The exocyst complex contributes to PIN auxin efflux carrier recycling and polar auxin transport in Arabidopsis

Plant Journal

Volumn 73, Issue 5, 2013, Pages 709-719

  Drdová, Edita Janková ^a   Synek, Lukáš ^a   Pečenková, Tamara ^a,b   Hála, Michal ^a,b   Kulich, Ivan ^b   Fowler, John E ^c   Murphy, Angus S ^d   Žárský, Viktor ^a,b  

^a INSTITUTE OF EXPERIMENTAL BOTANY   (Czech Republic)

^b CHARLES UNIVERSITY   (Czech Republic)

^c OREGON STATE UNIVERSITY   (United States)

^d PURDUE UNIVERSITY   (United States)

Author keywords

Arabidopsis thaliana; EXO70A1 subunit; exocyst; PIN recycling; polar auxin transport

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; AUXIN EFFLUX CARRIER; ENDOMEMBRANE COMPARTMENTS; ENDOSOMES; EXO70A1 SUBUNIT; EXOCYST; EXOCYST COMPLEX; LAND PLANTS; LOSS-OF-FUNCTION MUTANTS; MEMBRANE LOCALIZATION; POLAR AUXIN TRANSPORTS; RE-LOCALIZATION; RHO GTPASES; ROOT CELLS; TRANS-GOLGI NETWORK; WHOLE PLANTS;

CELL MEMBRANES; PROTEINS;

RECYCLING;

ARABIDOPSIS PROTEIN; BREFELDIN A; CARRIER PROTEIN; EXO70A1 PROTEIN, ARABIDOPSIS; HYBRID PROTEIN; INDOLEACETIC ACID DERIVATIVE; PIN1 PROTEIN, ARABIDOPSIS; PIN2 PROTEIN, ARABIDOPSIS; SEC8 PROTEIN, ARABIDOPSIS; VESICULAR TRANSPORT PROTEIN;

ARABIDOPSIS; ARTICLE; CELL MEMBRANE; CYTOLOGY; DRUG EFFECT; ENDOSOME; GENETICS; METABOLISM; MORPHOGENESIS; MUTATION; PHENOTYPE; PLANT EPIDERMIS; PLANT ROOT; SEEDLING; TRANS GOLGI NETWORK; TRANSGENIC PLANT; TRANSPORT AT THE CELLULAR LEVEL;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BIOLOGICAL TRANSPORT; BODY PATTERNING; BREFELDIN A; CELL MEMBRANE; ENDOSOMES; INDOLEACETIC ACIDS; MEMBRANE TRANSPORT PROTEINS; MUTATION; PHENOTYPE; PLANT EPIDERMIS; PLANT ROOTS; PLANTS, GENETICALLY MODIFIED; RECOMBINANT FUSION PROTEINS; SEEDLING; TRANS-GOLGI NETWORK; VESICULAR TRANSPORT PROTEINS;

ANIMALIA; ARABIDOPSIS; ARABIDOPSIS THALIANA; EMBRYOPHYTA;

EID: 84874494172     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12074     Document Type: Article

References (65)

