Apical F-actin-regulated exocytic targeting of NtPPME1 is essential for construction and rigidity of the pollen tube cell wall

Plant Journal

Volumn 76, Issue 3, 2013, Pages 367-379

  Wang, Hao ^a   Zhuang, Xiaohong ^a   Cai, Yi ^a   Cheung, Alice Y ^b   Jiang, Liwen ^a  

^a CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^b UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

apical F actin; cell wall; endocytosis; exocytosis; NtPPME1; wortmannin

Indexed keywords

CELL WALLS; ENDOCYTOSIS; EXOCYTOSIS; F-ACTIN; NTPPME1; WORTMANNIN;

CELLS; CYTOLOGY; MOLECULAR BIOLOGY; RIGIDITY; TUBES (COMPONENTS);

PROTEINS;

NICOTIANA TABACUM;

ACTIN; ANDROSTANE DERIVATIVE; CARBOXYLESTERASE; PECTINESTERASE; VEGETABLE PROTEIN; WORTMANNIN;

APICAL F-ACTIN; ARTICLE; CELL WALL; ENDOCYTOSIS; EXOCYTOSIS; FLUORESCENCE; GROWTH, DEVELOPMENT AND AGING; IMMUNOHISTOCHEMISTRY; METABOLISM; NTPPME1; PHYSIOLOGY; POLLEN TUBE; SECRETION (PROCESS); TOBACCO; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE;

APICAL F-ACTIN; CELL WALL; ENDOCYTOSIS; EXOCYTOSIS; NTPPME1; WORTMANNIN;

ACTINS; ANDROSTADIENES; CARBOXYLIC ESTER HYDROLASES; CELL WALL; ENDOCYTOSIS; EXOCYTOSIS; FLUORESCENCE; IMMUNOHISTOCHEMISTRY; MICROSCOPY, ELECTRON, TRANSMISSION; PLANT PROTEINS; POLLEN TUBE; TOBACCO;

EID: 84885633266     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12300     Document Type: Article

References (90)

