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

Volumn 25, Issue 6, 2013, Pages 2217-2235

  Sauer, Michael ^a   Delgadillo, M Otilia ^a   Zouhar, Jan ^a,b   Reynolds, Gregory D ^c   Pennington, Janice G ^c   Jiang, Liwen ^d   Liljegren, Sarah J ^e   Stierho, York Dieter ^f   de Jaeger, Geert ^g,h   Otegui, Marisa S ^c   Bednarek, Sebastian Y ^c   Rojoa, Enrique ^a  

^a CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

^b UNIVERSIDAD POLITÉCNICA DE MADRID   (Spain)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

^d CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^e UNIVERSITY OF MISSISSIPPI   (United States)

^f UNIVERSITY OF TÜBINGEN   (Germany)

^g DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^h GHENT UNIVERSITY   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS PROTEIN; CLATHRIN; GREEN FLUORESCENT PROTEIN; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; MTV1 PROTEIN, ARABIDOPSIS; NEV PROTEIN, ARABIDOPSIS;

AMINO ACID SEQUENCE; ARTICLE; CELL VACUOLE; CLASSIFICATION; CONFOCAL MICROSCOPY; ELECTRON MICROSCOPY; GENETICS; IMMUNOBLOTTING; MERISTEM; METABOLISM; MOLECULAR GENETICS; MUTATION; PHYLOGENY; PROTEIN BINDING; PROTEIN TRANSPORT; SEQUENCE HOMOLOGY; TRANS GOLGI NETWORK; TRANSGENIC PLANT; ULTRASTRUCTURE;

AMINO ACID SEQUENCE; ARABIDOPSIS PROTEINS; CLATHRIN; GREEN FLUORESCENT PROTEINS; GTPASE-ACTIVATING PROTEINS; IMMUNOBLOTTING; MERISTEM; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON; MOLECULAR SEQUENCE DATA; MUTATION; PHYLOGENY; PLANTS, GENETICALLY MODIFIED; PROTEIN BINDING; PROTEIN TRANSPORT; SEQUENCE HOMOLOGY, AMINO ACID; TRANS-GOLGI NETWORK; VACUOLES;

EID: 84880957255     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.113.111724     Document Type: Article

References (99)

