This Article Full Text Full Text (PDF) Supplemental Data All Versions of this Article: 18/12/3519    most recent tpc.106.047373v1 Alert me when this article is cited Alert me if a correction is posted Services Email this article to a friend Similar articles in this journal Similar articles in ISI Web of Science Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via CrossRef Citing Articles via ISI Web of Science (34) Citing Articles via Google Scholar Google Scholar Articles by Helling, D. Articles by Kost, B. Search for Related Content PubMed PubMed Citation Articles by Helling, D. Articles by Kost, B. Agricola Articles by Helling, D. Articles by Kost, B.

Pollen Tube Tip Growth Depends on Plasma Membrane Polarization Mediated by Tobacco PLC3 Activity and Endocytic Membrane Recycling^[W]

Heidelberg Institute of Plant Sciences, University of Heidelberg, 69120 Heidelberg, Germany

¹ To whom correspondence should be addressed. E-mail bkost{at}hip.uni-hd.de; fax 49-6221-54-5859.

Phosphatidyl inositol 4,5-bisphosphate (PI 4,5-P₂) accumulates in a Rac/Rop-dependent manner in the pollen tube tip plasma membrane, where it may control actin organization and membrane traffic. PI 4,5-P₂ is hydrolyzed by phospholipase C (PLC) activity to the signaling molecules inositol 1,4,5-trisphosphate and diacyl glycerol (DAG). To investigate PLC activity during tip growth, we cloned Nt PLC3, specifically expressed in tobacco (Nicotiana tabacum) pollen tubes. Recombinant Nt PLC3 displayed Ca²⁺-dependent PI 4,5-P₂–hydrolyzing activity sensitive to U-73122 and to mutations in the active site. Nt PLC3 overexpression, but not that of inactive mutants, inhibited pollen tube growth. Yellow fluorescent protein (YFP) fused to Nt PLC3, or to its EF and C2 domains, accumulated laterally at the pollen tube tip plasma membrane in a pattern complementary to the distribution of PI 4,5-P₂. The DAG marker Cys1:YFP displayed a similar intracellular localization as PI 4,5-P₂. Blocking endocytic membrane recycling affected the intracellular distribution of DAG but not of PI 4,5-P₂. U-73122 at low micromolar concentrations inhibited and partially depolarized pollen tube growth, caused PI 4,5-P₂ spreading at the apex, and abolished DAG membrane accumulation. We show that Nt PLC3 is targeted by its EF and C2 domains to the plasma membrane laterally at the pollen tube tip and that it maintains, together with endocytic membrane recycling, an apical domain enriched in PI 4,5-P₂ and DAG required for polar cell growth.

This article has been cited by other articles:

				L. Li, N. Saga, and K. Mikami Ca2+ influx and phosphoinositide signalling are essential for the establishment and maintenance of cell polarity in monospores from the red alga Porphyra yezoensis J. Exp. Bot., June 16, 2009; (2009) erp183v1. [Abstract] [Full Text] [PDF]

				T. Munnik and C. Testerink Plant phospholipid signaling: "in a nutshell" J. Lipid Res., April 1, 2009; 50(Supplement): S260 - S265. [Abstract] [Full Text] [PDF]

				G. Cai and M. Cresti Organelle motility in the pollen tube: a tale of 20 years J. Exp. Bot., February 1, 2009; 60(2): 495 - 508. [Abstract] [Full Text] [PDF]

				X. Ma, O. Shor, S. Diminshtein, L. Yu, Y. J. Im, I. Perera, A. Lomax, W. F. Boss, and N. Moran Phosphatidylinositol (4,5)Bisphosphate Inhibits K+-Efflux Channel Activity in NT1 Tobacco Cultured Cells Plant Physiology, February 1, 2009; 149(2): 1127 - 1140. [Abstract] [Full Text] [PDF]

				T. Ischebeck, I. Stenzel, and I. Heilmann Type B Phosphatidylinositol-4-Phosphate 5-Kinases Mediate Arabidopsis and Nicotiana tabacum Pollen Tube Growth by Regulating Apical Pectin Secretion PLANT CELL, December 1, 2008; 20(12): 3312 - 3330. [Abstract] [Full Text] [PDF]

				J. Dyachok, M.-R. Shao, K. Vaughn, A. Bowling, M. Facette, S. Djakovic, L. Clark, and L. Smith Plasma Membrane-Associated SCAR Complex Subunits Promote Cortical F-Actin Accumulation and Normal Growth Characteristics in Arabidopsis Roots Mol Plant, November 1, 2008; 1(6): 990 - 1006. [Abstract] [Full Text] [PDF]

