- Email: [email protected]
pit-fields, and cell-to-cell coupling
Cell Biology International 27 (2003) 289–291
Cell Biology International www.elsevier.com/locate/jnlabr/ycbir
Short communication
Unconventional myosins of the plant-specific class VIII: endocytosis, cytokinesis, plasmodesmata/pit-fields, and cell-to-cell coupling D. Volkmann a,*, T. Mori b, U.K. Tirlapur c, K. Ko¨nig c, T. Fujiwara b, J. Kendrick-Jones d, F. Balusˇka a a
Department of Plant Cell Biology, Botanisches Institut, Rheinische Friedrich-Wilhelms-Universita¨t Bonn, Kirschallee 1, D-53115 Bonn, Germany Laboratory of Plant Nutrition and Fertilizers, Department of Applied Biological Chemistry, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Yayoi, Bunkyo-ku, Tokyo 113-8657, Japan c Laser Microscopy Division, Institute of Anatomy II, Friedrich Schiller University Jena, Teichgraben 7, D-07743 Jena, Germany d Structural Studies Division, MRC Laboratory of Molecular Biology, Hills Road, Cambridge CB2 2QH, UK
b
Accepted 15 October 2002
AtATM1 myosin of Arabidopsis thaliana was the first plant myosin to be identified and sequenced (Knight and Kendrick-Jones, 1993). Based on its N-terminal motor domain and C-terminal sequences, it was assigned into its own class VIII (Reichelt et al., 1999). Currently, the sequences of seven myosins of this class can be found in the genomic databases (Balusˇka et al., 2001a; Liu et al., 2001; Reddy and Day, 2001; Reichelt and KendrickJones, 2000). They are characterized by a unique C-terminal tail region showing no apparent homologies to any other known myosins. This region, however, is highly conserved amongst individual members of this myosin class and contains multiple potential phosphorylation sites (Balusˇka et al., 2001a). Besides this tail region, AtATM1 myosin VIII contains an unusual N-terminal extension with a PEST domain prior to their conserved motor domain, 4 IQ motifs, and a short region of predicted -helical coiled coil domain which maybe responsible for dimerization (Balusˇka et al., 2001a; Reichelt and Kendrick-Jones, 2000). At the very end of C-terminus, clusters of basic residues are present which might be involved in binding to phospholipids (Knight and Kendrick-Jones, 1993). A polyclonal antibody was raised against the whole tail domain of AtATM1 myosin VIII (predicted coiled coil domain and unique C-terminal region) (Reichelt et al., 1999) which localizes these plant-specific myosins to the plasma * Corresponding author. Tel.: +49-228-734747; fax: +49-228-739004. E-mail address: [email protected] (D. Volkmann).
membrane at subcellular structures only observed in plant cells: namely cytokinetic cell plates and plasmodesmata (Balusˇka et al., 2000, 2001a; Reichelt et al., 1999). In addition, immunofluorescence spots of variable size are found distributed throughout the cytoplasm. Detailed analysis of subcellular distributions of myosin VIII and actin in cells of root apices suggest that myosin VIII maybe less important for intracellular motility and more involved in anchoring of actin filaments at cell peripheries (Balusˇka et al., 2000; Reichelt et al., 1999; Volkmann and Balusˇka, 1999). For example, abundant myosin VIII is highly localized at actin-enriched crosswalls, which anchor spindle poles in mitotic cells and longitudinal F-actin bundles in elongating cells. These patterns of subcellular distributions are dramatically altered during strong osmotic stress when almost all myosin VIII associates with callosic pit-fields of plasmolysing cells (F. Balusˇka and D. Volkmann, preliminary data). Additional possible roles for myosin VIII may include the following: organizing F-actin at cell peripheries, stabilizing the structurally delicate callosic cell plates during cytokinesis, and as structural supports for the cortical ER elements tightly underlying the plasma membrane both outside and within plasmodesmata. Moreover, our preliminary data suggest that myosin VIII might also drive invagination of the plasma membrane during fluid-phase endocytosis (Balusˇka et al., 2002) and interconnect the cytoskeleton with the plant extracellular matrix via putative binding of myosin VIII to the callose synthase complexes.
