Subcellular trafficking of the Arabidopsis auxin influx carrier AUX1 uses a novel pathway distinct from PIN1

Plant Cell

Volumn 18, Issue 11, 2006, Pages 3171-3181

  Kleine Vehn, Jürgen ^a   Dhonukshe, Pankaj ^a   Swarup, Ranjan ^b   Bennett, Malcolm ^b   Friml, Jiří ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MEMBRANES; GROWTH KINETICS; PLANTS (BOTANY);

AUXIN FLOW; PLANT HORMONES; SUBCELLULAR TRAFFICKING;

PLANT CELL CULTURE;

CELLS; GROWTH; HORMONES; PLANTS;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 33845784713     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.106.042770     Document Type: Article

References (51)

1. Benjamins, R., Malenica, N., and Luschnig, C. (2005). Regulating the regulator: The control of auxin transport. Bioessays 27, 1246-1255.
2. Benková, E., Michniewicz, M., Sauer, M., Teichmann, T., Seifertova, D., Jurgens, G., and Friml, J. (2003). Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115, 591-602.
3. Bennett, M.J., Marchant, A., Green, H.G., May, S.T., Ward, S.P., Millner, P.A., Walker, A.R., Schulz, B., and Feldmann, K.A. (1996). Arabidopsis AUX1 gene: A permease-like regulator of root gravitropism. Science 273, 948-950.
4. 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.
5. Dharmasiri, S., Swarup, R., Mockaitis, K., Dharmasiri, M., Singh, S.K., Kowalchyk, M., Marchant, A., Mills, S., Sandberg, G., Bennett, M.J., and Estelle, M. (2006). AXR4 is required for localization of the auxin influx facilitator AUX1. Science 312, 1218-1220.
6. 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.
7. Friml, J., Benkova, E., Blilou, I., Wiśniewska, J., Hamann, T., Ljung, K., Woody, S., Sandberg, G., Scheres, B., Jurgens, G., and Palme, K. (2002b). AtPIN4 mediates sink-driven auxin gradients and root patterning in Arabidopsis. Cell 108, 661-673.
8. 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.
9. Friml, J., Wisniewska, J. Benková, E., Mendgen, K., and Palme, K. (2002a). Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature 415, 806-809.
10. Gälweiler, L., Guan, C., Muller, A., Wisman, E., Mendgen, K., Yephremov, A., and Palme, K. (1998). Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 282, 2226-2230.
11. 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.
12. Geldner, N., Friml, J., Stierhof, Y.D., Jurgens, G., and Palme, K. (2001). Auxin transport inhibitors block PIN1 cycling and vesicle trafficking. Nature 413, 425-428.
13. Grebe, M., Friml, J., Swarup, R., Ljung, K., Sandberg, G., Terlou, M., Palme, K., Bennett, M.J., and Scheres, B. (2002). Cell polarity signaling in Arabidopsis involves a BFA-sensitive auxin influx pathway. Curr. Biol. 12, 329-334.
14. Grebe, M., Xu, J., Mobius, 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.
15. Hugdahl, J.D., and Morejohn, L.C. (1993). Rapid and reversible high-affinity binding of the dinitroaniline herbicide oryzalin to tubulin from Zea mays L. Plant Physiol. 102, 725-740.
16. Keller, P., and Simons, K. (1998). Cholesterol is required for surface transport of influenza virus hemagglutinin. J. Cell Biol. 140, 1357-1367.
17. 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.
18. Marchant, A., Kargul, J., May, S.T., Muller, P., Delbarre, A., Perrot-Rechenmann, C., and Bennett, M.J. (1999). AUX1 regulates root gravitropism in Arabidopsis by facilitating auxin uptake within root apical tissues. EMBO J. 18, 2066-2073.
19. Marella, M., Lehmann, S., Grassi, J., and Chabry, J. (2002). Filipin prevents pathological prion protein accumulation by reducing endocytosis and inducing cellular PrP release. J. Biol. Chem. 277, 25457-25464.
20. Michaux, G., Gansmuller, A., Hindelang, C., and Labouesse, M. (2000). CHE-14, a protein with a sterol-sensing domain, is required for apical sorting in C. elegans ectodermal epithelial cells. Curr. Biol. 10, 1098-1107.
21. Miller, R.G. (1984). The use and abuse of filipin to localize cholesterol in membranes. Cell Biol. Int. Rep. 8, 519-535.
22. Morris, D.A. (2000). Transmembrane auxin carrier systems-Dynamic regulators of polar auxin transport. Plant Growth Regul. 32, 161-172.
23. Morris, D.A., and Robinson, J.S. (1998). Targeting of auxin carriers to the plasma membrane: Differential effects of brefeldin A on the traffic of auxin uptake and efflux carriers. Planta 205, 606-612.
24. 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.
25. Müller, A., Guan, C., Galweiler, L., Tanzler, P., Huijser, P., Marchant, A., Parry, G., Bennett, M., Wisman, E., and Palme, K. (1998). AtPIN2 defines a locus of Arabidopsis for root gravitropism control. EMBO J. 17, 6903-6911.
