). Vesicles modulate an actin network for asymmetric spindle positioning. Nat. Cell Biol. 15 937–947 10.1038/ncb2802 PubMed DOI PMC

Hsu S. C., Ting A. E., Hazuka C. D., Davanger S., Kenny J. W., Kee Y., et al. (1996). The mammalian brain rsec6/8 complex. Neuron 6 209–219 PubMed

Jin R., Junutula J. R., Matern H. T., Ervin K. E., Scheller R. H., Brunger A T. (2005). Exo84 and Sec5 are competitive regulatory Sec6/8 effectors to the RalA GTPase. EMBO J. 24 2064–2074 10.1038/sj.emboj.7600699 PubMed DOI PMC

Jin Y., Sultana A., Gandhi P., Franklin E., Hamamoto S., Khan A. R., et al. (2011). Myosin V transports secretory vesicles via a Rab GTPase cascade and interaction with the exocyst complex. Dev. Cell 21 1156–1170 10.1016/j.devcel.2011.10.009 PubMed DOI PMC

Jourdain I., Dooley H. C., Toda T. (2012). Fission yeast sec3 bridges the exocyst complex to the actin cytoskeleton. Traffic 13 1481–1495 10.1111/j.1600-0854.2012.01408.x PubMed DOI PMC

Kono K., Saeki Y., Yoshida S., Tanaka K., Pellman D. (2012). Proteasomal degradation resolves competition between cell polarization and cellular wound healing. Cell 150 151–164 10.1016/j.cell.2012.05.030 PubMed DOI

Krendel M., Zenke F. T., Bokoch G. M. (2002). Nucleotide exchange factor GEF-H1 mediates cross-talk between microtubules and the actin cytoskeleton. Nat. Cell Biol. 4 294–301 10.1038/ncb773 PubMed DOI

Kulich I., Cole R., Drdová E., Cvrčková F., Soukup A., Fowler J., et al. (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 10.1111/j.1469-8137.2010.03372.x PubMed DOI

Lavy M., Bloch D., Hazak O., Gutman I., Poraty L., Sorek N., et al. (2007). A Novel ROP/RAC effector links cell polarity, root-meristem maintenance, and vesicle trafficking. Curr. Biol. 17 947–952 10.1016/j.cub.2007.04.038 PubMed DOI

Li S., Gu Y., Yan A., Lord E., Yang Z. B. (2008). RIP1 (ROP Interactive Partner 1)/ICR1 marks pollen germination sites and may act in the ROP1 pathway in the control of polarized pollen growth. Mol. Plant 1 1021–1035 10.1093/mp/ssn051 PubMed DOI PMC

Liu J., Guo W. (2012). The exocyst complex in exocytosis and cell migration. Protoplasma 249 587–597 10.1007/s00709-011-0330-1 PubMed DOI

Liu J., Zhao Y., Sun Y., He B., Yang C., Svitkina T., et al. (2012). Exo70 stimulates the Arp2/3 complex for lamellipodia formation and directional cell migration. Curr. Biol. 22 1510–1515 10.1016/j.cub.2012.05.055 PubMed DOI PMC

Lovy-Wheeler A., Wilsen K. L., Baskin T. I., Hepler P. K. (2005). Enhanced fixation reveals the apical cortical fringe of actin filaments as a consistent feature of the pollen tube. Planta 221 95–104 10.1007/s00425-004-1423-2 PubMed DOI

Martiniere A., Gayral P., Hawes C., Runions J. (2011). Building bridges: formin1 of Arabidopsis forms a connection between the cell wall and the actin cytoskeleton. Plant J. 66 354–365 10.1111/j.1365-313X.2011.04497.x PubMed DOI

Martinière A., Lavagi I., Nageswaran G., Rolfe D. J., Maneta-Peyret L., Luu D. T., et al. (2012). Cell wall constrains lateral diffusion of plant plasma-membrane proteins. Proc. Natl. Acad. Sci. U.S.A. 109 12805–12810 10.1073/pnas.1202040109 PubMed DOI PMC

