The AP-3 β adaptin mediates the biogenesis and function of lytic vacuoles in Arabidopsis

Plant Cell

Volumn 22, Issue 8, 2010, Pages 2812-2824

  Feraru, Elena ^a,b,c   Paciorek, Tomasz ^c   Feraru, Mugurel I ^a,b,c   Zwiewka, Marta ^a,b   de Groodt, Ruth ^a,b   de Rycke, Rie ^b   Kleine Vehn, Jürgen ^a,b,c   Friml, Jiří ^a,b  

^a DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^b GHENT UNIVERSITY   (Belgium)

^c UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; EUKARYOTA;

EID: 77957818090     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.110.075424     Document Type: Article

References (50)

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.
2. Alberti, S., Gitler, A.D., and Lindquist, S. (2007). A suite of Gateway cloning vectors for high-throughput genetic analysis in Saccharomyces cerevisiae. Yeast 24: 913-919.
3. Bassham, D.C., Brandizzi, F., Otegui, M., and Sanderfoot, A.A. (2008). The secretory system of Arabidopsis. The Arabidopsis Book, C.R. Somerville and E.M. Meyerowitz, eds (Rockville, MD: American Society of Plant Biologists), doi/10.1199/tab.0116, http://www.aspb.org/publications/arabidopsis/.
4. 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.
5. Blilou, I., Xu, J., Wildwater, M., Willemsen, V., Paponov, I., Friml, J., Heidstra, R., Aida, M., Palme, K., and Scheres, B. (2005). The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433: 39-44.
6. Boehm, M., and Bonifacino, J.S. (2002). Genetic analyses of adaptin function from yeast to mammals. Gene 286: 175-186.
7. Cowles, C.R., Odorizzi, G., Payne, G.S., and Emr, S.D. (1997). The AP-3 adaptor complex is essential for cargo-selective transport to the yeast vacuole. Cell 91: 109-118.
8. Cutler, S.R., Ehrhardt, D.W., Griffitts, J.S., and Somerville, C.R. (2000). Random GFP, cDNA fusions enable visualization of subcellular structures in cells of Arabidopsis at a high frequency. Proc. Natl. Acad. Sci. USA 97: 3718-3723.
9. De Clercq, A., Vandewiele, M., De Ryke, R., Van Damme, J., Van Montagu, M., Krebbers, E., and Vandekerckhove, J. (1990). Expression and processing of an Arabidopsis 2S albumin in transgenic tobacco. Plant Physiol. 92: 899-907.
10. Dell'Angelica, E.C. (2009). AP-3 dependent trafficking and disease: The first decade. Curr. Opin. Cell Biol. 21: 552-559.
11. Dell'Angelica, E.C., Shotelersuk, V., Aquilar, R.C., Gahl, W.A., and Bonifacino, J.S. (1999). Altered trafficking of lysosomal proteins in Hermansky-Pudlak Syndrome due to mutations in the b3A subunit of the AP-3 adaptor. Mol. Cell 3: 11-21.
12. 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.
13. Dhonukshe, P., Aniento, F., Hwang, I., Robinson, D.G., Mravec, J., Stierhof, Y.-D., and Friml, J. (2007). Clathrin-mediated constitutive endocytosis of PIN auxin efflux carriers in Arabidopsis. Curr. Biol. 17: 520-527.
14. Dhonukshe, P., et al. (2008). Generation of cell polarity in plants links endocytosis, auxin distribution and cell fate decisions. Nature 456: 962-966.
15. di Sansebastiano, G.P., Paris, N., Marc-Martin, S., and Neuhaus, J.M. (2001). Regeneration of a lytic central vacuole and of neutral peripheral vacuoles can be visualized by green fluorescent proteins targeted to either type of vacuoles. Plant Physiol. 126: 78-86.
16. 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). SNARE complex unique to seed plants is required for protein storage vacuole biogenesis and seed development of Arabidopsis thaliana. Plant Cell 20: 3006-3021.
17. Feng, L., Seymour, A.B., Jiang, S., To, A., Peden, A.A., Novak, E.K., Zhen, L., Rusiniak, M.E., Eicher, E.M., Robinson, M.S., Gorin, M.B., and Swank, R.T. (1999). The beta3A subunit gene (Ap3b1) of the AP-3 adaptor complex is altered in the mouse hypopigmentation mutant pearl, a model for Hermansky-Pudlak syndrome and night blindness. Hum. Mol. Genet. 8: 323-330.
18. Frigerio, L., Hinz, G., and Robinson, D.G. (2008). Multiple vacuoles in plant cells: Rule or exception? Traffic 9: 1564-1570.
19. 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.
20. Geldner, N., Friml, J., Stierhof, Y.-D., Jürgens, G., and Palme, K. (2001). Auxin transport inhibitors block PIN1 cycling and vesicle trafficking. Nature 413: 425-428.