1065-6995/03/$ - see front matter 2003 Elsevier Science Ltd. All rights reserved. doi:10.1016/S1065-6995(02)00330-X
290
D. Volkmann et al. / Cell Biology International 27 (2003) 289–291
Table 1 Cell-to-cell coupling of FITC dextran and Lucifer Yellow between cells before and after microinjection of the myosin VIII antibody (0.2 mg/µl) Tobacco Mesophyll Cells 12 kDa FITC dextran 0% of cell-to-cell coupling 12 kDa FITC dextran/antibody 61% of cell-to-cell coupling Arabidopsis Root Epidermis Cells Lucifer Yellow 0% of cell-to-cell coupling Lucifer Yellow/antibody 30% of cell-to-cell coupling
The plasmodesmata of plant cells provide direct communication pathways within plant tissues for trafficking of diverse proteins and nucleic acids. These cell-to-cell channels are equipped with central ER element and are supported by the dynamic actin cytoskeleton (Balusˇka et al., 2001a; Volkmann and Balusˇka, 1999). Recent data have clearly revealed that plasmodesmata are gateable (Jackson, 2000; Wu et al., 2002; Zambryski and Crawford, 2000) and that this active gating process requires an intact actin cytoskeleton (Ding et al., 1996) which maybe controlled by actomyosin-based contractile forces (Balusˇka et al., 2001a; Overall et al., 2000). In addition to actin and myosin VIII, several myosin-like proteins were localized to plasmodesmata (Blackman and Overall, 1998; Overall et al., 2000; Radford and White, 1998; White et al., 1994). Moreover, Arp3-like protein (Van Gestel et al., submitted), ER-based calreticulin (Balusˇka et al., 1999), calcium-dependent protein kinase (F. Balusˇka and D. Volkmann, preliminary data; Yahalom et al., 1998), and centrin (Blackman et al., 1999) also localize to plasmodesmata and might participate in their active gating. Microinjection of the polyclonal antibody raised against the tail domain of myosin VIII (Reichelt et al., 1999) into living root epidermis cells of Arabidopsis roots and mesophyll cells of tobacco leafs resulted in dilatation of plasmodesmata, as evidenced by enhanced cell-to-cell coupling monitored by comicroinjected dextran FITC and Lucifer Yellow dye (Table 1). These findings strongly suggest that myosin VIII-based forces are required for the maintenance of the structural integrity of plasmodesmata and their immunodepletion causes nonspecific opening of plasmodesmata. This would be in agreement with findings that depletion of cellular ATP, either with azide or due to anaerobiosis, induces opening of plasmodesmata (Cleland et al., 1994; Tucker, 1993). In plant tissues, there are two well-known examples where the cell-to-cell coupling is shut off on a developmental basis. First, root trichoblast become symplastically isolated during root hair formation (Duckett et al., 1994; Tirlapur and Ko¨nig, 1999). Secondly, stomatal plasmodesmata are closed, and later even truncated, during development of guard cells of functional stomata (Palevitz and Hepler, 1985; Wille and Lucas, 1984). Our recent experimental data obtained using two-photon
near-infrared femtosecond laser scanning microscopy (Tirlapur and Ko¨nig, 2002a,b), which allows noninvasive laser-assisted propidium iodide loading into target cells (Tirlapur and Ko¨nig, 1999, 2002a,b), have revealed that postmitotic root cap statocytes are also symplastically isolated (U. Tirlapur, K. Ko¨nig, F. Balusˇka, and D. Volkmann, in preparation). This surprising result may be related to their well-known role as the gravisensing statocytes (Sack, 1991). Such speculation is strongly supported by our observations that gravistimulation of roots resulted in differential opening of statocyte plasmodesmata depending on their position within root caps (U. Tirlapur, K. Ko¨nig, F. Balusˇka, and D. Volkmann, in preparation). As postmitotic root cap statocytes, like trichoblasts initiating root hairs, do not show abundant myosin VIII at their plasmodesmata and pit-fields (Balusˇka et al., 2000), myosin VIII might be expected to be abundant within those plasmodesmata which are engaged in extensive cell-to-cell trafficking. In fact, plasmodesmata and pit-fields in the inner cortex cells of maize root apices, located within the transition root apex zone (Balusˇka et al., 2001b) where phloemunloading takes place, are equipped with abundant F-actin and myosin VIII molecules (Balusˇka et al., 2001a). Intriguingly, these callosic and actomyosinenriched domains act as selective platforms specialized for fluid-phase endocytosis (Balusˇka et al., submitted). All this suggest that unconventional myosins of the plant-specific class VIII act as a multifunctional molecules at callose-enriched subcellular domains of higher plant cells like cytokinetic cell plates, plasmodesmata, and pit-fields.
