Inactivation of plasma membrane-localized CDPK-RELATED KINASE5 decelerates PIN2 exocytosis and root gravitropic response in Arabidopsis

Plant Cell

Volumn 25, Issue 5, 2013, Pages 1592-1608

  Rigó, Gábor ^a   Ayaydin, Ferhan ^a   Tietz, Olaf ^a,b   Zsigmond, Laura ^a,c   Kovács, Hajnalka ^a   Páy, Anikó ^a   Salchert, Klaus ^d   Darula, Zsuzsanna ^e   Medzihradszky, Katalin F ^e,f   Szabados, László ^a   Palme, Klaus ^b   Koncz, Csaba ^a,g   Cséplo, Ágnes ^a  

^a INSTITUTE OF BIOCHEMISTRY   (Hungary)

^b UNIVERSITY OF FREIBURG   (Germany)

^c UNIVERSITY OF SZEGED   (Hungary)

^d DNA LandMarks   (Canada)

^e INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 84879466713     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.113.110452     Document Type: Article

References (92)

1. Abas, L., Benjamins, R., Malenica, N., Paciorek, T., Wiśniewska, J., Moulinier-Anzola, J.C., Sieberer, T., Friml, J., and Luschnig, C. (2006). Intracellular trafficking and proteolysis of the Arabidopsis auxin-efflux facilitator PIN2 are involved in root gravitropism. Nat. Cell Biol. 8: 249-256. Erratum. Nat. Cell Biol. 8: 424.
2. Alonso, J.M., et al. (2003). Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653-657.
3. Baldwin, K.L., Strohm, A.K., and Masson, P.H. (2013). Gravity sensing and signal transduction in vascular plant primary roots. Am. J. Bot. 100: 126-142.
4. Baster, P., Robert, S., Kleine-Vehn, J., Vanneste, S., Kania, U., Grunewald, W., De Rybel, B., Beeckman, T., and Friml, J. (2013). SCF(TIR1/AFB)-auxin signalling regulates PIN vacuolar trafficking and auxin fluxes during root gravitropism. EMBO J. 32: 260-274.
5. Benjamins, R., Ampudia, C.S., Hooykaas, P.J., and Offringa, R. (2003). PINOID-mediated signaling involves calcium-binding proteins. Plant Physiol. 132: 1623-1630.
6. 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.
7. Blakeslee, J.J., et al. (2007). Interactions among PIN-FORMED and P-glycoprotein auxin transporters in Arabidopsis. Plant Cell 19: 131-147.
8. Blancaflor, E.B. (2013). Regulation of plant gravity sensing and signaling by the actin cytoskeleton. Am. J. Bot. 100: 143-152.
9. Bandyopadhyay, A., et al. (2007). Interactions of PIN and PGP auxin transport mechanisms. Biochem. Soc. Trans. 35: 137-141.
10. 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.
11. Dammann, C., Ichida, A., Hong, B., Romanowsky, S.M., Hrabak, E.M., Harmon, A.C., Pickard, B.G., and Harper, J.F. (2003). Subcellular targeting of nine calcium-dependent protein kinase isoforms from Arabidopsis. Plant Physiol. 132: 1840-1848.
12. Dhonukshe, P., Huang, F., Galvan-Ampudia, C.S., Mähönen, A.P., Kleine-Vehn, J., Xu, J., Quint, A., Prasad, K., Friml, J., Scheres, B., and Offringa, R. (2010). Plasma membrane-bound AGC3 kinases phosphorylate PIN auxin carriers at TPRXS(N/S) motifs to direct apical PIN recycling. Development 137: 3245-3255.
13. Dhonukshe, P., et al. (2008). Generation of cell polarity in plants links endocytosis, auxin distribution and cell fate decisions. Nature 456: 962-966.
14. Ding, Z., Galván-Ampudia, C.S., Demarsy, E., Łangowski, 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.
15. Ditengou, F.A., Teale, W.D., Kochersperger, P., Flittner, K.A., Kneuper, I., van der Graaff, E., Nziengui, H., Pinosa, F., Li, X., Nitschke, R., Laux, T., and Palme, K. (2008). Mechanical induction of lateral root initiation in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 105: 18818-18823.
16. Du, W., Wang, Y., Liang, S., and And Lu, Y.-T. (2005). Biochemical and expression analysis of an Arabidopsis calcium-dependent protein kinase-related kinase. Plant Sci. 168: 1181-1192.
17. Estelle, M. (1996). Plant tropisms: The ins and outs of auxin. Curr. Biol. 6: 1589-1591.
18. Feiz, L., Irshad, M., Pont-Lezica, R.F., Canut, H., and Jamet, E. (2006). Evaluation of cell wall preparations for proteomics: A new procedure for purifying cell walls from Arabidopsis hypocotyls. Plant Methods 2: 10.