1. Arighi, C.N., Hartnell, L.M., Aguilar, R.C., Haft, C.R., and, Bonifacino, J.S., (2004) Role of the mammalian retromer in sorting of the cation-independent mannose 6-phosphate receptor. J. Cell Biol. 165, 123-133.
2. Bosch, M., and, Hepler, P.K., (2005a) Pectin methylesterases and pectin dynamics in pollen tubes. Plant Cell, 17, 3219-3226.
3. Bosch, M., and, Hepler, P.K., (2005b) Pectin methylesterases and pectin dynamics in pollen tubes. Plant Cell, 17, 3219-3226.
4. Bosch, M., and, Hepler, P.K., (2006) Silencing of the tobacco pollen pectin methylesterase NtPPME1 results in retarded in vivo pollen tube growth. Planta, 223, 736-745.
5. Bosch, M., Cheung, A.Y., and, Hepler, P.K., (2005a) Pectin methylesterase, a regulator of pollen tube growth. Plant Physiol. 138, 1334-1346.
6. Bou Daher, F., and, Geitmann, A., (2011) Actin is involved in pollen tube tropism through redefining the spatial targeting of secretory vesicles. Traffic, 12, 1537-1551.
7. Cai, G., and, Cresti, M., (2009) Organelle motility in the pollen tube: a tale of 20 years. J. Exp. Bot. 60, 495-508.
8. Cai, Y., Jia, T., Lam, S.K., Ding, Y., Gao, C., San, M.W., Pimpl, P., and, Jiang, L., (2011) Multiple cytosolic and transmembrane determinants are required for the trafficking of SCAMP1 via an ER-Golgi-TGN-PM pathway. Plant J. 65, 882-896.
9. Cai, Y., Zhuang, X., Wang, J., Wang, H., Lam, S.K., Gao, C., Wang, X., and, Jiang, L., (2012) Vacuolar degradation of two integral plasma membrane proteins, AtLRR84A and OsSCAMP1, is cargo ubiquitination-independent and prevacuolar compartment-mediated in plant cells. Traffic, 13, 1023-1040.
10. 2+ and GTPases. J. Exp. Bot. 54, 83-92.
11. Carnero, A., and, Lacal, J.C., (1998) Wortmannin, an inhibitor of phosphatidyl-inositol 3-kinase, induces oocyte maturation through a MPF-MAPK-dependent pathway. FEBS Lett. 422, 155-159.
12. Chen, C.Y., Cheung, A.Y., and, Wu, H.M., (2003) Actin-depolymerizing factor mediates Rac/Rop GTPase-regulated pollen tube growth. Plant Cell, 15, 237-249.
13. Cheung, A.Y., and, Wu, H.M., (2007) Structural and functional compartmentalization in pollen tubes. J. Exp. Bot. 58, 75-82.
14. 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.
15. Cheung, A.Y., and, Wu, H.M., (2011) THESEUS 1, FERONIA and relatives: a family of cell wall-sensing receptor kinases? Curr. Opin. Plant Biol. 14, 632-641.
16. Cheung, A.Y., Duan, Q.H., Costa, S.S., de Graaf, B.H., Di Stilio, V.S., Feijo, J., and, Wu, H.M., (2008) The dynamic pollen tube cytoskeleton: live cell studies using actin-binding and microtubule-binding reporter proteins. Mol. Plant, 1, 686-702.
17. Cheung, A.Y., Niroomand, S., Zou, Y.J., and, Wu, H.M., (2010) A transmembrane formin nucleates subapical actin assembly and controls tip-focused growth in pollen tubes. Proc. Natl Acad. Sci. USA, 107, 16390-16395.
18. Dardelle, F., Lehner, A., Ramdani, Y., Bardor, M., Lerouge, P., Driouich, A., and, Mollet, J.C., (2010) Biochemical and immunocytological characterizations of Arabidopsis pollen tube cell wall. Plant Physiol. 153, 1563-1576.
19. Davidson, H.W., (1995) Wortmannin causes mistargeting of procathepsin D. evidence for the involvement of a phosphatidylinositol 3-kinase in vesicular transport to lysosomes. J. Cell Biol. 130, 797-805.
20. Ding, Y., Wang, J., Stierhof, Y.D., Robinson, D.G., and, Jiang, L., (2012) Unconventional protein secretion. Trends Plant Sci. 17, 606-615.
21. Emans, N., Zimmermann, S., and, Fischer, R., (2002) Uptake of a fluorescent marker in plant cells is sensitive to brefeldin A and wortmannin. Plant Cell, 14, 71-86.
22. Fu, Y., (2010) The actin cytoskeleton and signaling network during pollen tube tip growth. J. Integr. Plant Biol. 52, 131-137.
23. Gao, C., Yu, C.K., Qu, S., San, M.W., Li, K.Y., Lo, S.W., and, Jiang, L., (2012) The Golgi-localized Arabidopsis endomembrane protein12 contains both endoplasmic reticulum export and Golgi retention signals at its C terminus. Plant Cell, 24, 2086-2104.
