Actin-Based Domains of the “Cell Periphery Complex” and their Associations with Polarized “Cell Bodies” in Higher Plants

F. Baluka; D. Volkmann; P. W. Barlow

doi:10.1055/s-2000-3705

Plant Biology, Table of Contents

Plant Biol (Stuttg) 2000; 2(3): 253-267
DOI: 10.1055/s-2000-3705

Review Article

Georg Thieme Verlag Stuttgart ·New York

Actin-Based Domains of the “Cell Periphery Complex” and their Associations with Polarized “Cell Bodies” in Higher Plants

F. Baluška ^1,3 , D. Volkmann ¹ , P. W. Barlow ²

¹ Institute of Botany, Department of Plant Cell Biology, University of Bonn, Bonn, Germany
² IACR - Long Ashton Research Station, Department of Agricultural Sciences, University of Bristol, Long Ashton, Bristol, UK
³ Institute of Botany, Slovak Academy of Sciences, Bratislava, Slovakia

Abstract

Nascent cellulosic cell wall microfibrils and transverse (with respect of cell growth axis) arrays of cortical microtubules (MTs) beneath the plasma membrane (PM) are two well established features of the periphery of higher plant cells. Together with transmembrane synthase complexes, they represent the most characteristic form of a “cell periphery complex” of higher plant cells which determines the orientation of the diffuse (intercalary) type of their cell growth. However, there are some plant cell types having distinct cell cortex domains which are depleted of cortical MTs. These particular cell cortex domains are, instead, typically enriched with components of the actin-based cytoskeleton. In higher plants, this feature is prominent at extending apices of two cell types displaying tip growth - pollen tubes and root hairs. In the latter cell type, highly dynamic F-actin meshworks accumulate at extending tips, and they appear to be critical for the apparently motile character of these subcellular domains. Importantly, tip growth of both root hairs and pollen tubes is immediately stopped when the most dynamic F-actin population is depolymerized with low levels of anti-F-actin drugs. Intriguingly, MTs of tip-growing plant cells are organized in the form of longitudinal arrays, throughout the cytoplasm, which interconnect the extending tips with the subapical nuclei. This suggests that actin-rich cell cortex domains polarize plant “cell bodies” represented by nucleus-MTs complexes. A similar polarization of “cell bodies” is typical of mitotic and cytokinetic plant cells. A further type of MT-depleted and actomyosin-enriched plant cell cortex domain comprises the plasmodesmata. Primary plasmodesmata are formed during cytokinesis as part of the myosin VIII-enriched callosic cell plates, representing “juvenile” forms of the plant “cell periphery complex”. In phylogenetic terms the association between F-actin and the PM may be considered for a more “primitive” form of cellular organization than does the association of cortical MTs with the PM. We hypothesize that the actin cytoskeleton is a natural partner of the PM in all eukaryotic cells. In most plant cells, however, it was replaced by a tubulin-based “cell periphery apparatus” which regulates, via still unknown mechanisms, the spatial deposition of nascent cellulosic microfibrils synthesized by PM-associated synthase complexes.

Abbreviations

AFs: actin filaments

ER: endoplasmic reticulum

MTs: microtubules

PM: plasma membrane

Key words

Actin - callose - cell cortex - cell plate - cytokinesis - microtubules - myosin - phragmoplast - plant “cell body” - plant cell polarity - plasmodesmata - tip growth

