VPS9a, the common activator for two distinct types of Rab5 GTPases, is essential for the development of Arabidopsis thaliana

Plant Cell

Volumn 19, Issue 11, 2007, Pages 3504-3515

  Goh, Tatsuaki ^a,b   Uchida, Wakana ^b   Arakawa, Satoko ^b,c   Ito, Emi ^a   Dainobu, Tomoko ^a   Ebine, Kazuo ^a   Takeuchi, Masaki ^b,d   Sato, Ken ^a,b   Ueda, Takashi ^a   Nakano, Akihiko ^a,b  

^a UNIVERSITY OF TOKYO   (Japan)

^b Japan Science and Technology Agency   (Japan)

^c TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^d INSTITUTE FOR MOLECULAR SCIENCE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ENZYME ACTIVITY; GENE EXPRESSION; MOLECULAR BIOLOGY; MUTAGENESIS;

EMBRYOGENESIS; ENDOSOMAL FUNCTIONS; GTPASES; MOLECULAR SWITCH;

PLANT CELL CULTURE;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 37849024683     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.107.053876     Document Type: Article

References (57)

1. Aida, M., Ishida, T., Fukaki, H., Fujisawa, H., and Tasaka, M. (1997). Genes involved in organ separation in Arabidopsis: An analysis of the cup-shaped cotyledon mutant. Plant Cell 9: 841-857.
2. Alonso, J.M., et al. (2003). Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653-657.
3. An, Q., Ehlers, K., Kogel, K.H., van Bel, A.J., and Huckelhoven, R. (2006a). Multivesicular compartments proliferate in susceptible and resistant MLA12-barley leaves in response to infection by the biotrophic powdery mildew fungus. New Phytol. 172: 563-576.
4. An, Q., Huckelhoven, R., Kogel, K.H., and van Bel, A.J. (2006b). Multivesicular bodies participate in a cell wall-associated defence response in barley leaves attacked by the pathogenic powdery mildew fungus. Cell. Microbiol. 8: 1009-1019.
5. Anai, T., Matsui, M., Nomura, N., Ishizaki, R., and Uchimiya, H. (1994). In vitro mutation analysis of Arabidopsis thaliana small GTP-binding proteins and detection of GAP-like activities in plant cells. FEBS Lett. 346: 175-180.
6. 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.
7. Baluska, F., Liners, F., Hlavacka, A., Schlicht, M., Van Cutsem, P., McCurdy, D.W., and 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.
8. Barbieri, M.A., Kong, C., Chen, P.I., Horazdovsky, B.F., and Stahl, P.D. (2003). The SRC homology 2 domain of Rin1 mediates its binding to the epidermal growth factor receptor and regulates receptor endocytosis. J. Biol. Chem. 278: 32027-32036.
9. 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.
10. Bolte, S., Brown, S., and Satiat-Jeunemaitre, B. (2004). The N-myristoylated Rab-GTPase m-Rabmc is involved in post-Golgi trafficking events to the lytic vacuole in plant cells. J. Cell Sci. 117: 943-954.
11. Broek, D., Toda, T., Michaeli, T., Levin, L., Birchmeier, C., Zoller, M., Powers, S., and Wigler, M. (1987). The S. cerevisiae CDC25 gene product regulates the RAS/adenylate cyclase pathway. Cell 48: 789-799.
12. Burd, C.G., Mustol, P.A., Schu, P.V., and Emr, S.D. (1996). A yeast protein related to a mammalian Ras-binding protein, Vps9p, is required for localization of vacuolar proteins. Mol. Cell. Biol. 16: 2369-2377.
13. Carney, D.S., Davies, B.A., and Horazdovsky, B.F. (2005). Vps9 domain-containing proteins: Activators of Rab5 GTPases from yeast to neurons. Trends Cell Biol. 16: 27-35.
14. Christoforidis, S., and Zerial, M. (2000). Purification and identification of novel Rab effectors using affinity chromatography. Methods 20: 403-410.
15. Clough, S.J., and Bent, A.F. (1998). Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16: 735-743.
16. Cox, G.C., and Juniper, B.E. (1973). Autoradiographic evidence for paramural-body function. Nat. New Biol. 243: 116-117.
17. Delprato, A., Merithew, E., and Lambright, D.G. (2004). Structure, exchange determinants, and family-wide Rab specificity of the tandem helical bundle and Vps9 domains of Rabex-5. Cell 118: 607-617.
