Electron tomographic analysis of somatic cell plate formation in meristematic cells of arabidopsis preserved by high-pressure freezing

Plant Cell

Volumn 16, Issue 4, 2004, Pages 836-856

  Seguí Simarro, José M ^a   Austin II, Jotham R ^a   White, Erin A ^a   Staehelin, L Andrew ^a  

^a UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MEMBRANES; CYTOLOGY; ELECTRONS; SUBSTITUTION REACTIONS; TOMOGRAPHY;

CYTOKINESIS; MERISTEM CELLS; RIBOSOME; SOMATIC CELLS;

PLANT CELL CULTURE;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 1842813514     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.017749     Document Type: Article

References (75)

1. Asada, T., Sonobe, S., and Shibaoka, H. (1991). Microtubule translocation in the cytokinetic apparatus of cultured tobacco cells. Nature 350, 238-241.
2. Assaad, F.F. (2001). Plant cytokinesis. Exploring the links. Plant Physiol. 126, 509-516.
3. Bajer, A.S. (1968). Fine structure studies on phragmoplast and cell plate formation. Chromosoma 24, 383-417.
4. Baskin, T.I., and Cande, W.Z. (1990). The structure and function of the mitotic spindle in flowering plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 41, 277-315.
5. Becker, W.A. (1932). Recherches expérimentales sur la cytocinèse et la formation de la plaque cellulaire dans la cellule vivante. C. R. Acad. Sci. Paris 194, 1850-1852.
6. Bednarek, S.Y., and Falbel, T.G. (2002). Membrane trafficking during plant cytokinesis. Traffic 3, 621-629.
7. Brown, R.C., and Lemmon, B.E. (1991). Pollen development in orchids. 5. A generative cell domain Involved in spatial control of the hemispherical cell plate. J. Cell Sci. 100, 559-565.
8. Brown, R.C., and Lemmon, B.E. (1992). Pollen development in orchids. 4. Cytoskeleton and ultrastructure of the unequal pollen mitosis in Phalenopsis. Protoplasma 167, 183-192.
9. Buvat, R., and Puissant, A. (1958). Observations sur la cytodlerese et l'origine des plasmodesmes. C. R. Acad. Sci. Paris 247, 233-236.
10. Carvalho, P., Tirnauer, J.S., and Pellman, D. (2003). Surfing on microtubule ends. Trends Cell Biol. 13, 229-237.
11. Cutler, S.R., and Ehrhardt, D.W. (2002). Polarized cytokinesis in vacuolate cells of Arabidopsis. Proc. Natl. Acad. Sci. USA 99, 2812-2817.
12. Cvrckova, F., Ellas, M., Hala, M., Obermeyer, G., and Zarsky, V. (2001). Small GTPases and conserved signalling pathways in plant cell morphogenesis: From exocytosis to the exocyst. In Cell Biology of Plant and Fungal Tip Growth, A. Geitmann, M. Cresti, and I.B. Heath, eds (Amsterdam, The Netherlands: IOS Press), pp. 105-122.
13. Errera, L. (1888). Ueber Zellformen und Seifenblasen. Beihefte z. Botan. Zentralblatt. 34, 395-398.
14. Finger, F.P., Hughes, T.E., and Novick, P. (1998). Sec3p is a spatial landmark for polarized secretion in budding yeast. Cell 92, 559-571.
15. Fu, D., Libson, A., Miercke, L.J.W., Weitzman, C., Nollert, P., Krucinski, J., and Stroud, R.M. (2000). Structure of a glycerol-conducting channel and the basis for its selectivity. Science 290, 481-486.
16. Gilbert, P.F.C. (1972). Reconstruction of a 3-dimensional structure from projections and its application to electron-microscopy II. Direct Methods. Proc. R. Soc. Lond. B Biol. Sci. 182, 89-102.
17. Gilkey, J.C., and Staehelin, L.A. (1986). Advances in ultra-rapid freezing for the preservation of cellular ultrastructure. J. Electron Microsc. Tech. 3, 177-210.