McFarlane H. E., Young R. E., Wasteneys G. O., Samuels A. L. (2008). Cortical microtubules mark the mucilage secretion domain of the plasma membrane in Arabidopsis seed coat cells. Planta 227 1363–1375 10.1007/s00425-008-0708-2 PubMed DOI

Mohammadi S., Isberg R. R. (2013). Cdc42 interacts with the exocyst complex to promote phagocytosis. J. Cell Biol. 200 81–93 10.1083/jcb.201204090 PubMed DOI PMC

Morgera F., Sallah M. R., Dubuke M. L., Gandhi P., Brewer D. N., Carr C. M., et al. (2012). Regulation of exocytosis by the exocyst subunit Sec6 and the SM protein Sec1. Mol. Biol. Cell 23 337–346 10.1091/mbc.E11-08-0670 PubMed DOI PMC

Moskalenko S., Tong C., Rosse C., Mirey G., Formstecher E., Daviet L., et al. (2003). Ral GTPases regulate exocyst assembly through dual subunit interactions. J. Biol. Chem. 278 51743–51748 10.1074/jbc.M308702200 PubMed DOI

Mucha E., Hoefle C., Hückelhoven R., Berken A. (2010). RIP3 and AtKinesin-13A - a novel interaction linking Rho proteins of plants to microtubules. Eur. J. Cell. Biol. 89 906–916 10.1016/j.ejcb.2010.08.003 PubMed DOI

Mucha E., Fricke I., Schaefer A., Wittinghofer A., Berken A. (2011). Rho proteins of plants-functional cycle and regulation of cytoskeletal dynamics. Eur. J. Cell Biol. 90 934–943 10.1016/j.ejcb.2010.11.009 PubMed DOI

Mukerji J., Olivieri K. C., Misra V., Agopian K. A., Gabuzda D. (2012). Proteomic analysis of HIV-1 Nef cellular binding partners reveals a role for exocyst complex proteins in mediating enhancement of intercellular nanotube formation. Retrovirology 9 33 10.1186/1742-4690-9-33 PubMed DOI PMC

Nakano K., Toya M., Yoneda A., Asami Y., Yamashita A., Kamasawa N., et al. (2011). Pob1 ensures cylindrical cell shape by coupling two distinct Rho signaling events during secretory vesicle targeting. Traffic 12 726–739 10.1111/j.1600-0854.2011.01190.x PubMed DOI

Nalbant P., Chang Y. C., Birkenfeld J., Chang Z. F., Bokoch G. M. (2009). Guanine nucleotide exchange factor-H1 regulates cell migration via localized activation of RhoA at the leading edge. Mol. Biol. Cell 20 4070–4082 10.1091/mbc.E09-01-0041 PubMed DOI PMC

Nichols C. D., Casanova J. E. (2010). Salmonella-directed recruitment of new membrane to invasion foci via the host exocyst complex. Curr. Biol. 20 1316–1320 10.1016/j.cub.2010.05.065 PubMed DOI PMC

Novick P., Field C., Schekman R. (1980). Identification of 23 complementation groups required for post-translational events in the yeast secretory pathway. Cell 21 205–215 10.1016/0092-8674(80)90128-2 PubMed DOI

Oda Y., Fukuda H. (2012). Secondary cell wall patterning during xylem differentiation. Curr. Opin. Plant Biol. 15 38–44 10.1016/j.pbi.2011.10.005 PubMed DOI

Ohno H., Hase K., Kimura S. (2010). M-Sec: emerging secrets of tunneling nanotube formation. Commun. Integr. Biol. 3 231–233 10.4161/cib.3.3.11242 PubMed DOI PMC

Pathak R., Delorme-Walker V. D., Howell M. C., Anselmo A. N., White M. A., Bokoch G. M., et al. (2012). The microtubule-associated Rho activating factor GEF-H1 interacts with exocyst complex to regulate vesicle traffic. Dev. Cell 23 397–411 10.1016/j.devcel.2012.06.014 PubMed DOI PMC

