Type B phosphatidylinositol-4-phosphate 5-kinases mediate Arabidopsis and Nicotiana tabacum pollen tube growth by regulating apical pectin secretion

Plant Cell

Volumn 20, Issue 12, 2008, Pages 3312-3330

  Ischebeck, Till ^a   Stenzel, Irene ^a   Heilmann, Ingo ^a  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; NICOTIANA TABACUM;

EID: 61649088270     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.108.059568     Document Type: Article

References (99)

1. Balla, T. (2006). Phosphoinositide-derived messengers in endocrine signaling. J. Endocrinol. 188: 135-153.
2. Balla, T., Bondeva, T., and Varnai, P. (2000). How accurately can we image inositol lipids in living cells? Trends Pharmacol. Sci. 21: 238-241.
3. Balla, T., and Varnai, P. (2002). Visualizing cellular phosphoinositide pools with GFP-fused protein-modules. Sci. STKE 2002: PL3.
4. Berridge, M.J. (1983). Rapid accumulation of inositol trisphosphate reveals that agonists hydrolyse polyphosphoinositides instead of phosphatidylinositol. Biochem. J. 212: 849-858.
5. Boavida, L.C., and McCormick, S. (2007). Temperature as a determinant factor for increased and reproducible in vitro pollen germination in Arabidopsis thaliana. Plant J. 52: 570-582.
6. Bordenave, M., Breton, C., Goldberg, R., Huet, J.C., Perez, S., and Pernollet, J.C. (1996). Pectinmethylesterase isoforms from Vigna radiata hypocotyl cell walls: Kinetic properties and molecular cloning of a cDNA encoding the most alkaline isoform. Plant Mol. Biol. 31: 1039-1049.
7. Bosch, M., and Hepler, P.K. (2005). Pectin methylesterases and pectin dynamics in pollen tubes. Plant Cell 17: 3219-3226.
8. Braun, M., Baluska, F., von Witsch, M., and Menzel, D. (1999). Redistribution of actin, profilin and phosphatidylinositol-4,5-bisphosphate in growing and maturing root hairs. Planta 209: 435-443.
9. Bustin, S.A. (2000). Absolute quantification of mRNA using real-time reverse transcription polymerase chain reaction assays. J. Mol. Endocrinol. 25: 169-193.
10. Cardenas, L., Lovy-Wheeler, A., Kunkel, J.G., and Hepler, P.K. (2008). Pollen tube growth oscillations and intracellular calcium levels are reversibly modulated by actin polymerization. Plant Physiol. 146: 1611-1621.
11. Catoire, L., Pierron, M., Morvan, C., du Penhoat, C.H., and Goldberg, R. (1998). Investigation of the action patterns of pectinmethylesterase isoforms through kinetic analyses and NMR spectroscopy. Implications in cell wall expansion. J. Biol. Chem. 273: 33150-33156.
12. Cheung, A.Y., and Wu, H.M. (2008). Structural and signaling networks for the polar cell growth machinery in pollen tubes. Annu. Rev. Plant Biol. 59: 547-572.
13. Cho, M.H., and Boss, W.F. (1995). Transmembrane signaling and phosphoinositides. Methods Cell Biol. 49: 543-554.
14. 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.
15. Cole, R.A., and Fowler, J.E. (2006). Polarized growth: Maintaining focus on the tip. Curr. Opin. Plant Biol. 9: 579-588.
16. Cole, R.A., Synek, L., Zarsky, 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: 2005-2018.
17. Cremona, O., and De Camilli, P. (2001). Phosphoinositides in membrane traffic at the synapse. J. Cell Sci. 114: 1041-1052.
18. Di Paolo, G., Moskowitz, H.S., Gipson, K., Wenk, M.R., Voronov, S., Obayashi, M., Flavell, R., Fitzsimonds, R.M., Ryan, T.A., and De Camilli, P. (2004). Impaired PtdIns(4,5)P2 synthesis in nerve terminals produces defects in synaptic vesicle trafficking. Nature 431: 415-422.