18. Goldberg, R., Morvan, C., Jauneau, A., and Jarvis, M. (1996). Methylesterification, de-esterification and gelation of pectins in the primary cell wall. In Progress in Biotechnology: Pectins and Pectinases, J. Visser and A.G.J. Voragen, eds (Amsterdam, The Netherlands: Elsevier Science), pp. 151-172.
19. Gu, X., and Verma, D.P. (1996). Phragmoplastin, adynamin-like protein associated with cell plate formation in plants. EMBO J. 15, 695-704.
20. Gu, X., and Verma, D.P. (1997). Dynamics of phragmoplastin in living cells during cell plate formation and uncoupling of cell elongation from the plane of cell division. Plant Cell 9, 157-169.
21. Guertin, D.A., Trautmann, S., and McCollum, D. (2002). Cytokinesis in eukaryotes. Microbiol. Mol. Biol. Rev. 66, 155-178.
22. Gunning, B.E.S. (1982). The cytokinetic apparatus: Its developmental and spatial regulation. In The Cytoskeleton in Plant Growth and Development, C. Lloyd, ed (London: Academic Press), pp. 229-292.
23. Guo, W., Tamanol, F., and Novick, P. (2001). Spatial regulation of the exocyst complex by Rho1 GTPase. Nat. Cell Biol. 3, 353-360.
24. Hepler, P.K. (1982). Endoplasmic-Reticulum in the Formation of the Cell Plate and Plasmodesmata. Protoplasma 111, 121-133.
25. Hepler, P.K. (1994). The role of calcium in cell division. Cell Calcium 16, 322-330.
26. Hepler, P.K., and Jackson, W.T. (1968). Microtubules and early stages of cell-plate formation in the endosperm of Haemanthus katherinae Baker. J. Cell Biol. 38, 437-446.
27. Hepler, P.K., and Newcomb, E.H. (1967). Fine structure of cell plate formation in the apical meristem of Phaseolus roots. J. Ultrastruct. Res. 19, 499-513.
28. Hepler, P.K., Palevitz, B.A., Lancelle, S.A., McCauley, M.M., and Lichtscheidl, I. (1990). Cortical endoplasmic reticulum in plants. J. Cell Sci. 96, 355-373.
29. Hepler, P.K., Valster, A., Molchan, T., and Vos, J.W. (2002). Roles for kinesin and myosin during cytokinesis. Philos. Trans. R. Soc. Lond., B, Biol. Sci. 357, 761-766.
30. Hsu, S.C., Hazuka, C.D., Foletti, D.L., and Scheller, R.H. (1999). Targeting vesicles to specific sites on the plasma membrane: The role of the sec6/8 complex. Trends Cell Biol. 9, 150-153.
31. Hsu, S.C., Hazuka, C.D., Roth, R., Foletti, D.L., Heuser, J., and Scheller, R.H. (1998). Subunit composition, protein interactions, and structures of the mammalian brain sec6/8 complex and septin filaments. Neuron 20, 1111-1122.
32. Kakimoto, T., and Shibaoka, H. (1992). Synthesis of polysaccharides in phragmoplasts isolated from tobacco BY-2 cells. Plant Cell Physiol. 33, 353-361.
33. Kang, B.-H., Busse, J.S., and Bednarek, S.Y. (2003). Members of the Arabidopsis dynamin-like gene family, ADL1, are essential for plant cytokinesis and polarized cell growth. Plant Cell 15, 899-913.
34. Kang, B.-H., Busse, J.S., Dickey, C., Rancour, D.M., and Bednarek, S.Y. (2001). The Arabidopsis cell plate-associated dynamin-like protein, ADL1Ap, is required for multiple stages of plant growth and development. Plant Physiol. 126, 47-68.
35. Kremer, J.R., Mastronarde, D.N., and McIntosh, J.R. (1996). Computer visualization of three-dimensional image data using IMOD. J. Struct. Biol. 116, 71-76.
36. Ladinsky, M.S., Mastronarde, D.N., McIntosh, J.R., Howell, K.E., and Staehelin, L.A. (1999). Golgi structure in three dimensions: Functional insights from the normal rat kidney cell. J. Cell Biol. 144, 1135-1149.