References Balusˇka F, Sˇamaj J, Napier R, Volkmann D. Maize calreticulin localizes preferentially to plasmodesmata in root apex. Plant J 1999;19:481–8. Balusˇka F, Barlow PW, Volkmann D. Actin and myosin VIII in developing root cells. In: Staiger CJ, Balusˇka F, Volkmann D, Barlow PW, editors. Actin: a dynamic framework for multiple plant cell functions. Dordrecht: Kluwer Academic, 2000;457–76. Balusˇka F, Cvrcˇkova´ F, Kendrick-Jones J, Volkmann D. Sink plasmodesmata as gateways for phloem unloading. Myosin VIII and calreticulin as molecular determinants of sink strength? Plant Physiol 2001a;126:39–46. Balusˇka F, Volkmann D, Barlow PW. A polarity crossroad in the transition growth zone of maize root apices: cytoskeletal and developmental implications. J Plant Growth Regul 2001b; 20:170–81. Balusˇka F, Sˇamaj J, Hlavacˇka A, Kendrick-Jones J, Volkmann D. Myosin VIII and F-actin enriched plasmodesmata in maize root inner cortex cells accomplish fluid-phase endocytosis via an actomyosin-dependent process; 2003 (submitted for publication). Blackman LM, Overall RL. Immunolocalisation of the cytoskeleton to plasmodesmata of Chara corallina. Plant J 1998;14:733–41. Blackman LM, Harper JDI, Overall RL. Localization of a centrin-like protein to higher plant plasmodesmata. Eur J Cell Biol 1999; 78:297–304.
D. Volkmann et al. / Cell Biology International 27 (2003) 289–291 Cleland RE, Fujiwara T, Lucas WJ. Plasmodesmal-mediated cell-tocell transport in wheat roots is modulated by anaerobic stress. Protoplasma 1994;178:81–5. Ding B, Kwon M-O, Warnberg L. Evidence that actin filaments are involved in controlling the permeability of plasmodesmata in tobacco mesophyll. Plant J 1996;10:157–64. Duckett CM, Oparka KJ, Prior DAM, Dolan L, Roberts K. Dyecoupling in the root epidermis of Arabidopsis is progressively reduced during development. Development 1994;120:3247–55. Jackson D. Opening up the communication channels. Recent insights into plasmodesmal function. Curr Opin Cell Biol 2000;3:394–9. Knight A, Kendrick-Jones J. A myosin-like protein from a higher plant. J Mol Biol 1993;231:148–54. Liu L, Zhou J, Pesacreta TC. Maize myosins: diversity, localization, and function. Cell Motil Cytoskeleton 2001;48:130–48. Overall RL, White RG, Blackman LM, Radford JE. Actin and myosin in plasmodesmata. In: Staiger CJ, Balusˇka F, Volkmann D, Barlow PW, editors. Actin: a dynamic framework for multiple plant cell functions. Dordrecht: Kluwer Academic, 2000;513–31. Palevitz BA, Hepler PK. Changes in dye coupling of stomatal cells of Allium and Commelina demonstrated by microinjection of Lucifer yellow. Planta 1985;164:473–9. Radford JE, White RG. Localization of a myosin-like protein to plasmodesmata. Plant J 1998;14:743–50. Reddy ASN, Day IS. Analysis of the myosin encoded in the recently completed Arabidopsis thaliana genome sequence. Genome Biol 2001;2(7):0024.1–24.17. Reichelt S, Kendrick-Jones J. Myosins. In: Staiger CJ, Balusˇka F, Volkmann D, Barlow PW, editors. Actin: a dynamic framework for multiple plant cell functions. Dordrecht: Kluwer Academic, 2000;29–44. Reichelt S, Knight AE, Hodge TP, Balusˇka F, Sˇamaj J, Volkmann D et al. Characterization of the unconventional myosin VIII in plant cells and its localization at the post-cytokinetic cell wall. Plant J 1999;19:555–69.