1. Abas, L., Benjamins, R., Malenica, N., Paciorek, T., Wiśniewska, J., Moulinier-Anzola, J.C., Sieberer, T., Friml, J., and Luschnig, C. (2006). Intracellular trafficking and proteolysis of the Arabidopsis auxin-efflux facilitator PIN2 are involved in root gravitropism. Nat. Cell Biol. 8: 249-256. Erratum. Nat. Cell Biol. 8: 424.
2. Ahmed, S.U., Rojo, E., Kovaleva, V., Venkataraman, S., Dombrowski, J.E., Matsuoka, K., and Raikhel, N.V. (2000). The plant vacuolar sorting receptor AtELP is involved in transport of NH(2)-terminal propeptide-containing vacuolar proteins in Arabidopsis thaliana. J. Cell Biol. 149: 1335-1344.
3. Bai, M., et al. (2011). ARFGAP1 promotes AP-2-dependent endocytosis. Nat. Cell Biol. 13: 559-567.
4. Bar-Peled, M., and Raikhel, N.V. (1997). Characterization of AtSEC12 and AtSAR1. Proteins likely involved in endoplasmic reticulum and Golgi transport. Plant Physiol. 114: 315-324.
5. Bassham, D.C., and Raikhel, N.V. (1998). An Arabidopsis VPS45p homolog implicated in protein transport to the vacuole. Plant Physiol. 117: 407-415.
6. Benková, E., Michniewicz, M., Sauer, M., Teichmann, T., Seifertová, D., Jürgens, G., and Friml, J. (2003). Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115: 591-602.
7. Betsuyaku, S., Sawa, S. and Yamada, M. (2011). The function of the CLE peptides in plant development and plant-microbe interactions. In The Arabidopsis Book 9: e0149, doi/10.1199/tab.0149.
8. Bolte, S., Talbot, C., Boutte, Y., Catrice, O., Read, N.D., and Satiat- Jeunemaitre, B. (2004). FM-dyes as experimental probes for dissecting vesicle trafficking in living plant cells. J. Microsc. 214: 159-173.
9. Bonangelino, C.J., Chavez, E.M., and Bonifacino, J.S. (2002). Genomic screen for vacuolar protein sorting genes in Saccharomyces cerevisiae. Mol. Biol. Cell 13: 2486-2501.
10. Carter, C., Pan, S., Zouhar, J., Avila, E.L., Girke, T., and Raikhel, N.V. (2004). The vegetative vacuole proteome of Arabidopsis thaliana reveals predicted and unexpected proteins. Plant Cell 16: 3285-3303.
11. Dacks, J.B., and Field, M.C. (2007). Evolution of the eukaryotic membranetrafficking system: Origin, tempo and mode. J. Cell Sci. 120: 2977-2985.
12. da Silva Conceição, A., Marty-Mazars, D., Bassham, D.C., Sanderfoot, A.A., Marty, F., and Raikhel, N.V. (1997). The syntaxin homolog AtPEP12p resides on a late post-Golgi compartment in plants. Plant Cell 9: 571-582.
13. Delgado, I.J., Wang, Z., de Rocher, A., Keegstra, K., and Raikhel, N.V. (1998). Cloning and characterization of AtRGP1. A reversibly autoglycosylated Arabidopsis protein implicated in cell wall biosynthesis. Plant Physiol. 116: 1339-1350.
14. Dell'Angelica, E.C., Puertollano, R., Mullins, C., Aguilar, R.C., Vargas, J.D., Hartnell, L.M., and Bonifacino, J.S. (2000). GGAs: A family of ADP ribosylation factor-binding proteins related to adaptors and associated with the Golgi complex. J. Cell Biol. 149: 81-94.
15. De Marcos Lousa, C., Gershlick, D.C., and Denecke, J. (2012). Mechanisms and concepts paving the way towards a complete transport cycle of plant vacuolar sorting receptors. Plant Cell 24: 1714-1732.
16. Denecke, J., Aniento, F., Frigerio, L., Hawes, C., Hwang, I., Mathur, J., Neuhaus, J.-M., and Robinson, D.G. (2012). Secretory pathway research: The more experimental systems the better. Plant Cell 24: 1316-1326.
17. Depta, H., and Robinson, D.G. (1986). The isolation and enrichment of coated vesicles from suspension-cultured carrot cells. Protoplasma 130: 162-170.
18. Dettmer, J., Hong-Hermesdorf, A., Stierhof, Y.-D., and Schumacher, K. (2006). Vacuolar H+-ATPase activity is required for endocytic and secretory trafficking in Arabidopsis. Plant Cell 18: 715-730.
19. Ebine, K., Okatani, Y., Uemura, T., Goh, T., Shoda, K., Niihama, M., Morita, M.T., Spitzer, C., Otegui, M.S., Nakano, A., and 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 20: 3006-3021.
