Molecular mechanisms of Sar/Arf GTPases in vesicular trafficking in yeast and plants

Frontiers in Plant Science

Volumn 5, Issue AUG, 2014, Pages

  Yorimitsu, Tomohiro ^a   Sato, Ken ^a   Takeuchi, Masaki ^a  

^a UNIVERSITY OF TOKYO   (Japan)

Author keywords

Endoplasmic reticulum; Endosome; Golgi apparatus; Small GTPase; Vesicular trafficking

Indexed keywords

EID: 84907311745     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00411     Document Type: Review

References (109)

1. Anders, N., and Jurgens, G. (2008). Large ARF guanine nucleotide exchange factors in membrane trafficking. Cell. Mol. Life Sci. 65, 3433-3445. doi: 10.1007/s00018-008-8227-7
2. Antonny, B., Beraud-Dufour, S., Chardin, P., and Chabre, M. (1997). N-terminal hydrophobic residues of the G-protein ADP-ribosylation factor-1 insert into membrane phospholipids upon GDP to GTP exchange. Biochemistry 36, 4675-4684. doi: 10.1021/bi962252b
3. Antonny, B., Madden, D., Hamamoto, S., Orci, L., and Schekman, R. (2001). Dynamics of the COPII coat with GTP and stable analogues. Nat. Cell Biol. 3, 531-537. doi: 10.1038/35078500
4. Barlowe, C., D'Enfert, C., and Schekman, R. (1993). Purification and characterization of SAR1p, a small GTP-binding protein required for transport vesicle formation from the endoplasmic reticulum. J. Biol. Chem. 268, 873-879.
5. Barlowe, C., Orci, L., Yeung, T., Hosobuchi, M., Hamamoto, S., Salama, N., et al. (1994). COPII: a membrane coat formed by Sec proteins that drive vesicle budding from the endoplasmic reticulum. Cell 77, 895-907. doi: 10.1016/00928674(94)90138-4
6. Batoko, H., Zheng, H. Q., Hawes, C., and Moore, I. (2000). A rab1 GTPase is required for transport between the endoplasmic reticulum and golgi apparatus and for normal golgi movement in plants. Plant Cell 12, 2201-2218. doi: 10.1105/tpc.12.11.2201
7. Beck, R., Sun, Z., Adolf, F., Rutz, C., Bassler, J., Wild, K., et al. (2008). Membrane curvature induced by Arf1-GTP is essential for vesicle formation. Proc. Natl. Acad. Sci. U.S.A. 105, 11731-11736. doi: 10.1073/pnas.0805182105
8. Bi, X., Corpina, R. A., and Goldberg, J. (2002). Structure of the Sec23/24-Sar1 pre-budding complex of the COPII vesicle coat. Nature 419, 271-277. doi: 10.1038/nature01040
9. Bi, X., Mancias, J. D., and Goldberg, J. (2007). Insights into COPII coat nucleation from the structure of Sec23 • Sar1 complexed with the active fragment of Sec31. Dev. Cell 13, 635-645. doi: 10.1016/j.devcel.2007.10.006
10. Bielli, A., Haney, C. J., Gabreski, G., Watkins, S. C., Bannykh, S. I., and Aridor, M. (2005). Regulation of Sar1 NH2 terminus by GTP binding and hydrolysis promotes membrane deformation to control COPII vesicle fission. J. Cell Biol. 171, 919-924. doi: 10.1083/jcb.200509095
11. Bigay, J., Casella, J. F., Drin, G., Mesmin, B., and Antonny, B. (2005). ArfGAP1 responds to membrane curvature through the folding of a lipid packing sensor motif. EMBO J. 24, 2244-2253. doi: 10.1038/sj.emboj.7600714
