A Role for the RabA4b Effector Protein PI-4Kbeta1 in Polarized Expansion of Root Hair Cells in Arabidopsis Thaliana

Overview

Journal J Cell Biol

Specialty Cell Biology

Date 2006 Mar 29

PMID 16567499

Citations 117

Authors

Mary L Preuss

Aaron J Schmitz

Julie M Thole

Heather K S Bonner

Marisa S Otegui

Erik Nielsen

Affiliations

Soon will be listed here.

Abstract

The RabA4b GTPase labels a novel, trans-Golgi network compartment displaying a developmentally regulated polar distribution in growing Arabidopsis thaliana root hair cells. GTP bound RabA4b selectively recruits the plant phosphatidylinositol 4-OH kinase, PI-4Kbeta1, but not members of other PI-4K families. PI-4Kbeta1 colocalizes with RabA4b on tip-localized membranes in growing root hairs, and mutant plants in which both the PI-4Kbeta1 and -4Kbeta2 genes are disrupted display aberrant root hair morphologies. PI-4Kbeta1 interacts with RabA4b through a novel homology domain, specific to eukaryotic type IIIbeta PI-4Ks, and PI-4Kbeta1 also interacts with a Ca2+ sensor, AtCBL1, through its NH2 terminus. We propose that RabA4b recruitment of PI-4Kbeta1 results in Ca2+-dependent generation of PI-4P on this compartment, providing a link between Ca2+ and PI-4,5P2-dependent signals during the polarized secretion of cell wall components in tip-growing root hair cells.

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References

Bubb M, Baines I, Korn E . Localization of actobindin, profilin I, profilin II, and phosphatidylinositol-4,5-bisphosphate (PIP2) in Acanthamoeba castellanii. Cell Motil Cytoskeleton. 1998; 39(2):134-46. DOI: 10.1002/(SICI)1097-0169(1998)39:2<134::AID-CM4>3.0.CO;2-6. View

Zerial M, McBride H . Rab proteins as membrane organizers. Nat Rev Mol Cell Biol. 2001; 2(2):107-17. DOI: 10.1038/35052055. View

Wymer C, Bibikova T, Gilroy S . Cytoplasmic free calcium distributions during the development of root hairs of Arabidopsis thaliana. Plant J. 1997; 12(2):427-39. DOI: 10.1046/j.1365-313x.1997.12020427.x. View

Kim J, Harter K, Theologis A . Protein-protein interactions among the Aux/IAA proteins. Proc Natl Acad Sci U S A. 1997; 94(22):11786-91. PMC: 23574. DOI: 10.1073/pnas.94.22.11786. View

Hama H, Schnieders E, Thorner J, Takemoto J, Dewald D . Direct involvement of phosphatidylinositol 4-phosphate in secretion in the yeast Saccharomyces cerevisiae. J Biol Chem. 1999; 274(48):34294-300. DOI: 10.1074/jbc.274.48.34294. View

Balla T . Phosphatidylinositol 4-kinases. Biochim Biophys Acta. 1998; 1436(1-2):69-85. DOI: 10.1016/s0005-2760(98)00134-9. View

Bankaitis V, Morris A . Lipids and the exocytotic machinery of eukaryotic cells. Curr Opin Cell Biol. 2003; 15(4):389-95. DOI: 10.1016/s0955-0674(03)00076-0. View

Kudla J, Xu Q, Harter K, Gruissem W, Luan S . Genes for calcineurin B-like proteins in Arabidopsis are differentially regulated by stress signals. Proc Natl Acad Sci U S A. 1999; 96(8):4718-23. PMC: 16398. DOI: 10.1073/pnas.96.8.4718. View

Taylor L, Hepler P . POLLEN GERMINATION AND TUBE GROWTH. Annu Rev Plant Physiol Plant Mol Biol. 1997; 48:461-491. DOI: 10.1146/annurev.arplant.48.1.461. View

10.

de Graaf P, Zwart W, van Dijken R, Deneka M, Schulz T, Geijsen N . Phosphatidylinositol 4-kinasebeta is critical for functional association of rab11 with the Golgi complex. Mol Biol Cell. 2004; 15(4):2038-47. PMC: 379297. DOI: 10.1091/mbc.e03-12-0862. View

11.

Stevenson-Paulik J, Love J, Boss W . Differential regulation of two Arabidopsis type III phosphatidylinositol 4-kinase isoforms. A regulatory role for the pleckstrin homology domain. Plant Physiol. 2003; 132(2):1053-64. PMC: 167043. DOI: 10.1104/pp.103.021758. View

12.

Yanagisawa L, Marchena J, Xie Z, Li X, Poon P, Singer R . Activity of specific lipid-regulated ADP ribosylation factor-GTPase-activating proteins is required for Sec14p-dependent Golgi secretory function in yeast. Mol Biol Cell. 2002; 13(7):2193-206. PMC: 117305. DOI: 10.1091/mbc.01-11-0563.. View

13.

Kost B, Lemichez E, Spielhofer P, Hong Y, Tolias K, Carpenter C . Rac homologues and compartmentalized phosphatidylinositol 4, 5-bisphosphate act in a common pathway to regulate polar pollen tube growth. J Cell Biol. 1999; 145(2):317-30. PMC: 2133117. DOI: 10.1083/jcb.145.2.317. View

14.

Christoforidis S, Miaczynska M, Ashman K, Wilm M, Zhao L, Yip S . Phosphatidylinositol-3-OH kinases are Rab5 effectors. Nat Cell Biol. 1999; 1(4):249-52. DOI: 10.1038/12075. View

15.

Hama H, Takemoto J, Dewald D . Analysis of phosphoinositides in protein trafficking. Methods. 2000; 20(4):465-73. DOI: 10.1006/meth.2000.0959. View

16.

Olsen H, Hoy M, Zhang W, Bertorello A, Bokvist K, Capito K . Phosphatidylinositol 4-kinase serves as a metabolic sensor and regulates priming of secretory granules in pancreatic beta cells. Proc Natl Acad Sci U S A. 2003; 100(9):5187-92. PMC: 154320. DOI: 10.1073/pnas.0931282100. View

17.

Novick P, Brennwald P . Friends and family: the role of the Rab GTPases in vesicular traffic. Cell. 1993; 75(4):597-601. DOI: 10.1016/0092-8674(93)90478-9. View

18.

Levine T, Munro S . Targeting of Golgi-specific pleckstrin homology domains involves both PtdIns 4-kinase-dependent and -independent components. Curr Biol. 2002; 12(9):695-704. DOI: 10.1016/s0960-9822(02)00779-0. View

19.

Sciorra V, Audhya A, Parsons A, Segev N, Boone C, Emr S . Synthetic genetic array analysis of the PtdIns 4-kinase Pik1p identifies components in a Golgi-specific Ypt31/rab-GTPase signaling pathway. Mol Biol Cell. 2004; 16(2):776-93. PMC: 545911. DOI: 10.1091/mbc.e04-08-0700. View

20.

Preuss M, Serna J, Falbel T, Bednarek S, Nielsen E . The Arabidopsis Rab GTPase RabA4b localizes to the tips of growing root hair cells. Plant Cell. 2004; 16(6):1589-603. PMC: 490048. DOI: 10.1105/tpc.021634. View