Full Text

References

01 Aist, J. R.. (1976); Papillae and related wound plugs of plant cells. Annu. Rev. Phytopathol.. 14 145-163
02 Akashi, T., and Shibaoka, H.. (1991); Involvement of transmembrane proteins in the association of cortical microtubules with the plasma membrane in tobacco BY-2 cells. J. Cell Sci.. 98 169-174
03 Ayscough, K. R.,, Stryker, J.,, Pokala, N.,, Sanders, M.,, Crews, P.,, and Drubin, D. G.. (1997); High rates of actin filament turnover in budding yeast and roles for actin in establishment and maintenance of cell polarity revealed using the actin inhibitor latrunculin A. J. Cell Biol.. 137 399-416
04 Asada, T., and Collings, D.. (1997); Molecular motors in higher plants. Trends Plant Sci.. 2 29-37
05 Asada, T.,, Kuriyama, R.,, and Shibaoka, H.. (1997); TKRP125, a kinesin-related protein involved in the centrosome-independent organization of the cytokinetic apparatus in tobacco BY-2 cells. J. Cell Sci.. 110 179-189
06 Bajer, A., and Smirnova, E. A.. (1999); Reorganization of microtubular cytoskeleton and formation of cellular processes during post-telophase in Haemanthus endosperm. Cell Motil. Cytoskel.. 44 96-109
07 Baluška, F.,, Bacigálová, K.,, Oud, J. L.,, Hauskrecht, M.,, and Kubica, Š.. (1995 a); Rapid reorganization of microtubular cytoskeleton accompanies early changes in nuclear ploidy and chromatin structure in postmitotic cells of barley leaves infected with powdery mildew. Protoplasma. 185 140-151
08 Baluška, F.,, Barlow, P. W.,, Hauskrecht, M.,, Kubica, Š.,, Parker, J. S.,, and Volkmann, D.. (1995 b); Microtubule arrays in maize root cells. Interplay between the cytoskeleton, nuclear organization and post-mitotic cellular growth patterns. New Phytol.. 130 177-192
09 Baluška, F.,, Barlow, P. W.,, Parker, J. S.,, and Volkmann, D.. (1996); Symmetric reorganization of radiating microtubules around pre- and post-mitotic nuclei of dividing cells organized within intact root meristems. J. Plant Physiol.. 149 119-128
10 Baluška, F.,, Vitha, S.,, Barlow, P. W.,, and Volkmann, D.. (1997 a); Rearrangements of F-actin arrays in growing cells of intact maize root apex tissues: A major developmental switch occurs in the postmitotic transition region. Eur. J. Cell Biol.. 72 113-121
11 Baluška, F.,, Volkmann, D.,, and Barlow, P. W.. (1997 b); Nuclear components with microtubule organizing properties in multicellular eukaryotes: Functional and evolutionary considerations. Int. Rev. Cytol.. 175 91-135
12 Baluška, F.,, Šamaj, J.,, Volkmann, D.,, and Barlow, P. W.. (1997 c); Impact of taxol-mediated stabilization of microtubules on nuclear morphology, ploidy levels and cell growth in maize roots. Biol. Cell. 89 221-231
13 Baluška, F.,, Barlow, P. W.,, Lichtscheidl, I. K.,, and Volkmann, D.. (1998 a); The plant cell body: A cytoskeletal tool for cellular development and morphogenesis. Protoplasma. 202 1-10
14 Baluška, F.,, Volkmann, D.,, and Barlow, P. W.. (1998 b); Tissue- and development-specific distributions of cytoskeletal elements in growing cells of the maize root apex. Plant Biosystems. 132 251-265
15 Baluška, F.,, Šamaj, J.,, Napier, R.,, and Volkmann, D.. (1999); Maize calreticulin localizes preferentially to plasmodesmata. Plant J.. 19 481-488
16 Baluška, F.. (1999) Morphogenic Shaping of Maize Root Cells via Dynamic Cytoskeleton. University of Bonn; Habilitation Thesis
17 Baluška, F.,, Barlow, P. W.,, and Volkmann, D.. (2000) Actin and myosin VIII in developing root cells. Actin: A Dynamic Framework for Multiple Plant Cell Functions. Staiger, C. J., Baluška, F., Volkmann, D., and Barlow, P. W., eds. Dordrecht; Kluwer Academic Publishers pp. 457-476
18 Barlow, P. W.. (1994) Cell division in meristem and their contribution to organogenesis and plant form. Shape and Form in Plants and Fungi. Ingram, D. S. and Hudson, A., eds. London; Academic Press pp. 169-193
19 Barlow, P. W., and Baluška, F.. (2000); Cytoskeletal perspective on root growth and morphogenesis. Annu. Rev. Plant Physiol. Plant Mol. Biol.. 51 289-322
20 Bartnicki-Garcia, S.,, Hegert, F.,, and Gierz, G.. (1989); Computer simulation of fungal morphogenesis and the mathematical basis of hyphal (tip) growth. Protoplasma. 153 46-57
21 Baskin, T. I., and Wilson, J. E.. (1997); Inhibitors of protein kinases and phosphatases alter root morphology and disorganize cortical microtubules. Plant Physiol.. 113 493-502
22 Bayles, C. J.,, Ghemawat, M. S.,, and Aist, J. R.. (1990); Inhibition by 2-deoxy-D-glucose of callose formation, papilla deposition, and resistance to powdery mildew in an ml-o barley mutant. Physiol. Mol. Plant Pathol.. 36 63-72
23 Beffa, R. S.,, Hofer, R.-S.,, Thomas, M.,, and Meins, F. J.. (1996); Decreased susceptibility to viral disease of β-1,3 glucanase-deficient plants generated by antisense transformation. Plant Cell. 8 1001-1011
24 Benkert, R.,, Obermeyer, G.,, and Bentrup, F.-W.. (1997); The turgor pressure of growing lily pollen tubes. Protoplasma. 198 1-8
25 Bibikova, T. N.,, Blancaflor, E. B.,, and Gilroy, S.. (1999); Microtubules regulate tip growth and orientation in root hairs of Arabidopsis thaliana. . Plant J.. 17 657-665
26 Blackman, L. M., and Overall, R. L.. (1998); Immunolocalisation of the cytoskeleton to plasmodesmata of Chara corallina. . Plant J.. 14 733-741
27 Blackman, L. M.,, Harper, J. D. I.,, and Overall, R. L.. (1999); Localization of a centrin-like protein to higher plant plasmodesmata. Eur. J. Cell Biol.. 78 297-304
28 Braun, M., and Wasteneys, G. O.. (1998); Reorganization of the actin and microtubule cytoskeleton throughout blue-light-induced differentiation of Characean protonemata into multicellular thalli. Protoplasma. 202 38-53
29 Braun, M.,, Baluška, F.,, von Witsch, M.,, and Menzel, D.. (1999); Redistribution of actin, profilin and phosphatidylinositol-4,5-bisphosphate (PIP₂) in growing and maturing root hairs. Planta. 209 435-443
30 Brown, R. C., and Lemmon, B. E.. (1988); Cytokinesis occurs at boundaries of domains delimited by nuclear-based microtubules in sporocytes of Conocephalum conicum (Bryophyta). . Cell Motil. Cytoskel.. 11 139-146
31 Brown, R. C.,, Lemmon, B. E.,, and Olsen, O.-A.. (1994); Endosperm development in barley: microtubule involvement in the morphogenetic pathway. Plant Cell. 6 1241-1252
32 Brown, R. C.,, Lemmon, B. E.,, and Olsen, O.-A.. (1996); Polarization predicts the pattern of cellularization in cereal endosperm. Protoplasma. 192 168-177