20. Foresti, O., Gershlick, D.C., Bottanelli, F., Hummel, E., Hawes, C., and Denecke, J. (2010). A recycling-defective vacuolar sorting receptor reveals an intermediate compartment situated between prevacuoles and vacuoles in tobacco. Plant Cell 22: 3992-4008.
21. Geldner, N., Anders, N., Wolters, H., Keicher, J., Kornberger, W., Muller, P., Delbarre, A., Ueda, T., Nakano, A., and Jürgens, G. (2003). The Arabidopsis GNOM ARF-GEF mediates endosomal recycling, auxin transport, and auxin-dependent plant growth. Cell 112: 219-230.
22. Geldner, N., Dénervaud-Tendon, V., Hyman, D.L., Mayer, U., Stierhof, Y.-D., and Chory, J. (2009). Rapid, combinatorial analysis of membrane compartments in intact plants with a multicolor marker set. Plant J. 59: 169-178.
23. Gendre, D., Oh, J., Boutté, Y., Best, J.G., Samuels, L., Nilsson, R., Uemura, T., Marchant, A., Bennett, M.J., Grebe, M., and Bhalerao, R.P. (2011). Conserved Arabidopsis ECHIDNA protein mediates trans- Golgi-network trafficking and cell elongation. Proc. Natl. Acad. Sci. USA 108: 8048-8053.
24. Grefen, C., Donald, N., Hashimoto, K., Kudla, J., Schumacher, K., and Blatt, M.R. (2010). A ubiquitin-10 promoter-based vector set for fluorescent protein tagging facilitates temporal stability and native protein distribution in transient and stable expression studies. Plant J. 64: 355-365.
25. Happel, N., Höning, S., Neuhaus, J.-M., Paris, N., Robinson, D.G., and Holstein, S.E.H. (2004). Arabidopsis mu A-adaptin interacts with the tyrosine motif of the vacuolar sorting receptor VSR-PS1. Plant J. 37: 678-693.
26. Harley, S.M., and Beevers, L. (1989). Coated vesicles are involved in the transport of storage proteins during seed development in Pisum sativum L. Plant Physiol. 91: 674-678.
27. Hinz, G., Colanesi, S., Hillmer, S., Rogers, J.C., and Robinson, D.G. (2007). Localization of vacuolar transport receptors and cargo proteins in the Golgi apparatus of developing Arabidopsis embryos. Traffic 8: 1452-1464.
28. Hinz, G., Hillmer, S., Baumer, M., and Hohl, I. (1999). Vacuolar storage proteins and the putative vacuolar sorting receptor BP-80 exit the Golgi apparatus of developing pea cotyledons in different transport vesicles. Plant Cell 11: 1509-1524.
29. Horvath, C.A.J., Vanden Broeck, D., Boulet, G.A.V., Bogers, J., and De Wolf, M.J.S. (2007). Epsin: Inducing membrane curvature. Int. J. Biochem. Cell Biol. 39: 1765-1770.
30. Hunter, P.R., Craddock, C.P., Di Benedetto, S., Roberts, L.M., and Frigerio, L. (2007). Fluorescent reporter proteins for the tonoplast and the vacuolar lumen identify a single vacuolar compartment in Arabidopsis cells. Plant Physiol. 145: 1371-1382.
31. Ito, E., Fujimoto, M., Ebine, K., Uemura, T., Ueda, T., and Nakano, A. (2012). Dynamic behavior of clathrin in Arabidopsis thaliana unveiled by live imaging. Plant J. 69: 204-216.
32. Kang, B.H., Nielsen, E., Preuss, M.L., Mastronarde, D., and Staehelin, L.A. (2011). Electron tomography of RabA4b- and PI-4Kb1-labeled trans Golgi network compartments in Arabidopsis. Traffic 12: 313-329.
33. Kirsch, T., Paris, N., Butler, J.M., Beevers, L., and Rogers, J.C. (1994). Purification and initial characterization of a potential plant vacuolar targeting receptor. Proc. Natl. Acad. Sci. USA 91: 3403-3407.
34. Kleine-Vehn, J., Dhonukshe, P., Sauer, M., Brewer, P.B., Wiśniewska, J., Paciorek, T., Benková, E., and Friml, J. (2008). ARF GEF-dependent transcytosis and polar delivery of PIN auxin carriers in Arabidopsis. Curr. Biol. 18: 526-531
35. Kon, S., Funaki, T., and Satake, M. (2011). Putative terminator and/or effector functions of Arf GAPs in the trafficking of clathrin-coated vesicles. Cell. Logist. 1: 86-89.
36. Konopka, C.A., Backues, S.K., and Bednarek, S.Y. (2008). Dynamics of Arabidopsis dynamin-related protein 1C and a clathrin light chain at the plasma membrane. Plant Cell 20: 1363-1380.
37. Lafer, E.M. (2002). Clathrin-protein interactions. Traffic 3: 513-520.