19. Friml, J. (2010). Subcellular trafficking of PIN auxin efflux carriers in auxin transport. Eur. J. Cell Biol. 89: 231-235.
20. Friml, J., Benková, E., Mayer, U., Palme, K., and Muster, G. (2003). Automated whole mount localisation techniques for plant seedlings. Plant J. 34: 115-124.
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.
22. Friml, J., et al. (2004). A PINOID-dependent binary switch in apical-basal PIN polar targeting directs auxin efflux. Science 306: 862-865.
23. Furumoto, T., Ogawa, N., Hata, S., and Izui, K. (1996). Plant calciumdependent protein kinase-related kinases (CRKs) do not require calcium for their activities. FEBS Lett. 396: 147-151.
24. Gallagher, S.R. (1992). GUS Protocols: Using the GUS Gene as a Reporter of Gene Expression. (London: Academic Press).
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.
26. Ganguly, A., Sasayama, D., and Cho, H.T. (2012). Regulation of the polarity of protein trafficking by phosphorylation. Mol. Cells 33: 423-430.
27. Geisler, M., et al. (2005). Cellular efflux of auxin catalyzed by the Arabidopsis MDR/PGP transporter AtPGP1. Plant J. 44: 179-194.
28. Grunewald, W., and Friml, J. (2010). The march of the PINs: Developmental plasticity by dynamic polar targeting in plant cells. EMBO J. 29: 2700-2714.
29. Harmon, A.C. (2003). Calcium-regulated protein kinases of plants. Gravit. Space Biol. Bull. 16: 83-90.
30. (2+) signals through plant protein kinases. Annu. Rev. Plant Biol. 55: 263-288.
31. Hegeman, A.D., Rodriguez, M., Han, B.W., Uno, Y., Phillips, G.N., Jr., Hrabak, E.M., Cushman, J.C., Harper, J.F., Harmon, A.C., and Sussman, M.R. (2006). A phyloproteomic characterization of in vitro autophosphorylation in calcium-dependent protein kinases. Proteomics 6: 3649-3664.
32. Henrichs, S., et al. (2012). Regulation of ABCB1/PGP1-catalysed auxin transport by linker phosphorylation. EMBO J. 31: 2965-2980.
33. Hrabak, E.M., et al. (2003). The Arabidopsis CDPK-SnRK superfamily of protein kinases. Plant Physiol. 132: 666-680.
34. Hua, W., Liang, S., and Lu, Y.T. (2003). A tobacco (Nicotiana tabacum) calmodulin-binding protein kinase, NtCBK2, is regulated differentially by calmodulin isoforms. Biochem. J. 376: 291-302.
35. Hua, W., Zhang, L., Liang, S., Jones, R.L., and Lu, Y.T. (2004). A tobacco calcium/calmodulin-binding protein kinase functions as a negative regulator of flowering. J. Biol. Chem. 279: 31483-31494.
36. Jeong, J.C., Shin, D., Lee, J., Kang, C.H., Baek, D., Cho, M.J., Kim, M.C., and Yun, D.J. (2007). Isolation and characterization of a novel calcium/calmodulin-dependent protein kinase, AtCK, from Arabidopsis. Mol. Cells 24: 276-282.
37. Kakar, K., Zhang, H., Scheres, B., and Dhonukshe, P. (2013). CLASP-mediated cortical microtubule organization guides PIN polarization axis. Nature 495: 529-533.
38. 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.
39. 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.
40. Kleine-Vehn, J., Langowski, L., Wisniewska, J., Dhonukshe, P., Brewer, P.B., and Friml, J. (2008a). Cellular and molecular requirements for polar PIN targeting and transcytosis in plants. Mol. Plant 1: 1056-1066.
41. Kleine-Vehn, J., Leitner, J., Zwiewka, M., Sauer, M., Abas, L., Luschnig, C., and Friml, J. (2008b). Differential degradation of PIN2 auxin efflux carrier by retromer-dependent vacuolar targeting. Proc. Natl. Acad. Sci. USA 105: 17812-17817.
42. Koncz, C., Dejong, F., Villacorta, N., Szakonyi, D., and Koncz, Z. (2012). The spliceosome-activating complex: Molecular mechanisms underlying the function of a pleiotropic regulator. Front. Plant Sci. 3: 9.
43. Koncz, C., Martini, N., Szabados, L., Hrouda, M., Bachmair, A., and Schell, J. (1994). Specialized vectors for gene tagging and expression studies. In Plant Molecular Biology Manual, S. Gelvin and B. Schilperoort, eds (Dordrecht-Boston-London: Kluwer Academic Publishers), pp. 1-22.