33 Carazo-Salas, R. E.,, Guarguaglini, G.,, Gruss, O. J.,, Segref, A.,, Karsenti, E.,, and Mattaj, I. W.. (1999); Generation of GTP-bound Ran by RCC1 is required for chromatin-induced mitotic spindle formation. Nature. 400 178-181
34 Cárdenas, L.,, Vidali, L.,, Domínguez, J.,, Pérez, H.,, Sánchez, F.,, Hepler, P. K.,, and Quinto, C.. (1998); Rearrangement of actin microfilaments in plant root hairs responding to Rhizobium etli nodulation signals. Plant Physiol.. 116 871-877
35 Casero, P. J., and Knox, J. P.. (1995); The monoclonal antibody JIM5 indicates patterns of pectin deposition in relation to pit fields at the plasma-membrane-face of tomato pericarp cell walls. Protoplasma. 188 133-137
36 Chaffey, N.,, Barnett, J.,, and Barlow, P. W.. (1999); A cytoskeletal basis for wood formation in angiosperm trees: The involvement of cortical microtubules. Planta. 208 19-30
37 Chaffey, N., and Barlow, P. W.. (2000) Actin in the secondary vascular system of woody plants. Actin: A Dynamic Framework for Multiple Plant Cell Functions. Staiger, C. J., Baluška, F., Volkmann, D., and Barlow, P. W., eds. Dordrecht; Kluwer Academic Publishers pp. 587-600
38 Chant, J.. (1994); Cell polarity in yeast. Curr. Opin. Cell Biol.. 6 110-119
39 Cho, S.-O., and Wick, S. M.. (1990); Distribution and function of actin in the developing stomatal complex of winter rye (Secale cereale cv. Puma). Protoplasma. 157 154-164
40 Cho, S.-O., and Wick, S. M.. (1991); Actin in the developing stomatal complex of winter rye: a comparison of actin antibodies and Rh-phalloidin labelling of control and CB-treated tissues. Cell Motil. Cytoskel.. 19 25-36
41 Clayton, L., and Lloyd, C. W.. (1985); Actin organization during the cell cycle in meristematic plant cells. Exp. Cell Res.. 156 231-238
42 Cleary, A. L.. (1995); F-actin redistributions at the division site in living Tradescantia stomatal complexes as revealed by microinjection of rhodamine-phalloidin. Protoplasma. 185 152-165
43 Cleary, A. L., and Mathesius, U.. (1996); Rearrangements of F-actin during stomatogenesis visualized by confocal microscopy in fixed and permeabilised Tradescantia leaf epidermis. Bot. Acta. 109 15-24
44 Cyr, R. J.. (1994); Microtubules in plant morphogenesis: Role of the cortical array. Annu. Rev. Cell Biol.. 10 153-180
45 Delmer, D. H., and Stone, B. A.. (1988) Biosynthesis of plant cell walls. Biochemistry of Plants. A Comprehensive Treatise, Vol. 14. Preiss, J., ed. San Diego; Academic Press pp. 373-420
46 Delmer, D. H.,, Volokita, M.,, Solomon, M.,, Fritz, U.,, Delphendahl, W.,, and Herth, W.. (1993); A monoclonal antibody recognizes a 65 kD higher plant membrane polypeptide which undergoes cation-dependent association with callose synthase in vitro and co-localizes with sites of high callose deposition in vivo. . Protoplasma. 176 33-42
47 Derksen, J.,, Rutten, T.,, Lichtscheidl, I. K.,, de Win, A. H. N.,, Pierson, E. S.,, and Rongen, G.. (1995); Quantitative analysis of the distribution of organelles in tobacco pollen tubes: implications for exocytosis and endocytosis. Protoplasma. 188 267-276
48 Derksen, J.,, Li, Y.-Q.,, Knuiman, B.,, and Geurts, H.. (1999); The wall of Pinus sylvestris L. pollen tubes. Protoplasma. 208 26-36
49 Dickinson, H. G., and Sheldon, J. M.. (1984); A radial system of microtubules extending between the nucleus envelope and the plasma membrane during early male haplophase in flowering plants. Planta. 161 86-90
50 Didry, D.,, Carlier, M.-F.,, and Pantaloni, D.. (1998); Synergy between actin depolymerizing factor/cofilin and profilin in increasing actin filament turnover. J. Biol. Chem.. 273 25 602-25 611
51 Ding, B.. (1997); Cell-to-cell transport of macromolecules through plasmodesmata: A novel signalling pathway in plants. Trends Cell Biol.. 7 5-9
52 Ding, B., and Lucas, W. J.. (1996) Secondary plasmodesmata: Biogenesis, special functions and evolution. Membranes: Specialized Functions in Plants. Smallwood, M., Knox, J. P., and Bowles, D. J., eds. Oxford; Bios Scientific Publishers pp. 489-506
53 Ding, B.,, Haudenshield, J. S.,, Hull, R. J.,, Wolf, S.,, Beachy, R. N.,, and Lucas, W. J.. (1992); Secondary plasmodesmata are specific sites of localization of the tobacco mosaic virus movement protein in transgenic tobacco plants. Plant Cell. 4 915-928
54 Ding, B.,, Kwon, M.-O.,, and Warnberg, L.. (1996); Evidence that actin filaments are involved in controlling the permeability of plasmodesmata in tobacco mesophyll. Plant J.. 10 157-164
55 Drubin, D. G.. (1991); Development of cell polarity in budding yeast. Cell. 65 1093-1096
56 Du, H.,, Clarke, A. E.,, and Bacic, A.. (1996); Arabinogalactan-proteins: A class of extracellular matrix proteoglycans involved in plant growth and development. Trends Cell Biol.. 6 411-414
57 Ehlers, K., and Kollmann, R.. (1996); Formation of branched plasmodesmata in regenerating Solanum nigrum-protoplasts. Planta. 199 126-138
58 Ehlers, K.,, Schulz, M.,, and Kollmann, R.. (1996); Subcellular localization of ubiquitin in plant protoplasts and the function of ubiquitin in selective degradation of outer-wall plasmodesmata in regenerating protoplasts. Planta. 199 139-151
59 Endlé, M.-C.,, Stoppin, V.,, Lambert, A.-M.,, and Schmit, A.-C.. (1998); The growing cell plate of higher plants is a site of both actin assembly and vinculin-like antigen recruitment. Eur. J. Cell Biol.. 77 10-18
60 Eleftheriou, E. P.. (1995); Phloem structure and cytochemistry. Bios (Macedonia, Greece). 3 81-124
61 Erickson, H. P.. (1995); FtsZ, a prokaryotic homolog of tubulin?. Cell. 80 367-370
62 Esau, K., and Thorsch, J.. (1985); Sieve plate pores and plasmodesmata, the communication channels of the symplast: Ultrastructural aspects and developmental relations. Am. J. Bot.. 72 1641-1653
63 Ettinger, L., and Doljanski, F.. (1992); On the generation of form by the continuous interactions between cells and their extracellular matrix. Biol. Rev. Cambr. Philosoph. Soc.. 67 459-489
64 Fowler, J. E., and Quatrano, R. S.. (1997); Plant cell morphogenesis: Plasma membrane interactions with the cytoskeleton and cell wall. Annu. Rev. Cell Dev. Biol.. 13 697-743
65 Friedman, W. E.. (1992); Evidence of a pre-angiosperm origin of endosperm: Implications for the evolution of flowering plants. Science. 255 336-339