291
Sack F. Plant gravity sensing. Int Rev Cytol 1991;127:193–252. Tirlapur UK, Ko¨nig K. Near-infrared femtosecond laser pulses as a novel non-invasive means for dye-permeation and 3D imaging of localised dye-coupling in the Arabidopsis root meristem. Plant J 1999;20:363–70. Tirlapur UK, Ko¨nig K. Femtosecond near-infrared laser pulses as a versatile non-invasive tool for intra-tissue nanoprocessing in plants without compromising viability. Plant J 2002;31:1–12. Tirlapur UK, Ko¨nig K. Two-photon near-infrared femtosecond laser scanning microscopy in plant biology. In: Diaspro A, editor. Confocal and two-photon microscopy: foundations, applications, and advances. New York: Wiley-Liss, 2002;449–68. Tucker EB. Azide treatment enhances cell-to-cell diffusion in staminal hairs of Setcreasea purpurea. Protoplasma 1993;174:45–9. Van Gestel K, Slegers H, von Witsch M, Sˇamaj J, Balusˇka F, Verbelen J-P. Immunological evidence for the presence of homologues of actin related proteins Arp2 and Arp3 in tobacco and maize plants; 2003 (submitted for publication). Volkmann D, Balusˇka F. The actin cytoskeleton in plants: from transport networks to signaling networks. Microsc Res Tech 1999; 47:135–54. White RG, Badelt K, Overall RL, Vesk M. Actin associated with plasmodesmata. Protoplasma 1994;180:169–84. Wille AC, Lucas WJ. Ultrastructural and histochemical studies on guard cells. Planta 1984;160:129–42. Wu X, Weigel D, Wigge PA. Signaling in plants by intracellular RNA and protein movement. Genes Dev 2002;16:151–8. Yahalom A, Lando R, Katz A, Epel BL. A calcium-dependent protein kinase is associated with maize mesocotyl plasmodesmata. J Plant Physiol 1998;153:354–62. Zambryski P, Crawford K. Plasmodesmata: gatekeepers for cell-to-cell transport of developmental signals in plants. Annu Rev Cell Dev Biol 2000;16:393–421.
Cell Biology International www.elsevier.com/locate/jnlabr/ycbir
Short communication
Unconventional myosins of the plant-specific class VIII: endocytosis, cytokinesis, plasmodesmata/pit-fields, and cell-to-cell coupling D. Volkmann a,*, T. Mori b, U.K. Tirlapur c, K. Ko¨nig c, T. Fujiwara b, J. Kendrick-Jones d, F. Balusˇka a a
Department of Plant Cell Biology, Botanisches Institut, Rheinische Friedrich-Wilhelms-Universita¨t Bonn, Kirschallee 1, D-53115 Bonn, Germany Laboratory of Plant Nutrition and Fertilizers, Department of Applied Biological Chemistry, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Yayoi, Bunkyo-ku, Tokyo 113-8657, Japan c Laser Microscopy Division, Institute of Anatomy II, Friedrich Schiller University Jena, Teichgraben 7, D-07743 Jena, Germany d Structural Studies Division, MRC Laboratory of Molecular Biology, Hills Road, Cambridge CB2 2QH, UK
b
Accepted 15 October 2002
AtATM1 myosin of Arabidopsis thaliana was the first plant myosin to be identified and sequenced (Knight and Kendrick-Jones, 1993). Based on its N-terminal motor domain and C-terminal sequences, it was assigned into its own class VIII (Reichelt et al., 1999). Currently, the sequences of seven myosins of this class can be found in the genomic databases (Balusˇka et al., 2001a; Liu et al., 2001; Reddy and Day, 2001; Reichelt and KendrickJones, 2000). They are characterized by a unique C-terminal tail region showing no apparent homologies to any other known myosins. This region, however, is highly conserved amongst individual members of this myosin class and contains multiple potential phosphorylation sites (Balusˇka et al., 2001a). Besides this tail region, AtATM1 myosin VIII contains an unusual N-terminal extension with a PEST domain prior to their conserved motor domain, 4 IQ motifs, and a short region of predicted -helical coiled coil domain which maybe responsible for dimerization (Balusˇka et al., 2001a; Reichelt and Kendrick-Jones, 2000). At the very end of C-terminus, clusters of basic residues are present which might be involved in binding to phospholipids (Knight and Kendrick-Jones, 1993). A polyclonal antibody was raised against the whole tail domain of AtATM1 myosin VIII (predicted coiled coil domain and unique C-terminal region) (Reichelt et al., 1999) which localizes these plant-specific myosins to the plasma * Corresponding author. Tel.: +49-228-734747; fax: +49-228-739004. E-mail address: [email protected] (D. Volkmann).
