Cell polarity and PIN protein positioning in Arabidopsis require STEROL METHYLTRANSFERASE1 function

Plant Cell

Volumn 15, Issue 3, 2003, Pages 612-625

  Willemsen, Viola ^a   Friml, Jirí ^b,d   Grebe, Markus ^a   Van Den Toorn, Albert ^a   Palme, Klaus ^c   Scheres, Ben ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

^b Max Delbruck Laboratorium der Max Planck Gesellschaft   (Germany)

^c UNIVERSITY OF FREIBURG   (Germany)

^d UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS; CLONING; GENES; PROTEINS;

CELL POLARITY;

PLANTS (BOTANY);

ARABIDOPSIS; COLUMELLA;

EID: 0346665865     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.008433     Document Type: Article

References (67)

1. Altmann, T. (1998). Recent advances in brassinosteroid molecular genetics. Curr. Opin. Plant Biol. 1, 378-383.
2. Athenstaedt, K., Zweytick, D., Jandrositz, A., Kohlwin, S.D., and Daum, G. (1999). Identification and characterization of major lipid particle proteins of the yeast Saccharomyces cerevisiae. J. Bacteriol. 181, 6441-6448.
3. Bagnat, M., and Simons, K. (2002). Cell surface polarization during yeast mating. Proc. Natl. Acad. Sci. USA 99, 14183-14188.
4. Bechtold, N., Ellis, J., and Pelletier, G. (1993). In planta Agrobacterium-mediated gene transfer by infiltration of adult Arabidopsis plants. C. R. Acad. Sci. Paris 316, 1194-1199.
5. Bligh, E.G., and Dyer, W.J. (1959). A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37, 91-97.
6. Boot, K.J.M., van Brussel, A.A.N., Tak, T., Spaink, H.P., and Kijne, J.W. (1999). Lipochitin oligosaccharides from Rhizobium leguminosarum bv. viciae reduce auxin transport capacity in Vicia sativa subsp. nigra. Mol. Plant-Microbe Interact. 12, 839-844.
7. Brown, D.A., and London, E. (2000). Structure and function of sphingolipid- and cholesterol-rich membrane rafts. J. Cell Biol. 275, 17221-17224.
8. Busch, M., Mayer, U., and Jurgens, G. (1996). Molecular analysis of the Arabidopsis pattern formation gene GNOM: Gene structure and intragenic complementation. Mol. Gen. Genet. 250, 681-691.
9. Carland, F.M., Fujioka, S., Takatsuto, S., Yoshido, S., and Nelson, T. (2002). The identification of CVP1 reveals a role for sterols in vascular patterning. Plant Cell 14, 2045-2058.
10. Casimiro, I., Marchant, A., Bhalerao, R.P., Beeckman, T., Dhooge, S., Swarup, R., Graham, N., Inzé, D., Sandberg, G., Casero, P.J., and Bennett M. (2001). Auxin transport promotes Arabidopsis lateral root initiation. Plant Cell 13, 843-852.
11. Chen, R., Hilson, P., Sedbrook, J., Rosen, E., Caspar, T., and Masson, P.H. (1998). The Arabidopsis thaliana AGRAVITROPIC 1 gene encodes a component of the polar-auxin-transport efflux carrier. Proc. Natl. Acad. Sci. USA 95, 15112-15117.
12. 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.
13. Clouse, S., and Feldmann, K. (1999). Molecular genetics of brassinosteroid action. In Brassinosteroids: Steroidal Plant Hormones, A. Sakurai, T. Yokota, and S. Clouse, eds (Tokyo: Springer), pp. 163-190.
14. Delbarre, A., Muller, P., and Guern, J. (1998). Short-lived and phosphorylated proteins contribute to carrier-mediated efflux, but not to influx, of auxin in suspension-cultured tobacco cells. Plant Physiol. 116, 833-844.
15. Delbarre, A., Muller, P., Imhoff, V., and Guern, J. (1996). Comparison of mechanisms controlling uptake and accumulation of 1,4-dichlorophenoxy acetic acid, naphthalene-1-acetic acid, and indole-3-acetic acid in suspension-cultured tobacco cells. Planta 198, 532-541.
16. Deyholos, M.K., Cordner, G., Beebe, D., and Sieburth, L.E. (2000). The SCARFACE gene is required for cotyledon and leaf veinpatterning. Development 127, 3205-3213.
17. Diener, A.C., Li, H., Zhou, W., Whoriskey, W.J., Nes, W.D., and Fink, G.R. (2000). Sterol methyltransferase 1 controls the level of cholesterol in plants. Plant Cell 12, 853-870.
18. Dolan, L., Janmaat, K., Willemsen, V., Linstead, P., Poethig, S., Roberts, R., and Scheres, B. (1993). Cellular organisation of the Arabidopsis thaliana root. Development 119, 71-84.
19. Estelle, M. (1998). Polar auxin transport: New support for an old model. Plant Cell 10, 1775-1778.
20. Friml, J., Benkova, E., Blilou, I., Wisniewska, J., Hamann, T., Ljung, K., Woody, S., Sandberg, G., Scheres, B., Jürgens, G., and Palme, K. (2002a). AtPIN4 mediates sink-driven auxin gradients and root patterning in Arabidopsis. Cell 108, 661-673.