66 Fulcher, R. G.,, McCully, M. E.,, Setterfield, G.,, and Sutherland, J.. (1976); β-1,3-glucans may be associated with cell plate formation during cytokinesis. Can. J. Bot.. 54 539-542
67 Galway, M. E., and McCully, M. E.. (1987); The time course of the induction of callose in wounded pea roots. Protoplasma. 139 77-91
68 Genre, A., and Bonfante, P.. (1998); Actin versus tubulin configurations in arbuscule-containing cells from mycorrhizal tobacco roots. New Phytol.. 140 745-752
69 Gibbon, B. C.,, Kovar, D. R.,, and Staiger, C. J.. (1999); Latrunculin B has different effects on pollen germination and tube growth. Plant Cell. 11 2349-2364
70 Giddings, T. H., Jr., and Staehelin, L. A.. (1991) Microtubule-mediated control of microfibril deposition: A re-examination of the hypothesis. The Cytoskeletal Basis of Plant Growth and Form. Lloyd, C. W., ed. San Diego; Academic Press pp. 85-100
71 Gindullis, F., and Meier, I.. (1999); Matrix attachment region binding protein MFP-1 is localized in discrete domains at the nuclear envelope. Plant Cell. 11 1117-1128
72 Green, P. B.. (1984) Analysis of axis extension. Positional Controls in Plant Development. Barlow, P. W. and Carr, D. J., eds. Cambridge; Cambridge University Press pp. 53-82
73 Green, P. B.. (1986) Plasticity in shoot development: A biophysical view. Plasticity in Plants. Jennings, D. H. and Trewavas, A. J., eds. Cambridge; Company of Biologists pp. 211-232
74 Gross, P.,, Julius, C.,, Schmelzer, E.,, and Hahlbrock, K.. (1993); Translocation of cytoplasm and nucleus to fungal penetration sites is associated with depolymerization of microtubules and defence gene activation in infected, cultured parsley cells. EMBO J.. 12 1735-1744
75 Guens-Longly, B., and Waterkeyn, L.. (1976); Les étapes callosiques de la plaque cellulaire dans la mitose somatique chez Hyacinthus orientalis L. C. R. Acad. Sci., Ser. D. 283 761-763
76 Gundersen, G. G., and Bulinski, J. C.. (1988); Selective stabilization of microtubules oriented towards the direction of cell migration. Proc. Natl. Acad. Sci. USA. 85 5946-5950
77 Gunning, B. E. S.. (1982) The cytokinetic apparatus: Its development and spatial regulation. The Cytoskeleton in Plant Growth and Development. Lloyd, C. W., ed. London; Academic Press pp. 229-292
78 Gunning, B. E. S., and Wick, S. M.. (1985); Preprophase bands, phragmoplasts, and spatial control of cytokinesis. J. Cell Sci., Suppl.. 2 157-179
79 Gupta, G. D., and Heath, I. B.. (1997); Actin disruption by latrunculin B causes turgor-related changes in tip growth of Saprolegnia ferax hyphae. Fung. Genet. Biol.. 21 64-75
80 Gupta, R. S., and Golding, G. B.. (1996); The origin of the eukaryotic cell. Trends Biochem. Sci.. 21 166-171
81 Gupta, R. S.,, Aitken, K.,, Falah, M.,, and Singh, B.. (1994); Cloning of Giardia lamblia HSP70 homologs: Implications regarding origin of eukaryotic cells and of endoplasmic reticulum. Proc. Natl. Acad. Sci. USA. 91 2895-2899
82 Hardham, A. R.,, Green, P. B.,, and Lang, J. M.. (1980); Reorganization of cortical microtubules and cellulose deposition during leaf formation in Graptopetalum paraguayense. . Planta. 149 181-195
83 Harold, F. M.. (1997); How hyphae grow: Morphogenesis explained?. Protoplasma. 197 137-147
84 Harold, R. L.,, Money, F. P.,, and Harold, F. M.. (1996); Growth and morphogenesis in Saprolegnia ferax: Is turgor required?. Protoplasma. 191 105-114
85 Hasegawa, Y.,, Nakamura, S.,, and Nakamura, N.. (1996); Immunocytochemical localization of callose in the germinated pollen of Camellia japonica. . Protoplasma. 194 133-139
86 Hasezawa, S., and Nozaki, H.. (1999); Role of cortical microtubules in the orientation of cellulose microfibrils deposition in higher-plant cells. Protoplasma. 209 98-104
87 Hasezawa, S.,, Kumagai, F.,, and Nagata, T.. (1997); Sites of microtubule reorganization in tobacco BY-2 cells during cell-cycle progression. Protoplasma. 198 202-209
88 Hauser, M.-Th.,, Morikami, A.,, and Benfey, P. N.. (1995); Conditional root expansion mutants of Arabidopsis. . Development. 121 1237-1252
89 Heath, I. B.. (1990); The roles of actin in tip growth of fungi. Int. Rev. Cytol.. 123 95-127
90 Heath, M. C.,, Nimchuk, Z. L.,, and Xu, H.. (1997); Plant nuclear migrations as indicators of critical interactions between resistant or susceptible cowpea epidermal cells and invasion hyphae of the cowpea rust fungus. New Phytol.. 135 689-700
91 Heinlein, M.,, Epel, B. L.,, Padgett, H. S.,, and Beachy, R. N.. (1995); Interactions of tobamovirus movement protein with the plant cytoskeleton. Science. 270 1983-1985
92 Heinlein, M.,, Padgett, H. S.,, Gens, J. S.,, Pickard, B. G.,, Casper, S. J.,, Epel, B. L.,, and Beachy, R. N.. (1998); Changing patterns of localization of the tobacco mosaic virus movement protein and replicase to the endoplasmic reticulum and microtubules during infection. Plant Cell. 10 1107-1120
93 Hepler, P. K.. (1982); Endoplasmic reticulum in the formation of the cell plate and plasmodesmata. Protoplasma. 111 121-133
94 Hirai, N.,, Sonobe, S.,, and Hayashi, T.. (1998); In situ synthesis of β-glucan microfibrils on tobacco plasma membrane sheets. Proc. Nat. Acad. Sci. USA. 95 15 102-15 106
95 Huang, M., and Zhang, L.. (1999); Association of the movement protein of alfalfa mosaic virus with the endoplasmic reticulum and its trafficking in epidermal cells of onion bulb scales. MPMI. 12 680-690
96 Hughes, J. E., and Gunning, B. E. S.. (1980); Glutaraldehyde-induced deposition of callose. Can. J. Bot.. 58 250-258
97 Hussey, R. S.,, Mims, C. W.,, and Westcott, S. W. III. (1992); Immunocytochemical localization of callose in root cortical cells parasitized by the ring nematode Criconemella xenoplax. . Protoplasma. 171 1-6
98 Itaya, A.,, Woo, Y.-M.,, Masuta, C.,, Bao, Y.,, Nelson, R.,, and Ding, B.. (1998); Developmental regulation of intercellular protein trafficking through plasmodesmata in tobacco leaf epidermis. Plant Physiol.. 118 373-385
99 Jacob, S. R., and Northcote, D. H.. (1985); In vitro glucan synthesis by membranes of celery petioles: The role of the membrane in determining the type of linkage formed. J. Cell Sci. Suppl.. 2 1-11
100 Jauh, G. Y. et al.. (1997); Adhesion of lily pollen tubes on an artificial matrix. Sex. Plant Reprod.. 10 173-180
101 Jensen, L. C. W.. (1981); Division, growth, and branch formation in protonemata of the moss Physcomitrium turbinatum: Studies of sequential cytological changes in living cells. Protoplasma. 107 301-317