18. Dhonukshe, P., Baluska, F., Schlicht, M., Hlavacka, A., Samaj, J., Friml, J., and Gadella, T. W., Jr. (2006). Endocytosis of cell surface material mediates cell plate formation during plant cytokinesis. Dev. Cell 10: 137-150.
19. Friml, J., Vieten, A., Sauer, M., Weijers, D., Schwarz, H., Hamann, T., Offringa, R., and Jurgens, G. (2003). Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 426: 147-153.
20. Geldner, N., Anders, N., Wolters, H., Keicher, J., Kornberger, W., Muller, P., Delbarre, A., Ueda, T., Nakano, A., and Jurgens, G. (2003). The Arabidopsis GNOM ARF-GEF mediates endosomal recycling, auxin transport, and auxin-dependent plant growth. Cell 112: 219-230.
21. Grosshans, B.L., Ortiz, D., and Novick, P. (2006). Rabs and their effectors: Achieving specificity in membrane traffic. Proc. Natl. Acad. Sci. USA 103: 11821-11827.
22. Haas, T.J., Sliwinski, M.K., Martinez, D.E., Preuss, M., Ebine, K., Ueda, T., Nielsen, E., Odorizzi, G., and Otegui, M.S. (2007). The Arabidopsis AAA ATPase SKD1 is involved in multivesicular endosome function and interacts with its positive regulator LIP5. Plant Cell 19: 1295-1312.
23. Hama, H., Tall, G.G., and Horazdovsky, B.F. (1999). Vps9p is a guanine nucleotide exchange factor involved in vesicle-mediated vacuolar protein transport. J. Biol. Chem. 274: 15284-15291.
24. Herman, E.M., and Lamb, C.J. (1992). Arabinogalactan-rich glycoproteins are localized on the cell surface and in intravacuolar multivesicular bodies. Plant Physiol. 98: 264-272.
25. Horiuchi, H., Lippe, R., McBride, H.M., Rubino, M., Woodman, P., Stenmark, H., Rybin, V., Wilm, M., Ashman, K., Mann, M., and Zerial, M. (1997). A novel Rab5 GDP/GTP exchange factor complexed to Rabaptin-5 links nucleotide exchange to effector recruitment and function. Cell 90: 1149-1159.
26. Ichikawa, M., and Ichikawa, A. (1987). The fine structure of sublingual gland acinar cells of the Mongolian gerbil, Meriones unguiculatus, processed by rapid freezing followed by freeze-substitution fixation. Cell Tissue Res. 250: 305-314.
27. Karnovsky, M. (1965). A formaldehyde-glutaraldehyde fixative of high osmolality for use in electron microscopy. J. Cell Biol. 27: 137A-138A.
28. Kotzer, A.M., Brandizzi, F., Neumann, U., Paris, N., Moore, I., and Hawes, C. (2004). AtRabF2b (Ara7) acts on the vacuolar trafficking pathway in tobacco leaf epidermal cells. J. Cell Sci. 117: 6377-6389.
29. Lee, G.J., Sohn, E.J., Lee, M.H., and Hwang, I. (2004). The Arabidopsis Rab5 homologs Rha1 and Ara7 localize to the prevacuolar compartment. Plant Cell Physiol. 45: 1211-1220.
30. Marchant, R., and Robards, A.W. (1968). Membrane systems associated with the plasmalemma of plant cells. Ann. Bot. (Lond.) 32: 457-471.
31. Nair, J., Muller, H., Peterson, M., and Novick, P. (1990). Sec2 protein contains a coiled-coil domain essential for vesicular transport and a dispensable carboxy terminal domain. J. Cell Biol. 110: 1897-1909.
32. Nakano, A., and Muramatsu, M. (1989). A novel GTP-binding protein, Sar1p, is involved in transport from the endoplasmic reticulum to the Golgi apparatus. J. Cell Biol. 109: 2677-2691.
33. Otegui, M., and Staehelin, L.A. (2000). Syncytial-type cell plates: A novel kind of cell plate involved in endosperm cellularization of Arabidopsis. Plant Cell 12: 933-947.
34. Pan, J.Y., Sanford, J.C., and Wessling-Resnick, M. (1995). Effect of guanine nucleotide binding on the intrinsic tryptophan fluorescence properties of Rab5. J. Biol. Chem. 270: 24204-24208.
35. Reynolds, E.S. (1963). The use of lead citrate at high pH as an electronopaque stain in electron microscopy. J. Cell Biol. 17: 208-212.
36. Robatzek, S., Chinchilla, D., and Boller, T. (2006). Ligand-induced endocytosis of the pattern recognition receptor FLS2 in Arabidopsis. Genes Dev. 20: 537-542.