21. Friml, J., Wisniewska, J., Benkova, E., Mendgen, K., and Palme, K. (2002b). Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature 415, 806-809.
22. 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.
23. 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.
24. 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.
25. Grebenok, R.J., Ohnmeiss, T.E., Yamamoto, A., Huntley, E.D., Galbraith, D.W., and Della Penna, D. (1998). Isolation and characterization of an Arabidopsis thaliana C-8,7 sterol isomerase: Functional and structural similarities to mammalian C-8,7 sterol isomerase/emopamil-binding protein. Plant Mol. Biol. 38, 807-815.
26. Hadfi, K., Speth, V., and Neuhaus, G. (1998). Auxin-induced developmental patterns in Brassica juncea embryos. Development 125, 879-887.
27. Hellens, R.P., Edwards, E.A., Leyland, N.R., Bean, S., and Mullineaux, P.M. (2000). pGreen: A versatile and flexible binary Ti vector for Agrobacterium-mediated plant transformation. Plant Mol. Biol. 42, 819-832.
28. Hertel, R., Lomax, T.L., and Briggs, W.R. (1983). Auxin transport in membrane vesicles from Cucurbita pepo L. Planta 157, 193-201.
29. Heyn, A., Hoffmann, S., and Hertel, R. (1987). In vitro auxin transport in membrane vesicles from maize coleoptiles. Planta 172, 285-287.
30. Keller, P., and Simons, K. (1998). Cholesterol is required for surface transport of influenza virus hemagglutinin. J. Cell Biol. 140, 1357-1367.
31. Knoblich, J.A. (2001). Asymmetric cell division during animal development. Nat. Rev. Mol. Cell. Biol. 2, 11-20.
32. Lafont, F., Lecat, S., Verkade, P., and Simons, K. (1998). Annexin XIIIb associates with lipid microdomains to function in apical delivery. J. Cell Biol. 142, 1413-1427.
33. Lafont, F., Verkade, P., Galli, T., Wimmer, C., Louvard, D., and Simons, K. (1999). Raft association of SNAP receptors acting in apical trafficking in Madin-Darby canine kidney cells. Proc. Natl. Acad. Sci. USA 96, 3734-3738.
34. Lang, T., Bruns, D., Wenzel, D., Riedel, D., Holroyd, P., Thiele, C., and Jahn, R. (2001). SNAREs are concentrated in cholesterol-dependent clusters that define docking and fusion sites for exocytosis. EMBO J. 20, 2202-2213.
35. Liu, Y., Shirano, Y., Fukaki, H., Yanai, Y., Tasaka, M., Tabata, S., and Shibata, D. (1999). Complementation of plant mutants with large genomic DNA fragments by a transformation-competent artificial chromosome vector accelerates positional cloning. Proc. Natl. Acad. Sci. USA 96, 6535-6540.
36. Lui, C.-M., Xu, Z.-H., and Chua, N.-H. (1993). Auxin polar transport is essential for the establishment of bilateral symmetry during early plant embryogenesis. Plant Cell 5, 621-630.
37. Lukowitz, W., Mayer, U., and Jürgens, G. (1996). Cytokinesis in the Arabidopsis embryo involves the syntaxin-related KNOLLE gene product. Cell 84, 61-71.
38. Luschnig, C., Gaxiola, R.A., Grisafi, P., and Fink, G.R. (1998). EIR1, a root-specific protein involved in auxin transport, is required for gravitropism in Arabidopsis thaliana. Genes Dev. 12, 2175-2187.
39. MacCleery, S.A., and Kiss, J.Z. (1999). Plastid sedimentation kinetics in roots of wild-type and starch-deficient mutants of Arabidopsis. Plant Physiol. 120, 183-192.
40. Marchant, A., Kargul, J., May, S.T., Muller, P., Delbarre, A., Perot-Rechenmann, C., and Bennett, M.J. (1999). AUX1 regulates root gravitropism in Arabidopsis by facilitating auxin uptake within the root apical tissues. EMBO J. 18, 2066-2073.
41. Massucci, J.D., and Schiefelbein, J.W. (1994). The rhd6 mutation of Arabidopsis thaliana alters root hair initiation through an auxin- and ethylene-associated process. Plant Physiol. 106, 1335-1346.
42. Mattsson, J., Sung, Z.R., and Berleth, T. (1999). Responses of plant vascular systems to auxin transport inhibition. Development 126, 2979-2991.
43. Mayer, U., Büttner, G., and Jürgens, G. (1993). Apical-basal pattern formation in the Arabidopsis embryo: Studies on the role of the GNOM gene. Development 117, 149-162.
44. Mora, M.P., Tourne-Peteilh, C., Charveron, M., Fabre, B., Milon, A., and Muller, I. (1999). Optimisation of plant sterols incorporation in human keratinocyte plasma membrane and modulation of membrane fluidity. Chem. Phys. Lipids 101, 255-265.