Pecenkova T., Hala M., Kulich I., Kocourkova D., Drdova E., Fendrych M., et al. (2011). The role for the exocyst complex subunits Exo70B2 and Exo70H1 in the plant-pathogen interaction. J. Exp. Bot. 62 2107–2116 10.1093/jxb/erq402 PubMed DOI PMC

Rivera-Molina F., Toomre D. (2013). Live-cell imaging of exocyst links its spatiotemporal dynamics to various stages of vesicle fusion. J. Cell Biol. 201 673–680 10.1083/jcb.201212103 PubMed DOI PMC

Sakurai-Yageta M., Recchi C., Le Dez G., Sibarita J. B., Daviet L., Camonis J., et al. (2008). The interaction of IQGAP1 with the exocyst complex is required for tumor cell invasion downstream of Cdc42 and RhoA. J. Cell Biol. 181 985–998 10.1083/jcb.200709076 PubMed DOI PMC

Schiller C., Diakopoulos K. N., Rohwedder I., Kremmer E., von Toerne C., Ueffing M., et al. (2013). LST1 promotes the assembly of a molecular machinery responsible for tunneling nanotube formation. J. Cell Sci. 126 767–777 10.1242/jcs.114033 PubMed DOI

Shen D., Yuan H., Hutagalung A., Verma A., Kümmel D., Wu X., et al. (2013). The synaptobrevin homologue Snc2p recruits the exocyst to secretory vesicles by binding to Sec6p. J. Cell Biol. 202 509–526 10.1083/jcb.201211148 PubMed DOI PMC

Sivaram M. V., Saporita J. A., Furgason M. L., Boettcher A. J., Munson M. (2005). Dimerization of the exocyst protein Sec6p and its interaction with the t-SNARE Sec9p. Biochemistry 44 6302–6311 10.1021/bi048008z PubMed DOI

Snaith H. A., Thompson J., Yates J. R., Sawin K. E. (2011). Characterization of Mug33 reveals complementary roles for actin cable-dependent transport and exocyst regulators in fission yeast exocytosis. J. Cell Sci. 124 2187–2199 10.1242/jcs.084038 PubMed DOI PMC

Songer J. A., Munson M. (2009). Sec6p anchors the assembled exocyst complex at sites of secretion. Mol. Biol. Cell 20 973–982 10.1091/mbc.E08-09-0968 PubMed DOI PMC

Staehelin L. A., Moore I. (1995). The plant golgi apparatus: structure, functional organization and trafficking mechanisms. Annu. Rev. Plant Physiol. Plant Mol. Biol. 46 261–288 10.1146/annurev.pp.46.060195.001401 DOI

Sugihara K., Asano S., Tanaka K., Iwamatsu A., Okawa K., Ohta Y. (2002). The exocyst complex binds the small GTPase RalA to mediate filopodia formation. Nat. Cell Biol. 1 73–78 10.1038/ncb720 PubMed DOI

Sutter J. U., Campanoni P., Tyrrell M., Blatt M. R. (2006). Selective mobility and sensitivity to SNAREs is exhibited by the Arabidopsis KAT1 K+ channel at the plasma membrane. Plant Cell 18 935–954 10.1105/tpc.105.038950 PubMed DOI PMC

Swiech L., Blazejczyk M., Urbanska M., Pietruszka P., Dortland B. R., Malik A. R., et al. (2011). CLIP-170 and IQGAP1 cooperatively regulate dendrite morphology. J. Neurosci. 31 4555–4568 10.1523/JNEUROSCI.6582-10.2011 PubMed DOI PMC

Synek L., Schlager N., Eliáš M., Quentin M., Hauser M. T, Žárský 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 10.1111/j.1365-313X.2006.02854.x PubMed DOI PMC

TerBush D. R., Maurice T., Roth D., Novick P. (1996). The Exocyst is a multiprotein complex required for exocytosis in Saccharomyces cerevisiae. EMBO J. 15 6483–6494 PubMed PMC