membrane at subcellular structures only observed in plant cells: namely cytokinetic cell plates and plasmodesmata (Balusˇka et al., 2000, 2001a; Reichelt et al., 1999). In addition, immunofluorescence spots of variable size are found distributed throughout the cytoplasm. Detailed analysis of subcellular distributions of myosin VIII and actin in cells of root apices suggest that myosin VIII maybe less important for intracellular motility and more involved in anchoring of actin filaments at cell peripheries (Balusˇka et al., 2000; Reichelt et al., 1999; Volkmann and Balusˇka, 1999). For example, abundant myosin VIII is highly localized at actin-enriched crosswalls, which anchor spindle poles in mitotic cells and longitudinal F-actin bundles in elongating cells. These patterns of subcellular distributions are dramatically altered during strong osmotic stress when almost all myosin VIII associates with callosic pit-fields of plasmolysing cells (F. Balusˇka and D. Volkmann, preliminary data). Additional possible roles for myosin VIII may include the following: organizing F-actin at cell peripheries, stabilizing the structurally delicate callosic cell plates during cytokinesis, and as structural supports for the cortical ER elements tightly underlying the plasma membrane both outside and within plasmodesmata. Moreover, our preliminary data suggest that myosin VIII might also drive invagination of the plasma membrane during fluid-phase endocytosis (Balusˇka et al., 2002) and interconnect the cytoskeleton with the plant extracellular matrix via putative binding of myosin VIII to the callose synthase complexes.
1065-6995/03/$ - see front matter 2003 Elsevier Science Ltd. All rights reserved. doi:10.1016/S1065-6995(02)00330-X
290
D. Volkmann et al. / Cell Biology International 27 (2003) 289–291
Table 1 Cell-to-cell coupling of FITC dextran and Lucifer Yellow between cells before and after microinjection of the myosin VIII antibody (0.2 mg/µl) Tobacco Mesophyll Cells 12 kDa FITC dextran 0% of cell-to-cell coupling 12 kDa FITC dextran/antibody 61% of cell-to-cell coupling Arabidopsis Root Epidermis Cells Lucifer Yellow 0% of cell-to-cell coupling Lucifer Yellow/antibody 30% of cell-to-cell coupling
The plasmodesmata of plant cells provide direct communication pathways within plant tissues for trafficking of diverse proteins and nucleic acids. These cell-to-cell channels are equipped with central ER element and are supported by the dynamic actin cytoskeleton (Balusˇka et al., 2001a; Volkmann and Balusˇka, 1999). Recent data have clearly revealed that plasmodesmata are gateable (Jackson, 2000; Wu et al., 2002; Zambryski and Crawford, 2000) and that this active gating process requires an intact actin cytoskeleton (Ding et al., 1996) which maybe controlled by actomyosin-based contractile forces (Balusˇka et al., 2001a; Overall et al., 2000). In addition to actin and myosin VIII, several myosin-like proteins were localized to plasmodesmata (Blackman and Overall, 1998; Overall et al., 2000; Radford and White, 1998; White et al., 1994). Moreover, Arp3-like protein (Van Gestel et al., submitted), ER-based calreticulin (Balusˇka et al., 1999), calcium-dependent protein kinase (F. Balusˇka and D. Volkmann, preliminary data; Yahalom et al., 1998), and centrin (Blackman et al., 1999) also localize to plasmodesmata and might participate in their active gating. Microinjection of the polyclonal antibody raised against the tail domain of myosin VIII (Reichelt et al., 1999) into living root epidermis cells of Arabidopsis roots and mesophyll cells of tobacco leafs resulted in dilatation of plasmodesmata, as evidenced by enhanced cell-to-cell coupling monitored by comicroinjected dextran FITC and Lucifer Yellow dye (Table 1). These findings strongly suggest that myosin VIII-based forces are required