45. Morris, D.A., and Robinson, J.S. (1998). Targeting of auxin carriers to the plasma membrane: Differential effects of brefeldin A on the traffic and auxin uptake of efflux carriers. Planta 205, 606-612.
46. Mossessova, E., Gulbis, J.M., and Goldberg, J. (1998). Structure of the guanine nucleotide exchange factor sec 7 domain of human ARNO and analysis of the interaction with ARF GTPase. Cell 92, 415-423.
47. Müller, A., Guan, C., Gälweiler, L., Tänzler, 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 17, 6903-6911.
48. Okada, K., Ueda, J., Kornake, M.K., Bell, C.J., and Shimura, Y. (1991). Requirement of the auxin polar transport system in early stages of Arabidopsis floral bud formation. Plant Cell 3, 677-684.
49. Patterson, M.C., Di Bisceglie, A.M., Higgins, J.J., Abel, R.B., Schiffmann, R., Parker, C.C., Argoff, C.E., Grewal, R.P., Yu, K., and Pentchev, P.G. (1993). The effect of cholesterol-lowering agents on hepatic and plasma cholesterol in Niemann-Pick disease type C. Neurology 43, 61-64.
50. Przemeck, G.K.H., Mattsson, J., Hardtke, C.S., Sung, A.R., and Bedeth, T. (1996). Studies on the role of the Arabidopsis gene MONOPTEROS in vascular development and plant axialization. Planta 200, 229-237.
51. Rahman, A., Ahamed, A., Amakwa, T., Goto, N., and Tsurumi, S. (2001). Chromosaponin I specifically interacts with AUX1 protein in regulating the gravitropic response of Arabidopsis roots. Plant Physiol. 125, 990-1000.
52. Rodriguez-Boulan, E., and Nelson, W.J. (1989). Morphogenesis of the polarized epithelial cell phenotype. Science 245, 718-725.
53. 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.
54. Scheres, B., DiLaurenzio, L., Willemsen, V., Hauser, M.-T., Janmaat, K., Weisbeek, P., and Benfey, P. (1995). Mutations affecting the radial organisation of the Arabidopsis root display specific defects throughout the embryonic axis. Development 121, 53-62.
55. Scheres, B., McKhann, H., van den Berg, C., Willemsen, V., Wolkenfelt, H., de Vrieze, G., and Weisbeek, P. (1996). Experimental and genetic analysis of root development in Arabidopsis thaliana. Plant Soil 187, 97-105.
56. Scheres, B., Wolkenfelt, H., Willemsen, V., Terlouw, M., Lawson, E., Dean, C., and Weisbeek, P. (1994). Embryonic origin of the Arabidopsis primary root and root meristem initials. Development 120, 2475-2487.
57. Schrick, K., Mayer, U., Horrichs, A., Kuhnt, C., Bellini, C., Dangl, J., Schmidt, J., and Jürgens, G. (2000). FACKEL is a sterol C-14 reductase required for organized cell division and expansion in Arabidopsis embryogenesis. Genes Dev. 14, 1471-1484.
58. Schrick, K., Mayer, U., Martin, G., Bellini, C., Kuhnt, C., Schmidt, J., and Jürgens, G. (2002). Interactions between sterol biosynthesis genes in embryonic development of Arabidopsis. Plant J. 30, 61-73.
59. Sieburth, L. (1999). Auxin is required for leaf vein pattern in Arabidopsis. Plant Physiol. 121, 1179-1190.
60. Souter, M., Topping, J., Pullen, M., Friml, J., Palme, K., Hackett, R., Grierson, D., and Lindsey, K. (2002). hydra mutants of Arabidopsis are defective in sterol profiles and auxin and ethylene signaling. Plant Cell 14, 1017-1031.
61. Steinmann, T., Geldner, N., Grebe, M., Mangold, S., Jackson, C.L., Paris, S., Gälweiler, L., Palme, K., and Jürgens, G. (1999). Coordinated polar localization of auxin efflux carrier PIN1 by GNOM ARF GEF. Science 286, 316-318.
62. 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.
63. Ulmasov, T., Murfett, J., Hagen, G., and Guilfoyle, T.J. (1997). Aux/ IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9, 1963-1971.
64. van den Berg, C., Willemsen, V., Hendriks, G., Weisbeek, P., and Scheres, B. (1997). Short-range control of cell differentiation in the Arabidopsis root meristem. Nature 390, 287-289.
65. Vroemen, C.W., Langeveld, S., Mayer, U., Ripper, G., Jürgens, G., van Kammen, A., and de Vries, S.C. (1996). Pattern formation in the Arabidopsis embryo revealed by position-specific lipid transfer protein gene expression. Plant Cell 8, 783-791.
66. White, R.G., and Sack, F.D. (1990). Actin microfilaments in presumptive statocytes of root cap and coleoptiles. Am. J. Bot. 77, 17-26.
67. Willemsen, V., Wolkenfelt, H., de Vrieze, G., Weisbeek, P., and Scheres, B. (1998). The HOBBIT gene is required for formation of the root meristem in the Arabidopsis embryo. Development 125, 521-531.