24. Gu, Y., Vernoud, V., Fu, Y., and, Yang, Z., (2003) ROP GTPase regulation of pollen tube growth through the dynamics of tip-localized F-actin. J. Exp. Bot. 54, 93-101.
25. Hill, A.E., Shachar-Hill, B., Skepper, J.N., Powell, J., and, Shachar-Hill, Y., (2012) An osmotic model of the growing pollen tube. PLoS One, 7, e36585. doi: 10.1371/journal.pone.0036585.
26. Holdaway-Clarke, T.L., Weddle, N.M., Kim, S., Robi, A., Parris, C., Kunkel, J.G., and, Hepler, P.K., (2003) Effect of extracellular calcium, pH and borate on growth oscillations in Lilium formosanum pollen tubes. J. Exp. Bot. 54, 65-72.
27. Holmes, D., (2011) PI3K pathway inhibitors approach junction. Nat. Rev. Drug Discov. 10, 563-564.
28. Jaillais, Y., Fobis-Loisy, I., Miege, C., and, Gaude, T., (2008) Evidence for a sorting endosome in Arabidopsis root cells. Plant J. 53, 237-247.
29. Jiang, L., and, Rogers, J.C., (1998) Integral membrane protein sorting to vacuoles in plant cells: evidence for two pathways. J. Cell Biol. 143, 1183-1199.
30. Knox, J.P., Linstead, P.J., King, J., Cooper, C., and, Roberts, K., (1990) Pectin esterification Is spatially regulated both within cell-walls and BETWEEN developing-tissues of root apices. Planta, 181, 512-521.
31. Kost, B., (2008) Spatial control of Rho (Rac-Rop) signaling in tip-growing plant cells. Trends Cell Biol. 18, 119-127.
32. 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.
33. 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.
34. Kroeger, J., and, Geitmann, A., (2012) The pollen tube paradigm revisited. Curr. Opin. Plant Biol. 15, 618-624.
35. Kulich, I., Cole, R., Drdova, E., Cvrckova, F., Soukup, A., Fowler, J., and, Zarsky, V., (2010) Arabidopsis exocyst subunits SEC8 and EXO70A1 and exocyst interactor ROH1 are involved in the localized deposition of seed coat pectin. New Phytol. 188, 615-625.
36. Lam, S.K., Siu, C.L., Hillmer, S., Jang, S., An, G., Robinson, D.G., and, Jiang, L., (2007a) Rice SCAMP1 defines clathrin-coated, trans-golgi-located tubular-vesicular structures as an early endosome in tobacco BY-2 cells. Plant Cell, 19, 296-319.
37. Lam, S.K., Tse, Y.C., Robinson, D.G., and, Jiang, L., (2007b) Tracking down the elusive early endosome. Trends Plant Sci. 12, 497-505.
38. Lee, Y.J., and, Yang, Z., (2008a) Tip growth: signaling in the apical dome. Curr. Opin. Plant Biol. 11, 662-671.
39. Lee, Y., Bak, G., Choi, Y., Chuang, W.I., and, Cho, H.T., (2008a) Roles of phosphatidylinositol 3-kinase in root hair growth. Plant Physiol. 147, 624-635.
40. Lee, Y., Kim, E.S., Choi, Y., Hwang, I., Staiger, C.J., and, Chung, Y.Y., (2008b) The Arabidopsis phosphatidylinositol 3-kinase is important for pollen development. Plant Physiol. 147, 1886-1897.
41. Lee, Y.J., Szumlanski, A., Nielsen, E., and, Yang, Z., (2008c) Rho-GTPase-dependent filamentous actin dynamics coordinate vesicle targeting and exocytosis during tip growth. J. Cell Biol. 181, 1155-1168.
42. Matsuoka, K., Bassham, D.C., Raikhel, N.V., and, Nakamura, K., (1995) Different sensitivity to wortmannin of two vacuolar sorting signals indicates the presence of distinct sorting machineries in tobacco cells. J. Cell Biol. 130, 1307-1318.
43. McKenna, S.T., Kunkel, J.G., Bosch, M., Rounds, C.M., Vidali, L., Winship, L.J., and, Hepler, P.K., (2009) Exocytosis precedes and predicts the increase in growth in oscillating pollen tubes. Plant Cell, 21, 3026-3040.
44. Miao, Y., Yan, P.K., Kim, H., Hwang, I., and, Jiang, L., (2006) Localization of green fluorescent protein fusions with the seven Arabidopsis vacuolar sorting receptors to prevacuolar compartments in tobacco BY-2 cells. Plant Physiol. 142, 945-962.
45. Miao, Y., Li, H.Y., Shen, J., Wang, J., and, Jiang, L., (2011) QUASIMODO 3 (QUA3) is a putative homogalacturonan methyltransferase regulating cell wall biosynthesis in Arabidopsis suspension-cultured cells. J. Exp. Bot. 62, 5063-5078.
46. Micheli, F., (2001) Pectin methylesterases: cell wall enzymes with important roles in plant physiology. Trends Plant Sci. 6, 414-419.