12. Bohlenius, H., Morch, S. M., Godfrey, D., Nielsen, M. E., and Thordal-Christensen, H. (2010). The multivesicular body-localized GTPase ARFA1b/1c is important for callose deposition and ROR2 syntaxin-dependent preinvasive basal defense in barley. Plant Cell 22, 3831-3844. doi: 10.1105/tpc.55-56110. 078063
13. Brandizzi, F., and Barlowe, C. (2013). Organization of the ER-Golgi interface for membrane traffic control. Nat. Rev. Mol. Cell Biol. 14, 382-392. doi: 10.1038/nrm3588
14. Cai, H., Yu, S., Menon, S., Cai, Y., Lazarova, D., Fu, C., et al. (2007). TRAPPI tethers COPII vesicles by binding the coat subunit Sec23. Nature 445, 941-944. doi: 10.1038/nature05527
15. Chantalat, S., Courbeyrette, R., Senic-Matuglia, F., Jackson, C. L., Goud, B., and Peyroche, A. (2003). A novel golgi membrane protein is a partner of the ARF exchange factors Gea1p and Gea2p. Mol. Biol. Cell 14, 2357-2371. doi: 10.1091/mbc.E02-10-0693
16. Connerly, P. L., Esaki, M., Montegna, E. A., Strongin, D. E., Levi, S., Soderholm, J., et al. (2005). Sec16 is a determinant of transitional ER organization. Curr. Biol. 15, 1439-1447. doi: 10.1016/j.cub.2005.06.065
17. Dasilva, L. L., Snapp, E. L., Denecke, J., Lippincott-Schwartz, J., Hawes, C., and Brandizzi, F. (2004). Endoplasmic reticulum export sites and golgi bodies behave as single mobile secretory units in plant cells. Plant Cell 16, 1753-1771. doi: 10.1105/tpc.022673
18. De Craene, J. O., Courte, F., Rinaldi, B., Fitterer, C., Herranz, M. C., SchmittKeichinger, C., et al. (2014). Study of the plant COPII vesicle coat subunits by functional complementation of yeast Saccharomyces cerevisiae mutants. PLoS ONE 9:e90072. sdoi: 10.1371/journal.pone.0090072
19. D'Enfert, C., Gensse, M., and Gaillardin, C. (1992). Fission yeast and a plant have functional homologues of the Sar1 and Sec12 proteins involved in ER to golgi traffic in budding yeast. EMBO J. 11, 4205-4211.
20. Du, W., Tamura, K., Stefano, G., and Brandizzi, F. (2013). The integrity of the plant golgi apparatus depends on cell growth-controlled activity of GNL1. Mol. Plant 6, 905-915. doi: 10.1093/mp/sss124
21. Espenshade, P., Gimeno, R. E., Holzmacher, E., Teung, P., and Kaiser, C. A. (1995). Yeast SEC16 gene encodes a multidomain vesicle coat protein that interacts with Sec23p. J. Cell Biol. 131, 311-324. doi: 10.1083/jcb.131.2.311
22. Faso, C., Chen, Y. N., Tamura, K., Held, M., Zemelis, S., Marti, L., et al. (2009). A missense mutation in the Arabidopsis COPII coat protein Sec24A induces the formation of clusters of the endoplasmic reticulum and golgi apparatus. Plant Cell 21, 3655-3671. doi: 10.1105/tpc.109.068262
23. Fatal, N., Karhinen, L., Jokitalo, E., and Makarow, M. (2004). Active and specific recruitment of a soluble cargo protein for endoplasmic reticulum exit in the absence of functional COPII component Sec24p. J. Cell Sci. 117, 1665-1673. doi: 10.1242/jcs.01019