102 Jiang, C.-J.,, Weeds, A. G.,, and Hussey, P. J.. (1997); The maize actin-depolymerizing factor, ZmADF3, redistributes to the growing tip of elongating root hairs and can be induced to translocate into the nucleus with actin. Plant J.. 12 1035-1043
103 Kadota, A., and Wada, M.. (1995); Cytoskeletal aspects of nuclear migration during tip-growth in the fern Adiantum protonemal cell. Protoplasma. 188 170-179
104 Kakimoto, T., and Shibaoka, H.. (1987); Actin filaments and microtubules in the preprophase band and phragmoplast of tobacco cells. Protoplasma. 140 151-156
105 Kakimoto, T., and Shibaoka, H.. (1988); Cytoskeletal ultrastructure of phragmoplast-nuclei complexes isolated from cultured tobacco cells. Protoplasma, Suppl.. 2 95-103
106 Kasteel, D. T. J.,, Perbal, M.-C.,, Boyer, J.-C.,, Welling, J.,, Goldbach, R. W.,, Maule, A. J.,, and van Lent, J. W. M.. (1996); The movement protein of cowpea mosaic virus and cauliflower mosaic virus induce tubular structures in plant and insect cells. J. Gen. Virol.. 77 2857-2864
107 Kaverina, I.,, Rottner, K.,, and Small, J. V.. (1998); Targeting, capture, and stabilization of microtubules at early focal adhesions. J. Cell Biol.. 142 181-190
108 Kauss, H.. (1996) Callose synthesis. Membranes: Specialized Functions in Plants. Smallwood, M., Knox, J. P., and Bowles, D. J., eds. Oxford; Bios Scientific Publishers pp. 77-92
109 Kennard, J. L., and Cleary, A. L.. (1997); Pre-mitotic nuclear migration in subsidiary mother cells of Tradescantia occurs in G1 of the cell cycle and requires F-actin. Cell Motil. Cytoskel.. 36 55-67
110 Kimura, S., and Itoh, T.. (1996); New cellulose synthesizing complexes (terminal complexes) involved in animal cellulose biosynthesis in the tunicate Metandrocarpa uedai. . Protoplasma. 194 151-163
111 Kimura, S.,, Laosinchai, W.,, Itoh, T.,, Cui, X.,, Lindner, C. R.,, and Brown, R. M. Jr.. (1999); Immunogold labeling of rosette terminal cellulose-synthesizing complex in the vascular plant Vigna angularis. . Plant Cell. 11 2075-2086
112 Klein, A. S.,, Montezinos, D.,, and Delmer, D. P.. (1981); Cellulose and 1,3-glucan synthesis during the early stages of wall regeneration in soybean protoplasts. Planta. 152 105-114
113 Knox, J. P.. (1992); Cell adhesion, cell separation and plant morphogenesis. Plant J.. 2 137-141
114 Kobayashi, I.,, Kobayashi, Y.,, and Hardham, A. R.. (1994); Dynamic reorganization of microtubules and microfilaments in flax cells during the resistance response to flax rust infection. Planta. 195 237-247
115 Kobayashi, Y.,, Kobayashi, I.,, Funaki, Y.,, Fujimoto, S.,, Takemoto, T.,, and Kunoh, H.. (1997); Dynamic reorganization of microfilaments and microtubules is necessary for expression of non-host resistance in barley coleoptile cells. Plant J.. 11 525-537
116 Koonce, M. P.. (1996); Making a connection: The “other” microtubule end. Cell Motil. Cytoskel.. 35 85-93
117 Kropf, D. L.,, Berger, S. K.,, and Quatrano, R. S.. (1989); Actin localization during Fucus embryogenesis. Plant Cell. 1 191-200
118 Kumarasinghe, R. M. K., and Nutman, P. S.. (1977); Rhizobium-stimulated callose formation in clover root hairs and its relation to infection. J. Exp. Bot.. 28 961-976
119 Lachaud, S., and Maurousset, L.. (1996); Occurrence of plasmodesmata between differentiating vessels and other xylem cells in Sorbus torminalis L. Crantz and their fate during xylem maturation. Protoplasma. 191 220-226
120 Lancelle, S. A., and Hepler, P. K.. (1992); Ultrastructure of freeze-substituted pollen tubes of Lilium longiflorum. . Protoplasma. 167 215-230
121 Langan, K. J., and Nothnagel, E. A.. (1997); Cell surface arabinogalactan-proteins and their relation to cell proliferation and viability. Protoplasma. 196 87-98
122 Li, R.,, Zheng, Y.,, and Drubin, D. G.. (1995); Regulation of cortical actin cytoskeleton assembly during polarized cell growth in budding yeast. J. Cell Biol.. 128 599-615
123 Li, H.,, Bacic, A.,, and Read, S. M.. (1997); Activation of pollen tube callose synthase by detergents. Evidence for different mechanisms of action. Plant Physiol.. 114 1255-1265
124 Lin, C.-H., and Forscher, P.. (1993); Cytoskeletal remodeling during growth cone-target interactions. J. Cell Biol.. 121 1369-1383
125 Liu, B., and Palevitz, B. A.. (1992); Organization of cortical microfilaments in dividing root cells. Cell Motil. Cytoskel.. 23 252-264
126 Lloyd, C. W., and Traas, J. A.. (1988); The role of F-actin in determining the division plane of carrot suspension cells. Drug studies. Development. 102 211-222
127 Lloyd, C. W.,, Pearce, K. J.,, Rawlins, D. J.,, Ridge, R. W.,, and Shaw, P. J.. (1987); Endoplasmic microtubules connect the advancing nucleus to the tip of legume root hairs, but F-actin is involved in basipetal migration. Cell Motil. Cytoskel.. 8 27-36
128 Lord, E. M., and Sanders, L. C.. (1992); Roles for the extracellular matrix in plant development and pollination: A special case of cell movements in plants. Dev. Biol.. 153 16-28
129 Lord, E. M.,, Walling, L. L.,, and Jauh, G. Y.. (1996) Cell adhesion in plants and its role in pollination. Membranes: Specialized Functions in Plants. Smallwood, M., Knox, J. P., and Bowles, D. J., eds. Oxford; Bios Scientific Publishers pp. 21-37
130 Lucas, W. J.,, Ding, B.,, and van der Schoot, C.. (1993); Plasmodesmata and the supracellular nature of plants. New Phytol.. 125 435-476
131 Machesky, L. M., and Insall, R. H.. (1999); Signaling to actin dynamics. J. Cell Biol.. 146 267-272
132 Margulis, L.. (1981) Symbiosis in Cell Evolution. San Francisco; WH Freeman and Company
133 Margulis, L.. (1996); Archaeal-eubacterial mergers in the origin of eukarya: Phylogenetic classification of life. Proc. Natl. Acad. Sci. USA. 93 1071-1076
134 Martin, W., and Herrmann, R. G.. (1998); Gene transfer from organelles to the nucleus: How much, what happens, and why?. Plant Physiol.. 118 9-17
135 Mathur, J.,, Spielhofer, P.,, Kost, B.,, and Chua, N.-H.. (1999); The actin cytoskeleton is required to elaborate and maintain spatial patterning during trichome cell morphogenesis in Arabidopsis thaliana. . Development. 126 5559-5568
136 McClinton, R. S., and Sung, Z. R.. (1997); Organization of cortical microtubules at the plasma membrane in Arabidopsis. . Planta. 201 252-260
137 McLean, B. G.,, Zupan, J.,, and Zambryski, P. C.. (1995); Tobacco mosaic virus movement protein associates with the cytoskeleton in tobacco cells. Plant Cell. 7 2101-2114
