News and views into the SNARE complexity in Arabidopsis

Frontiers in Plant Science

Volumn 3, Issue FEB, 2012, Pages

  Kim, Sang Jin ^a   Brandizzi, Federica ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

Arabidopsis; Membrane fusion; SNARE; Vesicle trafficking

Indexed keywords

EID: 84897124898     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2012.00028     Document Type: Article

References (58)

1. Ahmed, S. U., Barpeled, M., and Raikhel, N. V. (1997). Cloning and subcellular location of an Arabidopsis receptor-like protein that shares common features with protein-sorting receptors of eukaryotic cells. Plant Physiol. 115, 311-312.
2. Assaad, F. F., Qiu, J. L., Youngs, H., Ehrhardt, D., Zimmerli, L., Kalde, M., Wanner, G., Peck, S. C., Edwards, H., Ramonell, K., Somerville, C. R., and 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.
3. Bassham, D. C., Sanderfoot, A. A., Kovaleva, V., Zheng, H. Y., and Raikhel, N. V. (2000). AtVPS45 complex formation at the trans-Golgi network. Mol. Biol. Cell 11, 2251-2265.
4. Blatt, M. R. (2000). Cellular signaling and volume control in stomatal movements in plants. Annu. Rev. Cell Dev. Biol. 16, 221-241.
5. Bock, J. B., Matern, H. T., Peden, A. A., and Scheller, R. H. (2001). A genomic perspective on membrane compartment organization. Nature 409, 839-841.
6. Boutte, Y., Frescatada-Rosa, M., Men, S. Z., Chow, C. M., Ebine, K., Gustavsson, A., Johansson, L., Ueda, T., Moore, I., Jurgens, G., and Grebe, M. (2010). Endocytosis restricts Arabidopsis KNOLLE syntaxin to the cell division plane during late cytokinesis. EMBO J. 29, 546-558.
7. Bubeck, J., Scheuring, D., Hummel, E., Langhans, M., Viotti, C., Foresti, O., Denecke, J., Banfield, D. K., and Robinson, D. G. (2008). The syntaxins SYP31 and SYP81 control ER-Golgi trafficking in the plant secretory pathway. Traffic 9, 1629-1652.
8. Chatre, L., Brandizzi, F., Hocquellet, A., Hawes, C., and Moreau, P. (2005). Sec22 and Memb11 are v-SNAREs of the anterograde endoplasmic reticulum-Golgi pathway in tobacco leaf epidermal cells. Plant Physiol. 139, 1244-1254.
9. Chow, C. M., Neto, H., Foucart, C., and 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.
10. Collins, N. C., Thordal-Christensen, H., Lipka, V., Bau, S., Kombrink, E., Qiu, J. L., Huckelhoven, R., Stein, M., Freialdenhoven, A., Somerville, S. C., and Schulze-Lefert, P. (2003). SNARE-protein-mediated disease resistance at the plant cell wall. Nature 425, 973-977.
11. 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.
12. Dhonukshe, P., Tanaka, H., Goh, T., Ebine, K., Mahonen, A. P., Prasad, K., Blilou, I., Geldner, N., Xu, J., Uemura, T., Chory, J., Ueda, T., Nakano, A., Scheres, B., and Friml, J. (2008). Generation of cell polarity in plants links endocytosis, auxin distribution and cell fate decisions. Nature 456, U962-U975.
13. Drakakaki, G., Van De Ven, W., Pan, S., Miao, Y., Wang, J., Keinath, N. K., Weatherly, B., Jiang, L., Schumacher, K., Hicks, G., and Raikhel, N. (2011). Isolation and proteomic analysis of the SYP61 compartment reveal its role in exocytic trafficking in Arabidopsis. Cell Res. 1-12.
