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Rhodospirillum rubrum. Biochim. Biophys. Acta thylakoids. Biochem. Biophys. Res. Commun. 138, Rhodopseudomonas acidophila strain 10050. 935, 72–78 146–152 Prog. Biophys. Mol. Biol. 68, 1–27 47 Bingsmark, S. et al. (1990) Phosphorylation of 56 Dilly-Hartwig, H. et al. (1998) Truncated 65 Papiz, M.Z. et al. (1996) A model for the LHC II at low temperatures. In Current Research recombinant light harvesting complex II proteins photosynthetic apparatus of purple bacteria. in Photosynthesis (Vol. 2) (Baltscheffsky, M., ed.), are substrates for a protein kinase associated Trends Plant Sci. 1, 198–206 pp. 799–802, Kluwer Academic Publishers with photosystem II core complexes. FEBS Lett. 66 Muller, D.J. et al. (2000) Atomic force microscopy 48 Mamedov, F. et al. (2000) Photosystem II in 435, 101–104 of native purple membrane. Biochim. Biophys. different parts of the thylakoid membrane: a 57 Tullberg, A. et al. (1998) A protein tyrosine kinase Acta 1460, 27–38 functional comparison between different of chloroplast thylakoid membranes 67 Mehta, M. et al. (1999) Thylakoid membrane domains. Biochemistry 39, 10478–10486 phosphorylates light harvesting complex II architecture. Aust. J. Plant Physiol. 26, 695–708 49 Michel, H. et al. (1988) Tandem mass proteins. Biochem. Biophys. Res. Commun. 68 Mullineaux, C.W. et al. (1997) Mobility of spectrometry reveals that three photosystem II 250, 617–622 photosynthetic complexes in thylakoid proteins of spinach chloroplasts contain N-acetyl- 58 Forsberg, J. and Allen, J.F. Protein tyrosine membranes. Nature 390, 421–424

O-phosphothreonine at their NH2 termini. J. Biol. phosphorylation in the transition to light state 2 69 Anderson, J. and Andersson, B. (1982) The Chem. 263, 1123–1130 of chloroplast thylakoids. Photosynth. Res. architecture of thylakoid membranes: lateral 50 Vener, A.V. et al. (2001) Mass spectrometric (in press) and transverse organization. Trends Biochem. resolution of reversible protein phosphorylation 59 Race, H.L. et al. (1999) Why have organelles Sci. 7, 288–292 in photosynthetic membranes of Arabidopsis retained genomes? Trends Genet. 15, 364–370 70 Buchanan, B.B. et al. (2000) Biochemistry and thaliana. J. Biol. Chem. 276, 6959–6966 60 Pfannschmidt, T. et al. (1999) Photosynthetic Molecular Biology of Plants, American Society of 51 Whitelegge, J.P. et al. (1998) Imaging the native control of chloroplast gene expression. Nature Plant Physiologists state of thylakoid proteins by electrospray- 397, 625–628 71 Andersson, B. and Anderson, J.M. (1980) Lateral ionization mass spectrometry. In Photosynthesis: 61 Allen, J.F. and Pfannschmidt, T. (2000) Balancing heterogeneity in the distribution of Mechanisms and Effects (Vol. 5) (Garab, G., ed.), the two photosystems: photosynthetic electron chlorophyll–protein complexes of the thylakoid pp. 4381–4384, Kluwer Academic Publishers transfer governs transcription of reaction centre membranes of spinach chloroplasts. Biochim. 52 Bennett, J. (1977) Phosphorylation of chloroplast genes in chloroplasts. Philos. Trans. R. Soc. Biophys. Acta 593, 427–440 membrane polypeptides. Nature 269, 344–346 London Ser. B 355, 1351–1359 72 Junge, W. (1999) ATP synthase and other motor 53 Gómez, S.M. et al. (1998) Isolation and 62 Allen, J.F. (1993) Control of gene expression by proteins. Proc. Natl. Acad. Sci. U. S. A. characterization of a novel xanthophyll-rich redox potential and the requirement for 96, 4735–4737 pigment-protein complex from spinach. In chloroplast and mitochondrial genomes. J. Theor. 73 Zhang, Z. et al. (1998) Electron transfer by domain Photosynthesis: Mechanisms and Effects (Vol. 1) Biol. 165, 609–631 movement in cytochrome bc1. Nature 392, 677–684 (Garab, G., ed.), pp. 353–356, Kluwer Academic 63 Deisenhofer, J. and Michel, H. (1989) Nobel 74 Xia, D. et al. (1997) Crystal structure of the Publishers lecture. The photosynthetic reaction centre from cytochrome bc1 complex from bovine heart 54 Hird, S.M. et al. (1986) The gene for the 10 kDa the purple bacterium Rhodopseudomonas viridis. mitochondria. Science 277, 60–66 phosphoprotein of photosystem II is located in EMBO J. 8, 2149–2170 75 Finazzi, G. et al. (1999) State transitions, cyclic chloroplast DNA. FEBS Lett. 209, 181–186 64 Cogdell, R.J. et al. (1997) The structure and and linear electron transport and 55 Allen, J.F. and Findlay, J.B. (1986) Amino acid function of the LH2 (B800–850) complex from the photophosphorylation in Chlamydomonas composition of the 9 kDa phosphoprotein of pea purple photosynthetic bacterium reinhardtii. Biochim. Biophys. Acta 1413, 117–129