19. Doughman, R.L., Firestone, A.J., and Anderson, R.A. (2003). Phosphatidylinositol phosphate kinases put PI4,5P(2) in its place. J. Membr. Biol. 194: 77-89.
20. Dowd, P.E., Coursol, S., Skirpan, A.L., Kao, T.H., and Gilroy, S. (2006). Petunia phospholipase c1 is involved in pollen tube growth. Plant Cell 18: 1438-1453.
21. Drobak, B.K., Dewey, R.E., and Boss, W.F. (1999). Phosphoinositide kinases and the synthesis of polyphosphoinositides in higher plant cells. Int. Rev. Cytol. 189: 95-130.
22. Drobak, B.K., Watkins, P.A.C., Valenta, R., Dove, S.K., Lloyd, C.W., and Staiger, C.J. (1994). Inhibition of plant plasma membrane phosphoinositide phospholipase C by the actin-binding protein, profilin. Plant J. 6: 389-400.
23. Elge, S., Brearley, C., Xia, H.J., Kehr, J., Xue, H.W., and Mueller-Roeber, B. (2001). An Arabidopsis inositol phospholipid kinase strongly expressed in procambial cells: Synthesis of PtdIns(4,5)P2 and PtdIns(3,4,5)P3 in insect cells by 5-phosphorylation of precursors. Plant J. 26: 561-571.
24. Ercetin, M.E., and Gillaspy, G.E. (2004). Molecular characterization of an Arabidopsis gene encoding a phospholipid-specific inositol polyphosphate 5-phosphatase. Plant Physiol. 135: 938-946.
25. Ferguson, C., Teeri, T.T., Siika, A.M., Read, S.M., and Bacic, A. (1998). Location of cellulose and callose in pollen tubes and grains of Nicotiana tabacum. Planta 206: 452-460.
26. Franklin-Tong, V.E. (1999). Signaling and the modulation of pollen tube growth. Plant Cell 11: 727-738.
27. Fukumoto, T., Hayashi, N., and Sasamoto, H. (2005). Atomic force microscopy and laser confocal scanning microscopy analysis of callose fibers developed from protoplasts of embryogenic cells of a conifer. Planta 223: 40-45.
28. Gong, L.W., Di Paolo, G., Diaz, E., Cestra, G., Diaz, M.E., Lindau, M., De Camilli, P., and Toomre, D. (2005). Phosphatidylinositol phosphate kinase type I gamma regulates dynamics of large dense-core vesicle fusion. Proc. Natl. Acad. Sci. USA 102: 5204-5209.
29. Gu, Y., Fu, Y., Dowd, P., Li, S., Vernoud, V., Gilroy, S., and Yang, Z. (2005). A Rho family GTPase controls actin dynamics and tip growth via two counteracting downstream pathways in pollen tubes. J. Cell Biol. 169: 127-138.
30. Gubbels, M.J., Vaishnava, S., Boot, N., Dubremetz, J.F., and Striepen, B. (2006). A MORN-repeat protein is a dynamic component of the Toxoplasma gondii cell division apparatus. J. Cell Sci. 119: 2236-2245.
31. Hala, M., Cole, R., Synek, L., Drdova, E., Pecenkova, T., Nordheim, A., Lamkemeyer, T., Madlung, J., Hochholdinger, F., Fowler, J.E., and Zarsky, V. (2008). An exocyst complex functions in plant cell growth in Arabidopsis and tobacco. Plant Cell 20: 1330-1345.
32. 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.
33. 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.
34. Helling, D., Possart, A., Cottier, S., Klahre, U., and Kost, B. (2006). Pollen tube tip growth depends on plasma membrane polarization mediated by tobacco PLC3 activity and endocytic membrane recycling. Plant Cell 18: 3519-3534.