Valentijn K. M., Gumkowski F. D., Jamieson J. D. (1999). The subapical actin cytoskeleton regulates secretion and membrane retrieval in pancreatic acinar cells. J. Cell Sci. 112 81–96 PubMed

Vaškovičová K., Žárský V., Rösel D., Nikolič M., Buccione R., Cvrčková F., et al. (2013). Invasive cells in animals and plants: searching for LECA machineries in later eukaryotic life. Biol. Direct 8 8 10.1186/1745-6150-8-8 PubMed DOI PMC

Vega I. E., Hsu S. C. (2001). The exocyst complex associates with microtubules to mediate vesicle targeting and neurite outgrowth. J. Neurosci. 21 3839–3848 PubMed PMC

Wang S., Liu Y., Adamson C. L., Valdez G., Guo W., Hsu S. C. (2004). The mammalian exocyst, a complex required for exocytosis, inhibits tubulin polymerization. J. Biol. Chem. 279 35958–35966 10.1074/jbc.M313778200 PubMed DOI

White C. D., Erdemir H. H., Sacks D. B. (2012). IQGAP1 and its binding proteins control diverse biological functions. Cell. Signal 24 826–834 10.1016/j.cellsig.2011.12.005 PubMed DOI PMC

Wu S., Mehta S. Q., Pichaud F., Bellen H. J., Quiocho F. A. (2005). Sec15 interacts with Rab11 via a novel domain and affects Rab11 localization in vivo. Nat. Struct. Mol. Biol. 12 879–885 10.1038/nsmb987 PubMed DOI

Wu H., Rossi G., Brennwald P. (2008). The ghost in the machine: small GTPases as spatial regulators of exocytosis. Trends Cell Biol. 18 397–404 10.1016/j.tcb.2008.06.007 PubMed DOI PMC

Wu H., Turner C., Gardner J., Temple B., Brennwald P. (2010). The Exo70 subunit of the exocyst is an effector for both Cdc42 and Rho3 function in polarized exocytosis. Mol. Biol. Cell 21 430–442 10.1091/mbc.E09-06-0501 PubMed DOI PMC

Yalovsky S., Bloch D., Sorek N., Kost B. (2008). Regulation of membrane trafficking, cytoskeleton dynamics and cell polarity by ROP/RAC GTPases. Plant Phys. 147 1527–1543 10.1104/pp.108.122150 PubMed DOI PMC

Zakharenko S., Popov S. (1998). Dynamics of axonal microtubules regulate the topology of new membrane insertion into the growing neurites. J. Cell Biol. 143 1077–1086 PubMed PMC

Žárský V., Cvrčková F., Potocký M., Hála M. (2009). Exocytosis and cell polarity in plants - exocyst and recycling domains. New Phytol. 183 255–272 10.1111/j.1469-8137.2009.02880.x PubMed DOI

Zhang X., Orlando K., He B., Xi F., Zhang J., Zajac A., et al. (2008). Membrane association and functional regulation of Sec3 by phospholipids and Cdc42. J. Cell Biol. 180 145–158 10.1083/jcb.200704128 PubMed DOI PMC

Zhao Y., Liu J., Yang C., Capraro B. R., Baumgart T., Bradley R. P., et al. (2013). Exo70 generates membrane curvature for morphogenesis and cell migration. Dev. Cell 26 266–278 10.1083/jcb.200704128 PubMed DOI PMC

Zuo X., Zhang J., Zhang Y., Hsu S. C., Zhou D., Guo W. (2006). Exo70 interacts with the Arp2/3 complex and regulates cell migration. Nat. Cell Biol. 8 1383–1388 PubMed

Lessons from the deep: mechanisms behind diversification of eukaryotic protein complexes

Synergy among Exocyst and SNARE Interactions Identifies a Functional Hierarchy in Secretion during Vegetative Growth

Evolution of late steps in exocytosis: conservation and specialization of the exocyst complex

Analysis of Exocyst Subunit EXO70 Family Reveals Distinct Membrane Polar Domains in Tobacco Pollen Tubes