26. Nabi, I.R., and Le, P.U. (2003). Caveolae/raft-dependent endocytosis. J. Cell Biol. 161, 673-677.
27. Ottenschläger, I., Wolff, P., Wolverton, C., Bhalerao, R.P., Sandberg, G., Ishikawa, H., Evans, M., and Palme, K. (2003). Gravity-regulated differential auxin transport from columella to lateral root cap cells. Proc. Natl. Acad. Sci. USA 100, 2987-2991.
28. Paciorek, T., Zazimalova, E., Ruthardt, W., Petrasek, J., Stierhof, Y.D., Kleine-Vehn, J., Morris, D.A., Emans, N., Jurgens, G., Geldner, M., and Friml, J. (2005). Auxin inhibits endocytosis and promotes its own efflux from cells. Nature 435, 1251-1256.
29. Parry, G., Delbarre, A., Marchant, A., Swarup, R., Napier, R., Perrot-Rechenmann, C., and Bennett, M.J. (2001). Novel auxin transport inhibitors phenocopy the auxin influx carrier mutation aux1. Plant J. 25, 399-406.
30. Petrasek, J., et al. (2006). PIN proteins perform a rate-limiting function in cellular auxin efflux. Science 312, 914-918.
31. 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.
32. Raven, J.A. (1975). Transport of indolacetic acid in plant cells in relation to pH and electrical potential gradients, and its significance for polar IAA transport. New Phytol. 74, 163-172.
33. 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.
34. Ritzenthaler, C., Nebenfuhr, A., Movafeghi, A., Stussi-Garaud, C., Behnia, L., Pimpl, P., Staehelin, L.A., and Robinson, D.G. (2002). Reevaluation of the effects of brefeldin A on plant cells using tobacco Bright Yellow 2 cells expressing Golgi-targeted green fluorescent protein and COPI antisera. Plant Cell 14, 237-261.
35. Rubery, P.H., and Sheldrake, A.R. (1974). Carrier-mediated auxin transport. Planta 188, 101-121.
36. Russinova, E., Borst, J.W., Kwaaitaal, M., Cano-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.
37. Sabatini, S., Beis, D., Wolkenfelt, H., Murfett, J., Guilfoyle, T., Malamy, J., Benfey, P., Leyser, O., Bechtold, N., Weisbeek, P., and Scheres, B. (1999). An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell 99, 463-472.
38. Schuck, S., and Simons, K. (2004). Polarized sorting in epithelial cells: Raft clustering and the biogenesis of the apical membrane. J. Cell Sci. 117, 5955-5964.
39. Shevell, D.E., Leu, W.M., Gillmor, C.S., Xia, G., Feldmann, K.A., and Chua, N.H. (1994). EMB30 is essential for normal cell division, cell expansion, and cell adhesion in Arabidopsis and encodes a protein that has similarity to Sec7. Cell 77, 1051-1062.
40. Spector, I., Shochet, N.R., Kashman, Y., and Groweiss, A. (1983). Latrunculins: Novel marine toxins that disrupt microfilament organization in cultured cells. Science 219, 493-495.
41. 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.
42. Swarup, R., Friml, J., Marchant, A., Ljung, K., Sandberg, G., Palme, K., and Bennett, M. (2001). Localization of the auxin permease AUX1 suggests two functionally distinct hormone transport pathways operate in the Arabidopsis root apex. Genes Dev. 15, 2648-2653.
43. Swarup, R., et al. (2004). Structure-function analysis of the presumptive Arabidopsis auxin permease AUX1. Plant Cell 16, 3069-3083.
44. Swarup, R., Kramer, E.M., Perry, P., Knox, K., Leyser, H.M., Haseloff, J., Beemster, G.T., Bhalerao, R., and Bennett, M.J. (2005). Root gravitropism requires lateral root cap and epidermal cells for transport and response to a mobile auxin signal. Nat. Cell Biol. 7, 1057-1065.
45. Tanaka, H., Dhonukshe, P., and Friml, J. (2006). Spatio-temporal asymmetric auxin distribution: Means to coordinate plant development. Cell. Mol. Life Sci., in press.
46. Voigt, B., et al. (2005). Actin-based motility of endosomes is linked to the polar tip growth of root hairs. Eur. J. Cell Biol. 84, 609-621.
47. Willemsen, V., Friml, J., Grebe, M., van den Toorn, A., Palme, K., and Scheres, B. (2003). Cell polarity and PIN protein positioning in Arabidopsis require STEROL METHYLTRANSFERASE1 function. Plant Cell 15, 612-625.
48. Wiśniewska, J., Xu, J., Seifertová, D., Brewer, P., Růžička, K., Blilou, I., Roquie, D., Benková, 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 FACTOR1 function in epidermal cell polarity. Plant Cell 17, 525-536.
50. Yamamoto, M., and Yamamoto, K.T. (1998). Effects of natural and synthetic auxins on the gravitropic growth habit of roots in two auxin-resistant mutants of Arabidopsis, axr1 and axr4: Evidence for defects in the auxin influx mechanism of axr4. J. Plant Res. 112, 391-396.
51. Yang, Y., Hammes, U.Z., Taylor, C.G., Schachtman, D.P., and Nielsen, E. (2006). High-affinity auxin transport by the AUX1 influx carrier protein. Curr. Biol. 16, 1123-1127.