24. Franco, M., Chardin, P., Chabre, M., and Paris, S. (1996). Myristoylation-facilitated binding of the G protein ARF1GDP to membrane phospholipids is required for its activation by a soluble nucleotide exchange factor. J. Biol. Chem. 271, 1573-1578. doi: 10.1074/jbc.271.3.1573
25. Futai, F., Hamamoto, S., Orci, L., and Schekman, R. (2004). GTP/GDP exchange by Sec12p enables COPII vesicle bud formation on synthetic liposomes. EMBO J. 23, 4146-4155. doi: 10.1038/sj.emboj.7600428
26. Geldner, N., Anders, N., Wolters, H., Keicher, J., Kornberger, W., Muller, P., et al. (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
27. Goldberg, J. (1998). Structural basis for activation of ARF GTPase: mechanisms of guanine nucleotide exchange and GTP-myristoyl switching. Cell 95, 237-248. doi: 10.1016/S0092-8674(00)81754-7
28. Gonzalez, E., Solano, R., Rubio, V., Leyva, A., and Paz-Ares, J. (2005). PHOSPHATE TRANSPORTER TRAFFIC FACILITATOR1 is a plant-specific SEC12-related protein that enables the endoplasmic reticulum exit of a highaffinity phosphate transporter in Arabidopsis. Plant Cell 17, 3500-3512. doi: 10.1105/tpc.105.036640
29. Hanton, S. L., Chatre, L., Matheson, L. A., Rossi, M., Held, M. A., and Brandizzi, F. (2008). Plant Sar1 isoforms with near-identical protein sequences exhibit different localisations and effects on secretion. Plant Mol. Biol. 67, 283-294. doi: 10.1007/s11103-008-9317-5
30. Hara-Kuge, S., Kuge, O., Orci, L., Amherdt, M., Ravazzola, M., Wieland, F. T., et al. (1994). En bloc incorporation of coatomer subunits during the assembly of COP-coated vesicles. J. Cell Biol. 124, 883-892. doi: 10.1083/jcb.124.6.883
31. Jensen, R. B., Lykke-Andersen, K., Frandsen, G. I., Nielsen, H. B., Haseloff, J., Jespersen, H. M., et al. (2000). Promiscuous and specific phospholipid binding by domains in ZAC, a membrane-associated Arabidopsis protein with an ARF GAP zinc finger and a C2 domain. Plant Mol. Biol. 44, 799-814. doi: 10.1023/A:1026509002161
32. Jia, D. J., Cao, X., Wang, W., Tan, X. Y., Zhang, X. Q., Chen, L. Q., et al. (2009). GNOM-LIKE 2, encoding an adenosine diphosphate-ribosylation factor-guanine nucleotide exchange factor protein homologous to GNOM and GNL1, is essential for pollen germination in Arabidopsis. J. Integr. Plant Biol. 51, 762-773. doi: 10.1111/j.1744-7909.2009.00858.x
33. Jurgens, G., and Geldner, N. (2002). Protein secretion in plants: from the transGolgi network to the outer space. Traffic 3, 605-613. doi: 10.1034/j.16000854.2002.30902.x
34. Kahn, R. A., Clark, J., Rulka, C., Stearns, T., Zhang, C. J., Randazzo, P. A., et al. (1995). Mutational analysis of Saccharomyces cerevisiae ARF1. J. Biol. Chem. 270, 143-150. doi: 10.1074/jbc.270.1.143
35. Kahn, R. A., Goddard, C., and Newkirk, M. (1988). Chemical and immunological characterization of the 21-kDa ADP-ribosylation factor of adenylate cyclase. J. Biol. Chem. 263, 8282-8287.