37. Lauber, M.H., Waizenegger, I., Steinmann, T., Schwarz, H., Mayer, U., Hwang, I., Lukowitz, W., and Jurgens, G. (1997). The Arabidopsis KNOLLE protein is a cytokinesis-specific syntaxin. J. Cell Biol. 139, 1485-1493.
38. Ledbetter, M.C., and Porter, K.R. (1963). A "microtubule" in plant cell fine structure. J. Cell Biol. 19, 239-250.
39. Lipschutz, J.H., and Mostov, K.E. (2002). Exocytosis: The many masters of the exocyst. Curr. Biol. 12, R212-R214.
40. Liu, B., Lee, Y.R.J., and Pan, R. (2003). Identification of kinesin-related proteins in the phragmoplast. Cell Biol. Int. 27, 227-228.
41. Marks, B., Stowell, M.H.B., Vallis, Y., Mills, I.G., Gibson, A., Hopkins, C.R., and McMahon, H.T. (2001). GTPase activity of dynamin and resulting conformation change are essential for endocytosis. Nature 410, 231-235.
42. Marsh, B.J., Mastronarde, D.N., Buttle, K.F., Howell, K.E., and McIntosh, J.R. (2001). Organellar relationships in the Golgi region of the pancreatic beta cell line, HIT-T15, visualized by high resolution electron tomography. Proc. Natl. Acad. Sci. USA 98, 2399-2406.
43. Mastronarde, D.N. (1997). Dual-axis tomography: An approach with alignment methods that preserve resolution. J. Struct. Biol. 120, 343-352.
44. Matern, H.T., Yeaman, C., Nelson, W.J., and Scheller, R.H. (2001). The Sec6/8 complex in mammalian cells: Characterization of mammalian Sec3, subunit interactions, and expression of subunits in polarized cells. Proc. Natl. Acad. Sci. USA 98, 9648-9653.
45. Molchan, T.M., Valster, A.H., and Hepler, P.K. (2002). Actomyosin promotes cell plate alignment and late lateral expansion in Tradescantia stamen hair cells. Planta 214, 683-693.
46. Mollenhauer, H.H., and Mollenhauer, B.A. (1976). Changes in Golgi apparatus secretory pattern with relation to cell-division in maize root-tips. Plant Physiol. 57, 10.
47. Nacry, P., Mayer, U., and Jürgens, G. (2000). Genetic dissection of cytokinesis. Plant Mol. Biol. 43, 719-733.
48. Otegui, M.S., Mastronarde, D.N., Kang, B.H., Bednarek, S.Y., and Staehelin, L.A. (2001). Three-dimensional analysis of syncytial-type cell plates during endosperm cellularization visualized by high resolution electron tomography. Plant Cell. 13, 2033-2051.
49. Otegui, M.S., and Staehelin, L.A. (2004). 3D Tomographic analysis of post-meiotic cytokinesis during pollen development in Arabidopsis thaliana. Planta 218, 501-515.
50. Porter, K.R., and Caulfield, J.B. (1958). The formation of the cell plate during cytokinesis in Allium cepa L. In Proceedings of the Fourth Congress on Electron Microcopy, Vol. 2. (Berlin, Germany), pp. 503-507.
51. Porter, K.R., and Machado, R.D. (1960). Studies on the endoplasmic reticulum IV. Its form and distribution during mitosis in cells of onion root tip. J. Biophys. Biochem. Cytol. 7, 167-180.
52. Rees, D.A. (1977). Polysaccharide Shapes. (New York: John Wiley & Sons).
53. Rensing, K.H., Samuels, A.L., and Savidge, R.A. (2002). Ultrastructure of vascular cambial cell cytokinesis in pine seedlings preserved by cryofixation and substitution. Protoplasma 220, 39-49.
54. Samuels, A.L., Giddings, T.H., Jr., and Staehelin, L.A. (1995). Cytokinesis in tobacco BY-2 and root tip cells: A new model of cell plate formation in higher plants. J. Cell Biol. 130, 1345-1357.
55. Sanderfoot, A.A., Assaad, F.F., and Raikhel, N.V. (2000). The Arabidopsis genome. An abundance of soluble N-ethylmaleimide-sensitive factor adaptor protein receptors. Plant Physiol. 124, 1558-1569.