Plasmodesmata and plant cytoskeleton

Rachid Aaziz, Sylvie Dinant and Bernard L. Epel

Plant cell-to-cell communication is achieved by membranous conduits called microfilaments (polymers of tubulin and actin, plasmodesmata, which bridge the cytoplasm of neighboring cells. A growing respectively) and diverse associated proteins. body of immunolocalization data shows an association of the cytoskeleton Whereas direct cell-to-cell communication is provided machinery with plasmodesmata. The role of the cytoskeleton in the in animals and fungi by gap junctions and septal plasmodesmata-mediated transport has been well documented for virus pores, respectively, within plants, cell-to-cell movement. Because viruses are known to exploit existing host pathways and cytoplasmic trafficking takes place through because the cytoskeleton is involved in intracellular trafficking, the plasmodesmata, wall spanning co-axial membranous cytoskeleton is thought to drive and target macromolecules to organelles that bridge the cytoplasm of contiguous plasmodesmata. It is this link between plasmodesmata and the cytoskeleton cells3,4. Plasmodesmata are considered to enable both that will be described here. physiological and developmental coordination of the plant5. Major insights in plasmodesmata functions The plant cytoskeleton plays an important role in have arisen from both viral movement studies and many biological processes, including cell division and microinjection experiments4, and by the use of expansion, organogenesis, tip growth and transiently expressed green fluorescent protein (GFP) intracellular signaling1,2. The plant cytoskeleton is fusion proteins6. Functional studies have underlined composed primarily of a network of microtubules and that plasmodesmata are dynamic structures that