35. Hepler, P.K., Vidali, L., and Cheung, A.Y. (2001). Polarized cell growth in higher plants. Annu. Rev. Cell Dev. Biol. 17: 159-187.
36. Hornung, E., Krueger, C., Pernstich, C., Gipmans, M., Porzel, A., and Feussner, I. (2005). Production of (10E,12Z)-conjugated linoleic acid in yeast and tobacco seeds. Biochim. Biophys. Acta 1738: 105-114.
37. Im, Y.J., Perera, I.Y., Brglez, I., Davis, A.J., Stevenson-Paulik, J., Phillippy, B.Q., Johannes, E., Allen, N.S., and Boss, W.F. (2007). Increasing plasma membrane phosphatidylinositol(4,5)bisphosphate biosynthesis increases phosphoinositide metabolism in Nicotiana tabacum. Plant Cell 19: 1603-1616.
38. Ishihara, H., Shibasaki, Y., Kizuki, N., Wada, T., Yazaki, Y., Asano, T., and Oka, Y. (1998). Type I phosphatidylinositol-4-phosphate 5-kinases. Cloning of the third isoform and deletion/substitution analysis of members of this novel lipid kinase family. J. Biol. Chem. 273: 8741-8748.
39. Iwai, H., Hokura, A., Oishi, M., Chida, H., Ishii, T., Sakai, S., and Satoh, S. (2006). The gene responsible for borate cross-linking of pectin Rhamnogalacturonan-II is required for plant reproductive tissue development and fertilization. Proc. Natl. Acad. Sci. USA 103: 16592-16597.
40. Janke, C., Magiera, M.M., Rathfelder, N., Taxis, C., Reber, S., Maekawa, H., Moreno-Borchart, A., Doenges, G., Schwob, E., Schiebel, E., and Knop, M. (2004). A versatile toolbox for PCR-based tagging of yeast genes: New fluorescent proteins, more markers and promoter substitution cassettes. Yeast 21: 947-962.
41. Jefferson, R.A., Kavanagh, T.A., and Bevan, M.W. (1987). GUS fusions: Beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6: 3901-3907.
42. Jiang, L., Yang, S.L., Xie, L.F., Puah, C.S., Zhang, X.Q., Yang, W.C., Sundaresan, V., and Ye, D. (2005). VANGUARD1 encodes a pectin methylesterase that enhances pollen tube growth in the Arabidopsis style and transmitting tract. Plant Cell 17: 584-596.
43. Klahre, U., and Kost, B. (2006). Tobacco RhoGTPase ACTIVATING PROTEIN1 spatially restricts signaling of RAC/Rop to the apex of pollen tubes. Plant Cell 18: 3033-3046.
44. König, S., Hoffmann, M., Mosblech, A., and Heilmann, I. (2008a). Determination of content and fatty acid composition of unlabeled phosphoinositide species by thin layer chromatography and gas chromatography. Anal. Biochem. 378: 197-201.
45. König, S., Ischebeck, T., Lerche, J., Stenzel, I., and Heilmann, I. (2008b). Salt stress-induced association of phosphatidylinositol-4,5- bisphosphate with clathrin-coated vesicles in plants. Biochem. J. 415: 387-399.
46. König, S., Mosblech, A., and Heilmann, I. (2007). Stress-inducible and constitutive phosphoinositide pools have distinct fatty acid patterns in Arabidopsis thaliana. FASEB J. 21: 1958-1967.
47. Kost, B., Lemichez, E., Spielhofer, P., Hong, Y., Tolias, K., Carpenter, C., and Chua, N.H. (1999). Rac homologues and compartmentalized phosphatidylinositol 4, 5-bisphosphate act in a common pathway to regulate polar pollen tube growth. J. Cell Biol. 145: 317-330.
48. Kost, B., Spielhofer, P., and Chua, N.H. (1998). A GFP-mouse talin fusion protein labels plant actin filaments in vivo and visualizes the actin cytoskeleton in growing pollen tubes. Plant J. 16: 393-401.
