BEX5/RabA1b regulates trans-Golgi network-to-plasma membrane protein trafficking in Arabidopsis

Plant Cell

Volumn 24, Issue 7, 2012, Pages 3074-3086

  Feraru, Elena ^a,d   Feraru, Mugurel I ^a,d   Asaoka, Rin ^b   Paciorek, Tomasz ^a,e   De Rycke, Riet ^a   Tanaka, Hirokazu ^a,f   Nakano, Akihiko ^b,c   Frimla, Jir̂í ^a  

^a GHENT UNIVERSITY   (Belgium)

^b UNIVERSITY OF TOKYO   (Japan)

^c RIKEN   (Japan)

^d UNIVERSITY OF NATURAL RESOURCES AND LIFE SCIENCES   (Austria)

^e STANFORD UNIVERSITY   (United States)

^f OSAKA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84865331816     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.112.098152     Document Type: Article

References (71)

1. Alonso, J.M., et al. (2003). Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653-657.
2. Anders, N., and Jürgens, G. (2008). Large ARF guanine nucleotide exchange factors in membrane trafficking. Cell. Mol. Life Sci. 65: 3433-3445.
3. Bassham, D.C., Brandizzi, F., Otegui, M.S., and Sanderfoot, A.A. (2008). The secretory system of Arabidopsis. In The Arabidopsis Book, C.R. Somerville and E.M. Meyerowitz, eds (Rockville, MD: American Society of Plant Biologists), doi/10.1199/tab.0099, http://www.aspb.org/publications/arabidopsis/.
4. Benková, E., Michniewicz, M., Sauer, M., Teichmann, T., Seifertová, D., Jürgens, G., and Friml, J. (2003). Local, effluxdependent auxin gradients as a common module for plant organ formation. Cell 115: 591-602.
5. Chen, S.H., Chen, S., Tokarev, A.A., Liu, F., Jedd, G., and Segev, N. (2005). Ypt31/32 GTPases and their novel F-box effector protein Rcy1 regulate protein recycling. Mol. Biol. Cell 16: 178-192.
6. 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.
7. 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.
8. de Graaf, B.H.J., Cheung, A.Y., Andreyeva, T., Levasseur, K., Kieliszewski, M., and Wu, H.M. (2005). Rab11 GTPase-regulated membrane trafficking is crucial for tip-focused pollen tube growth in tobacco. Plant Cell 17: 2564-2579.
9. 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.
10. 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.
11. Ding, Z., Galván-Ampudia, C.S., Demarsy, E., Langowski, L., Kleine-Vehn, J., Fan, Y., Morita, M.T., Tasaka, M., Fankhauser, C., Offringa, R., and Friml, J. (2011). Light-mediated polarization of the PIN3 auxin transporter for the phototropic response in Arabidopsis. Nat. Cell Biol. 13: 447-452.
12. Feraru, E., Paciorek, T., Feraru, M.I., Zwiewka, M., De Groodt, R., De Rycke, R., Kleine-Vehn, J., and Friml, J. (2010). The AP-3b adaptin mediates the biogenesis and function of lytic vacuoles in Arabidopsis. Plant Cell 22: 2812-2824.
13. Friml, J., Vieten, A., Sauer, M., Weijers, D., Schwarz, H., Hamann, T., Offringa, R., and Jürgens, G. (2003). Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 426: 147-153.
14. Friml, J., Wisniewska, J., Benková, E., Mendgen, K., and Palme, K. (2002). Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature 415: 806-809.
15. 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.
16. 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.
17. 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.
18. 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.
19. Green, E.G., Ramm, E., Riley, N.M., Spiro, D.J., Goldenring, J.R., and Wessling-Resnick, M. (1997). Rab11 is associated with transferrin-containing recycling compartments in K562 cells. Biochem. Biophys. Res. Commun. 239: 612-616.
20. 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.
21. Heisler, M.G., Ohno, C., Das, P., Sieber, P., Reddy, G.V., Long, J.A., and Meyerowitz, E.M. (2005). Patterns of auxin transport and gene expression during primordium development revealed by live imaging of the Arabidopsis inflorescence meristem. Curr. Biol. 15: 1899-1911
22. Heo, J.B., Rho, H.S., Kim, S.W., Hwang, S.M., Kwon, H.J., Nahm, M.Y., Bang, W.Y., and Bahk, J.D. (2005). OsGAP1 functions as a positive regulator of OsRab11-mediated TGN to PM or vacuole trafficking. Plant Cell Physiol. 46: 2005-2018.