14. Ebine, K., Fujimoto, M., Okatani, Y., Nishiyama, T., Goh, T., Ito, E., Dainobu, T., Nishitani, A., Uemura, T., Sato, M. H., Thordal-Christensen, H., Tsutsumi, N., Nakano, A., and Ueda, T. (2011). A membrane trafficking pathway regulated by the plant-specific RAB GTPase ARA6. Nat. Cell Biol. 13, U853-U859.
15. 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.
16. El-Kasmi, F., Pacher, T., Strompen, G., Stierhof, Y. D., Müller, L. M., Koncz, C., Mayer, U., and Jürgens, G. (2011). Arabidopsis SNARE protein SEC22 is essential for gametophyte development and maintenance of Golgi-stack integrity. Plant J. 66, 268-279.
17. Fasshauer, D., Sutton, R. B., Brunger, A. T., and Jahn, R. (1998). Conserved structural features of the synaptic fusion complex: SNARE proteins reclassified as Q-and R-SNAREs. Proc. Natl. Acad. Sci. U.S.A. 95, 15781-15786.
18. Foresti, O., Dasilva, L. L., and Denecke, J. (2006). Overexpression of the Arabidopsis syntaxin PEP12/SYP21 inhibits transport from the prevacuolar compartment to the lytic vacuole in vivo. Plant Cell 18, 2275-2293.
19. Hara-Nishimura, I., Shimada, T., Hatano, K., Takeuchi, Y., and Nishimura, M. (1998). Transport of storage proteins to protein storage vacuoles is mediated by large precursor-accumulating vesicles. Plant Cell 10, 825-836.
20. Hayashi, Y., Yamada, K., Shimada, T., Matsushima, R., Nishizawa, N. K., Nishimura, M., and Hara-Nishimura, I. (2001). A proteinase-storing body that prepares for cell death or stresses in the epidermal cells of Arabidopsis. Plant Cell Physiol. 42, 894-899.
21. Heese, M., Gansel, X., Sticher, L., Wick, P., Grebe, M., Granier, F., and Jurgens, G. (2001). Functional characterization of the KNOLLE-interacting t-SNARE AtSNAP33 and its role in plant cytokinesis. J. Cell Biol. 155, 239-249.
22. Honsbein, A., Sokolovski, S., Grefen, C., Campanoni, P., Pratelli, R., Paneque, M., Chen, Z. H., Johansson, I., and Blatt, M. R. (2009). A tripartite SNARE-K+ channel complex mediates in channel-dependent K+ nutrition in Arabidopsis. Plant Cell 21, 2859-2877.
23. Kwon, C., Neu, C., Pajonk, S., Yun, H. S., Lipka, U., Humphry, M., Bau, S., Straus, M., Kwaaitaal, M., Rampelt, H., El Kasmi, F., Jurgens, G., Parker, J., Panstruga, R., Lipka, V., and Schulze-Lefert, P. (2008). Co-option of a default secretory pathway for plant immune responses. Nature 451, 835-840.
24. Lauber, M. H., Waizenegger, I., Steinmann, T., Schwarz, H., Mayer, U., Hwang, I., Lukowitz, W., and Jurgens, G. (1997). The Arabidopsis KNOLLE protein is a cytokinesis-specific syntaxin. J. Cell Biol. 139, 1485-1493.
25. Leshem, Y., Golani, Y., Kaye, Y., and Levine, A. (2010). Reduced expression of the v-SNAREs AtVAMP71/AtVAMP7C gene family in Arabidopsis reduces drought tolerance by suppression of abscisic acid-dependent stomatal closure. J. Exp. Bot. 61, 2615-2622.
26. Lukowitz, W., Mayer, U., and Jurgens, G. (1996). Cytokinesis in the Arabidopsis embryo involves the syntaxin-related KNOLLE gene product. Cell 84, 61-71.
27. Malsam, J., Kreye, S., and Sollner, T. H. (2008). Membrane fusion: SNAREs and regulation. Cell. Mol. Life Sci. 65, 2814-2832.
28. Mancias, J., and Goldberg, J. (2008). Structural basis of cargo membrane protein discrimination by the human COPII coat machinery. EMBO J. 27, 2918-2928.
