Regulation of the polarity of protein trafficking by phosphorylation

Molecules and Cells

Volumn 33, Issue 5, 2012, Pages 423-430

  Ganguly, Anindya ^a   Sasayama, Daisuke ^a   Cho, Hyung Taeg ^a  

^a Seoul National University   (South Korea)

Author keywords

Auxin; Auxin transport; Phosphorylation; PIN FORMED (PIN); Protein trafficking

Indexed keywords

AUXIN; BORON;

CELL DIVISION; CELL ENLARGEMENT; CELL POLARITY; EMBRYO DEVELOPMENT; EUKARYOTE; EXOCYTOSIS; HYDROPHILICITY; MORPHOGENESIS; NONHUMAN; ORGANOGENESIS; PHOSPHORYLATION; PLANT; PROKARYOTE; PROTEIN STRUCTURE; REVIEW;

ANIMALS; CELL POLARITY; INDOLEACETIC ACIDS; PHOSPHORYLATION; PLANTS; PROTEIN TRANSPORT;

EUKARYOTA; PROKARYOTA;

EID: 84863476197     PISSN: 10168478     EISSN: 02191032     Source Type: Journal    
DOI: 10.1007/s10059-012-0039-9     Document Type: Review

References (74)

1. Anthony, R.G., Khan, S., Costa, J., Pais, M.S., and Bögre, L. (2006). The Arabidopsis protein kinase PTI1-2 is activated by convergent phosphatidic acid and oxidative stress signaling pathways downstream of PDK1 and OXI1. J. Biol. Chem. 281, 37536-37546. (Pubitemid 46042057)
2. Benjamins, R., Quint, A., Weijers, D., Hooykaas, P., and Offringa, R. (2001). The PINOID protein kinase regulates organ development in Arabidopsis by enhancing polar auxin transport. Development 128, 4057-4067. (Pubitemid 33040612)
3. 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)
4. Bögre, L., Ökrész, L., Henriques, R., and Anthony, R.G. (2003). Growth signalling pathways in Arabidopsis and the AGC protein kinases. Trends Plant Sci. 8, 424-431. (Pubitemid 37216195)
5. Bryant, D.M., and Mostov, K.E. (2008). From cells to organs: building polarized tissue. Nat. Rev. Mol. Cell. Biol. 9, 887-901.
6. Cheng, Y., Qin, G., Dai, X., and Zhao, Y. (2007). NPY1, a BTB-NPH3-like protein, plays a critical role in auxin-regulated organo-genesis in Arabidopsis. Proc. Natl. Acad. Sci. USA 104, 18825-18829. (Pubitemid 350210781)
7. Cho, M., Lee, O.R., Ganguly, A., and Cho, H.-T. (2007a). Auxin-signaling: short and long. J. Plant Biol. 50, 79-89. (Pubitemid 46814600)
8. Cho, M., Lee, S.H., and Cho, H-T. (2007b). P-glycoprotein4 displays auxin efflux transporter-like action in Arabidopsis root hair cells and tobacco cells. Plant Cell 19, 3930-3943. (Pubitemid 351253111)
9. Christensen, S.K., Dagenais, N., Chory, J., and Weigel, D. (2000). Regulation of auxin response by the protein kinase PINOID. Cell 100, 469-478.
10. Cove, D.J. (2000). The generation and modification of cell polarity. J. Exp. Bot. 51, 831-838. (Pubitemid 30319706)
11. Davies, P.J. (2005). The plant hormones: their nature, occurrence and function. In Plant Hormones: Biosynthesis, Signal Trans-duction, Action! P.J. Davies, ed. 3rd ed. (Dordrecht, Netherlands: Kluwer Academic Publishers), pp. 1-15.
12. Dettmer, J., and Friml, J. (2011). Cell polarity in plants: when two do the same, it is not the same.... Curr. Opin. Plant Biol. 23, 686-696.
13. Devarenne, T.P., Ekengren, S.K., Pedley, K.F., and Martin, G.B. (2006). Adi3 is a Pdk1-interacting AGC kinase that negatively regulates plant cell death. EMBO J. 25, 255-265. (Pubitemid 43077313)
14. Dhonukshe, P., Tanaka, H., Goh, T., Ebine, K., Mahonen, A.P., Prasad, K., Blilou, I., Geldner, N., Xu, J., Uemura, T., et al. (2008). Generation of cell polarity in plants links endocytosis, auxin distribution and cell fate decisions. Nature 456, 962-966.
15. Dhonukshe, P., Huang, F., Galvan-Ampudia, C.S., Mähönen, A.P., Kleine-Vehn, J., Xu, J., Quint, A., Prasad, K., Friml, J., Scheres, B., 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.