for the maintenance of the structural integrity of plasmodesmata and their immunodepletion causes nonspecific opening of plasmodesmata. This would be in agreement with findings that depletion of cellular ATP, either with azide or due to anaerobiosis, induces opening of plasmodesmata (Cleland et al., 1994; Tucker, 1993). In plant tissues, there are two well-known examples where the cell-to-cell coupling is shut off on a developmental basis. First, root trichoblast become symplastically isolated during root hair formation (Duckett et al., 1994; Tirlapur and Ko¨nig, 1999). Secondly, stomatal plasmodesmata are closed, and later even truncated, during development of guard cells of functional stomata (Palevitz and Hepler, 1985; Wille and Lucas, 1984). Our recent experimental data obtained using two-photon
near-infrared femtosecond laser scanning microscopy (Tirlapur and Ko¨nig, 2002a,b), which allows noninvasive laser-assisted propidium iodide loading into target cells (Tirlapur and Ko¨nig, 1999, 2002a,b), have revealed that postmitotic root cap statocytes are also symplastically isolated (U. Tirlapur, K. Ko¨nig, F. Balusˇka, and D. Volkmann, in preparation). This surprising result may be related to their well-known role as the gravisensing statocytes (Sack, 1991). Such speculation is strongly supported by our observations that gravistimulation of roots resulted in differential opening of statocyte plasmodesmata depending on their position within root caps (U. Tirlapur, K. Ko¨nig, F. Balusˇka, and D. Volkmann, in preparation). As postmitotic root cap statocytes, like trichoblasts initiating root hairs, do not show abundant myosin VIII at their plasmodesmata and pit-fields (Balusˇka et al., 2000), myosin VIII might be expected to be abundant within those plasmodesmata which are engaged in extensive cell-to-cell trafficking. In fact, plasmodesmata and pit-fields in the inner cortex cells of maize root apices, located within the transition root apex zone (Balusˇka et al., 2001b) where phloemunloading takes place, are equipped with abundant F-actin and myosin VIII molecules (Balusˇka et al., 2001a). Intriguingly, these callosic and actomyosinenriched domains act as selective platforms specialized for fluid-phase endocytosis (Balusˇka et al., submitted). All this suggest that unconventional myosins of the plant-specific class VIII act as a multifunctional molecules at callose-enriched subcellular domains of higher plant cells like cytokinetic cell plates, plasmodesmata, and pit-fields.
References Balusˇka F, Sˇamaj J, Napier R, Volkmann D. Maize calreticulin localizes preferentially to plasmodesmata in root apex. Plant J 1999;19:481–8. Balusˇka F, Barlow PW, Volkmann D. Actin and myosin VIII in developing root cells. In: Staiger CJ, Balusˇka F, Volkmann D, Barlow PW, editors. Actin: a dynamic framework for multiple plant cell functions. Dordrecht: Kluwer Academic, 2000;457–76. Balusˇka F, Cvrcˇkova´ F, Kendrick-Jones J, Volkmann D. Sink plasmodesmata as gateways for phloem unloading. Myosin VIII and calreticulin as molecular determinants of sink strength? Plant Physiol 2001a;126:39–46. Balusˇka F, Volkmann D, Barlow PW. A polarity crossroad in the transition growth zone of maize root apices: cytoskeletal and developmental implications. J Plant Growth Regul 2001b; 20:170–81. Balusˇka F, Sˇamaj J, Hlavacˇka A, Kendrick-Jones J, Volkmann D. Myosin VIII and F-actin enriched plasmodesmata in maize root inner cortex cells accomplish fluid-phase endocytosis via an actomyosin-dependent process; 2003 (submitted for publication). Blackman LM, Overall RL. Immunolocalisation of the cytoskeleton to plasmodesmata of Chara corallina. Plant J 1998;14:733–41. Blackman LM, Harper JDI, Overall RL. Localization of a centrin-like protein to higher plant plasmodesmata. Eur J Cell Biol 1999; 78:297–304.