38. Lam, S.K., Cai, Y., Tse, Y.C., Wang, J., Law, A.H.Y., Pimpl, P., Chan, H.Y.E., Xia, J., and Jiang, L. (2009). BFA-induced compartments from the Golgi apparatus and trans-Golgi network/early endosome are distinct in plant cells. Plant J. 60: 865-881.
39. Langhans, M., Förster, S., Helmchen, G., and Robinson, D.G. (2011). Differential effects of the brefeldin A analogue (6R)-hydroxy- BFA in tobacco and Arabidopsis. J. Exp. Bot. 62: 2949-2957.
40. Lee, M.H., Min, M.K., Lee, Y.J., Jin, J.B., Shin, D.H., Kim, D.H., Lee, K.-H., and Hwang, I. (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.
41. Lee, G.-J., Kim, H., Kang, H., Jang, M., Lee, D.W., Lee, S., and Hwang, I. (2007). EpsinR2 interacts with clathrin, adaptor protein-3, AtVTI12, and phosphatidylinositol-3-phosphate. Implications for EpsinR2 function in protein trafficking in plant cells. Plant Physiol. 143: 1561-1575.
42. Legendre-Guillemin, V., Wasiak, S., Hussain, N.K., Angers, A., and McPherson, P.S. (2004). ENTH/ANTH proteins and clathrin-mediated membrane budding. J. Cell Sci. 117: 9-18.
43. Li, L., Shimada, T., Takahashi, H., Ueda, H., Fukao, Y., Kondo, M., Nishimura, M., and Hara-Nishimura, I. (2006). MAIGO2 is involved in exit of seed storage proteins from the endoplasmic reticulum in Arabidopsis thaliana. Plant Cell 18: 3535-3547.
44. Liljegren, S.J., Leslie, M.E., Darnielle, L., Lewis, M.W., Taylor, S.M., Luo, R., Geldner, N., Chory, J., Randazzo, P.A., Yanofsky, M.F., and Ecker, J.R. (2009). Regulation of membrane trafficking and organ separation by the NEVERSHED ARF-GAP protein. Development 136: 1909-1918.
45. López-Méndez, B., et al. (2004). NMR assignment of the hypothetical ENTH-VHS domain At3g16270 from Arabidopsis thaliana. J. Biomol. NMR 29: 205-206.
46. Meyerowitz, E.M. (2002). Plants compared to animals: The broadest comparative study of development. Science 295: 1482-1485.
47. Min, M.K., Jang, M., Lee, M., Lee, J., Song, K., Lee, Y., Choi, K.Y., Robinson, D.G., and Hwang, I. (2013). Recruitment of Arf1-GDP to Golgi by Glo3p-type ArfGAPs is crucial for Golgi maintenance and plant growth. Plant Physiol. 161: 676-691.
48. Nakagawa, T., Kurose, T., Hino, T., Tanaka, K., Kawamukai, M., Niwa, Y., Toyooka, K., Matsuoka, K., Jinbo, T., and Kimura, T. (2007). Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation. J. Biosci. Bioeng. 104: 34-41.
49. Natsume, W., Tanabe, K., Kon, S., Yoshida, N., Watanabe, T., Torii, T., and Satake, M. (2006). SMAP2, a novel ARF GTPase-activating protein, interacts with clathrin and clathrin assembly protein and functions on the AP-1-positive early endosome/trans-Golgi network. Mol. Biol. Cell 17: 2592-2603.
50. Nie, Z., and Randazzo, P.A. (2006). Arf GAPs and membrane traffic. J. Cell Sci. 119: 1203-1211.
51. Otegui, M.S., Herder, R., Schulze, J., Jung, R., and Staehelin, L.A. (2006). The proteolytic processing of seed storage proteins in Arabidopsis embryo cells starts in the multivesicular bodies. Plant Cell 18: 2567-2581.
52. Pérez-Pérez, J.M., Candela, H., and Micol, J.L. (2009). Understanding synergy in genetic interactions. Trends Genet. 25: 368-376.
53. Peterson, R., Slovin, J.P. and Chen, C. (2010). A simplified method for differential staining of aborted and non-aborted pollen grains. Int. J. Plant Biol. 1: 66-69.
54. 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.
55. Reichardt, I., Stierhof, Y.-D., Mayer, U., Richter, S., Schwarz, H., Schumacher, K., and Jürgens, G. (2007). Plant cytokinesis requires de novo secretory trafficking but not endocytosis. Curr. Biol. 17: 2047-2053.
56. Ricarte, F., Menjivar, R., Chhun, S., Soreta, T., Oliveira, L., Hsueh, T., Serranilla, M., and Gharakhanian, E. (2011). A genome-wide immunodetection screen in S. cerevisiae uncovers novel genes involved in lysosomal vacuole function and morphology. PLoS ONE 6: e23696.
57. Robert, S., Chary, S.N., Drakakaki, G., Li, S., Yang, Z., Raikhel, N.V., and Hicks, G.R. (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.