44. Kramer, E.M. (2004). PIN and AUX/LAX proteins: Their role in auxin accumulation. Trends Plant Sci. 9: 578-582.
45. (2+) transport. Trends Plant Sci. 18: 227-233.
46. Langhans, M., Ratajczak, R., Lützelschwab, M., Michalke, W., Wächter, R., Fischer-Schliebs, E., and Ullrich, C.I. (2001). Immunolocalization of plasma-membrane H+-ATPase and tonoplast-type pyrophosphatase in the plasma membrane of the sieve element-companion cell complex in the stem of Ricinus communis L. Planta 213: 11-19.
47. Langowski, L., Rúzicka, 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.
48. Leclercq, J., Ranty, B., Sanchez-Ballesta, M.T., Li, Z., Jones, B., Jauneau, A., Pech, J.C., Latché, A., Ranjeva, R., and Bouzayen, M. (2005). Molecular and biochemical characterization of LeCRK1, a ripening-associated tomato CDPK-related kinase. J. Exp. Bot. 56: 25-35.
49. Lewis, D.R., Miller, N.D., Splitt, B.L., Wu, G., and Spalding, E.P. (2007). Separating the roles of acropetal and basipetal auxin transport on gravitropism with mutations in two Arabidopsis multidrug resistance-like ABC transporter genes. Plant Cell 19: 1838-1850.
50. Lin, D., et al. (2012). A ROP GTPase-dependent auxin signaling pathway regulates the subcellular distribution of PIN2 in Arabidopsis roots. Curr. Biol. 22: 1319-1325.
51. Lindzen, E., and Choi, J.H. (1995). A carrot cDNA encoding an atypical protein kinase homologous to plant calcium-dependent protein kinases. Plant Mol. Biol. 28: 785-797.
52. Löfke, C., Luschnig, C., and Kleine-Vehn, J. (2013). Posttranslational modification and trafficking of PIN auxin efflux carriers. Mech. Dev. 130: 82-94.
53. Lu, Y.T., Hidaka, H., and Feldman, L.J. (1996). Characterization of a calcium/calmodulin-dependent protein kinase homolog from maize roots showing light-regulated gravitropism. Planta 199: 18-24.
54. Mano, Y., and Nemoto, K. (2012). The pathway of auxin biosynthesis in plants. J. Exp. Bot. 63: 2853-2872.
55. Mathur, J., and Koncz, C. (1998). Callus culture and regeneration. Methods Mol. Biol. 82: 31-34.
56. Mei, Y., Jia, W.J., Chu, Y.J., and Xue, H.W. (2012). Arabidopsis phosphatidylinositol monophosphate 5-kinase 2 is involved in root gravitropism through regulation of polar auxin transport by affecting the cycling of PIN proteins. Cell Res. 22: 581-597.
57. Michniewicz, M., et al. (2007). Antagonistic regulation of PIN phosphorylation by PP2A and PINOID directs auxin flux. Cell 130: 1044-1056.
58. Miwa, K., Takano, J., Omori, H., Seki, M., Shinozaki, K., and Fujiwara, T. (2007). Plants tolerant of high boron levels. Science 318: 1417.
59. Morita, M.T. (2010). Directional gravity sensing in gravitropism. Annu. Rev. Plant Biol. 61: 705-720.
60. Muraro, D., Byrne, H., King, J., and Bennett, M. (2013). The role of auxin and cytokinin signalling in specifying the root architecture of Arabidopsis thaliana. J. Theor. Biol. 317: 71-86.
61. 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 J. 17: 6903-6911.
62. Nagashima, A., Uehara, Y., and Sakai, T. (2008). The ABC subfamily B auxin transporter AtABCB19 is involved in the inhibitory effects of N-1-naphthyphthalamic acid on the phototropic and gravitropic responses of Arabidopsis hypocotyls. Plant Cell Physiol. 49: 1250-1255.
63. Nagawa, S., Xu, T., Lin, D., Dhonukshe, P., Zhang, X., Friml, J., Scheres, B., Fu, Y., and Yang, Z. (2012). ROP GTPase-dependent actin microfilaments promote PIN1 polarization by localized inhibition of clathrin-dependent endocytosis. PLoS Biol. 10: e1001299.
64. Németh, K., et al. (1998). Pleiotropic control of glucose and hormone responses by PRL1, a nuclear WD protein, in Arabidopsis. Genes Dev. 12: 3059-3073.
65. 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.
66. Rademacher, E.H., and Offringa, R. (2012). Evolutionary adaptations of plant AGC kinases: From light signaling to cell polarity regulation. Front. Plant Sci. 3: 250.
67. Rahman, A., Takahashi, M., Shibasaki, K., Wu, S., Inaba, T., Tsurumi, 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.