49. Krichevsky, A., Kozlovsky, S.V., Tian, G.W., Chen, M.H., Zaltsman, A., and Citovsky, V. (2007). How pollen tubes grow. Dev. Biol. 303: 405-420.
50. Krinke, O., Ruelland, E., Valentova, O., Vergnolle, C., Renou, J.P., Taconnat, L., Flemr, M., Burketova, L., and Zachowski, A. (2007). Phosphatidylinositol 4-kinase activation is an early response to salicylic acid in Arabidopsis suspension cells. Plant Physiol. 144: 1347-1359.
51. Kunz, J., Wilson, M.P., Kisseleva, M., Hurley, J.H., Majerus, P.W., and Anderson, R.A. (2000). The activation loop of phosphatidylinositol phosphate kinases determines signaling specificity. Mol. Cell 5: 1-11.
52. Kusano, H., Testerink, C., Vermeer, J.E.M., Tsuge, T., Shimada, H., Oka, A., Munnik, T., and Aoyama, T. (2008). The Arabidopsis phosphatidylinositol phosphate 5-kinase PIP5K3 is a key regulator of root hair tip growth. Plant Cell 20: 367-380.
53. Lee, Y., Kim, Y.W., Jeon, B.W., Park, K.Y., Suh, S.J., Seo, J., Kwak, J.M., Martinoia, E., and Hwang, I. (2007). Phosphatidylinositol 4,5-bisphosphate is important for stomatal opening. Plant J. 52: 803-816.
54. Lee, Y.J., Szumlanski, A., Nielsen, E., and Yang, Z. (2008). Rho-GTPase-dependent filamentous actin dynamics coordinate vesicle targeting and exocytosis during tip growth. J. Cell Biol. 181: 1155-1168.
55. Lemmon, M.A., Ferguson, K.M., and Abrams, C.S. (2002). Pleckstrin homology domains and the cytoskeleton. FEBS Lett. 513: 71-76.
56. Li, H., Bacic, A., and Read, S.M. (1999). Role of a callose synthase zymogen in regulating wall deposition in pollen tubes of Nicotiana alata. Planta 208: 528-538.
57. Liu, J., Zuo, X., Yue, P., and Guo, W. (2007). Phosphatidylinositol 4,5-bisphosphate mediates the targeting of the exocyst to the plasma membrane for exocytosis in mammalian cells. Mol. Biol. Cell 18: 4483-4492.
58. Lovy-Wheeler, A., Wilsen, K.L., Baskin, T.I., and Hepler, P.K. (2005). Enhanced fixation reveals the apical cortical fringe of actin filaments as a consistent feature of the pollen tube. Planta 221: 95-104.
59. Maple, J., Vojta, L., Soll, J., and Moller, S.G. (2007). ARC3 is a stromal Z-ring accessory protein essential for plastid division. EMBO Rep. 8: 293-299.
60. Meijer, H.J., and Munnik, T. (2003). Phospholipid-based signaling in plants. Annu. Rev. Plant Biol. 54: 265-306.
61. Milosevic, I., Sorensen, J.B., Lang, T., Krauss, M., Nagy, G., Haucke, V., Jahn, R., and Neher, E. (2005). Plasmalemmal phosphatidylinositol-4,5- bisphosphate level regulates the releasable vesicle pool size in chromaffin cells. J. Neurosci. 25: 2557-2565.
62. Monteiro, D., Castanho Coelho, P., Rodrigues, C., Camacho, L., Quader, H., and Malho, R. (2005). Modulation of endocytosis in pollen tube growth by phosphoinositides and phospholipids. Protoplasma 226: 31-38.
63. Moscatelli, A., Ciampolini, F., Rodighiero, S., Onelli, E., Cresti, M., Santo, N., and Idilli, A. (2007). Distinct endocytic pathways identified in tobacco pollen tubes using charged nanogold. J. Cell Sci. 120: 3804-3819.