138 McLusky, S. R.,, Bennett, M. H.,, Beale, M. H.,, Lewis, M. J.,, Gaskin, P.,, and Mansfield, J. W.. (1999); Cell wall alterations and localized accumulation of feruloyl-3′-methoxytyramine in onion epidermis at sites of attempted penetration by Botrytis allii are associated with actin polarisation, peroxidase activity and suppression of flavonoid biosynthesis. Plant J.. 17 523-535
139 Meyer, Y., and Herth, W.. (1978); Chemical inhibition of cell wall formation and cytokinesis, but not of nuclear division, in protoplasts of Nicotiana tabacum L. cultivated in vitro. . Planta. 142 253-262
140 Miller, D. D.,, de Ruijter, N. C. A.,, Bisseling, B.,, and Emons, A. M. C.. (1999); The role of actin in root hair morphogenesis: Studies with lipochito-oligosaccharide as a growth stimulator and cytochalasin as an actin perturbing drug. Plant J.. 17 141-154
141 Mineyuki, Y., and Gunning, B. E. S.. (1990); A role for preprophase bands of microtubules in maturation of new cell walls, and a general proposal on the function of preprophase band sites in cell division in higher plants. J. Cell Sci.. 97 527-537
142 Mineyuki, Y., and Palevitz, B. A.. (1990); Relationship between preprophase band organization, F-actin and the division site in Allium. Fluorescence and morphometric studies on cytochalasin-treated cells. J. Cell Sci.. 97 283-295
143 Mineyuki, Y.,, Iida, H.,, and Anraku, Y.. (1994); Loss of microtubules in the interphase cells of onion (Allium cepa L.) root tips from the cell cortex and their appearance in the cytoplasm after treatment with cycloheximide. Plant Physiol.. 104 281-284
144 Mitchison, T. J.. (1995); Evolution of a dynamic cytoskeleton. Phil. Trans. Royal Soc. London, B. 349 299-304
145 Mitchison, T. J., and Cramer, L. P.. (1996); Actin-based cell motility and cell locomotion. Cell. 84 371-379
146 Mollenhauer, H. H., and Morré, D. J.. (1976); Cytochalasin B, but not colchicine, inhibits migration of secretory vesicles in root tips of maize. Protoplasma. 87 39-48
147 Money, N. P., and Harold, F. M.. (1993); Two water molds can grow without measurable turgor pressure. Planta. 190 426-430
148 Morvan, O.,, Quentin, M.,, Jauneau, A.,, Mareck, A.,, and Morvan, C.. (1998); Immunogold localization of pectin methylesterases in the cortical tissues of flax hypocotyl. Protoplasma. 202 175-184
149 Mueller, S. C., and Brown, R. M. Jr.. (1982); The control of cellulose microfibril deposition in the cell wall of higher plants. I. Can directed membrane flow orient cellulose microfibrils? Indirect evidence from freeze-fractured plasma membranes of maize and pine seedlings. Planta. 154 489-500
150 Nakamura, A., and Kohama, K.. (1999); Calcium regulation of the actin-myosin interaction of Physarum polycephalum. . Int. Rev. Cytol.. 191 53-98
151 Nagata, Y.,, Kumagai, F.,, and Hasezawa, S.. (1994); The origin and organization of cortical microtubules during the transition between M and G1 phases of the cell cycle as observed in highly synchronized cells of tobacco BY-2. Planta. 193 567-572
152 Nedukha, E. M.. (1998); Effects of clinorotation on the polysaccharide content of resynthesised walls of protoplasts. Adv. Space Res.. 21 1121-1126
153 Nickle, T. C., and Meinke, D. W.. (1998); A cytokinesis-defective mutant of Arabidopsis (cyt1) characterized by embryonic lethality, incomplete cell walls, and excessive callose accumulation. Plant J.. 15 321-332
154 Nishikata, T.,, Hibino, T.,, and Nishida, H.. (1992); The centrosome-attracting body, microtubule system, and posterior egg cytoplasm are involved in positioning of cleavage planes in the ascidian embryo. Dev. Biol.. 209 72-85
155 Northcote, D. H.. (1991) Site of cellulose synthesis. Biosynthesis and Biodegradation of Cellulose. Haigler, C. H. and Weimer, P. J., eds. New York; Marcel Dekker Inc.
156 Northcote, D. H.,, Davey, R.,, and Lay, J.. (1989); Use of antisera to localize callose, xylan and arabinogalactan in the cell plate, primary and secondary walls of plant cells. Planta. 178 353-366
157 Nothnagel, E. A.. (1997); Proteoglycans and related components in plant cells. Int. Rev. Cytol.. 174 195-291
158 Oparka, K. J.,, Roberts, A. G.,, Boevink, P.,, Santa Cruz, S.,, Roberts, I.,, Pradel, K. S.,, Imlau, A.,, Kotlitzky, G.,, Sauer, N.,, and Epel, B.. (1999); Simple, but not branched, plasmodesmata allow the nonspecific trafficking of proteins in developing tobacco leaves. Cell. 97 743-754
159 Ovecka, M.,, Baluška, F.,, Nadubinská, M.,, and Volkmann, D.. (2000); Actomyosin and exocytosis inhibitors alter root hair morphology in Poa annua L. Biológia. 55 105-114
160 Overall, R. L., and Blackman, L. M.. (1996); A model of the macromolecular structure of plasmodesmata. Trends Plant Sci.. 9 307-311
161 Palevitz, B. A.. (1980); Comparative effects of phalloidin and cytochalasin B on motility and morphogenesis in Allium. . Can. J. Bot.. 58 773-785
162 Palevitz, B. A.. (1987); Accumulation of F-actin during cytokinesis in Allium. Correlation with microtubule distribution and the effects of drugs. Protoplasma. 141 24-32
163 Palevitz, B. A.. (1988); Cytochalasin-induced reorganization of actin in Allium root cells. Cell Motil. Cytoskel.. 9 283-298
164 Palevitz, B. A., and Hepler, P. K.. (1974); The control of the plane of division during stomatal differentiation in Allium. II. Drug studies. Chromosoma. 46 327-341
165 Pappelis, A. J.,, Pappelis, G. A.,, and Kulfinski, F. B.. (1974); Nuclear orientation in onion epidermal cells in relation to wounding and infection. Phytopathology. 64 1010-1012
166 Pennell, R. I.,, Janniche, L.,, Scofield, G. N.,, Booij, H.,, de Vries, S. C.,, and Roberts, K.. (1992); Identification of a transitional cell state in the developmental pathway to carrot somatic embryogenesis. J. Cell Biol.. 119 1371-1380
167 Perbal, M.-C.,, Thomas, C. L.,, and Maule, A. J.. (1993); Cauliflower mosaic virus gene I product (P1) forms tubular structures which extend from the surface of infected protoplasts. Virology. 195 281-285
168 Pérez, H. E.,, Sánchez, N.,, Vidali, L.,, Hernández, J. M.,, Lara, M.,, and Sánchez, F.. (1994); Actin isoforms in non-infected roots and symbiotic root nodules of Phaseolus vulgaris L. Planta. 193 51-56
169 Phillips, G. D.,, Preshaw, C.,, and Steer, M. W.. (1988); Dictyosome vesicle production and plasma membrane turnover in auxin-stimulated outer epidermal cells of coleoptile segments from Avena sativa (L.). Protoplasma. 145 59-65