1. Benjamins, R., and, Scheres, B., (2008) Auxin: the looping star in plant development. Annu. Rev. Plant Biol. 59, 443-465. (Pubitemid 351813038)
2. 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. (Pubitemid 37506047)
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. (Pubitemid 26275169)
4. Blakeslee, J.J., Bandyopadhyay, A., Lee, O.R., et al. (2007) Interactions among PIN-FORMED and P-Glycoprotein auxin transporters in Arabidopsis. Plant Cell, 19, 131-147. (Pubitemid 46852707)
5. Blankenship, J.T., Fuller, M.T., and, Zallen, J.A., (2007) The Drosophila homolog of the Exo84 exocyst subunit promotes apical epithelial identity. J. Cell Sci. 120, 3099-3110. (Pubitemid 47517092)
6. 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. (Pubitemid 40101136)
7. Boyd, C., Hughes, T., Pypaert, M., and, Novick, P., (2004) Vesicles carry most exocyst subunits to exocytic sites marked by the remaining two subunits, Sec3p and Exo70p. J. Cell Biol. 167, 889-901. (Pubitemid 39628111)
8. 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. (Pubitemid 29003765)
9. Cole, R.A., Synek, L., Žárský, V., and, Fowler, J.E., (2005) SEC8, a subunit of the putative Arabidopsis exocyst complex, facilitates pollen germination and competitive pollen tube growth. Plant Physiol. 138, 34-45.
10. Cvrčková, F., Eliáš, M., Hála, M., Obermeyer, G., and, Žárský, V., (2001) Small GTPases and conserved signalling pathways in plant cell morphogenesis: from exocytosis to Exocyst. Cell Biol. Plant Fungal Tip Growth, 10, 5-22.
11. 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. (Pubitemid 43956173)
12. 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. (Pubitemid 46420535)
13. Dhonukshe, P., Tanaka, H., Goh, T., et al. (2008) Generation of cell polarity in plants links endocytosis, auxin distribution and cell fate decisions. Nature, 456, 962-966.
14. Dhonukshe, P., Huang, F., Galvan-Ampudia, C.S., et al. (2010) Plasma membrane-bound AGC3 kinases phosphorylate PIN auxin carriers at TPRXS(N/S) motifs to direct apical PIN recycling. Development, 137, 3245-3255.
15. Dupraz, S., Grassi, D., Bernis, M.E., Sosa, L., Bisbal, M., Gastaldi, L., Jausoro, I., Cáceres, A., Pfenninger, K.H., and, Quiroga, S., (2009) The TC10-Exo70 complex is essential for membrane expansion and axonal specification in developing neurons. J. Neurosci. 29, 13292-13301.
16. Durand, C., Vicré-Gibouin, M., Follet-Gueye, M.L., Duponchel, L., Moreau, M., Lerouge, P., and, Driouich, A., (2009) The organization pattern of root border-like cells of Arabidopsis is dependent on cell wall homogalacturonan. Plant Physiol. 150, 1411-1421.
17. Eliáš, M., Drdová, E., Žiak, D., Bavlnka, B., Hála, M., Cvrčková, F., Soukupová, H., and, Žárský, V., (2003) The exocyst complex in plants. Cell Biol. Int. 27, 199-201. (Pubitemid 36398116)
18. Faraway, J., (2006) Extending the Linear Model with R: Generalized Linear, Mixed Effects and Nonparametric Regression Models. Boca Raton: Chapman and Hall/CRC.
19. Fendrych, M., Synek, L., Pečenková, T., et al. (2010) The Arabidopsis exocyst complex is involved in cytokinesis and cell plate maturation. Plant Cell, 22, 3053-3065.
20. 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. (Pubitemid 37442576)
21. Friml, J., Wiśniewska, J., Benková, E., Mendgen, K., and, Palme, K., (2002) Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature, 415, 806-809. (Pubitemid 34150504)
22. Friml, J., Yang, X., Michniewicz, M., et al. (2004) A PINOID-dependent binary switch in apical-basal PIN polar targeting directs auxin efflux. Science, 306, 862-865. (Pubitemid 39446993)
23. Furutani, M., Kajiwara, T., Kato, T., Treml, B.S., Stockum, C., Torres-Ruiz, R.A., and, Tasaka, M., (2007) The gene MACCHI-BOU 4/ENHANCER OF PINOID encodes a NPH3-like protein and reveals similarities between organogenesis and phototropism at the molecular level. Development, 134, 3849-3859. (Pubitemid 350187344)
24. Furutani, M., Sakamoto, N., Yoshida, S., Kajiwara, T., Robert, H.S., Friml, J., and, Tasaka, M., (2011) Polar-localized NPH3-like proteins regulate polarity and endocytosis of PIN-FORMED auxin efflux carriers. Development, 138, 2069-2078.
