Tip growth: signaling in the apical dome

Current Opinion in Plant Biology

Volumn 11, Issue 6, 2008, Pages 662-671

  Lee, Yong Jik ^a   Yang, Zhenbiao ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GUANOSINE TRIPHOSPHATASE; PHOSPHATIDYLINOSITOL; REACTIVE OXYGEN METABOLITE;

CYTOLOGY; ENZYMOLOGY; GROWTH, DEVELOPMENT AND AGING; MERISTEM; METABOLISM; PLANT; REVIEW; SIGNAL TRANSDUCTION;

GTP PHOSPHOHYDROLASES; MERISTEM; PHOSPHATIDYLINOSITOLS; PLANTS; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION;

EID: 56349141069     PISSN: 13695266     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbi.2008.10.002     Document Type: Review

References (64)

1. Dickson B.J. Rho GTPases in growth cone guidance. Curr Opin Neurobiol 11 (2001) 103-110
2. Momany M. Polarity in filamentous fungi: establishment, maintenance and new axes. Curr Opin Microbiol 5 (2002) 580-585
3. Yang Z. Signaling tip growth in plants. Curr Opin Plant Biol 1 (1998) 525-530
4. Cole R.A., and Fowler J.E. Polarized growth: maintaining focus on the tip. Curr Opin Plant Biol 9 (2006) 579-588
5. Kost B. Spatial control of Rho (Rac-Rop) signaling in tip-growing plant cells. Trends Cell Biol 18 (2008) 119-127
6. Krichevsky A., Kozlovsky S.V., Tian G.W., Chen M.H., Zaltsman A., and Citovsky V. How pollen tubes grow. Dev Biol 303 (2007) 405-420
7. Gu Y., Fu Y., Dowd P., Li S., Vernoud V., Gilroy S., and Yang Z. A Rho family GTPase controls actin dynamics and tip growth via two counteracting downstream pathways in pollen tubes. J Cell Biol 169 (2005) 127-138
8. Hwang J.U., Gu Y., Lee Y.J., and Yang Z. Oscillatory ROP GTPase activation leads the oscillatory polarized growth of pollen tubes. Mol Biol Cell 16 (2005) 5385-5399
9. Xiang Y., Huang X., Wang T., Zhang Y., Liu Q., Hussey P.J., and Ren H. ACTIN BINDING PROTEIN 29 from Lilium pollen plays an important role in dynamic actin remodeling. Plant Cell 19 (2007) 1930-1946. This paper presents data suggesting that calcium and PI4,5P2 play an important role in the regulation of ABP29 activity, which controls actin remodeling in pollen tube growth.
10. Lovy-Wheeler A., Wilsen K.L., Baskin T.I., and Hepler P.K. Enhanced fixation reveals the apical cortical fringe of actin filaments as a consistent feature of the pollen tube. Planta 221 (2005) 95-104
11. Jones M.A., Shen J.J., Fu Y., Li H., Yang Z., and Grierson C.S. The Arabidopsis Rop2 GTPase is a positive regulator of both root hair initiation and tip growth. Plant Cell 14 (2002) 763-776
12. Vidali L., McKenna S.T., and Hepler P.K. Actin polymerization is essential for pollen tube growth. Mol Biol Cell 12 (2001) 2534-2545
13. 2+ influx, which promotes the depolymerization of apical actin filaments, is required for exocytosis of vesicles to the apical PM. A new technique developed to quantify exocytosis in this paper, which was based on FRAP analysis of a GFP-tagged PM-targeted protein, should add an important tool for the study of tip growth in plants.
14. Voigt B., Timmers A.C., Samaj J., Hlavacka A., Ueda T., Preuss M., Nielsen E., Mathur J., Emans N., Stenmark H., et al. Actin-based motility of endosomes is linked to the polar tip growth of root hairs. Eur J Cell Biol 84 (2005) 609-621
15. Ketelaar T., de Ruijter N.C., and Emons A.M. Unstable F-actin specifies the area and microtubule direction of cell expansion in Arabidopsis root hairs. Plant Cell 15 (2003) 285-292
16. Yang G., Gao P., Zhang H., Huang S., and Zheng Z.L. A mutation in MRH2 kinesin enhances the root hair tip growth defect caused by constitutively activated ROP2 small GTPase in Arabidopsis. PLoS ONE 2 (2007) e1074. This report demonstrates armadillo domain-containing protein, MRH2, controls microtubule organization in root hair and provides evidence suggesting MRH2 is involved in the coordination of microtubule and actin filaments during tip growth.