36. Kim, W. Y., Cheong, N. E., Je, D. Y., Kim, M. G., Lim, C. O., Bahk, J. D., et al. (1997). The presence of a Sar1 gene family in Brassica campestris that suppresses a yeast vesicular transport mutation Sec12-1. Plant Mol. Biol. 33, 1025-1035. doi: 10.1023/A:1005731209124
37. Kodera, C., Yorimitsu, T., Nakano, A., and Sato, K. (2011). Sed4p stimulates Sar1p GTP hydrolysis and promotes limited coat disassembly. Traffic 12, 591-599. doi: 10.1111/j.1600-0854.2011.01173.x
38. Koizumi, K., Naramoto, S., Sawa, S., Yahara, N., Ueda, T., Nakano, A., et al. (2005). VAN3 ARF-GAP-mediated vesicle transport is involved in leaf vascular network formation. Development 132, 1699-1711. doi: 10.1242/dev.01716
39. Krauss, M., Jia, J. Y., Roux, A., Beck, R., Wieland, F. T., De Camilli, P., et al. (2008). Arf1-GTP-induced tubule formation suggests a function of Arf family proteins in curvature acquisition at sites of vesicle budding. J. Biol. Chem. 283, 27717-27723. doi: 10.1074/jbc.M804528200
40. Kung, L. F., Pagant, S., Futai, E., D'Arcangelo, J. G., Buchanan, R., Dittmar, J. C., et al. (2012). Sec24p and Sec16p cooperate to regulate the GTP cycle of the COPII coat. EMBO J. 31, 1014-1027. doi: 10.1038/emboj.2011.444
41. Kurokawa, K., Okamoto, M., and Nakano, A. (2014). Contact of cis-Golgi with ER exit sites executes cargo capture and delivery from the ER. Nat. Commun. 5, 3653. doi: 10.1038/ncomms4653
42. Langhans, M., Meckel, T., Kress, A., Lerich, A., and Robinson, D. G. (2012). ERES (ER exit sites) and the "secretory unit concept." J. Microsc. 247, 48-59. doi: 10.1111/j.1365-2818.2011.03597.x
43. Lee, C., and Goldberg, J. (2010). Structure of coatomer cage proteins and the relationship among COPI, COPII, and clathrin vesicle coats. Cell 142, 123-132. doi: 10.1016/j.cell.2010.05.030
44. Lee, M. C., Orci, L., Hamamoto, S., Futai, E., Ravazzola, M., and Schekman, R. (2005). Sar1p N-terminal helix initiates membrane curvature and completes the fission of a COPII vesicle. Cell 122, 605-617. doi: 10.1016/j.cell.2005.07.025
45. Lee, M. H., Min, M. K., Lee, Y. J., Jin, J. B., Shin, D. H., Kim, D. H., et al. (2002). ADP-ribosylation factor 1 of Arabidopsis plays a critical role in intracellular trafficking and maintenance of endoplasmic reticulum morphology in Arabidopsis. Plant Physiol. 129, 1507-1520. doi: 10.1104/pp.003624
46. Lerich, A., Hillmer, S., Langhans, M., Scheuring, D., Van Bentum, P., and Robinson, D. G. (2012). ER import sites and their relationship to ER exit sites: a new model for bidirectional ER-Golgi transport in higher plants. Front. Plant Sci. 3:143. doi: 10.3389/fpls.2012.00143
47. Letourneur, F., Gaynor, E. C., Hennecke, S., Demolliere, C., Duden, R., Emr, S. D., et al. (1994). Coatomer is essential for retrieval of dilysine-tagged proteins to the endoplasmic reticulum. Cell 79, 1199-1207. doi: 10.1016/00928674(94)90011-6
48. Lord, C., Bhandari, D., Menon, S., Ghassemian, M., Nycz, D., Hay, J., et al. (2011). Sequential interactions with Sec23 control the direction of vesicle traffic. Nature 473, 181-186. doi: 10.1038/nature09969
49. Lundmark, R., Doherty, G. J., Vallis, Y., Peter, B. J., and McMahon, H. T. (2008). Arf family GTP loading is activated by, and generates, positive membrane curvature. Biochem. J. 414, 189-194. doi: 10.1042/BJ20081237
50. Macia, E., Chabre, M., and Franco, M. (2001). Specificities for the small G proteins ARF1 and ARF6 of the guanine nucleotide exchange factors ARNO and EFA6. J. Biol. Chem. 276, 24925-24930. doi: 10.1074/jbc.M103284200
51. Marti, L., Fornaciari, S., Renna, L., Stefano, G., and Brandizzi, F. (2010). COPII-mediated traffic in plants. Trends Plant Sci. 15, 522-528. doi: 10.1016/j.tplants.2010.05.010
52. Matheson, L. A., Suri, S. S., Hanton, S. L., Chatre, L., and Brandizzi, F. (2008). Correct targeting of plant ARF GTPases relies on distinct protein domains. Traffic 9, 103-120. doi: 10.1111/j.1600-0854.2007.00671.x