58. 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, author reply 849-850.
59. Rojo, E., and Denecke, J. (2008). What is moving in the secretory pathway of plants? Plant Physiol. 147: 1493-1503.
60. Rojo, E., Sharma, V.K., Kovaleva, V., Raikhel, N.V., and Fletcher, J.C. (2002). CLV3 is localized to the extracellular space, where it activates the Arabidopsis CLAVATA stem cell signaling pathway. Plant Cell 14: 969-977.
61. Rojo, E., Zouhar, J., Carter, C., Kovaleva, V., and Raikhel, N.V. (2003a). A unique mechanism for protein processing and degradation in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 100: 7389-7394.
62. Rojo, E., Zouhar, J., Kovaleva, V., Hong, S., and Raikhel, N.V. (2003b). The AtC-VPS protein complex is localized to the tonoplast and the prevacuolar compartment in Arabidopsis. Mol. Biol. Cell 14: 361-369.
63. Saint-Jean, B., Seveno-Carpentier, E., Alcon, C., Neuhaus, J.-M., and Paris, N. (2010). The cytosolic tail dipeptide Ile-Met of the pea receptor BP80 is required for recycling from the prevacuole and for endocytosis. Plant Cell 22: 2825-2837.
64. Sanderfoot, A. (2007). Increases in the number of SNARE genes parallels the rise of multicellularity among the green plants. Plant Physiol. 144: 6-17.
65. Sanderfoot, A.A., Ahmed, S.U., Marty-Mazars, D., Rapoport, I., Kirchhausen, T., Marty, F., and Raikhel, N.V. (1998). A putative vacuolar cargo receptor partially colocalizes with AtPEP12p on a prevacuolar compartment in Arabidopsis roots. Proc. Natl. Acad. Sci. USA 95: 9920-9925.
66. Sanmartín, M., Ordóñez, A., Sohn, E.J., Robert, S., Sánchez-Serrano, J.J., Surpin, M.A., Raikhel, N.V., and Rojo, E. (2007). Divergent functions of VTI12 and VTI11 in trafficking to storage and lytic vacuoles in Arabidopsis. Proc. Natl. Acad. Sci. USA 104: 3645-3650.
67. Santos-Mendoza, M., Dubreucq, B., Baud, S., Parcy, F., Caboche, M., and Lepiniec, L. (2008). Deciphering gene regulatory networks that control seed development and maturation in Arabidopsis. Plant J. 54: 608-620.
68. Scheele, U., Alves, J., Frank, R., Duwel, M., Kalthoff, C., and Ungewickell, E. (2003). Molecular and functional characterization of clathrin- and AP-2-binding determinants within a disordered domain of auxilin. J. Biol. Chem. 278: 25357-25368.
69. Schekman, R., and Novick, P. (2004). 23 genes, 23 years later. Cell 116 (2, suppl.) S13-S15, 1, S19.
70. Scheuring, D., Viotti, C., Krüger, F., Künzl, F., Sturm, S., Bubeck, J., Hillmer, S., Frigerio, L., Robinson, D.G., Pimpl, P., and Schumacher, K. (2011). Multivesicular bodies mature from the trans-Golgi network/early endosome in Arabidopsis. Plant Cell 23: 3463-3481.
71. Schumacher, K., Vafeados, D., McCarthy, M., Sze, H., Wilkins, T., and Chory, J. (1999). The Arabidopsis det3 mutant reveals a central role for the vacuolar H(+)-ATPase in plant growth and development. Genes Dev. 13: 3259-3270.
72. Shimada, T., Fuji, K., Tamura, K., Kondo, M., Nishimura, M., and Hara-Nishimura, I. (2003). Vacuolar sorting receptor for seed storage proteins in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 100: 16095-16100.
73. Sohn, E.J., Rojas-Pierce, M., Pan, S., Carter, C., Serrano-Mislata, A., Madueño, F., Rojo, E., Surpin, M., and Raikhel, N.V. (2007). The shoot meristem identity gene TFL1 is involved in flower development and trafficking to the protein storage vacuole. Proc. Natl. Acad. Sci. USA 104: 18801-18806.
74. Song, J., Lee, M.H., Lee, G.-J., Yoo, C.M., and Hwang, I. (2006a). Arabidopsis EPSIN1 plays an important role in vacuolar trafficking of soluble cargo proteins in plant cells via interactions with clathrin, AP-1, VTI11, and VSR1. Plant Cell 18: 2258-2274.
75. Song, K., Jang, M., Kim, S.Y., Lee, G., Lee, G.-J., Kim, D.H., Lee, Y., Cho, W., and Hwang, I. (2012). An A/ENTH domain-containing protein functions as an adaptor for clathrin-coated vesicles on the growing cell plate in Arabidopsis root cells. Plant Physiol. 159: 1013-1025.