17. Sakai T., Honing H., Nishioka M., Uehara Y., Takahashi M., Fujisawa N., Saji K., Seki M., Shinozaki K., Jones M.A., et al. Armadillo repeat-containing kinesins and a NIMA-related kinase are required for epidermal-cell morphogenesis in Arabidopsis. Plant J 53 (2008) 157-171
18. Muallem S., Kwiatkowska K., Xu X., and Yin H.L. Actin filament disassembly is a sufficient final trigger for exocytosis in nonexcitable cells. J Cell Biol 128 (1995) 589-598
19. Hsu S.C., TerBush D., Abraham M., and Guo W. The exocyst complex in polarized exocytosis. Int Rev Cytol 233 (2004) 243-265
20. Zajac A., Sun X., Zhang J., and Guo W. Cyclical regulation of the exocyst and cell polarity determinants for polarized cell growth. Mol Biol Cell 16 (2005) 1500-1512
21. Hala M., Cole R., Synek L., Drdova E., Pecenkova T., Nordheim A., Lamkemeyer T., Madlung J., Hochholdinger F., Fowler J.E., et al. An exocyst complex functions in plant cell growth in Arabidopsis and tobacco. Plant Cell 20 (2008) 1330-1345. An important and extensive study suggesting that plant homologs of exocyst subunits function together in vivo. This work demonstrates functional exocyst plays important roles in pollen tube growth and hypocotyl elongation.
22. Synek L., Schlager N., Elias M., Quentin M., Hauser M.T., and Zarsky V. 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 (2006) 54-72
23. Lavy M., Bloch D., Hazak O., Gutman I., Poraty L., Sorek N., Sternberg H., and Yalovsky S. A novel ROP/RAC effector links cell polarity, root-meristem maintenance, and vesicle trafficking. Curr Biol 17 (2007) 947-952
24. Yang Z., and Fu Y. ROP/RAC GTPase signaling. Curr Opin Plant Biol 10 (2007) 490-494
25. Marco E., Wedlich-Soldner R., Li R., Altschuler S.J., and Wu L.F. Endocytosis optimizes the dynamic localization of membrane proteins that regulate cortical polarity. Cell 129 (2007) 411-422. By measuring parameters from experiments, authors develop a mathematical model for the dynamic distribution of polarized proteins. The modeling suggests that endocytosis plays a pivotal role in determining a polarized cortical region whereas positive feedback loops are important for polarity maintenance in yeast cells.
26. Dhonukshe P., Aniento F., Hwang I., Robinson D.G., Mravec J., Stierhof Y.D., and Friml J. Clathrin-mediated constitutive endocytosis of PIN auxin efflux carriers in Arabidopsis. Curr Biol 17 (2007) 520-527
27. Robert S., Chary S.N., Drakakaki G., Li S., Yang Z., Raikhel N.V., and Hicks G.R. Endosidin1 defines a compartment involved in endocytosis of the brassinosteroid receptor BRI1 and the auxin transporters PIN2 and AUX1. Proc Natl Acad Sci U S A 105 (2008) 8464-8469
28. Li S, Gu Y, Yan A, Lord EM, Yang Z: RIP1 (ROP interactive partner 1)/ICR1 marks pollen germination sites and may act in the ROP1 pathway in the control of polarized pollen tube growth. Mol Plant 2008, doi:10.1093/mp/ssn051.
29. Moscatelli A., Ciampolini F., Rodighiero S., Onelli E., Cresti M., Santo N., and Idilli A. Distinct endocytic pathways identified in tobacco pollen tubes using charged nanogold. J Cell Sci 120 (2007) 3804-3819. This elegant study using charged nanogold particle and in vivo time-lapse experiments provides evidence that two distinct endocytic pathways exist at the specific regions of the pollen tube.
30. Zonia L., and Munnik T. Vesicle trafficking dynamics and visualization of zones of exocytosis and endocytosis in tobacco pollen tubes. J Exp Bot 59 (2008) 861-873
31. Lisboa S., Scherer G.E., and Quader H. Localized endocytosis in tobacco pollen tubes: visualisation and dynamics of membrane retrieval by a fluorescent phospholipid. Plant Cell Rep 27 (2008) 21-28