23. Inaba, T., Nagano, Y., Nagasaki, T., and Sasaki, Y. (2002). Distinct localization of two closely related Ypt3/Rab11 proteins on the trafficking pathway in higher plants. J. Biol. Chem. 277: 9183-9188.
24. Irani, N.G., and Russinova, E. (2009). Receptor endocytosis and signaling in plants. Curr. Opin. Plant Biol. 12: 653-659.
25. Jedd, G., Mulholland, J., and Segev, N. (1997). Two new Ypt GTPases are required for exit from the yeast trans-Golgi compartment. J. Cell Biol. 137: 563-580.
26. Jelínková, A., Malínská, K., Simon, S., Kleine-Vehn, J., Parezová, M., Pejchar, P., Kubeš, M., Martinec, J., Friml, J., Zazímalová, E., and Petrásek, J. (2010). Probing plant membranes with FM dyes: Tracking, dragging or blocking? Plant J. 61: 883-892.
27. 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.
28. Karimi, M., Inzé, D., and Depicker, A. (2002). GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 7: 193-195.
29. Kleine-Vehn, J., Dhonukshe, P., Sauer, M., Brewer, P.B., Wisniewska, 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.
30. Kleine-Vehn, J., Ding, Z., Jones, A.R., Tasaka, M., Morita, M.T., and Friml, J. (2010). Gravity-induced PIN transcytosis for polarization of auxin fluxes in gravity-sensing root cells. Proc. Natl. Acad. Sci. USA 107: 22344-22349.
31. Kleine-Vehn, J., and Friml, J. (2008). Polar targeting and endocytic recycling in auxin-dependent plant development. Annu. Rev. Cell Dev. Biol. 24: 447-473.
32. 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.
33. Matheson, L.A., Hanton, S.L., and Brandizzi, F. (2006). Traffic between the plant endoplasmic reticulum and Golgi apparatus: To the Golgi and beyond. Curr. Opin. Plant Biol. 9: 601-609.
34. Movafeghi, A., Happel, N., Pimpl, P., Tai, G.-H., and Robinson, D.G. (1999). Arabidopsis Sec21p and Sec23p homologs. Probable coat proteins of plant COP-coated vesicles. Plant Physiol. 119: 1437-1446.
35. Murphy, A.S., Bandyopadhyay, A., Holstein, S.E., and Peer, W.A. (2005). Endocytotic cycling of PM proteins. Annu. Rev. Plant Biol. 56: 221-251.
36. Nielsen, E., Cheung, A.Y., and Ueda, T. (2008). The regulatory RAB and ARF GTPases for vesicular trafficking. Plant Physiol. 147: 1516-1526.
37. Nomura, K., Debroy, S., Lee, Y.H., Pumplin, N., Jones, J., and He, S.Y. (2006). A bacterial virulence protein suppresses host innate immunity to cause plant disease. Science 313: 220-223.
38. Paciorek, T., Zazímalová, E., Ruthardt, N., Petrásek, J., Stierhof, Y.-D., Kleine-Vehn, J., Morris, D.A., Emans, N., Jürgens, G., Geldner, N., and Friml, J. (2005). Auxin inhibits endocytosis and promotes its own efflux from cells. Nature 435: 1251-1256.
39. Paul, M.J., and Frigerio, L. (2007). Coated vesicles in plant cells. Semin. Cell Dev. Biol. 18: 471-478.
40. Pereira-Leal, J.B., and Seabra, M.C. (2000). The mammalian Rab family of small GTPases: Definition of family and subfamily sequence motifs suggests a mechanism for functional specificity in the Ras superfamily. J. Mol. Biol. 301: 1077-1087.
41. Petrásek, J., et al. (2006). PIN proteins perform a rate-limiting function in cellular auxin efflux. Science 312: 914-918.
42. 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.
43. Prekeris, R., Klumperman, J., and Scheller, R.H. (2000). A Rab11/ Rip11 protein complex regulates apical membrane trafficking via recycling endosomes. Mol. Cell 6: 1437-1448.
44. Preuss, M.L., Serna, J., Falbel, T.G., Bednarek, S.Y., and Nielsen, E. (2004). The Arabidopsis Rab GTPase RabA4b localizes to the tips of growing root hair cells. Plant Cell 16: 1589-1603.
45. Rakusová, H., Gallego-Bartolomé, J., Vanstraelen, M., Robert, H.S., Alabadí, D., Blázquez, M.A., Benková, E., and Friml, J. (2011). Polarization of PIN3-dependent auxin transport for hypocotyl gravitropic response in Arabidopsis thaliana. Plant J. 67: 817-826.