37. Rojo, E., Gillmor, C.S., Kovaleva, V., Somerville, C.R., and Raikhel, N.V. (2001). VACUOLELESS1 is an essential gene required for vacuole formation and morphogenesis in Arabidopsis. Dev. Cell 1: 303-310.
38. Rosso, M.G., Li, Y., Strizhov, N., Reiss, B., Dekker, K., and Weisshaar, B. (2003). An Arabidopsis thaliana T-DNA mutagenized population (GABI-Kat) for flanking sequence tag-based reverse genetics. Plant Mol. Biol. 53: 247-259.
39. Russinova, E., Borst, J.W., Kwaaitaal, M., Caño-Delgado, A., Yin, Y., Chory, J., and de Vries, S.C. (2004). Heterodimerization and endocytosis of Arabidopsis brassinosteroid receptors BRI1 and AtSERK3 (BAK1). Plant Cell 16: 3216-3229.
40. Rutherford, S., and Moore, I. (2002). The Arabidopsis Rab GTPase family: Another enigma variation. Curr. Opin. Plant Biol. 5: 518-528.
41. Sato, M., Sato, K., Fonarev, P., Huang, C., Liou, W., and Grant, B. (2005). Caenorhabditis elegans RME-6 is a novel regulator of RAB-5 at the clathrin-coated pit. Nat. Cell Biol. 7: 559-569.
42. Schmid, M., Davison, T.S., Henz, S.R., Pape, U.J., Demar, M., Vingron, M., Scholkopf, B., Weigel, D., and Lohmann, J.U. (2005). A gene expression map of Arabidopsis thaliana development. Nat. Genet. 37: 501-506.
43. Seabra, M.C., and Wasmeier, C. (2004). Controlling the location and activation of Rab GTPases. Curr. Opin. Cell Biol. 16: 451-457.
44. Shimada, T., Koumoto, Y., Li, L., Yamazaki, M., Kondo, M., Nishimura, M., and Hara-Nishimura, I. (2006). AtVPS29, a putative component of a retromer complex, is required for the efficient sorting of seed storage proteins. Plant Cell Physiol. 47: 1187-1194.
45. Siniossoglou, S., Peak-Chew, S.Y., and Pelham, H.R. (2000). Ric1p and Rgp1p form a complex that catalyses nucleotide exchange on Ypt6p. EMBO J. 19: 4885-4894.
46. Sohn, E.J., Kim, E.S., Zhao, M., Kim, S.J., Kim, H., Kim, Y.W., Lee, Y.J., Hillmer, S., Sohn, U., Jiang, L., and Hwang, I. (2003). Rha1, an Arabidopsis Rab5 homolog, plays a critical role in the vacuolar trafficking of soluble cargo proteins. Plant Cell 15: 1057-1070.
47. Steinmann, T., Geldner, N., Grebe, M., Mangold, S., Jackson, C.L., Paris, S., Galweiler, L., Palme, K., and Jurgens, G. (1999). Coordinated polar localization of auxin efflux carrier PIN1 by GNOM ARF GEF. Science 286: 316-318.
48. Takano, J., Miwa, K., Yuan, L., von Wiren, N., and Fujiwara, T. (2005). Endocytosis and degradation of BOR1, a boron transporter of Arabidopsis thaliana, regulated by boron availability. Proc. Natl. Acad. Sci. USA 102: 12276-12281.
49. Tall, G.G., Barbieri, M.A., Stahl, P.D., and Horazdovsky, B.F. (2001). Ras-activated endocytosis is mediated by the Rab5 guanine nucleotide exchange activity of RIN1. Dev. Cell 1: 73-82.
50. Tian, G.W., et al. (2004). High-throughput fluorescent tagging of full-length Arabidopsis gene products in planta. Plant Physiol. 135: 25-38.
51. Ueda, T., and Nakano, A. (2002). Vesicular traffic: An integral part of plant life. Curr. Opin. Plant Biol. 5: 513-517.
52. Ueda, T., Uemura, T., Sato, M.H., and Nakano, A. (2004). Functional differentiation of endosomes in Arabidopsis cells. Plant J. 40: 783-789.
53. Ueda, T., Yamaguchi, M., Uchimiya, H., and Nakano, A. (2001). Ara6, a plant-unique novel type Rab GTPase, functions in the endocytic pathway of Arabidopsis thaliana. EMBO J. 20: 4730-4741.
54. 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.
55. Wang, Q., Kong, L., Hao, H., Wang, X., Lin, J., Samaj, J., and Baluska, F. (2005). Effects of brefeldin A on pollen germination and tube growth. Antagonistic effects on endocytosis and secretion. Plant Physiol. 139: 1692-1703.
56. Zerial, M., and McBride, H. (2001). Rab proteins as membrane organizers. Nat. Rev. Mol. Cell Biol. 2: 107-117.
57. Ziman, M., and Johnson, D.I. (1994). Genetic evidence for a functional interaction between Saccharomyces cerevisiae CDC24 and CDC42. Yeast 10: 463-474.