29. McNew, J. A., Parlati, F., Fukuda, R., Johnston, R. J., Paz, K., Paumet, F., Sollner, T. H., and Rothman, J. E. (2000). Compartmental specificity of cellular membrane fusion encoded in SNARE proteins. Nature 407, 153-159.
30. Nakamura, K., Matsuoka, K., Mukumoto, F., and Watanabe, N. (1993). Processing and transport to the vacuole of a precursor to sweet-potato sporamin in transformed tobacco cell line-by-2. J. Exp. Bot. 44, 331-338.
31. Price, A., Wickner, W., and Ungermann, C. (2000). Proteins needed for vesicle budding from the Golgi complex are also required for the docking step of homotypic vacuole fusion. J. Cell Biol. 148, 1223-1229.
32. Reichardt, I., Slane, D., El Kasmi, F., Knöll, C., Fuchs, R., Mayer, U., Lipka, V., and Jürgens, G. (2011). Mechanisms of functional specificity among plasma-membrane syntaxins in Arabidopsis. Traffic 12, 1269-1280.
33. Reichardt, L., Stierhof, Y. D., Mayer, U., Richter, S., Schwarz, H., Schumacher, K., and Jurgens, G. (2007). Plant cytokinesis requires de novo secretory trafficking but not endocytosis. Curr. Biol. 17, 2047-2053.
34. Robinson, D. G., Herranz, M. C., Bubeck, J., Pepperkok, R., and Ritzenthaler, C. (2007). Membrane dynamics in the early secretory pathway. CRC Crit. Rev. Plant Sci. 26, 199-225.
35. Saito, C., and Ueda, T. (2009). Functions of Rab and SNARE proteins in plant life. Int. Rev. Cell Mol. Biol. 274, 183-233.
36. Sanderfoot, A. (2007). Increases in the number of SNARE genes parallels the rise of multicellularity among the green plants. Plant Physiol. 144, 6-17.
37. Sanderfoot, A. A., Kovaleva, V., Bassham, D. C., and Raikhel, N. V. (2001a). Interactions between syntaxins identify at least five SNARE complexes within the Golgi/prevacuolar system of the Arabidopsis cell. Mol. Biol. Cell 12, 3733-3743.
38. Sanderfoot, A. A., Pilgrim, M., Adam, L., and Raikhel, N. V. (2001b). Disruption of individual members of Arabidopsis syntaxin gene families indicates each has essential functions. Plant Cell 13, 659-666.
39. Scheuring, D., Viotti, C., Kruger, F., Kunzl, 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.
40. Schwacke, R., Schneider, A., Van Der Graaff, E., Fischer, K., Catoni, E., Desimone, M., Frommer, W. B., Flugge, U. I., and Kunze, R. (2003). ARAMEMNON, a novel database for Arabidopsis integral membrane proteins. Plant Physiol. 131, 16-26.
41. Seals, D. F., Eitzen, G., Margolis, N., Wickner, W. T., and Price, A. (2000). AYpt/Rab effector complex containing the Sec1 homolog Vps33p is required for homotypic vacuole fusion. Proc. Natl. Acad. Sci. U.S.A. 97, 9402-9407.
42. Shirakawa, M., Ueda, H., Shimada, T., Koumoto, Y., Shimada, T. L., Kondo, M., Takahashi, T., Okuyama, Y., Nishimura, M., and Hara-Nishimura, I. (2010). Arabidopsis Qa-SNARE SYP2 proteins localized to different subcellular regions function redundantly in vacuolar protein sorting and plant development. Plant J. 64, 924-935.
43. Shorter, J., Beard, M. B., Seemann, J., Dirac-Svejstrup, A. B., and Warren, G. (2002). Sequential tethering of Golgins and catalysis of SNAREpin assembly by the vesicle-tethering protein p115. J. Cell Biol. 157, 45-62.