				S. Li, Y. Gu, A. Yan, E. Lord, and Z.-B. Yang RIP1 (ROP Interactive Partner 1)/ICR1 Marks Pollen Germination Sites and May Act in the ROP1 Pathway in the Control of Polarized Pollen Growth Mol Plant, November 1, 2008; 1(6): 1021 - 1035. [Abstract] [Full Text] [PDF]

				E. Sousa, B. Kost, and R. Malho Arabidopsis Phosphatidylinositol-4-Monophosphate 5-Kinase 4 Regulates Pollen Tube Growth and Polarity by Modulating Membrane Recycling PLANT CELL, November 1, 2008; 20(11): 3050 - 3064. [Abstract] [Full Text] [PDF]

				L. Li, N. Saga, and K. Mikami Phosphatidylinositol 3-kinase activity and asymmetrical accumulation of F-actin are necessary for establishment of cell polarity in the early development of monospores from the marine red alga Porphyra yezoensis J. Exp. Bot., October 1, 2008; 59(13): 3575 - 3586. [Abstract] [Full Text] [PDF]

				S. Yalovsky, D. Bloch, N. Sorek, and B. Kost Regulation of Membrane Trafficking, Cytoskeleton Dynamics, and Cell Polarity by ROP/RAC GTPases Plant Physiology, August 1, 2008; 147(4): 1527 - 1543. [Full Text] [PDF]

				H.-J. Wang, A.-R. Wan, and G.-Y. Jauh An Actin-Binding Protein, LlLIM1, Mediates Calcium and Hydrogen Regulation of Actin Dynamics in Pollen Tubes Plant Physiology, August 1, 2008; 147(4): 1619 - 1636. [Abstract] [Full Text] [PDF]

				L. Cardenas, A. Lovy-Wheeler, J. G. Kunkel, and P. K. Hepler Pollen Tube Growth Oscillations and Intracellular Calcium Levels Are Reversibly Modulated by Actin Polymerization Plant Physiology, April 1, 2008; 146(4): 1611 - 1621. [Abstract] [Full Text] [PDF]

				J. M. Thole, J. E.M. Vermeer, Y. Zhang, T. W.J. Gadella Jr., and E. Nielsen ROOT HAIR DEFECTIVE4 Encodes a Phosphatidylinositol-4-Phosphate Phosphatase Required for Proper Root Hair Development in Arabidopsis thaliana PLANT CELL, February 1, 2008; 20(2): 381 - 395. [Abstract] [Full Text] [PDF]

				H. Kusano, C. Testerink, J. E.M. Vermeer, T. Tsuge, H. Shimada, A. Oka, T. Munnik, and T. Aoyama The Arabidopsis Phosphatidylinositol Phosphate 5-Kinase PIP5K3 Is a Key Regulator of Root Hair Tip Growth PLANT CELL, February 1, 2008; 20(2): 367 - 380. [Abstract] [Full Text] [PDF]

				I. Stenzel, T. Ischebeck, S. Konig, A. Holubowska, M. Sporysz, B. Hause, and I. Heilmann The Type B Phosphatidylinositol-4-Phosphate 5-Kinase 3 Is Essential for Root Hair Formation in Arabidopsis thaliana PLANT CELL, January 1, 2008; 20(1): 124 - 141. [Abstract] [Full Text] [PDF]

				A. Moscatelli, F. Ciampolini, S. Rodighiero, E. Onelli, M. Cresti, N. Santo, and A. Idilli Distinct endocytic pathways identified in tobacco pollen tubes using charged nanogold J. Cell Sci., November 1, 2007; 120(21): 3804 - 3819. [Abstract] [Full Text] [PDF]

				A. J. Davis, Y. J. Im, J. S. Dubin, K. B. Tomer, and W. F. Boss Arabidopsis Phosphatidylinositol Phosphate Kinase 1 Binds F-actin and Recruits Phosphatidylinositol 4-Kinase beta1 to the Actin Cytoskeleton J. Biol. Chem., May 11, 2007; 282(19): 14121 - 14131. [Abstract] [Full Text] [PDF]

				Y. J. Im, I. Y. Perera, I. Brglez, A. J. Davis, J. Stevenson-Paulik, B. Q. Phillippy, E. Johannes, N. S. Allen, and W. F. Boss Increasing Plasma Membrane Phosphatidylinositol(4,5)Bisphosphate Biosynthesis Increases Phosphoinositide Metabolism in Nicotiana tabacum PLANT CELL, May 1, 2007; 19(5): 1603 - 1616. [Abstract] [Full Text] [PDF]