53. Matsuoka, K., Orci, L., Amherdt, M., Bednarek, S. Y., Hamamoto, S., Schekman, R., et al. (1998). COPII-coated vesicle formation reconstituted with purified coat proteins and chemically defined liposomes. Cell 93, 263-275. doi: 10.1016/S0092-8674(00)81577-9
54. McMahon, C., Studer, S. M., Clendinen, C., Dann, G. P., Jeffrey, P. D., and Hughson, F. M. (2012). The structure of Sec12 implicates potassium ion coordination in Sar1 activation. J. Biol. Chem. 287, 43599-43606. doi: 10.1074/jbc.M112.420141
55. Miller, E. A., Beilharz, T. H., Malkus, P. N., Lee, M. C., Hamamoto, S., Orci, L., et al. (2003). Multiple cargo binding sites on the COPII subunit Sec24p ensure capture of diverse membrane proteins into transport vesicles. Cell 114, 497-509. doi: 10.1016/S0092-8674(03)00609-3
56. Min, M. K., Jang, M., Lee, M., Lee, J., Song, K., Lee, Y., et al. (2013). Recruitment of Arf1-GDP to Golgi by Glo3p-type ArfGAPs is crucial for golgi maintenance and plant growth. Plant Physiol. 161, 676-691. doi: 10.1104/pp.112.209148
57. Min, M. K., Kim, S. J., Miao, Y., Shin, J., Jiang, L., and Hwang, I. (2007). Overexpression of Arabidopsis AGD7 causes relocation of Golgi-localized proteins to the endoplasmic reticulum and inhibits protein trafficking in plant cells. Plant Physiol. 143, 1601-1614. doi: 10.1104/pp.106.095091
58. Mironov, A. A. (2014). ER-Golgi transport could occur in the absence of COPII vesicles. Nat. Rev. Mol. Cell Biol. 15, 1. doi: 10.1038/nrm3588-c1
59. Mossessova, E., Bickford, L. C., and Goldberg, J. (2003). SNARE selectivity of the COPII coat. Cell 114, 483-495. doi: 10.1016/S0092-8674(03)00608-1
60. Nakano, A., Brada, D., and Schekman, R. (1988). A membrane glycoprotein, Sec12p, required for protein transport from the endoplasmic reticulum to the Golgi apparatus in yeast. J. Cell Biol. 107, 851-863. doi: 10.1083/jcb. 107.3.851
61. Nakano, R. T., Matsushima, R., Ueda, H., Tamura, K., Shimada, T., Li, L., et al. (2009). GNOM-LIKE1/ERMO1 and SEC24a/ERMO2 are required for maintenance of endoplasmic reticulum morphology in Arabidopsis thaliana. Plant Cell 21, 3672-3685. doi: 10.1105/tpc.109.068270
62. Naramoto, S., Kleine-Vehn, J., Robert, S., Fujimoto, M., Dainobu, T., Paciorek, T., et al. (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
63. Naramoto, S., Otegui, M. S., Kutsuna, N., De Rycke, R., Dainobu, T., Karampelias, M., et al. (2014). Insights into the localization and function of the membrane trafficking regulator GNOM ARF-GEF at the Golgi apparatus in Arabidopsis. Plant Cell. doi: 10.1105/tpc.114.125880. [Epub ahead of print].
64. Naramoto, S., Sawa, S., Koizumi, K., Uemura, T., Ueda, T., Friml, J., et al. (2009). Phosphoinositide-dependent regulation of VAN3 ARF-GAP localization and activity essential for vascular tissue continuity in plants. Development 136, 1529-1538. doi: 10.1242/dev.030098
65. Novick, P., Field, C., and Schekman, R. (1980). Identification of 23 complementation groups required for post-translational events in the yeast secretory pathway. Cell 21, 205-215. doi: 10.1016/0092-8674(80)90128-2
66. Osterrieder, A., Hummel, E., Carvalho, C. M., and Hawes, C. (2010). Golgi membrane dynamics after induction of a dominant-negative mutant Sar1 GTPase in tobacco. J. Exp. Bot. 61, 405-422. doi: 10.1093/jxb/erp315
67. Paciorek, T., Zazimalova, E., Ruthardt, N., Petrasek, J., Stierhof, Y. D., Kleine-Vehn, J., et al. (2005). Auxin inhibits endocytosis and promotes its own efflux from cells. Nature 435, 1251-1256. doi: 10.1038/nature03633
68. Peyroche, A., Courbeyrette, R., Rambourg, A., and Jackson, C. L. (2001). The ARF exchange factors Gea1p and Gea2p regulate Golgi structure and function in yeast. J. Cell Sci. 114, 2241-2253.