16. Ding, Z., Galván-Ampudia, C.S., Demarsy, E., Łangowski, Ł., Kleine-Vehn, J., Fan, Y., Morita, M.T., Tasaka, M., Fankhauser, C., Offringa, R., et al. (2011). Light-mediated polarization of the PIN3 auxin transporter for the phototropic response in Arabidop-sis. Nat. Cell Biol. 13, 447-452.
17. Ebersbach, G., and Jacobs-Wagner, C. (2008). Exploration into the spatial and temporal mechanisms of bacterial polarity. Trend Mi-crobiol. 3, 101-108.
18. Ebine, K., Fujimoto, M., Okatani, Y., Nishiyama, T., Goh, T., Ito, E., Dainobu, T., Nishitani, A., Uemura, T., Sato, M.H., et al. (2011). A membrane trafficking pathway regulated by the plant-specific RAB GTPase ARA6. Nat. Cell Biol. 13, 853-860.
19. Farr, G.A., Hull, M., Mellman, I., and Caplan, M.J. (2009). Membrane proteins follow multiple pathways to the basolateral cell surface in polarized epithelial cells. J. Cell Biol. 186, 269-282.
20. Feraru, E., Feraru, M.I., Kleine-Vehn, J., Martinière, A., Mouille, G., Vanneste, S., Vernhettes, S., Runions, J., and Friml, J. (2011) PIN polarity maintenance by the cell wall in Arabidopsis. Curr. Biol. 21, 338-343.
21. Friml, J., Benková, E., Blilou, I., Wisniewska, J., Hamann, T., Ljung, K., Woody, S., Sandberg, G., Scheres, B., Jürgens, G., et al. (2002a). AtPIN4 mediates sink-driven auxin gradients and root patterning in Arabidopsis. Cell 108, 661-673. (Pubitemid 34241427)
22. Friml, J., Wiśniewska, J., Benková, E., Mendgen, K., and Palme, K. (2002b). Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature 415, 806-809. (Pubitemid 34150504)
23. Friml, J., Yang, X., Michniewicz, M., Weijers, D., Quint, A., Tietz, O., Benjamins, R., Ouwerkerk, P.B., Ljung, K., Sandberg, G., et al. (2004). A PINOID-dependent binary switch in apical-basal PIN polar targeting directs auxin efflux. Science 306, 862-865. (Pubitemid 39446993)
24. Fuji, K., Miwa, K., and Fujiwara, T. (2009). The interacellular transport of transporters: membrane trafficking of mineral transporters. Curr. Opin. Plant Biol. 12, 699-704.
25. 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 an NPH3-like protein and reveals similarities between organogenesis and phototropism at the molecular level. Development 134, 3849-3859. (Pubitemid 350187344)
26. 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.
27. Ganguly, A., Lee, S.H., Cho, M., Lee, O.R., Ryu, H., and Cho, H.-T. (2010). Differential auxin-transporting activities of PIN-FORMED proteins in Arabidopsis root hair cells. Plant Physiol. 153, 1046-1061.
28. Geldner, N. (2008). Cell polarity in plants: a PARspective on PINs. Curr. Opin. Plant Biol. 12, 42-48.
29. 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. (Pubitemid 32928597)
30. 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. (Pubitemid 36144111)
31. Gitai, Z. (2005). The new bacterial cell biology: moving parts and subcellular architecture. Cell 120, 577-586. (Pubitemid 40343071)
32. Goldstein, B., and Macara, I.G. (2007). The PAR proteins: Fundamental players in animal cell polarization. Dev. Cell 13, 609-622. (Pubitemid 350011991)
33. Haas, T.J., Sliwinski, M.K., Martínez, 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 en-dosome function and interacts with its positive regulator LYST-INTERACTING PROTEIN5. Plant Cell 19, 1295-1312. (Pubitemid 46941655)
34. Huang, F., Zago, M.K., Abas, L., Van, M.A., Galvan-Ampudia, C.S., and Offringa, R. (2010). Phosphorylation of conserved PIN motifs directs Arabidopsis PIN1 polarity and auxin transport. Plant Cell 22, 1129-1142.
