Abstract
Cell plate formation in tobacco root tips and synchronized dividing suspension cultured tobacco BY-2 cells was examined using cryofixation and immunocytochemical methods. Due to the much improved preservation of the cells, many new structural intermediates have been resolved, which has led to a new model of cell plate formation in higher plants. Our electron micrographs demonstrate that cell plate formation consists of the following stages: (1) the arrival of Golgi-derived vesicles in the equatorial plane, (2) the formation of thin (20 +/- 6 nm) tubes that grow out of individual vesicles and fuse with others giving rise to a continuous, interwoven, tubulo-vesicular network, (3) the consolidation of the tubulo-vesicular network into an interwoven smooth tubular network rich in callose and then into a fenestrated plate-like structure, (4) the formation of hundreds of finger-like projections at the margins of the cell plate that fuse with the parent cell membrane, and (5) cell plate maturation that includes closing of the plate fenestrae and cellulose synthesis. Although this is a temporal chain of events, a developing cell plate may be simultaneously involved in all of these stages because cell plate formation starts in the cell center and then progresses centrifugally towards the cell periphery. The "leading edge" of the expanding cell plate is associated with the phragmoplast microtubule domain that becomes concentrically displaced during this process. Thus, cell plate formation can be summarized into two phases: first the formation of a membrane network in association with the phragmoplast microtubule domain; second, cell wall assembly within this network after displacement of the microtubules. The phragmoplast microtubules end in a filamentous matrix that encompasses the delicate tubulo-vesicular networks but not the tubular networks and fenestrated plates. Clathrin-coated buds/vesicles and multivesicular bodies are also typical features of the network stages of cell plate formation, suggesting that excess membrane material may be recycled in a selective manner. Immunolabeling data indicate that callose is the predominant lumenal component of forming cell plates and that it forms a coat-like structure on the membrane surface. We postulate that callose both helps to mechanically stabilize the early delicate membrane networks of forming cell plates, and to create a spreading force that widens the tubules and converts them into plate-like structures. Cellulose is first detected in the late smooth tubular network stage and its appearance seems to coincide with the flattening and stiffening of the cell plate.
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- Asada T., Shibaoka H. Isolation of polypeptides with microtubule-translocating activity from phragmoplasts of tobacco BY-2 cells. J Cell Sci. 1994 Aug;107(Pt 8):2249–2257. doi: 10.1242/jcs.107.8.2249. [DOI] [PubMed] [Google Scholar]
- Ayala J. Transport and internal organization of membranes: vesicles, membrane networks and GTP-binding proteins. J Cell Sci. 1994 Apr;107(Pt 4):753–763. doi: 10.1242/jcs.107.4.753. [DOI] [PubMed] [Google Scholar]
- Cluett E. B., Wood S. A., Banta M., Brown W. J. Tubulation of Golgi membranes in vivo and in vitro in the absence of brefeldin A. J Cell Biol. 1993 Jan;120(1):15–24. doi: 10.1083/jcb.120.1.15. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cronshaw J., Esau K. Cell division in leaves of Nicotiana. Protoplasma. 1968;65(1):1–24. doi: 10.1007/BF01666368. [DOI] [PubMed] [Google Scholar]
- Dahl R., Staehelin L. A. High-pressure freezing for the preservation of biological structure: theory and practice. J Electron Microsc Tech. 1989 Nov;13(3):165–174. doi: 10.1002/jemt.1060130305. [DOI] [PubMed] [Google Scholar]
- Damke H., Baba T., Warnock D. E., Schmid S. L. Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. J Cell Biol. 1994 Nov;127(4):915–934. doi: 10.1083/jcb.127.4.915. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Euteneuer U., Jackson W. T., McIntosh J. R. Polarity of spindle microtubules in Haemanthus endosperm. J Cell Biol. 1982 Sep;94(3):644–653. doi: 10.1083/jcb.94.3.644. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Felder S., Miller K., Moehren G., Ullrich A., Schlessinger J., Hopkins C. R. Kinase activity controls the sorting of the epidermal growth factor receptor within the multivesicular body. Cell. 1990 May 18;61(4):623–634. doi: 10.1016/0092-8674(90)90474-s. [DOI] [PubMed] [Google Scholar]