64. Moustacas, A.M., Nari, J., Borel, M., Noat, G., and Ricard, J. (1991). Pectin methylesterase, metal ions and plant cell-wall extension. The role of metal ions in plant cell-wall extension. Biochem. J. 279: 351-354.
65. Mueller-Roeber, B., and Pical, C. (2002). Inositol phospholipid metabolism in Arabidopsis. Characterized and putative isoforms of inositol phospholipid kinase and phosphoinositide-specific phospholipase C. Plant Physiol. 130: 22-46.
66. O'Brien, T.P., Feder, N., and McCully, M.E. (1964). Polychromatic staining of plant cell walls by toluidine blue O. Protoplasma 59: 368-373.
67. Parton, R.M., Fischer-Parton, S., Watahiki, M.K., and Trewavas, A.J. (2001). Dynamics of the apical vesicle accumulation and the rate of growth are related in individual pollen tubes. J. Cell Sci. 114: 2685-2695.
68. Perera, I.Y., Davis, A.J., Galanopoulou, D., Im, Y.J., and Boss, W.F. (2005). Characterization and comparative analysis of Arabidopsis phosphatidylinositol phosphate 5-kinase 10 reveals differences in Arabidopsis and human phosphatidylinositol phosphate kinases. FEBS Lett. 579: 3427-3432.
69. Perera, I.Y., Love, J., Heilmann, I., Thompson, W.F., and Boss, W.F. (2002). Up-regulation of phosphoinositide metabolism in tobacco cells constitutively expressing the human type I inositol polyphosphate 5-phosphatase. Plant Physiol. 129: 1795-1806.
70. Picton, J.M., and Steer, M.W. (1983). Membrane recycling and the control of secretory activity in pollen tubes. J. Cell Sci. 63: 303-310.
71. Preuss, M.L., Schmitz, A.J., Thole, J.M., Bonner, H.K., Otegui, M.S., and Nielsen, E. (2006). A role for the RabA4b effector protein PI-4Kbeta1 in polarized expansion of root hair cells in Arabidopsis thaliana. J. Cell Biol. 172: 991-998.
72. Preuss, M.L., Serna, J., Falbel, T.G., Bednarek, S.Y., and Nielsen, E. (2004). The Arabidopsis Rab GTPase RabA4b localizes to the tips of growing root hair cells. Plant Cell 16: 1589-1603.
73. Rao, V.D., Misra, S., Boronenkov, I.V., Anderson, R.A., and Hurley, J.H. (1998). Structure of type IIbeta phosphatidylinositol phosphate kinase: a protein kinase fold flattened for interfacial phosphorylation. Cell 94: 829-839.
74. Read, S.M., Clarke, A.E., and Bacic, A. (1993). Stimulation of growth of cultured Nicotiana tabacum W 38 pollen tubes by poly(ethylene glycol) and Cu(II) salts. Protoplasma 177: 1-14.
75. Ren, C., and Kermode, A.R. (2000). An increase in pectin methyl esterase activity accompanies dormancy breakage and germination of yellow cedar seeds. Plant Physiol. 124: 231-242.
76. Ryan, E., Steer, M., and Dolan, L. (2001). Cell biology and genetics of root hair formation in Arabidopsis thaliana. Protoplasma 215: 140-149.
77. Santarius, M., Lee, C.H., and Anderson, R.A. (2006). Supervised membrane swimming: Small G-protein lifeguards regulate PIPK signalling and monitor intracellular PtdIns(4,5)P2 pools. Biochem. J. 398: 1-13.
78. Song, X.F., Yang, C.Y., Liu, J., and Yang, W.C. (2006). RPA, a class II ARFGAP protein, activates ARF1 and U5 and plays a role in root hair development in Arabidopsis. Plant Physiol. 141: 966-976.