25. Gälweiler, L., Guan, C., Müller, 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. (Pubitemid 29004064)
26. Geldner, N., Friml, J., Stierhof, Y.D., Jurgens, G., and, Palme, K., (2001) Auxin transport inhibitors block PIN1 cycling and vesicle trafficking. Nature, 413, 425-427.
27. 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. (Pubitemid 36144111)
28. Geldner, N., Richter, S., Vieten, A., Marquardt, S., Torres-Ruiz, R.A., Mayer, U., and, Jürgens, G., (2004) Partial loss-of-function alleles reveal a role for GNOM in auxin transport-related, post-embryonic development of Arabidopsis. Development, 131, 389-400. (Pubitemid 38181377)
29. Geldner, N., Hyman, D.L., Wang, X., Schumacher, K., and, Chory, J., (2007) Endosomal signaling of plant steroid receptor kinase BRI1. Genes Dev. 21, 1598-1602. (Pubitemid 47026363)
30. Geldner, N., Dénervaud-Tendon, V., Hyman, D.L., Mayer, U., Stierhof, Y., and, Chory, J., (2009) Rapid, combinatorial analysis of membrane compartments in intact plants with a multicolor marker set. Plant J. 59, 169-178.
31. Guo, W., Roth, D., Walch-Solimena, C., and, Novick, P., (1999) The exocyst is an effector for Sec4p, targeting secretory vesicles to sites of exocytosis. EMBO J. 18, 1071-1080. (Pubitemid 29082285)
32. Hála, M., Cole, R., Synek, L., et al. (2008) An exocyst complex functions in plant cell growth in Arabidopsis and tobacco. Plant Cell, 20, 1330-1345. (Pubitemid 352844186)
33. Hazak, O., Bloch, D., Poraty, L., Sternberg, H., Zhang, J., Friml, J., and, Yalovsky, S., (2010) A rho scaffold integrates the secretory system with feedback mechanisms in regulation of auxin distribution. PLoS Biol. 8, e1000282.
34. He, B., Xi, F., Zhang, X., Zhang, J., and, Guo, W., (2007) Exo70 interacts with phospholipids and mediates the targeting of the exocyst to the plasma membrane. EMBO J. 26, 4053-4065. (Pubitemid 47462093)
35. Ikeda, Y., Men, S., Fischer, U., Stepanova, A.N., Alonso, J.M., Ljung, K., and, Grebe, M., (2009) Local auxin biosynthesis modulates gradient-directed planar polarity in Arabidopsis. Nat. Cell Biol. 11, 731-738.
36. Inoue, M., Chang, L., Hwang, J., Chiang, S.H., and, Saltiel, A.R., (2003) The exocyst complex is required for targeting of Glut4 to the plasma membrane by insulin. Nature, 422, 629-633. (Pubitemid 36460418)
37. Jiang, K., Zhang, S., Lee, S., Tsai, G., Kim, K., Huang, H., Chilcott, C., Zhu, T., and, Feldman, L.J., (2006) Transcription profile analyses identify genes and pathways central to root cap functions in maize. Plant Mol. Biol. 60, 343-363. (Pubitemid 43327573)
38. Kitakura, S., Vanneste, S., Robert, S., Löfke, Ch., Teichmann, T., Tanaka, H., and, Friml, J., (2011) Clathrin mediates endocytosis and polar distribution of PIN auxin transporters in Arabidopsis. Plant Cell, 23, 1920-1931.
39. 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.
40. Koumandou, V.L., Dacks, J.B., Coulson, R.M., and, Field, M.C., (2007) Control systems for membrane fusion in the ancestral eukaryote; evolution of tethering complexes and SM proteins. BMC Evol. Biol. 7, 29.
41. Kulich, I., Cole, R., Drdová, E., Cvrčková, F., Soukup, A., Fowler, J., and, Žárský, V., (2010) Arabidopsis exocyst subunits SEC8 and EXO70A1 and exocyst interactor ROH1 are involved in the localized deposition of seed coat pectin. New Phytol. 188, 615-625.
42. Langevin, J., Morgan, M.J., Rossé, C., Racine, V., Sibarita, J.B., Aresta, S., Murthy, M., Schwarz, T., Camonis, J., and, Bellaïche, Y., (2005) Drosophila exocyst components Sec5, Sec6, and Sec15 regulate DE-Cadherin trafficking from recycling endosomes to the plasma membrane. Dev. Cell, 9, 365-376. (Pubitemid 41235806)
43. Lavy, M., Bloch, D., Hazak, O., Gutman, I., Poraty, L., Sorek, N., Sternberg, H., and, Yalovsky, S., (2007) A novel ROP/RAC effector links cell polarity, root-meristem maintenance, and vesicle trafficking. Curr. Biol. 17, 947-952. (Pubitemid 46829836)
44. Mayer, U., Buttner, G., and, Jurgens, G., (1993) Apical-basal pattern formation in the Arabidopsis embryo: studies on the role of the gnom gene. Development, 117, 149-162. (Pubitemid 23094164)