- Hepler P. K., Jackson W. T. Microtubules and early stages of cell-plate formation in the endosperm of Haemanthus katherinae Baker. J Cell Biol. 1968 Aug;38(2):437–446. doi: 10.1083/jcb.38.2.437. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hepler P. K., Newcomb E. H. Fine structure of cell plate formation in the apical meristem of Phaseolus roots. J Ultrastruct Res. 1967 Aug 30;19(5):498–513. doi: 10.1016/s0022-5320(67)80076-5. [DOI] [PubMed] [Google Scholar]
- Hinshaw J. E., Schmid S. L. Dynamin self-assembles into rings suggesting a mechanism for coated vesicle budding. Nature. 1995 Mar 9;374(6518):190–192. doi: 10.1038/374190a0. [DOI] [PubMed] [Google Scholar]
- Hopkins C. R., Gibson A., Shipman M., Miller K. Movement of internalized ligand-receptor complexes along a continuous endosomal reticulum. Nature. 1990 Jul 26;346(6282):335–339. doi: 10.1038/346335a0. [DOI] [PubMed] [Google Scholar]
- Hyde G. J., Lancelle S., Hepler P. K., Hardham A. R. Freeze substitution reveals a new model for sporangial cleavage in Phytophthora, a result with implications for cytokinesis in other eukaryotes. J Cell Sci. 1991 Dec;100(Pt 4):735–746. doi: 10.1242/jcs.100.4.735. [DOI] [PubMed] [Google Scholar]
- Jones G. J. On estimating freezing times during tissue rapid freezing. J Microsc. 1984 Dec;136(Pt 3):349–360. doi: 10.1111/j.1365-2818.1984.tb00546.x. [DOI] [PubMed] [Google Scholar]
- Jones M. G., Payne H. L. Cytokinesis in Impatiens balsamina and the effect of caffeine. Cytobios. 1978;20(78):79–91. [PubMed] [Google Scholar]
- Kiss J. Z., Giddings T. H., Jr, Staehelin L. A., Sack F. D. Comparison of the ultrastructure of conventionally fixed and high pressure frozen/freeze substituted root tips of Nicotiana and Arabidopsis. Protoplasma. 1990;157:64–74. doi: 10.1007/BF01322639. [DOI] [PubMed] [Google Scholar]
- Klausner R. D., Donaldson J. G., Lippincott-Schwartz J. Brefeldin A: insights into the control of membrane traffic and organelle structure. J Cell Biol. 1992 Mar;116(5):1071–1080. doi: 10.1083/jcb.116.5.1071. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lambert A. M. Microtubule-organizing centers in higher plants. Curr Opin Cell Biol. 1993 Feb;5(1):116–122. doi: 10.1016/s0955-0674(05)80016-x. [DOI] [PubMed] [Google Scholar]
- Pearse B. M., Robinson M. S. Clathrin, adaptors, and sorting. Annu Rev Cell Biol. 1990;6:151–171. doi: 10.1146/annurev.cb.06.110190.001055. [DOI] [PubMed] [Google Scholar]
- Platt-Aloia K. A., Thomson W. W. Freeze fracture of intact plant tissues. Stain Technol. 1982 Nov;57(6):327–334. doi: 10.3109/10520298209066734. [DOI] [PubMed] [Google Scholar]
- Poste G., Allison A. C. Membrane fusion. Biochim Biophys Acta. 1973 Dec 28;300(4):421–465. doi: 10.1016/0304-4157(73)90015-4. [DOI] [PubMed] [Google Scholar]
- Roberts K., Northcote D. H. The structure of sycamore callus cells during division in a partially synchronized suspension culture. J Cell Sci. 1970 Mar;6(2):299–321. doi: 10.1242/jcs.6.2.299. [DOI] [PubMed] [Google Scholar]
- Staehelin L. A., Giddings T. H., Jr, Kiss J. Z., Sack F. D. Macromolecular differentiation of Golgi stacks in root tips of Arabidopsis and Nicotiana seedlings as visualized in high pressure frozen and freeze-substituted samples. Protoplasma. 1990;157(1-3):75–91. doi: 10.1007/BF01322640. [DOI] [PubMed] [Google Scholar]
- Takei K., McPherson P. S., Schmid S. L., De Camilli P. Tubular membrane invaginations coated by dynamin rings are induced by GTP-gamma S in nerve terminals. Nature. 1995 Mar 9;374(6518):186–190. doi: 10.1038/374186a0. [DOI] [PubMed] [Google Scholar]
- Vantard M., Levilliers N., Hill A. M., Adoutte A., Lambert A. M. Incorporation of Paramecium axonemal tubulin into higher plant cells reveals functional sites of microtubule assembly. Proc Natl Acad Sci U S A. 1990 Nov;87(22):8825–8829. doi: 10.1073/pnas.87.22.8825. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wolniak S. M., Hepler P. K., Jackson W. T. Detection of the membrane-calcium distribution during mitosis in Haemanthus endosperm with chlorotetracycline. J Cell Biol. 1980 Oct;87(1):23–32. doi: 10.1083/jcb.87.1.23. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zhang D., Wadsworth P., Hepler P. K. Microtubule dynamics in living dividing plant cells: confocal imaging of microinjected fluorescent brain tubulin. Proc Natl Acad Sci U S A. 1990 Nov;87(22):8820–8824. doi: 10.1073/pnas.87.22.8820. [DOI] [PMC free article] [PubMed] [Google Scholar]