56. Schopfer, C.R., and Hepler, P.K. (1991). Distribution of membranes and the cytoskeleton during cell plate formation in pollen mother cells of Tradescantia. J. Cell Sci. 100, 717-728.
57. Seguí-Simarro, J.M., Testillano, P.S., and Risueño, M.C. (2003). Hsp70 and Hsp90 change their expression and subcellular localization after microspore embryogenesis induction in Brassica napus cv. Topas. J. Struct. Biol. 142, 379-391.
58. Sollner, R., Glasser, G., Wanner, G., Somerville, C.R., Jürgens, G., and Assaad, F.F. (2002). Cytokinesis-defective mutants of Arabidopsis. Plant Physiol. 129, 678-690.
59. Staehelin, L.A. (1997). The plant ER: A dynamic organelle composed of a large number of discrete functional domains. Plant J. 11, 1151-1165.
60. Staehelin, L.A., and Moore, I. (1995). The plant Golgi apparatus -Structure, functional organization and trafficking mechanisms. Annu. Rev. Plant Physiol. Plant Mol. Biol. 46, 261-288.
61. Stowell, M.H.B., Marks, B., Wigge, P., and McMahon, H.T. (1999). Nucleotide-dependent conformational changes in dynamin: Evidence for a mechanochemical molecular spring. Nat. Cell Biol. 1, 27-32.
62. Strasburger, E. (1875). Über Zellbildung und Zellteilung. (Jena, Germany: Fischer).
63. TerBush, D.R., Guo, W., Dunkelbarger, S., and Novick, P. (2001). Purification and characterization of yeast exocyst complex. Methods Enzymol. 329, 100-110.
64. TerBush, D.R., Maurice, T., Roth, D., and Novick, P. (1996). The Exocyst is a multiprotein complex required for exocytosis in Saccharomyces cerevisiae. EMBO J. 15, 6483-6494.
65. Thakur, B.R., Singh, R.K., and Handa, A.K. (1997). Chemistry and uses of pectin - A review. Crit. Rev. Food Sci. Nutr. 37, 47-73.
66. Ueda, K., Sakaguchi, S., Kumagai, F., Hasezawa, S., Quader, H., and Kristen, U. (2003). Development and disintegration of phragmoplasts in living cultured cells of a GFP::TUA6 transgenic Arabidopsis thaliana plant. Protoplasma 220, 111-118.
67. Valster, A.M., Pierson, E.S., Valenta, R., Hepler, P.K., and Emons, A.M.C. (1997). Probing the plant actin cytoskeleton during cytokinesis and interphase by profilin microinjection. Plant Cell 9, 1815-1824.
68. van der Bliek, A.M. (1999). Functional diversity in the dynamin family. Trends Cell Biol. 9, 96-102.
69. Verma, D.P., and Hong, Z. (2001). Plant callose synthase complexes. Plant Mol. Biol. 47, 693-701.
70. Verma, D.P.S. (2001). Cytokinesis and building of the cell plate in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52, 751-784.
71. Waizenegger, I., Lukowitz, W., Assaad, F., Schwarz, H., Jurgens, G., and Mayer, U. (2000). The Arabidopsis KNOLLE and KEULE genes interact to promote vesicle fusion during cytokinesis. Curr. Biol. 10, 1371-1374.
72. Whaley, W.G., and Mollenhauer, H.H. (1963). The Golgi apparatus and cell plate formation. A postulate. J. Cell Biol. 17, 216-221.
73. Wolfe, J., and Steponkus, P.L. (1983). Mechanical properties of the plasma membrane of isolated plant protoplasts - Mechanism of hyperosmotic and extracellular freezing-injury. Plant Physiol. 71, 276-285.
74. Zhang, D., Wadsworth, P., and Hepler, P.K. (1990). Microtubule dynamics in living dividing plant cells: Confocal imaging of microinjected fluorescent brain tubulin. Proc. Natl. Acad. Sci. USA 87, 8820-8824.
75. Zhang, G.F., and Staehelin, L.A. (1992). Functional compartmentation of the Golgi apparatus of plant cells - Immunocytochemical analysis of high pressure frozen and freeze-substituted sycamore maple suspension culture cells. Plant Physiol. 99, 1070-1083.