170 Pickard, B. G., and Beachy, R. N.. (1999); Intercellular connections are developmentally controlled to help move molecules through the plant. Cell. 98 5-8
171 Pickett-Heaps, J. D., and Klein, A. G.. (1998); Tip growth in plant cells may be amoeboid and not generated by turgor pressure. Proc. Royal Soc. London, B. 265 1453-1459
172 Pickett-Heaps, J. D.,, Gunning, B. E. S.,, Brown, R. C.,, Lemmon, B. E.,, and Cleary, A. L.. (1999); The cytoplast concept in dividing plant cells: cytoplasmic domains and the evolution of spatially organized cell division. Am. J. Bot.. 86 153-172
173 Pierson, E. S., and Cresti, M.. (1992); Cytoskeleton and cytoplasmic organization of pollen and pollen tubes. Int. Rev. Cytol.. 140 73-125
174 Pope, D. G.,, Thorpe, J. R.,, Al-Azzawi, M. J.,, and Hall, J. L.. (1979); The effect of cytochalasin B on the rate of growth and ultrastructure of wheat coleoptiles and maize roots. Planta. 144 373-383
175 Prosser, J. I.. (1990) Comparison of tip growth in prokaryotic and eukaryotic filamentous microorganisms. Tip Growth in Plant and Fungal Cells. Heath, I. B., ed. San Diego; Academic Press pp. 233-259
176 Radford, J. E., and White, R. G.. (1998); Localization of a myosin-like protein to plasmodesmata. Plant J.. 14 743-750
177 Radford, J. E.,, Vesk, M.,, and Overall, R. L.. (1998); Callose deposition at plasmodesmata. Protoplasma. 201 30-37
178 Reichel, C., and Beachy, R. N.. (1998); Tobacco mosaic virus infection induces severe morphological changes of the endoplasmic reticulum. Proc. Natl. Acad. Sci. USA. 95 11 169-11 174
179 Reichel, C.,, Más, P.,, and Beachy, R. N.. (1999); The role of the ER and cytoskeleton in plant viral trafficking. Trends Plant Sci.. 4 458-462
180 Reichelt, S.,, Knight, A. E.,, Hodge, T. P.,, Baluška, F.,, Šamaj, J.,, Volkmann, D.,, and Kendrick-Jones, J.. (1999); Characterization of the unconventional myosin VIII in plant cells and its localization at the post-cytokinetic cell wall. Plant J.. 19 555-569
181 Ridge, R. W.. (1990); Cytochalasin D causes abnormal wall ingrowths and organelle crowding in legume root hairs. Bot. Mag. (Tokyo). 103 87-96
182 Robbins, J. R.,, Barth, A.,, Marquis, H.,, de Hostos, E.,, Nelson, W. J.,, and Theriot, J. A.. (1999); Listeria monocytogenes exploits normal host cell processes to spread from cell to cell. J. Cell Biol.. 146 1333-1349
183 Roy, S. J.,, Holdaway-Clarke, T. L.,, Hackett, G. R.,, Kunkel, J. G.,, Lord, E M.,, and Hepler, P. K.. (1999); Uncoupling secretion and tip growth in lily pollen tubes: Evidence for the role of calcium in exocytosis. Plant J.. 19 379-386
184 de Ruijter, N. C. A.,, Rook, M. B.,, Bisseling, T., and Emons, A. M. C.. (1998); Lipochito-oligosaccharides re-initiate root hair tip growth in Vicia sativa with high calcium and spectrin-like antigen at the tip. Plant J.. 13 341-350
185 Šamaj, J.,, Peters, M.,, Volkmann, D.,, and Baluška, F.. (2000); Effects of myosin ATPase inhibitor 2,3-butanedione 2-monoxime on distributions of myosins, F-actin, microtubules, and cortical endoplasmic reticulum in maize root apices. Plant Cell Physiol.. 41 in press
186 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
187 Sanders, L. C., and Lord, E. M.. (1992); A dynamic role for the stylar matrix in pollen tube extension. Int. Rev. Cytol.. 140 297-318
188 Sato, S.,, Ogasawara, Y.,, and Sakuragi, S.. (1995) The relationship between growth, nucleus migration and cytoskeleton in root hairs of radish. Structure and Function of Roots. Baluška, F., Ciamporová, M., Gašparíková, O., and Barlow, P. W., eds. Dordrecht; Kluwer Academic Publishers pp. 69-74
189 Schmit, A.-C.. (2000) Actin during mitosis and cytokinesis. Actin: A Dynamic Framework for Multiple Plant Cell Functions. Staiger, C. J., Baluška, F., Volkmann, D., and Barlow, P. W., eds. Dordrecht; Kluwer Academic Publishers pp. 437-456
190 Schmidt, A., and Hall, M. N.. (1998); Signaling to the actin cytoskeleton. Annu. Rev. Cell Dev. Biol.. 14 305-338
191 Schnepf, E., and Sawidis, T.. (1991); Filament disruption in Funaria protonemata: Occlusion of plasmodesmata. Bot. Acta. 104 98-102
192 Shannon, T. M.,, Picton, J. M.,, and Steer, M. W.. (1984); The inhibition of dictyosome vesicle formation in higher plant cells by cytochalasin D. Eur. J. Cell Biol.. 33 144-147
193 Showalter, A. M.. (1993); Structure and function of plant cell wall proteins. Plant Cell. 5 9-23
194 Sievers, A., and Schnepf, E.. (1981) Morphogenesis and polarity of tubular cells with tip growth. Cytomorphogenesis in Plants. Cell Biology Monographs, Vol. 8. Kiermayer, O., ed. Wien - New York; Springer-Verlag pp. 165-299
195 Sitte, P.. (1993); Symbiogenetic evolution of complex cells and complex plastids. Eur. J. Protistol.. 29 131-143
196 Sivaguru, M., and Horst, W. J.. (1998); The distal part of the transition zone is the most aluminum-sensitive apical root zone of maize. Plant Physiol.. 116 155-163
197 Sivaguru, M.,, Baluška, F.,, Volkmann, D.,, Felle, H.,, and Horst, W. J.. (1999 a); Impacts of aluminum on cytoskeleton of maize root apex: Short-term effects on distal part of transition zone. Plant Physiol.. 119 1073-1082
198 Sivaguru, M.,, Yamamoto, Y.,, and Matsumoto, H.. (1999 b); Differential impacts of aluminium on microtubule organisation depends on growth phase in suspension-cultured tobacco cells. Physiol. Plant.. 107 110-119
199 Škalamera, D., and Heath, M. C.. (1995); Changes in plant endomembrane system associated with callose synthesis during the interaction between cowpea (Vigna unguiculata) and the cowpea rust fungus (Uromyces vignae). . Can. J. Bot.. 73 1731-1738
200 Škalamera, D., and Heath, M. C.. (1996); Cellular mechanisms of callose deposition in response to fungal infection or chemical damage. Can. J. Bot.. 74 1236-1242
201 Škalamera, D., and Heath, M. C.. (1998); Changes in the cytoskeleton accompanying infection-induced nuclear movements and the hypersensitive response in plant cells invaded by rust fungi. Plant J.. 16 191-200
202 Škalamera, D.,, Jibodh, S.,, and Heath, M. C.. (1997); Callose deposition during the interaction between cowpea (Vigna unguiculata) and the monokaryotic stage of the cowpea rust fungus (Uromyces vignae). . New Phytol.. 136 511-524
203 Smith, M. M., and McCully, M. E.. (1977); Mild temperature “stress” and callose synthesis. Planta. 136 65-70