69. Peyroche, A., Paris, S., and Jackson, C. L. (1996). Nucleotide exchange on ARF mediated by yeast Gea1 protein. Nature 384, 479-481. doi: 10.1038/384479a0
70. Phillipson, B. A., Pimpl, P., Dasilva, L. L., Crofts, A. J., Taylor, J. P., Movafeghi, A., et al. (2001). Secretory bulk flow of soluble proteins is efficient and COPII dependent. Plant Cell 13, 2005-2020. doi: 10.1105/tpc.13.9.2005
71. Pimpl, P., Hanton, S. L., Taylor, J. P., Pinto-Dasilva, L. L., and Denecke, J. (2003). The GTPase ARF1p controls the sequence-specific vacuolar sorting route to the lytic vacuole. Plant Cell 15, 1242-1256. doi: 10.1105/tpc.010140
72. Pimpl, P., Movafeghi, A., Coughlan, S., Denecke, J., Hillmer, S., and Robinson, D. G. (2000). In situ localization and in vitro induction of plant COPI-coated vesicles. Plant Cell 12, 2219-2236. doi: 10.1105/tpc.12.11.2219
73. Poon, P. P., Cassel, D., Spang, A., Rotman, M., Pick, E., Singer, R. A., et al. (1999). Retrograde transport from the yeast Golgi is mediated by two ARF GAP proteins with overlapping function. EMBO J. 18, 555-564. doi: 10.1093/emboj/18.3.555
74. Richter, S., Geldner, N., Schrader, J., Wolters, H., Stierhof, Y. D., Rios, G., et al. (2007). Functional diversification of closely related ARF-GEFs in protein secretion and recycling. Nature 448, 488-492. doi: 10.1038/nature05967
75. Robinson, D. G., Herranz, M. C., Bubeck, J., Pepperkok, R., and Ritzenthaler, C. (2007). Membrane dynamics in the early secretory pathway. Crit. Rev. Plant Sci. 26, 199-225. doi: 10.1080/07352680701495820
76. Robinson, D. G., Scheuring, D., Naramoto, S., and Friml, J. (2011). ARF1 localizes to the golgi and the trans-golgi network. Plant Cell 23, 846-849, 849-850. doi: 10.1105/tpc.110.082099
77. Saito, Y., Kimura, K., Oka, T., and Nakano, A. (1998). Activities of mutant Sar1 proteins in guanine nucleotide binding, GTP hydrolysis, and cell-free transport from the endoplasmic reticulum to the Golgi apparatus. J. Biochem. 124, 816-823. doi: 10.1093/oxfordjournals.jbchem.a022185
78. Sato, M., Sato, K., and Nakano, A. (1996). Endoplasmic reticulum localization of Sec12p is achieved by two mechanisms: Rer1p-dependent retrieval that requires the transmembrane domain and Rer1p-independent retention that involves the cytoplasmic domain. J. Cell Biol. 134, 279-293. doi: 10.1083/jcb.134.2.279
79. Sewell, J. L., and Kahn, R. A. (1988). Sequences of the bovine and yeast ADP-ribosylation factor and comparison to other GTP-binding proteins. Proc. Natl. Acad. Sci. U.S.A. 85, 4620-4624. doi: 10.1073/pnas.85.13.4620
80. Shaywitz, D. A., Espenshade, P. J., Gimeno, R. E., and Kaiser, C. A. (1997). COPII Subunit interactions in the assembly of the vesicle coat. J. Biol. Chem. 272, 25413-25416. doi: 10.1074/jbc.272.41.25413
81. Shevell, D. E., Leu, W. M., Gillmor, C. S., Xia, G., Feldmann, K. A., and Chua, N. H. (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. doi: 10.1016/0092-8674(94)90444-8
82. Shiba, Y., and Randazzo, P. A. (2012). ArfGAP1 function in COPI mediated membrane traffic: currently debated models and comparison to other coat-binding ArfGAPs. Histol. Histopathol. 27, 1143-1153.