68. 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.
69. Rigó, G., Ayaydin, F., Szabados, L., Koncz, C., and Cséplo{double acute}, A. (2008). Suspension protoplasts as useful experimental tool to study localization of GFP-tagged proteins in Arabidopsis thaliana. Acta Biol. Szeged. 52: 59-61.
70. Ríos, G., et al. (2002). Rapid identification of Arabidopsis insertion mutants by non-radioactive detection of T-DNA tagged genes. Plant J. 32: 243-253.
71. Rojas-Pierce, M., Titapiwatanakun, B., Sohn, E.J., Fang, F., Larive, C.K., Blakeslee, J., Cheng, Y., Cutler, S.R., Peer, W.A., Murphy, A.S., and Raikhel, N.V. (2007). Arabidopsis P-glycoprotein19 participates in the inhibition of gravitropism by gravacin. Chem. Biol. 14: 1366-1376. Erratum. Chem. Biol. 15: 87.
72. Sinclair, W., and Trewavas, A.J. (1997). Calcium in gravitropism. A re-examination. Planta 203 (suppl. 1): S85-S90.
73. 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.
74. 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.
75. 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.
76. Terasaka, K., Blakeslee, J.J., Titapiwatanakun, B., Peer, W.A., Bandyopadhyay, A., Makam, S.N., Lee, O.R., Richards, E.L., Murphy, A.S., Sato, F., and Yazaki, K. (2005). PGP4, an ATP binding cassette P-glycoprotein, catalyzes auxin transport in Arabidopsis thaliana roots. Plant Cell 17: 2922-2939.
77. Titapiwatanakun, B., et al. (2009). ABCB19/PGP19 stabilises PIN1 in membrane microdomains in Arabidopsis. Plant J. 57: 27-44.
78. Titapiwatanakun, B., and Murphy, A.S. (2009). Post-transcriptional regulation of auxin transport proteins: cellular trafficking, protein phosphorylation, protein maturation, ubiquitination, and membrane composition. J. Exp. Bot. 60: 1093-1107.
79. Verbelen, J.P., De Cnodder, T., Le, J., Vissenberg, K., and Baluska, F. (2006). The root apex of Arabidopsis thaliana consists of four distinct zones of growth activities: Meristematic zone, transition zone, fast elongation zone and growth terminating zone. Plant Signal. Behav. 1: 296-304.
80. Vieten, A., Vanneste, S., Wisniewska, 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.
81. Wang, L., Liang, S., and Lu, Y.T. (2001). Characterization, physical location and expression of the genes encoding calcium/calmodulindependent protein kinases in maize (Zea mays L.). Planta 213: 556-564.
82. 2+-dependent-protein-kinase-related protein kinase, AtCRK1, from Arabidopsis. Biochem. J. 383: 73-81.
83. Wang, Y., Zhang, M., Ke, K., and Lu, Y.T. (2005). Cellular localization and biochemical characterization of a novel calcium-dependent protein kinase from tobacco. Cell Res. 15: 604-612.
84. Went, F.W. (1974). Reflections and speculations. Annu. Rev. Plant Physiol. 25: 1-26.
85. Wu, G., Lewis, D.R., and Spalding, E.P. (2007). Mutations in Arabidopsis multidrug resistance-like ABC transporters separate the roles of acropetal and basipetal auxin transport in lateral root development. Plant Cell 19: 1826-1837.
86. Xu, J., and Scheres, B. (2005). Dissection of Arabidopsis ADPRIBOSYLATION FACTOR 1 function in epidermal cell polarity. Plant Cell 17: 525-536.
87. Zádníková, P., et al. (2010). Role of PIN-mediated auxin efflux in apical hook development of Arabidopsis thaliana. Development 137: 607-617.
88. Zegzouti, H., Anthony, R.G., Jahchan, N., Bögre, L., and Christensen, S.K. (2006). 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.
89. Zhang, J., Nodzynski, T., Pencík, A., Rolcík, 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.
90. 2+ signaling modulates auxin transport and PIN polarity. Dev. Cell 20: 855-866.
91. Zhang, L., Liu, B.F., Liang, S., Jones, R.L., and Lu, Y.T. (2002). Molecular and biochemical characterization of a calcium/calmodulin-binding protein kinase from rice. Biochem. J. 368: 145-157.
92. Zhang, L., and Lu, Y.T. (2003). Calmodulin-binding protein kinases in plants. Trends Plant Sci. 8: 123-127.