46. Rehman, R.U., Stigliano, E., Lycett, G.W., Sticher, L., Sbano, F., Faraco, M., Dalessandro, G., and Di Sansebastiano, G.-P. (2008). Tomato Rab11a characterization evidenced a difference between SYP121-dependent and SYP122-dependent exocytosis. Plant Cell Physiol. 49: 751-766.
47. Reinhardt, D., Pesce, E.-R., Stieger, P., Mandel, T., Baltensperger, K., Bennett, M., Traas, J., Friml, J., and Kuhlemeier, C. (2003). Regulation of phyllotaxis by polar auxin transport. Nature 426: 255-260.
48. Ren, M., Xu, G., Zeng, J., De Lemos-Chiarandini, C., Adesnik, M., and Sabatini, D.D. (1998). Hydrolysis of GTP on rab11 is required for the direct delivery of transferrin from the pericentriolar recycling compartment to the cell surface but not from sorting endosomes. Proc. Natl. Acad. Sci. USA 95: 6187-6192.
49. Richter, S., Geldner, N., Schrader, J., Wolters, H., Stierhof, Y.-D., Rios, G., Koncz, C., Robinson, D.G., and Jürgens, G. (2007). Functional diversification of closely related ARF-GEFs in protein secretion and recycling. Nature 448: 488-492.
50. Robert, S., et al. (2010). ABP1 mediates auxin inhibition of clathrindependent endocytosis in Arabidopsis. Cell 143: 111-121.
51. Robinson, D.G., Jiang, L., and Schumacher, K. (2008). The endosomal system of plants: Charting new and familiar territories. Plant Physiol. 147: 1482-1492.
52. Rutherford, S., and Moore, I. (2002). The Arabidopsis Rab GTPase family: Another enigma variation. Curr. Opin. Plant Biol. 5: 518-528.
53. Sanderfoot, A.A., Kovaleva, V., Bassham, D.C., and Raikhel, N.V. (2001). Interactions between syntaxins identify at least five SNARE complexes within the Golgi/prevacuolar system of the Arabidopsis cell. Mol. Biol. Cell 12: 3733-3743.
54. Sauer, M., Paciorek, T., Benková, E., and Friml, J. (2006). Immunocytochemical techniques for whole-mount in situ protein localization in plants. Nat. Protoc. 1: 98-103.
55. 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.
56. 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.
57. 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.
58. Tian, G.W. et al. (2004). High-throughput fluorescent tagging of full-length Arabidopsis gene products in planta. Plant Physiol. 135: 25-38.
59. 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.
60. Ueda, T., Anai, T., Tsukaya, H., Hirata, A., and Uchimiya, H. (1996). Characterization and subcellular localization of a small GTP-binding protein (Ara-4) from Arabidopsis: Conditional expression under control of the promoter of the gene for heat-shock protein HSP81-1. Mol. Gen. Genet. 250: 533-539.
61. Ueda, T., Uemura, T., Sato, M.H., and Nakano, A. (2004). Functional differentiation of endosomes in Arabidopsis cells. Plant J. 40: 783-789.
62. Ullrich, O., Reinsch, S., Urbé, S., Zerial, M., and Parton, R.G. (1996). Rab11 regulates recycling through the pericentriolar recycling endosome. J. Cell Biol. 135: 913-924.
63. 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.
64. 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.
65. Vitale, A., and Denecke, J. (1999). The endoplasmic reticulum: Gateway of the secretory pathway. Plant Cell 11: 615-628.
66. Vitale, A., and Galili, G. (2001). The endomembrane system and the problem of protein sorting. Plant Physiol. 125: 115-118.
67. von der Fecht-Bartenbach, J., Bogner, M., Krebs, M., Stierhof, Y.-D., Schumacher, K., and Ludewig, U. (2007). Function of the anion transporter AtCLC-d in the trans-Golgi network. Plant J. 50: 466-474.
68. Woollard, A.A.D., and Moore, I. (2008). The functions of Rab GTPases in plant membrane traffic. Curr. Opin. Plant Biol. 11: 610-619.
69. Xu, J., and Scheres, B. (2005). Dissection of Arabidopsis ADPRIBOSYLATION FACTOR 1 function in epidermal cell polarity. Plant Cell 17: 525-536.
70. Zerial, M., and McBride, H. (2001). Rab proteins as membrane organizers. Nat. Rev. Mol. Cell Biol. 2: 107-117.
71. Zwiewka, M., Feraru, E., Möller, B., Hwang, I., Feraru, M.I., Kleine-Vehn, J., Weijers, D., and Friml, J. (2011). The AP-3 adaptor complex is required for vacuolar function in Arabidopsis. Cell Res. 21: 1711-1722.