47. Micheli, F., Sundberg, B., Goldberg, R., and, Richard, L., (2000) Radial distribution pattern of pectin methylesterases across the cambial region of hybrid aspen at activity and dormancy. Plant Physiol. 124, 191-199.
48. 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.
49. Nakanishi, S., Kakita, S., Takahashi, I., et al. (1992) Wortmannin, a microbial product Inhibitor of myosin light chain kinase. J. Biol. Chem. 267, 2157-2163.
50. Palin, R., and, Geitmann, A., (2012) The role of pectin in plant morphogenesis. BioSystems, 109, 397-402.
51. Papakonstanti, E.A., and, Stournaras, C., (2002) Association of PI-3 kinase with PAK1 leads to actin phosphorylation and cytoskeletal reorganization. Mol. Biol. Cell, 13, 2946-2962.
52. 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.
53. Parton, R.M., Fischer-Parton, S., Trewavas, A.J., and, Watahiki, M.K., (2003) Pollen tubes exhibit regular periodic membrane trafficking events in the absence of apical extension. J. Cell Sci. 116, 2707-2719.
54. Ren, H., and, Xiang, Y., (2007) The function of actin-binding proteins in pollen tube growth. Protoplasma, 230, 171-182.
55. Ridley, B.L., O'Neill, M.A., and, Mohnen, D., (2001) Pectins: structure, biosynthesis, and oligogalacturonide-related signaling. Phytochemistry, 57, 929-967.
56. Rockel, N., Wolf, S., Kost, B., Rausch, T., and, Greiner, S., (2008) Elaborate spatial patterning of cell-wall PME and PMEI at the pollen tube tip involves PMEI endocytosis, and reflects the distribution of esterified and de-esterified pectins. Plant J. 53, 133-143.
57. Sasaki, H., Nakamura, M., Ohno, T., Matsuda, Y., Yuda, Y., and, Nonomura, Y., (1995) Myosin-actin interaction plays an important role in human-immunodeficiency-virus type-1 release from host-cells. Proc. Natl Acad. Sci. USA, 92, 2026-2030.
58. Schu, P.V., Takegawa, K., Fry, M.J., Stack, J.H., Waterfield, M.D., and, Emr, S.D., (1993) Phosphatidylinositol 3-kinase encoded by yeast VPS34 gene essential for protein sorting. Science, 260, 88-91.
59. Shen, J., Suen, P.K., Wang, X., Lin, Y., Lo, S.W., Rojo, E., and, Jiang, L.W., (2013a) An in vivo expression system for the identification of cargo proteins of vacuolar sorting receptors in Arabidopsis culture cells. Plant J. doi: 10.1111/tpj.12257.
60. Shen, J., Zeng, Y., Zhuang, X., Sun, L., Yao, X., Pimpl, P., and, Jiang, L.W., (2013b) Organelle pH in the Arabidopsis Endomembrane System. Mol. Plant, doi: 10.1093/mp/sst079.
61. Shpetner, H., Joly, M., Hartley, D., and, Corvera, S., (1996) Potential sites of PI-3 kinase function in the endocytic pathway revealed by the PI-3 kinase inhibitor, wortmannin. J. Cell Biol. 132, 595-605.
62. Spiro, D.J., Boll, W., Kirchhausen, T., and, WesslingResnick, M., (1996) Wortmannin alters the transferrin receptor endocytic pathway in vivo and in vitro. Mol. Biol. Cell, 7, 355-367.
63. Taylor, L.P., and, Hepler, P.K., (1997) Pollen Germination and Tube Growth. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48, 461-491.
64. 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.
65. Tse, Y.C., Mo, B., Hillmer, S., Zhao, M., Lo, S.W., Robinson, D.G., and, Jiang, L., (2004) Identification of multivesicular bodies as prevacuolar compartments in Nicotiana tabacum BY-2 cells. Plant Cell, 16, 672-693.
66. Tse, Y.C., Lo, S.W., Hillmer, S., Dupree, P., and, Jiang, L., (2006) Dynamic response of prevacuolar compartments to brefeldin a in plant cells. Plant Physiol. 142, 1442-1459.
67. Vermeer, J.E., van Leeuwen, W., Tobena-Santamaria, R., Laxalt, A.M., Jones, D.R., Divecha, N., Gadella, T.W. Jr, and, Munnik, T., (2006) Visualization of PtdIns3P dynamics in living plant cells. Plant J. 47, 687-700.
68. Vidali, L., and, Hepler, P.K., (2001) Actin and pollen tube growth. Protoplasma, 215, 64-76.
69. Vidali, L., McKenna, S.T., and, Hepler, P.K., (2001) Actin polymerization is essential for pollen tube growth. Mol. Biol. Cell, 12, 2534-2545.
70. Wang, H., and, Jiang, L., (2011a) Transient expression and analysis of fluorescent reporter proteins in plant pollen tubes. Nat. Protoc. 6, 419-426.