32. Berken A., Thomas C., and Wittinghofer A. A new family of RhoGEFs activates the Rop molecular switch in plants. Nature 436 (2005) 1176-1180
33. Gu Y., Li S., Lord E.M., and Yang Z. Members of a novel class of Arabidopsis Rho guanine nucleotide exchange factors control Rho GTPase-dependent polar growth. Plant Cell 18 (2006) 366-381
34. Zhang Y., and McCormick S. A distinct mechanism regulating a pollen-specific guanine nucleotide exchange factor for the small GTPase Rop in Arabidopsis thaliana. Proc Natl Acad Sci U S A 104 (2007) 18830-18835. This exciting paper provides evidence that phosphorylation of a C-terminal conserved serine residue in RopGEF12 has an important influence on its function and localization. Based on the co-overexpression phenotype of RopGEF12 and pollen RLK (PRK2a), the authors propose that PM-localized receptor-like kinases may be involved in the apical PM localization of RopGEFs and thus the initiation and maintenance of ROP signaling at the tip of pollen tubes.
35. Tang W., Kelley D., Ezcurra I., Cotter R., and McCormick S. LeSTIG1, an extracellular binding partner for the pollen receptor kinases LePRK1 and LePRK2, promotes pollen tube growth in vitro. Plant J 39 (2004) 343-353
36. Klahre U., Becker C., Schmitt A.C., and Kost B. Nt-RhoGDI2 regulates Rac/Rop signaling and polar cell growth in tobacco pollen tubes. Plant J 46 (2006) 1018-1031
37. Carol R.J., Takeda S., Linstead P., Durrant M.C., Kakesova H., Derbyshire P., Drea S., Zarsky V., and Dolan L. A RhoGDP dissociation inhibitor spatially regulates growth in root hair cells. Nature 438 (2005) 1013-1016
38. Klahre U., and Kost B. Tobacco RhoGTPase ACTIVATING PROTEIN1 spatially restricts signaling of RAC/Rop to the apex of pollen tubes. Plant Cell 18 (2006) 3033-3046
39. Yang Z. Cell polarity signaling in Arabidopsis. Ann Rev Cell Dev Biol 24 (2008) 551-575
40. Foreman J., Demidchik V., Bothwell J.H., Mylona P., Miedema H., Torres M.A., Linstead P., Costa S., Brownlee C., and Jones J.D. Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422 (2003) 442-446
41. Carol R.J., and Dolan L. The role of reactive oxygen species in cell growth: lessons from root hairs. J Exp Bot 57 (2006) 1829-1834
42. Potocký M., Jones M.A., Bezvoda R., Smirnoff N., and Zarsky V. Reactive oxygen species produced by NADPH oxidase are involved in pollen tube growth. New Phytol 174 (2007) 742-751. This study shows that tip-focused reactive oxygen species generated by pollen-specific NADPH oxidase is required for pollen tube growth, suggesting that it could be a general mechanism that controls tip growth in plant cells.
43. 2+ influx that in turn activates RHD2 activity to produce more ROS to establish tip-growing site in root hair cells.
44. Ringli C., Baumberger N., Diet A., Frey B., and Keller B. ACTIN2 is essential for bulge site selection and tip growth during root hair development of Arabidopsis. Plant Physiol 129 (2002) 1464-1472
45. Jones M.A., Raymond M.J., Yang Z., and Smirnoff N. NADPH oxidase-dependent reactive oxygen species formation required for root hair growth depends on ROP GTPase. J Exp Bot 58 (2007) 1261-1270. This interesting work provides evidence that activity of ROP is involved in root hair growth by regulating superoxide production at the tip.
46. Wong H.L., Pinontoan R., Hayashi K., Tabata R., Yaeno T., Hasegawa K., Kojima C., Yoshioka H., Iba K., Kawasaki T., et al. Regulation of rice NADPH oxidase by binding of Rac GTPase to its N-terminal extension. Plant Cell 19 (2007) 4022-4034
47. + efflux by the Na-H exchanger NHE1 for polarity of migrating cells. J Cell Biol 179 (2007) 403-410