35. Ito, H., and Gray, W.M. (2006). A gain-of-function mutation in the Arabidopsis pleiotropic drug resistance transporter PDR9 confers resistance to auxinic herbicides. Plant Physiol. 142, 63-74. (Pubitemid 44412230)
36. Kleine-Vehn, J., Dhonukshe, P., Swarup, R., Bennett, M., and Friml, J. (2006). Subcellular trafficking of the Arabidopsis auxin influx carrier AUX1 uses a novel pathway distinct from PIN1. Plant Cell 18, 3171-3181. (Pubitemid 46013284)
37. 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.
38. Kleine-Vehn, J., Dhonukshe, P., Sauer, M., Brewer, P.B., Wisnie-wska, J., Paciorek, T., Benkova, E., and Friml, J. (2008). ARF GEF-dependent transcytosis and polar delivery of PIN auxin carriers in Arabidopsis. Curr. Biol. 18, 526-531.
39. Kleine-Vehn, J., Huang, F., Naramoto, S., Zhang, J., Michniewicz, M., Offringa, R., and Friml, J. (2009). PIN auxin efflux carrier polarity is regulated by PINOID kinase-mediated recruitment into GNOM-independent trafficking in Arabidopsis. Plant Cell 21, 3839-3849.
40. 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.
41. Kocks, C., Hellio, R., Gounon, P., Ohayon, H., and Cossart, P. (1993). Polarized distribution of Listeria monocytogenes surface protein ActA at the site of directional actin assembly. J. Cell Sci. 105, 699-710. (Pubitemid 23243203)
42. Langowski, L., Ruzicka, K., Naramoto, S., Kleine-Vehn, J., and Friml, J. (2010). Trafficking to the outer polar domain defines the root-soil interface. Curr. Biol. 20, 904-908.
43. Lee, S.H., and Cho, H.-T. (2006). PINOID positively regulates auxin efflux in Arabidopsis root hair cells and tobacco cells. Plant Cell 18, 1604-1616. (Pubitemid 44025546)
44. 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. (Pubitemid 28348041)
45. Matroule, J.Y., Lam, H., Burnette, D.T., and Jacobs-Wagner, C. (2004). Cytokinesis monitoring during development; rapid pole-to-pole shuttling of a signaling protein by localized kinase and phosphatase in Caulobacter. Cell 118, 579-590. (Pubitemid 39179711)
46. Michniewicz, M., Zago, M.K., Abas, L., Weijers, D., Schweighofer, A., Meskiene, I., Heisler, M.G., Ohno, C., Zhang, J., Huang, F., et al. (2007). Antagonistic regulation of PIN phosphorylation by PP2A and PINOID directs auxin flux. Cell 130, 1044-1056. (Pubitemid 47410270)
47. Miwa, K., Takano, J., Omori, H., Seki, M., Shinozaki, K., and Fuji-wara, T. (2007). Plants tolerant of high boron levels. Science 318, 1417. (Pubitemid 350208946)
48. Mravec, J., Skupa, P., Bailly, A., Hoyerova, K., Krecek, P., Bielach, A., Petrasek, J., Zhang, J., Gaykova, V., Stierhof, Y.D., et al. (2009). Subcellular homeostasis of phytohormone auxin is mediated by the ER-localized PIN5 transporter. Nature 459, 1136-1140.
49. 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. (Pubitemid 28550284)
50. Nance, J., and Zallen, J.A. (2011). Elaborating polarity: PAR proteins and the cytoskeleton. Development 138, 799-809.
51. Nelson, J.W. (2003). Adaptation of core mechanisms to generate cell polarity. Nature 422, 766-774.
52. Plant, P.J., Fawcett, J.P., Lin, D.C., Holdorf, A.D., Binns, K., Kul-karni, S., and Pawson, T. (2003). A polarity complex of mPar-6 and atypical PKC binds, phosphorylates and regulates mammalian LGL. Nat. Cell Biol. 5, 301-308. (Pubitemid 36432294)
53. Rafelski, S.M., and Theriot, J.A. (2006). Mechanism of polarization of Listeria monocytogenes surface protein ActA. Mol. Microbiol. 59, 1262-1279.
54. Rahman, A., Takahashi, M., Shibasaki, K., Wu, S., Inaba, T., Tsu-rumi, S., and Baskin, T.I. (2010). Gravitropism of Arabidopsis thaliana roots requires the polarization of PIN2 toward the root tip in meristematic cortical cells. Plant Cell 22, 1762-1776.