D. Volkmann et al. / Cell Biology International 27 (2003) 289–291 Cleland RE, Fujiwara T, Lucas WJ. Plasmodesmal-mediated cell-tocell transport in wheat roots is modulated by anaerobic stress. Protoplasma 1994;178:81–5. Ding B, Kwon M-O, Warnberg L. Evidence that actin filaments are involved in controlling the permeability of plasmodesmata in tobacco mesophyll. Plant J 1996;10:157–64. Duckett CM, Oparka KJ, Prior DAM, Dolan L, Roberts K. Dyecoupling in the root epidermis of Arabidopsis is progressively reduced during development. Development 1994;120:3247–55. Jackson D. Opening up the communication channels. Recent insights into plasmodesmal function. Curr Opin Cell Biol 2000;3:394–9. Knight A, Kendrick-Jones J. A myosin-like protein from a higher plant. J Mol Biol 1993;231:148–54. Liu L, Zhou J, Pesacreta TC. Maize myosins: diversity, localization, and function. Cell Motil Cytoskeleton 2001;48:130–48. Overall RL, White RG, Blackman LM, Radford JE. Actin and myosin in plasmodesmata. In: Staiger CJ, Balusˇka F, Volkmann D, Barlow PW, editors. Actin: a dynamic framework for multiple plant cell functions. Dordrecht: Kluwer Academic, 2000;513–31. Palevitz BA, Hepler PK. Changes in dye coupling of stomatal cells of Allium and Commelina demonstrated by microinjection of Lucifer yellow. Planta 1985;164:473–9. Radford JE, White RG. Localization of a myosin-like protein to plasmodesmata. Plant J 1998;14:743–50. Reddy ASN, Day IS. Analysis of the myosin encoded in the recently completed Arabidopsis thaliana genome sequence. Genome Biol 2001;2(7):0024.1–24.17. Reichelt S, Kendrick-Jones J. Myosins. In: Staiger CJ, Balusˇka F, Volkmann D, Barlow PW, editors. Actin: a dynamic framework for multiple plant cell functions. Dordrecht: Kluwer Academic, 2000;29–44. Reichelt S, Knight AE, Hodge TP, Balusˇka F, Sˇamaj J, Volkmann D et al. Characterization of the unconventional myosin VIII in plant cells and its localization at the post-cytokinetic cell wall. Plant J 1999;19:555–69.
291
Sack F. Plant gravity sensing. Int Rev Cytol 1991;127:193–252. Tirlapur UK, Ko¨nig K. Near-infrared femtosecond laser pulses as a novel non-invasive means for dye-permeation and 3D imaging of localised dye-coupling in the Arabidopsis root meristem. Plant J 1999;20:363–70. Tirlapur UK, Ko¨nig K. Femtosecond near-infrared laser pulses as a versatile non-invasive tool for intra-tissue nanoprocessing in plants without compromising viability. Plant J 2002;31:1–12. Tirlapur UK, Ko¨nig K. Two-photon near-infrared femtosecond laser scanning microscopy in plant biology. In: Diaspro A, editor. Confocal and two-photon microscopy: foundations, applications, and advances. New York: Wiley-Liss, 2002;449–68. Tucker EB. Azide treatment enhances cell-to-cell diffusion in staminal hairs of Setcreasea purpurea. Protoplasma 1993;174:45–9. Van Gestel K, Slegers H, von Witsch M, Sˇamaj J, Balusˇka F, Verbelen J-P. Immunological evidence for the presence of homologues of actin related proteins Arp2 and Arp3 in tobacco and maize plants; 2003 (submitted for publication). Volkmann D, Balusˇka F. The actin cytoskeleton in plants: from transport networks to signaling networks. Microsc Res Tech 1999; 47:135–54. White RG, Badelt K, Overall RL, Vesk M. Actin associated with plasmodesmata. Protoplasma 1994;180:169–84. Wille AC, Lucas WJ. Ultrastructural and histochemical studies on guard cells. Planta 1984;160:129–42. Wu X, Weigel D, Wigge PA. Signaling in plants by intracellular RNA and protein movement. Genes Dev 2002;16:151–8. Yahalom A, Lando R, Katz A, Epel BL. A calcium-dependent protein kinase is associated with maize mesocotyl plasmodesmata. J Plant Physiol 1998;153:354–62. Zambryski P, Crawford K. Plasmodesmata: gatekeepers for cell-to-cell transport of developmental signals in plants. Annu Rev Cell Dev Biol 2000;16:393–421.