44. Sirichandra, C., Wasilewska, A., Vlad, F., Valon, C., and Leung, J. (2009). The guard cell as a single-cell model towards understanding drought tolerance and abscisic acid action. J. Exp. Bot. 60, 1439-1463.
45. Sollner, T., Whitehart, S., Brunner, M., Erdjumentbromage, H., Geromanos, S., Tempst, P., and Rothman, J. (1993). SNAP receptors implicated in vesicle targeting and fusion. Nature 362, 318-324.
46. Spang, A., and Schekman, R. (1998). Reconstitution of retrograde transport from the Golgi to the ER in vitro. J. Cell Biol. 143, 589-599.
47. Sutter, J. U., Campanoni, P., Blatt, M. R., and Paneque, M. (2006a). Setting SNAREs in a different wood. Traffic 7, 627-638.
48. Sutter, J. U., Campanoni, P., Tyrrell, M., and Blatt, M. R. (2006b). Selective mobility and sensitivity to SNAREs is exhibited by the Arabidopsis KAT1 K+ channel at the plasma membrane. Plant Cell 18, 935-954.
49. Suwastika, I. N., Uemura, T., Shiina, T., Sato, M., and Takeyasu, K. (2008). SYP71, a plant-specific Qc-SNARE protein, reveals dual localization to the plasma membrane and the endoplasmic reticulum in Arabidopsis. Cell Struct. Funct. 33, 185-192.
50. Toyooka, K., Goto, Y., Asatsuma, S., and Matsuoka, K. (2007). SCAMP-containing vesicle cluster (SVC), a post-Golgi exocytotic organelle. Plant Cell Physiol. 48, S122.
51. Toyooka, K., Okamoto, T., and Minamikawa, T. (2000). Mass transport of proform of a KDEL-tailed cysteine proteinase (SH-EP) to protein storage vacuoles by endoplasmic reticulum-derived vesicle is involved in protein mobilization in germinating seeds. J. Cell Biol. 148, 453-464.
52. Tsui, M. M., Tai, W. C., and Banfield, D. K. (2001). Selective formation of Sed5p-containing SNARE complexes is mediated by combinatorial binding interactions. Mol. Biol. Cell 12, 521-538.
53. Uemura, T., Morita, M. T., Ebine, K., Okatani, Y., Yano, D., Saito, C., Ueda, T., and Nakano, A. (2010). Vacuolar/pre-vacuolar compartment Qa-SNAREs VAM3/SYP22 and PEP12/SYP21 have interchangeable functions in Arabidopsis. Plant J. 64, 864-873.
54. Uemura, T., Ueda, T., Ohniwa, R. L., Nakano, A., Takeyasu, K., and Sato, M. H. (2004). Systematic analysis of SNARE molecules in Arabidopsis: dissection of the post-Golgi network in plant cells. Cell Struct. Funct. 29, 49-65.
55. Yano, D., Sato, M., Saito, C., Sato, M. H., Morita, M. T., and Tasaka, M. (2003). A SNARE complex containing SGR3/AtVAM3 and ZIG/VTI11 in gravity-sensing cells is important for Arabidopsis shoot gravitropism. Proc. Natl. Acad. Sci. U.S.A. 100, 8589-8594.
56. Zhang, Z. G., Feechan, A., Pedersen, C., Newman, M. A., Qiu, J. L., Olesen, K. L., and Thordal-Christensen, H. (2007). A SNARE-protein has opposing functions in penetration resistance and defence signalling pathways. Plant J. 49, 302-312.
57. Zhu, J. H., Gong, Z. Z., Zhang, C. Q., Song, C. P., Damsz, B., Inan, G., Koiwa, H., Zhu, J. K., Hasegawa, P. M., and Bressan, R. A. (2002). OSM1/SYP61: a syntaxin protein in Arabidopsis controls abscisic acid-mediated and non-abscisic acid-mediated responses to abiotic stress. Plant Cell 14, 3009-3028.
58. 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.