83. Spang, A., Matsuoka, K., Hamamoto, S., Schekman, R., and Orci, L. (1998). Coatomer, Arf1p, and nucleotide are required to bud coat protein complex Icoated vesicles from large synthetic liposomes. Proc. Natl. Acad. Sci. U.S.A. 95, 11199-11204. doi: 10.1073/pnas.95.19.11199
84. Spang, A., Shiba, Y., and Randazzo, P. A. (2010). Arf GAPs: gatekeepers of vesicle generation. FEBS Lett. 584, 2646-2651. doi: 10.1016/j.febslet.2010.04.005
85. Stachowiak, J. C., Schmid, E. M., Ryan, C. J., Ann, H. S., Sasaki, D. Y., Sherman, M. B., et al. (2012). Membrane bending by protein-protein crowding. Nat. Cell Biol. 14, 944-949. doi: 10.1038/ncb2561
86. Stagg, S. M., Gurkan, C., Fowler, D. M., Lapointe, P., Foss, T. R., Potter, C. S., et al. (2006). Structure of the Sec13/31 COPII coat cage. Nature 439, 234-238. doi: 10.1038/nature04339
87. Stefano, G., Renna, L., Chatre, L., Hanton, S. L., Moreau, P., Hawes, C., et al. (2006). In tobacco leaf epidermal cells, the integrity of protein export from the endoplasmic reticulum and of ER export sites depends on active COPI machinery. Plant J. 46, 95-110. doi: 10.1111/j.1365-313X.2006.02675.x
88. Stefano, G., Renna, L., Rossi, M., Azzarello, E., Pollastri, S., Brandizzi, F., et al. (2010). AGD5 is a GTPase-activating protein at the trans-Golgi network. Plant J. 64, 790-799. doi: 10.1111/j.1365-313X.2010.04369.x
89. Stierhof, Y. D., and 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. doi: 10.1016/j.ejcb.2009.12.003
90. Supek, F., Madden, D. T., Hamamoto, S., Orci, L., and Schekman, R. (2002). Sec16p potentiates the action of COPII proteins to bud transport vesicles. J. Cell Biol. 158, 1029-1038. doi: 10.1083/jcb.200207053
91. Tabata, K. V., Sato, K., Ide, T., Nishizaka, T., Nakano, A., and Noji, H. (2009). Visualization of cargo concentration by COPII minimal machinery in a planar lipid membrane. EMBO J. 28, 3279-3289. doi: 10.1038/emboj.2009.269
92. Takeuchi, M., Tada, M., Saito, C., Yashiroda, H., and Nakano, A. (1998). Isolation of a tobacco cDNA encoding Sar1 GTPase and analysis of its dominant mutations in vesicular traffic using a yeast complementation system. Plant Cell Physiol. 39, 590-599. doi: 10.1093/oxfordjournals.pcp.a029409
93. Takeuchi, M., Ueda, T., Sato, K., Abe, H., Nagata, T., and Nakano, A. (2000). A dominant negative mutant of sar1 GTPase inhibits protein transport from the endoplasmic reticulum to the Golgi apparatus in tobacco and Arabidopsis cultured cells. Plant J. 23, 517-525. doi: 10.1046/j.1365-313x.2000.00823.x
94. Takeuchi, M., Ueda, T., Yahara, N., and Nakano, A. (2002). Arf1 GTPase plays roles in the protein traffic between the endoplasmic reticulum and the Golgi apparatus in tobacco and Arabidopsis cultured cells. Plant J. 31, 499-515. doi: 10.1046/j.1365-313X.2002.01372.x
95. Tanabe, K., Torii, T., Natsume, W., Braesch-Andersen, S., Watanabe, T., and Satake, M. (2005). A novel GTPase-activating protein for ARF6 directly interacts with clathrin and regulates clathrin-dependent endocytosis. Mol. Biol. Cell 16, 1617-1628. doi: 10.1091/mbc.E04-08-0683