76. Song, X.-F., Yang, C.-Y., Liu, J., and Yang, W.-C. (2006b). RPA, a class II ARFGAP protein, activates ARF1 and U5 and plays a role in root hair development in Arabidopsis. Plant Physiol. 141: 966-976.
77. Spang, A., Shiba, Y., and Randazzo, P.A. (2010). Arf GAPs: Gatekeepers of vesicle generation. FEBS Lett. 584: 2646-2651.
78. Stefano, G., Renna, L., Chatre, L., Hanton, S.L., Moreau, P., Hawes, C., and Brandizzi, F. (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.
79. Stefano, G., Renna, L., Rossi, M., Azzarello, E., Pollastri, S., Brandizzi, F., Baluska, F., and Mancuso, S. (2010). AGD5 is a GTPase-activating protein at the trans-Golgi network. Plant J. 64: 790-799.
80. 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.
81. Surpin, M., Zheng, H., Morita, M.T., Saito, C., Avila, E., Blakeslee, J.J., Bandyopadhyay, A., Kovaleva, V., Carter, D., Murphy, A., Tasaka, M., and Raikhel, N. (2003). The VTI family of SNARE proteins is necessary for plant viability and mediates different protein transport pathways. Plant Cell 15: 2885-2899.
82. 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.
83. 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.
84. 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.
85. Tse, Y.C., Mo, B., Hillmer, S., Zhao, M., Lo, S.W., Robinson, D.G., and Jiang, L. (2004). Identification of multivesicular bodies as prevacuolar compartments in Nicotiana tabacum BY-2 cells. Plant Cell 16: 672-693.
86. Uemura, T., Kim, H., Saito, C., Ebine, K., Ueda, T., Schulze-Lefert, P., and 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. USA 109: 1784-1789.
87. Van Leene, J., Eeckhout, D., Persiau, G., Van De Slijke, E., Geerinck, J., Van Isterdael, G., Witters, E., and De Jaeger, G. (2011). Isolation of transcription factor complexes from Arabidopsis cell suspension cultures by tandem affinity purification. Methods Mol. Biol. 754: 195-218.
88. Van Leene, J., et al. (2010). Targeted interactomics reveals a complex core cell cycle machinery in Arabidopsis thaliana. Mol. Syst. Biol. 6: 397.
89. Van Leene, J., et al. (2007). A tandem affinity purification-based technology platform to study the cell cycle interactome in Arabidopsis thaliana. Mol. Cell. Proteomics 6: 1226-1238.
90. Van Leene, J., Witters, E., Inzé, D., and De Jaeger, G. (2008). Boosting tandem affinity purification of plant protein complexes. Trends Plant Sci. 13: 517-520.
91. 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.
92. Viotti, C., et al. (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.
93. Wang, J., Cai, Y., Miao, Y., Lam, S.K., and Jiang, L. (2009). Wortmannin induces homotypic fusion of plant prevacuolar compartments. J. Exp. Bot. 60: 3075-3083.
94. Waterhouse, A.M., Procter, J.B., Martin, D.M.A., Clamp, M., and Barton, G.J. (2009). Jalview Version 2-A multiple sequence alignment editor and analysis workbench. Bioinformatics 25: 1189-1191.
95. Yamazaki, M., Shimada, T., Takahashi, H., Tamura, K., Kondo, M., Nishimura, M., and Hara-Nishimura, I. (2008). Arabidopsis VPS35, a retromer component, is required for vacuolar protein sorting and involved in plant growth and leaf senescence. Plant Cell Physiol. 49: 142-156.
96. Zhang, Z., Feechan, A., Pedersen, C., Newman, M.-A., Qiu, J.L., Olesen, K.L., and Thordal-Christensen, H. (2007). A SNAREprotein has opposing functions in penetration resistance and defence signalling pathways. Plant J. 49: 302-312.
97. Zouhar, J., Muñoz, A., and Rojo, E. (2010). Functional specialization within the vacuolar sorting receptor family: VSR1, VSR3 and VSR4 sort vacuolar storage cargo in seeds and vegetative tissues. Plant J. 64: 577-588.
98. Zouhar, J., and Rojo, E. (2009). Plant vacuoles: Where did they come from and where are they heading? Curr. Opin. Plant Biol. 12: 677-684.
99. Zouhar, J., Rojo, E., and Bassham, D.C. (2009). AtVPS45 is a positive regulator of the SYP41/SYP61/VTI12 SNARE complex involved in trafficking of vacuolar cargo. Plant Physiol. 149: 1668-1678.