45. Michniewicz, M., Zago, M.K., Abas, L., et al. (2007) Antagonistic regulation of PIN phosphorylation by PP2A and PINOID directs auxin flux. Cell, 130, 1044-1056. (Pubitemid 47410270)
46. Migliaccio, F., and, Piconese, S., (2001) Spiralizations and tropisms in Arabidopsis roots. Trends Plant Sci. 6, 561-565. (Pubitemid 34004077)
47. Novick, P., Field, C., and, Schekman, R., (1980) Identification of 23 complementation groups required for post-translational events in the yeast secretory pathway. Cell, 21, 205-215. (Pubitemid 10040069)
48. Oztan, A., Silvis, M., Weisz, O.A., Bradbury, N.A., Hsu, S.C., Goldenring, J.R., Yeaman, C., and, Apodaca, G., (2007) Exocyst requirement for endocytic traffic directed toward the apical and basolateral poles of polarized MDCK cells. Mol. Biol. Cell, 18, 3978-3992. (Pubitemid 47519489)
49. Ponce, G., Barlow, P.W., Feldman, L.J., and, Cassab, G.I., (2005) Auxin and ethylene interactions control mitotic activity of the quiescent centre, root cap size, and pattern of cap cell differentiation in maize. Plant, Cell Environ. 28, 719-732. (Pubitemid 40886104)
50. Rashotte, A.M., DeLong, A., and, Muday, G.K., (2001) Genetic and chemical reductions in protein phosphatase activity alter auxin transport, gravity response, and lateral root growth. Plant Cell, 13, 1683-1697. (Pubitemid 32675728)
51. Rojas-Pierce, M., Titapiwatanakun, B., Sohn, E.J., et al. (2007) Arabidopsis P-glycoprotein19 participates in the inhibition of gravitropism by gravacin. Chem. Biol. 14, 1366-1376. (Pubitemid 350257005)
52. 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. (Pubitemid 41096002)
53. Sabatini, S., Beis, D., Wolkenfelt, H., et al. (1999) An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell, 99, 463-472.
54. Santner, A.A., and, Watson, J.C., (2006) The WAG1 and WAG2 protein kinases negatively regulate root waving in Arabidopsis. Plant J. 45, 752-764. (Pubitemid 43373693)
55. 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. (Pubitemid 29484699)
56. Synek, L., Schlager, N., Eliáš, M., Quentin, M., Hauser, M.T., and, Žárský, V., (2006) AtEXO70A1, a member of a family of putative exocyst subunits specifically expanded in land plants, is important for polar growth and plant development. Plant J. 48, 54-72. (Pubitemid 44379712)
57. 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. (Pubitemid 28174069)
58. Vieten, A., Vanneste, S., Wiśniewska, J., Benková, E., Benjamins, R., Beeckman, T., Luschnig, C., and, Friml, J., (2005) Functional redundancy of PIN proteins is accompanied by auxin-dependent cross-regulation of PIN expression. Development, 132, 4521-4531. (Pubitemid 41632230)
59. Wen, T.-J., Hochholdinger, F., Sauer, M., Bruce, W., and, Schnable, P.S., (2005) The roothairless1 gene of maize encodes a homolog of sec3, which is involved in polar exocytosis. Plant Physiol. 138, 1637-1643. (Pubitemid 43142108)
60. Wiśniewska, J., Xu, J., Seifertová, D., Brewer, P.B., Růžička, K., Blilou, I., Rouquié, D., Benková, E., Scheres, B., and, Friml, J., (2006) Polar PIN localization directs auxin flow in plants. Science, 312, 883. (Pubitemid 43727314)
61. Wu, H., Turner, C., Gardner, J., Temple, B., and, Brennwald, P., (2010) The Exo70 subunit of the exocyst is an effector for both Cdc42 and Rho3 function in polarized exocytosis. Mol. Biol. Cell, 21, 430-442.
62. Xu, J., and, Scheres, B., (2005) Dissection of Arabidopsis ADP-RIBOSYLATION FACTOR 1 function in epidermal cell polarity. Plant Cell, 17, 525-536. (Pubitemid 41672972)
63. Žárský, V., Cvrčková, F., Potocký, M., and, Hála, M., (2009) Exocytosis and cell polarity in plants-exocyst and recycling domains. New Phytol. 183, 255-272.
64. Zažímalová, E., Murphy, A.S., Yang, H., Hoyerová, K., and, Hosek, P., (2010) Auxin transporters-why so many? Cold Spring Harb. Perspect. Biol. 2, a001552.
65. Zhang, X., Orlando, K., He, B., Xi, F., Zhang, J., Zajac, A., and, Guo, W., (2008) Membrane association and functional regulation of Sec3 by phospholipids and Cdc42. J. Cell Biol. 180, 145-158.