21. Grebe, M., Xu, J., Möbius, W., Ueda, T., Nakano, A., Geuze, H.J., Rook, M.B., and Scheres, B. (2003). Arabidopsis sterol endocytosis involves actin-mediated trafficking via ARA6-positive early endosomes. Curr. Biol. 13: 1378-1387.
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 LYST-INTERACTING PROTEIN5. Plant Cell 19: 1295-1312.
23. Jaillais, Y., Fobis-Loisy, I., Miège, C., Rollin, C., and Gaude, T. (2006). AtSNX1 defines an endosome for auxin-carrier trafficking in Arabidopsis. Nature 443: 106-109.
24. Karimi, M., Inzé, D., and Depicker, A. (2002). GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 7: 193-195.
25. Kato, T., Morita, M.T., Fukaki, H., Yamauchi, Y., Uehara, M., Niihama, M., and Tasaka, M. (2002). SGR2, a phospholipase-like protein, and ZIG/SGR4, a SNARE, are involved in the shoot gravitropism of Arabidopsis. Plant Cell 14: 33-46.
26. Kleine-Vehn, J., Dhonukshe, P., Sauer, M., Brewer, P.B., Wiśniewska, J., Paciorek, T., Benková, E., and Friml, J. (2008a). ARF GEFdependent transcytosis and polar delivery of PIN auxin carriers in Arabidopsis. Curr. Biol. 18: 526-531.
27. Kleine-Vehn, J., Leitner, J., Zwiewka, M., Sauer, M., Abas, L., Luschnig, C., and Friml, J. (2008b). Differential degradation of PIN2 auxin efflux carrier by retromer-dependent vacuolar targeting. Proc. Natl. Acad. Sci. USA 105: 17812-17817.
28. Kretzschmar, D., Poeck, B., Roth, H., Ernst, R., Keller, A., Porsch, M., Strauss, R., and Pflugfelder, G.O. (2000). Defective pigment granule biogenesis and aberrant behavior cuased by mutations in the Drosophila AP-3b adaptin gene ruby. Genetics 155: 213-223.
29. Laxmi, A., Pan, J., Morsy, M., and Chen, R. (2008). Light plays an essential role in intracellular distribution of auxin efflux carrier PIN2 in Arabidopsis thaliana. PLOS One 3: e1510.
30. 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.
31. Marty, F. (1999). Plant vacuoles. Plant Cell 11: 587-599.
32. Niihama, M., Takemoto, N., Hashiguchi, Y., Tasaka, M., and Morita, M.T. (2009). ZIP genes encode proteins involved in membrane trafficking of the TGN-PVC/vacuoles. Plant Cell Physiol. 50: 2057-2068.
33. Petrásek, J., et al. (2006). PIN proteins perform a rate-limiting function in cellular auxin efflux. Science 312: 914-918.
34. Robert, S., Chary, S.N., Drakakaki, D., 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.
35. Robinson, D.G., Jiang, L., and Schumacher, K. (2008). The endosomal system of plants: Charting new and familiar territories. Plant Physiol. 147: 1482-1492.
36. 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.
37. Sanmartín, M., Ordonez, A., Sohn, E.J., Robert, S., Sanchez-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.
38. 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.
39. Silady, R.A., Ehrhardt, D.W., Jackson, K., Faulkner, C., Oparka, K., and Somerville, C.R. (2008). The GRV2/RME-8 protein of Aabidopsis functions in the late endocytic pathway and is required for vacuolar membrane flow. Plant J. 53: 29-41.
40. Sohn, E.J., Rojas-Pierce, M., Pan, S., Carter, C., Serrano-Mislata, A., Madueno, 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.
41. Stepp, J.D., Huang, K., and Lemmon, S.K. (1997). The yeast adaptor protein complex, AP-3, is essential for the efficient delivery of alkaline phosphatase by the alternate pathway to the vacuole. J. Cell Biol. 139: 1761-1774.
42. 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.
43. Swanson, S.J., and Jones, R.L. (1996). Gibberellic acid lnduces vacuolar acidification in barley aleurone. Plant Cell 8: 2211-2221.
44. Tamura, K., Shimada, T., Ono, E., Tanaka, Y., Nagatani, A., Higashi, S.I., Watanabe, M., Nishimura, M., and Hara-Nishimura, I. (2003). Why green fluorescent fusion proteins have not been observed in the vacuoles of higher plants. Plant J. 35: 545-555.
45. 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.
46. 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.
47. 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.
48. Wiśniewska, J., Xu, J., Seifertova, D., Brewer, P.B., Ruzicka, K., Blilou, I., Rouquie, D., Benkova, E., Scheres, B., and Friml, J. (2006). Polar PIN localization directs auxin flow in plants. Science 312: 883.
49. Xu, J., and Scheres, B. (2005). Dissection of Arabidopsis ADP-RIBOSYLATION FACTOR 1 function in epidermal cell polarity. Plant Cell 17: 525-536.
50. 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.