79. Steer, M.W., and Steer, J.M. (1989). Pollen tube tip growth. New Phytol. 111: 323-358.
80. Stenzel, I., Ischebeck, T., König, S., Holubowska, A., Sporysz, M., Hause, B., and Heilmann, I. (2008). The type B phosphatidylinositol-4- phosphate 5-kinase 3 is essential for root hair formation in Arabidopsis thaliana. Plant Cell 20: 124-141.
81. Sugita, S. (2008). Mechanisms of exocytosis. Acta Physiol. (Oxf.) 192: 185-193.
82. Synek, L., Schlager, N., Elias, M., Quentin, M., Hauser, M.T., and Zarsky, 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.
83. Takeshima, H., Komazaki, S., Nishi, M., Iino, M., and Kangawa, K. (2000). Junctophilins: A novel family of junctional membrane complex proteins. Mol. Cell 6: 11-22.
84. Taylor, L.P., and Hepler, P.K. (1997). Pollen germination and tube growth. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48: 461-491.
85. Tian, G.W., Chen, M.H., Zaltsman, A., and Citovsky, V. (2006). Pollen-specific pectin methylesterase involved in pollen tube growth. Dev. Biol. 294: 83-91.
86. Twell, D., Yamaguchi, J., and McCormick, S. (1990). Pollen-specific gene expression in transgenic plants: Coordinate regulation of two different tomato gene promoters during microsporogenesis. Development 109: 705-713.
87. Varnai, P., and Balla, T. (1998). Visualization of phosphoinositides that bind pleckstrin homology domains: Calcium- and agonist-induced dynamic changes and relationship to myo-[3H]inositol-labeled phosphoinositide pools. J. Cell Biol. 143: 501-510.
88. Vicogne, J., Vollenweider, D., Smith, J.R., Huang, P., Frohman, M.A., and Pessin, J.E. (2006). Asymmetric phospholipid distribution drives in vitro reconstituted SNARE-dependent membrane fusion. Proc. Natl. Acad. Sci. USA 103: 14761-14766.
89. Vidali, L., and Hepler, P.K. (2001). Actin and pollen tube growth. Protoplasma 215: 64-76.
90. Vincent, P., Chua, M., Nogue, F., Fairbrother, A., Mekeel, H., Xu, Y., Allen, N., Bibikova, T.N., Gilroy, S., and Bankaitis, V.A. (2005). A Sec14p-nodulin domain phosphatidylinositol transfer protein polarizes membrane growth of Arabidopsis thaliana root hairs. J. Cell Biol. 168: 801-812.
91. 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.
92. Wasteneys, G.O., and Galway, M.E. (2003). Remodeling the cytoskeleton for growth and form: An overview with some new views. Annu. Rev. Plant Biol. 54: 691-722.
93. Wen, F., Zhu, Y., and Hawes, M.C. (1999). Effect of pectin methylesterase gene expression on pea root development. Plant Cell 11: 1129-1140.
94. 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.
95. Wenk, M.R., and De Camilli, P. (2004). Protein-lipid interactions and phosphoinositide metabolism in membrane traffic: Insights from vesicle recycling in nerve terminals. Proc. Natl. Acad. Sci. USA 101: 8262-8269.
96. Yin, H.L., and Janmey, P.A. (2003). Phosphoinositide regulation of the actin cytoskeleton. Annu. Rev. Physiol. 65: 761-789.
97. Yuen, C.Y., Sedbrook, J.C., Perrin, R.M., Carroll, K.L., and Masson, P.H. (2005). Loss-of-function mutations of ROOT HAIR DEFECTIVE3 suppress root waving, skewing, and epidermal cell file rotation in Arabidopsis. Plant Physiol. 138: 701-714.
98. Zimmermann, P., Hirsch-Hoffmann, M., Hennig, L., and Gruissem, W. (2004). GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol. 136: 2621-2632.
99. Zonia, L., and Munnik, T. (2008). Vesicle trafficking dynamics and visualization of zones of exocytosis and endocytosis in tobacco pollen tubes. J. Exp. Bot. 59: 861-873.