48. Monshausen G.B., Bibikova T.N., Messerli M.A., Shi C., and Gilroy S. Oscillations in extracellular pH and reactive oxygen species modulate tip growth of Arabidopsis root hairs. Proc Natl Acad Sci U S A 104 (2007) 20996-21001
49. Kost B., Lemichez E., Spielhofer P., Hong Y., Tolias K., Carpenter C., and Chua N.H. Rac homologues and compartmentalized phosphatidylinositol 4,5-bisphosphate act in a common pathway to regulate polar pollen tube growth. J Cell Biol 145 (1999) 317-330
50. Lee Y., Bak G., Choi Y., Chuang W.I., Cho H.T., and Lee Y. Roles of phosphatidylinositol 3-kinase in root hair growth. Plant Physiol 147 (2008) 624-635
51. Di Paolo G., and De Camilli P. Phosphoinositides in cell regulation and membrane dynamics. Nature 443 (2006) 651-657
52. Leshem Y., Seri L., and Levine A. Induction of phosphatidylinositol 3-kinase-mediated endocytosis by salt stress leads to intracellular production of reactive oxygen species and salt tolerance. Plant J 51 (2007) 185-197
53. Choi Y., Lee Y., Jeon B.W., Staiger C.J., and Lee Y. Phosphatidylinositol 3- and 4-phosphate modulate actin filament reorganization in guard cells of day flower. Plant Cell Environ 31 (2008) 366-377
54. Wang J., Sun H.Q., Macia E., Kirchhausen T., Watson H., Bonifacino J.S., and Yin H.L. PI4P promotes the recruitment of the GGA adaptor proteins to the trans-Golgi network and regulates their recognition of the ubiquitin sorting signal. Mol Biol Cell 18 (2007) 2646-2655
55. Sciorra V.A., Audhya A., Parsons A.B., Segev N., Boone C., and Emr S.D. Synthetic genetic array analysis of the PtdIns 4-kinase Pik1p identifies components in a Golgi-specific Ypt31/rab-GTPase signaling pathway. Mol Biol Cell 16 (2005) 776-793
56. Thole J.M., Vermeer J.E., Zhang Y., Gadella Jr. T.W., and Nielsen E. Root hair defective4 encodes a phosphatidylinositol-4-phosphate phosphatase required for proper root hair development in Arabidopsis thaliana. Plant Cell 20 (2008) 381-395. This paper presents data suggesting that both the level of PI4P and its distribution in the cell are important for polarized secretion of vesicles, which is important for root hair morphogenesis.
57. Monteiro D., Castanho Coelho P., Rodrigues C., Camacho L., Quader H., and Malho R. Modulation of endocytosis in pollen tube growth by phosphoinositides and phospholipids. Protoplasma 226 (2005) 31-38
58. Kusano H., Testerink C., Vermeer J.E., Tsuge T., Shimada H., Oka A., Munnik T., and Aoyama T. The Arabidopsis phosphatidylinositol phosphate 5-kinase PIP5K3 is a key regulator of root hair tip growth. Plant Cell 20 (2008) 367-380
59. Stenzel I., Ischebeck T., Konig S., Holubowska A., Sporysz M., Hause B., and Heilmann I. The type B phosphatidylinositol-4-phosphate 5-kinase 3 is essential for root hair formation in Arabidopsis thaliana. Plant Cell 20 (2008) 124-141
60. Dowd P.E., Coursol S., Skirpan A.L., Kao T.H., and Gilroy S. Petunia phospholipase c1 is involved in pollen tube growth. Plant Cell 18 (2006) 1438-1453
61. Aoyagi K., Sugaya T., Umeda M., Yamamoto S., Terakawa S., and Takahashi M. The activation of exocytotic sites by the formation of phosphatidylinositol 4,5-bisphosphate microdomains at syntaxin clusters. J Biol Chem 280 (2005) 17346-17352
62. Golub T., and Caroni P. PI(4,5)P2-dependent microdomain assemblies capture microtubules to promote and control leading edge motility. J Cell Biol 169 (2005) 151-165
63. Preuss M.L., Schmitz A.J., Thole J.M., Bonner H.K., Otegui M.S., and Nielsen E. A role for the RabA4b effector protein PI-4Kbeta1 in polarized expansion of root hair cells in Arabidopsis thaliana. J Cell Biol 172 (2006) 991-998
64. Helling D., Possart A., Cottier S., Klahre U., and Kost B. Pollen tube tip growth depends on plasma membrane polarization mediated by tobacco PLC3 activity and endocytic membrane recycling. Plant Cell 18 (2006) 3519-3534