71. Wang, J., Cai, Y., Miao, Y., Lam, S.K., and, Jiang, L., (2009) Wortmannin induces homotypic fusion of plant prevacuolar compartments. J. Exp. Bot. 60, 3075-3083.
72. Wang, H., Tse, Y.C., Law, A.H., Sun, S.S., Sun, Y.B., Xu, Z.F., Hillmer, S., Robinson, D.G., and, Jiang, L., (2010a) Vacuolar sorting receptors (VSRs) and secretory carrier membrane proteins (SCAMPs) are essential for pollen tube growth. Plant J. 61, 826-838.
73. Wang, J., Ding, Y., Wang, J., Hillmer, S., Miao, Y., Lo, S.W., Wang, X., Robinson, D.G., and, Jiang, L., (2010b) EXPO, an exocyst-positive organelle distinct from multivesicular endosomes and autophagosomes, mediates cytosol to cell wall exocytosis in Arabidopsis and tobacco cells. Plant Cell, 22, 4009-4030.
74. Wang, H., Zhuang, X.H., Hillmer, S., Robinson, D.G., and, Jiang, L.W., (2011b) Vacuolar sorting receptor (VSR) proteins reach the plasma membrane in germinating pollen tubes. Mol. Plant, 4, 845-853.
75. Wang, J., Tse, Y.C., Hinz, G., Robinson, D.G., and, Jiang, L., (2012) Storage globulins pass through the Golgi apparatus and multivesicular bodies in the absence of dense vesicle formation during early stages of cotyledon development in mung bean. J. Exp. Bot. 63, 1367-1380.
76. Willats, W.G.T., Limberg, G., Buchholt, H.C., van Alebeek, G.J., Benen, J., Christensen, T.M.I.E., Visser, J., Voragen, A., Mikkelsen, J.D., and, Knox, J.P., (2000a) Analysis of pectin structure part 2-Analysis of pectic epitopes recognised by hybridoma and phage display monoclonal antibodies using defined oligosaccharides, polysaccharides, and enzymatic degradation. Carbohyd. Res. 327, 309-320.
77. Willats, W.G.T., Steele-King, C.G., McCartney, L., Orfila, C., Marcus, S.E., and, Knox, J.P., (2000b) Making and using antibody probes to study plant cell walls. Plant Physiol. Biochem. 38, 27-36.
78. Winship, L.J., Obermeyer, G., Geitmann, A., and, Hepler, P.K., (2011) Pollen tubes and the physical world. Trends Plant Sci. 16, 353-355.
79. Wurmser, A.E., Gary, J.D., and, Emr, S.D., (1999) Phosphoinositide 3-kinases and their FYVE domain-containing effectors as regulators of vacuolar/lysosomal membrane trafficking pathways. J. Biol. Chem. 274, 9129-9132.
80. Xie, L.H., Takano, M., Kakei, M., Okamura, M., and, Noma, A., (1999) Wortmannin, an inhibitor of phosphatidylinositol kinases, blacks the MgATP-dependent recovery of Kir6.2/SUR2A channels. J. Physiol. 514, 655-665.
81. Yang, Z., (2008) Cell polarity signaling in Arabidopsis. Annu. Rev. Cell Dev. Biol. 24, 551-575.
82. Zhang, Y., and, McCormick, S., (2010) The regulation of vesicle trafficking by small GTPases and phospholipids during pollen tube growth. Sex. Plant Reprod. 23, 87-93.
83. Zhang, G.Y., Feng, J., Wu, J., and, Wang, X.W., (2010a) BoPMEI1, a pollen-specific pectin methylesterase inhibitor, has an essential role in pollen tube growth. Planta, 231, 1323-1334.
84. Zhang, Y., He, J., Lee, D., and, McCormick, S., (2010b) Interdependence of endomembrane trafficking and actin dynamics during polarized growth of Arabidopsis pollen tubes. Plant Physiol. 152, 2200-2210.
85. Zhang, Y., Li, S., Zhou, L.Z., Fox, E., Pao, J., Sun, W., Zhou, C., and, McCormick, S., (2011) Overexpression of Arabidopsis thaliana PTEN caused accumulation of autophagic bodies in pollen tubes by disrupting phosphatidylinositol 3-phosphate dynamics. Plant J. 68, 1081-1092.
86. Zhao, F.L., and, Herness, S., (2009) Resynthesis of phosphatidylinositol 4,5-bisphosphate mediates adaptation of the caffeine response in rat taste receptor cells. J. Physiol. 587, 363-377.
87. Zonia, L., (2010) Spatial and temporal integration of signalling networks regulating pollen tube growth. J. Exp. Bot. 61, 1939-1957.
88. 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.
89. Zonia, L., and, Munnik, T., (2009) Uncovering hidden treasures in pollen tube growth mechanics. Trends Plant Sci. 14, 318-327.
90. Zonia, L., and, Munnik, T., (2011) Understanding pollen tube growth: the hydrodynamic model versus the cell wall model. Trends Plant Sci. 16, 347-352.