96. Tanaka, H., Kitakura, S., De Rycke, R., De Groodt, R., and 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
97. Tanaka, Y., Nishimura, K., Kawamukai, M., Oshima, A., and Nakagawa, T. (2013). Redundant function of two Arabidopsis COPII components, AtSec24B and AtSec24C, is essential for male and female gametogenesis. Planta 238, 561-575. doi: 10.1007/s00425-013-1913-1
98. Teh, O. K., and 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
99. Tian, L., Dai, L. L., Yin, Z. J., Fukuda, M., Kumamaru, T., Dong, X. B., et al. (2013). Small GTPase Sar1 is crucial for proglutelin and alpha-globulin export from the endoplasmic reticulum in rice endosperm. J. Exp. Bot. 64, 2831-2845. doi: 10.1093/jxb/ert128
100. Vernoud, V., Horton, A. C., Yang, Z., and Nielsen, E. (2003). Analysis of the small GTPase gene superfamily of Arabidopsis. Plant Physiol. 131, 1191-1208. doi: 10.1104/pp.013052
101. Xu, J., and Scheres, B. (2005). Dissection of Arabidopsis ADP-RIBOSYLATION FACTOR 1 function in epidermal cell polarity. Plant Cell 17, 525-536. doi: 10.1105/tpc.104.028449
102. Yahara, N., Ueda, T., Sato, K., and Nakano, A. (2001). Multiple roles of Arf1 GTPase in the yeast exocytic and endocytic pathways. Mol. Biol. Cell 12, 221-238. doi: 10.1091/mbc.12.1.221
103. Yang, Y. D., Elamawi, R., Bubeck, J., Pepperkok, R., Ritzenthaler, C., and Robinson, D. G. (2005). Dynamics of COPII vesicles and the Golgi apparatus in cultured Nicotiana tabacum BY-2 cells provides evidence for transient association of Golgi stacks with endoplasmic reticulum exit sites. Plant Cell 17, 1513-1531. doi: 10.1105/tpc.104.026757
104. Yoo, C. M., and Blancaflor, E. B. (2013). Overlapping and divergent signaling pathways for ARK1 and AGD1 in the control of root hair polarity in Arabidopsis thaliana. Front. Plant Sci. 4:528. doi: 10.3389/fpls.2013.00528
105. Yoo, C. M., Quan, L., Cannon, A. E., Wen, J., and Blancaflor, E. B. (2012). AGD1, a class 1 ARF-GAP, acts in common signaling pathways with phosphoinositide metabolism and the actin cytoskeleton in controlling Arabidopsis root hair polarity. Plant J. 69, 1064-1076. doi: 10.1111/j.1365-313X.2011.04856.x
106. Yorimitsu, T., and Sato, K. (2012). Insights into structural and regulatory roles of Sec16 in COPII vesicle formation at ER exit sites. Mol. Biol. Cell 23, 2930-2942. doi: 10.1091/mbc.E12-05-0356
107. Yoshihisa, T., Barlowe, C., and Schekman, R. (1993). Requirement for a GTPaseactivating protein in vesicle budding from the endoplasmic reticulum. Science 259, 1466-1468. doi: 10.1126/science.8451644
108. Yu, X., Breitman, M., and Goldberg, J. (2012). A structure-based mechanism for Arf1-dependent recruitment of coatomer to membranes. Cell 148, 530-542. doi: 10.1016/j.cell.2012.01.015
109. Zhang, C. J., Cavenagh, M. M., and Kahn, R. A. (1998). A family of Arf effectors defined as suppressors of the loss of Arf function in the yeast Saccharomyces cerevisiae. J. Biol. Chem. 273, 19792-19796. doi: 10.1074/jbc.273.31.19792