204 Staehelin, L. A., and Hepler, P. K.. (1996); Cytokinesis in higher plants. Cell. 84 821-824
205 Staiger, C. J.. (2000); Signaling to the actin cytoskeleton in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol.. 51 257-288
206 Staiger, C. J.,, Gibbon, B. C.,, Kovar, D. R.,, and Zonia, L. E.. (1997); Profilin and actin-depolymerizing factor: modulators of actin organization in plants. Trends Plant Sci.. 2 275-281
207 Steer, M. W.. (1990) The role of actin in tip growth. Tip Growth of Plant and Fungal Cells. Heath, I. B., ed. San Diego; Academic Press pp. 119-145
208 Takahashi, H., and Jaffe, M. J.. (1984); Thigmomorphogenesis: the relationship of mechanical perturbation to elicitor-like activity and ethylene production. Physiol. Plant.. 61 401-411
209 Takemoto, D.,, Furuse, K.,, Doke, N.,, and Kawakita, K.. (1997); Identification of chitinase and osmotin-like protein as actin-binding proteins in suspension-cultured potato cells. Plant Cell Physiol.. 38 441-448
210 Takemoto, D.,, Maeda, H.,, Yoshioka, H.,, Doke, N.,, and Kawakita, K.. (1999); Effect of cytochalasin D on defense responses of potato tuber discs treated with hyphal wall components of Phytophthora infestans. . Plant Sci.. 141 219-226
211 Taylor, L. P., and Hepler, P. K.. (1997); Pollen germination and tube growth. Annu. Rev. Plant Physiol. Plant Mol. Biol.. 48 461-491
212 Timmers, A. C. J.,, Auriac, M.-C.,, and Truchet, G.. (1999); Refined analysis of early symbiotic steps of the Rhizobium-Medicago interaction in relationship with microtubular cytoskeleton rearrangements. Development. 126 3617-3628
213 Traas, J.,, Bellini, C.,, Nacry, P.,, Kronenberger, J.,, Bouchez, D.,, and Caboche, M.. (1995); Normal differentiation patterns in plants lacking microtubular preprophase bands. Nature. 375 676-677
214 Turner, A.,, Wells, B.,, and Roberts, K.. (1994); Plasmodesmata of maize root tips: Structure and composition. J. Cell Sci.. 107 3351-3361
215 Uetake, Y.,, Farquhar, M. L.,, and Peterson, R. L.. (1997); Changes in microtubule arrays in symbiotic orchid protocorms during fungal colonization and senescence. New Phytol.. 135 701-709
216 Van Amstel, T. N. M., and Kengen, H. M. P.. (1996); Callose deposition in the primary wall of suspension cells and regenerating protoplasts, and its relationship to patterned cellulose synthesis. Can. J. Bot.. 74 1040-1049
217 Vasiliev, J. M.. (1987); Actin cortex and microtubular system in morphogenesis: Cooperation and competition. J. Cell Sci. Suppl.. 8 1-18
218 Vaughn, K. C.,, Hoffman, J. C.,, Hahn, M. G.,, and Staehelin, L. A.. (1996); The herbicide dichlobenil disrupts cell plate formation: Immunogold characterization. Protoplasma. 194 117-132
219 Vega, L. R., and Solomon, F.. (1997); Microtubule function in morphological differentiation: growth zones and growth cones. Cell. 89 825-828
220 Verma, D. P. S.. (1992); Signals in root nodule organogenesis and endocytosis of Rhizobium. . Plant Cell. 4 373-382
221 Verma, D. P. S., and Gu, X.. (1996); Vesicle dynamics during cell-plate formation in plants. Trends Plant Sci.. 1 145-149
222 Volkmann, D., and Baluška, F.. (1999); The actin cytoskeleton in plants: From transport networks to signaling networks. Microsc. Res. Tech.. 47 135-154
223 Waddle, J. A.,, Karpova, T. S.,, Waterston, R. H.,, and Cooper, J. A.. (1996); Movement of cortical actin patches in yeast. J. Cell Biol.. 132 861-870
224 Ward, B. M.,, Medville, R.,, Lazarowitz, S. G.,, and Turgeon, R.. (1997); The geminivirus BL1 movement protein is associated with endoplasmic reticulum-derived tubules in developing phloem cells. J. Virol.. 71 3726-3733
225 Waterkeyn, L.. (1961); Étude des dépôts de callose au niveau des parois sporocytaires au moyen de la microscopie de fluorescence. Compt. Rendus Acad. Sci., Ser. D (Paris). 252 4025-4027
226 Waterkeyn, L.. (1967); Sur l'existence d'un “stade callosique”, présenté par la paroi cellulaire, au cours de la cytocinèse. Compt. Rendus Acad. Sci., Ser. D (Paris). 265 1792-1794
227 Welch, M. D.,, Mallavarapu, A.,, Rosenblatt, J.,, and Mitchison, T. J.. (1997); Actin dynamics in vivo. . Curr. Opin. Cell Biol.. 9 54-61
228 Wessels, D.,, Voss, E.,, Von Bergen, N.,, Burns, R.,, Stites, J.,, and Soll, D. R.. (1998); A computer-assisted system for reconstructing and interpreting the dynamic three-dimensional relationships of the outer surface, nucleus and pseudopods of crawling cells. Cell Motil. Cytoskel.. 41 225-246
229 White, R. G.,, Badelt, K.,, Overall, R. L.,, and Vesk, M.. (1994); Actin associated with plasmodesmata. Protoplasma. 180 169-184
230 Whitehead, L. F.,, Day, D. A.,, and Hardham, A. R.. (1998); Cytoskeletal arrays in the cells of soybean root nodules: The role of actin microfilaments in the organisation of symbiosomes. Protoplasma. 203 194-2051184
231 Wick, S. M.. (1991); Spatial aspects of cytokinesis in plant cells. Curr. Opin. Cell Biol.. 3 253-260
232 Wilhelmi, L. K., and Preuss, D.. (1997); Blazing new trails. Pollen tube guidance in flowering plants. Plant Physiol.. 113 307-312
233 Williamson, R. E.. (1991); Orientation of cortical microtubules in interphase plant cells. Int. Rev. Cytol.. 129 135-206
234 Xu, J.-R.,, Staiger, C. J.,, and Hamer, J. E.. (1998); Inactivation of the mitogen-activated protein kinase Mps1 from the rice blast fungus prevents penetration of host cells but allows activation of plant defense response. Proc. Natl. Acad. Sci. USA. 95 12 713-12 718
235 Zheng, H.,, Wang, G.,, and Zhang, L.. (1997); Alfalfa mosaic virus movement protein induces tubules in plant protoplasts. MPMI. 10 1010-1014
236 Zigmond, S. H.. (1996); Signal transduction and actin filament organization. Curr. Opin. Cell Biol.. 8 66-73
237 Zinkl, G. M.,, Wilhelmi, L. K.,, and Preuss, D.. (1998); Sticking together: Cell adhesion interactions in Arabidopsis reproduction. J. Plant Res.. 111 299-305
238 Yahalom, A.,, Lando, R.,, Katz, A.,, and Epel, B. L.. (1998); A calcium-dependent protein kinase is associated with maize mesocotyl plasmodesmata. J. Plant Physiol.. 153 354-362
239 Yokota, E.,, Muto, S.,, and Shimmen, T.. (1999); Inhibitory regulation of higher-plant myosin by Ca²⁺ ions. Plant Physiol.. 119 231-239

F. Baluška

Botanisches Institut Rheinische Friedrich-Wilhelms-Universität Bonn

Kirschallee 1 53115 Bonn Germany

Email: baluska@uni-bonn.de

Section Editor: T. Nagata