55. 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.
56. 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.
57. Rubery, P.H., and Sheldrake, A.R. (1974). Carrier-mediated auxin transport. Planta 188, 101-121.
58. Rudner, D.J., and Losick, R. (2010). Protein Subcellular Localization in Bacteria. Cold Spring Harb. Perspect Biol. 2, a000307.
59. Stein, M., Dittgen, J., Sanchez-Rodriguez, C., Hou, B.H., Molina, A., Schulze-Lefert, P., Lipka, V., and Somerville, S. (2006). Arabi-dopsis PEN3/PDR8, an ATP binding cassette transporter, contributes to nonhost resistance to inappropriate pathogens that enter by direct penetration. Plant Cell 18, 731-746. (Pubitemid 43956174)
60. 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. (Pubitemid 29484699)
61. Takano, J., Noguchi, K., Yasumori, M., Kobayashi, M., Gajdos, Z., Miwa, K., Hayashi, H., Yoneyama, T., and Fujiwara, T. (2002). Arabidopsis boron transporter for xylem loading. Nature 420, 337-340. (Pubitemid 35398191)
62. Takano, J., Miwa, K., Yuan, L., Von Wiren, N., and Fujiwara, T. (2005). Endocytosis and degradation of BOR1, a boron transporter of Arabidopsis thaliana, regulated by boron availability. Proc. Natl. Acad. Sci. USA 102, 12276-12281. (Pubitemid 41291165)
63. Takano, J., Wada, M., Ludewig, U., Schaaf, G., Wirén, N., and Fujiwara, T. (2006). The Arabidopsis major intrinsic protein NIP5;1 is essential for efficient boron uptake and plant development under boron limitation. Plant Cell 18, 1498-1509. (Pubitemid 43956112)
64. Takano, J., Miwa, K., and Fujiwara, T. (2008). Boron transport mechanisms: collaboration of channels and transporters. Trends Plant Sci. 13, 451-457.
65. Takano, J., Tanaka, M., Toyoda, A., Miwa, K., Kasai, K., Fuji, K., Onouchi, H., Naito, S., and Fujiwara, T. (2010). Polar localization and degradation of Arabidopsis boron transporters through distinct trafficking pathways. Proc. Natl. Acad. Sci. USA 107, 5220-5225.
66. 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. (Pubitemid 47123523)
67. Tsokos, C.G., Perchuk, B.S., and Laub, M.T. (2011) A dynamic complex of signaling proteins uses polar localization to regulate cell-fate asymmetry in Caulobacter crescentus. Dev. Cell 20, 329-341.
68. Ueda, T., Uemura, T., Sato, M.H., and Nakano, A. (2004) Functional differentiation of endosomes in Arabidopsis cells. Plant J. 40, 783-789. (Pubitemid 39623251)
69. Wiśniewska, J., Xu, J., Seifertová, D., Brewer, P.B., Růička, 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)
70. Zegzouti, H., Anthony, R.G., Jahchan, N., Bögre, L., and Christen-sen, S.K. (2006a) Phosphorylation and activation of PINOID by the phospholipid signaling kinase 3-phosphoinositide-dependent protein kinase 1 (PDK1) in Arabidopsis. Proc. Natl. Acad. Sci. USA 103, 6404-6409.
71. Zegzouti, H., Li, W., Lorenz, T.C., Xie, M., Payne, C.T., Smith, K., Glenny, S., Payne, G.S., and Christensen, S.K. (2006b). Structural and functional insights into the regulation of Arabidopsis AGC VIIIa kinases. J. Biol. Chem. 281, 35520-30. (Pubitemid 46036587)
72. Zhang, Y., and McCormick, S. (2008). AGCVIII kinases: at the crossroads of cellular signaling. Trends Plant Sci. 14, 689-695.
73. Zhang, J., NodzyZski, T., Pěnčík, A., Rolčík, J., and Friml, J. (2010). PIN phosphorylation is sufficient to mediate PIN polarity and direct auxin transport. Proc. Natl. Acad. Sci. USA 107, 918-922.
74. Zourelidou, M., Müller, I., Willige, B.C., Nill, C., Jikumaru, Y., Li, H., and Schwechheimer, C. (2009). The polarly localized D6 PROTEIN KINASE is required for efficient auxin transport in Arabidopsis thaliana. Development 136, 627-636.