Fig. 1. A simple vesicles takes place along both microtubules and plasmodesma Endoplasmic microfilaments. This transport is mediated by (transversal section). The reticulum plasmodesma establishes Cell 1 molecular motor proteins exhibiting ATPase activity, a continuum state Plasma including members of the kinesin, dynein and myosin between adjacent cells. It membrane superfamilies. It is well accepted that microtubules, in corresponds to a channel embedded into the cell conjunction with kinesin and dynein motors, provide wall and delineated by the rails for long-distance movement of membranous plasma membranes of the vesicles, whereas microfilaments, powered by myosin two interconnected cells motors, direct their local movement12. Because (cells 1 and 2). An cytoskeletal elements were shown to be involved in the appressed form of Cell wall endoplasmic reticulum movement of intracellular vesicles and organelles, it crosses the was speculated that cytoskeleton might similarly be plasmodesma. Globular involved in plasmodesmata-mediated trafficking9. proteinaceous particles (blue and red spheres) Consistent with this is an ever-growing number of covering the inside of the reports on the close association between cytoskeletal plasmodesma are components and plasmodesmata. hypothetically represented. This review will focus on the relationship between Cell 2 the cytoskeleton and plasmodesmata and how cytoskeletal elements might be affecting the structure TRENDS in Plant Science and regulation of plasmodesmata, thus serving the plant for better or for worse. For the better by being involved in enable the intercellular transport of macromolecules, the regulation of information transfer for plant growth including endogenous and viral proteins, as well as and development, for the worse by being usurped by ribonucleoprotein complexes5. Recent data have viruses as a vehicle for the spread of viral infection. allowed non-targeted and targeted protein movement through plasmodesmata to be distinguished6,7. The Plasmodesmata: a concentrate of cytoskeletal non-targeted protein movement is considered to be a elements diffusion process and is limited only by the size of the Based on ultrastructural microscopic studies, a translocated protein. By contrast, targeted-protein simple plasmodesma appears as a coaxial movement is selective, requiring interactions between membranous conduit spanning the cell wall (Fig. 1). endogenous or exogenous (e.g. viral) factors and the The outer membrane is continuous with the plasma specific protein to direct and facilitate its translocation membranes of the interconnected cells, whereas the through plasmodesmata8. Over the past decade, the centrally tubular membranous component, termed discovery of interactions between viral proteins the desmotubule, is a derivative of and contiguous involved in virus movement and either with the cortical endoplasmic reticulum (ER). plasmodesmata or the cytoskeleton has led to exciting Contrary to the structural analysis, the composition models about the pathways of macromolecular of plasmodesmata still remains fragmentary because of trafficking through plasmodesmata9. the difficulty in isolating pure plasmodesmata without The cytoskeleton is also involved in intracellular subcellular membrane contaminants3,4. Several membranous movement processes such as exocytosis, putative plasmodesma-associated proteins from maize endocytosis, organelle anchoring and vesicle mesocotyl have been characterized3. One of them transport, as well as in other protein-sorting termed PAP26, was identified as cross-reacting with pathways10–12. The translocation of membranous affinity-purified antibodies raised against animal gap- junction connexin43 (Ref. 13). Immunocytochemical Table 1. Cytoskeleton proteins associated to studies have shown that PAP26 localized along the plasmodesmata entire plasmodesmal length. Likewise, a 41 kDa protein Protein Plant species Refs associated with a maize mesocotyl cell wall was also Actin-like Azolla pinnata 15 identified and immunolocalized to plasmodesmata and 14 Hordeum vulgare 15 to Golgi membranes . Nephrolepis exaltata 15 Using immuno-based techniques, several Nicotiana plumbaginifolia 15 cytoskeleton proteins have been shown to be Rachid Aaziz* Actin Chara corallina 16 associated with plasmodesmata (Table 1). An actin- Sylvie Dinant Calreticulin Zea mays 20 INRA-Laboratoire de like protein was immunolocalized to plasmodesmata Centrin-like Allium cepa 19 Biologie Cellulaire, 78026 in the fern Nephrolepis exaltata and in root tips of Brassica oleraceae 19 Versailles Cedex, France. Azolla pinnata and Hordeum vulgare (Ref. 15). In the *e-mail: Myosin Chara corallina 16 [email protected] Myosin-like Allium cepa 17 alga Chara corallina, actin and myosin were Hordeum vulgare 17 immunolocalized in nodal but not in inter-nodal cell Bernard L. Epel Zea mays 17 walls, which are devoid of plasmodesmata16. Dept of Plant Sciences, Tel Myosin VIII Lepidum sativum 18 Aviv University, Tel Aviv Moreover, a myosin-like protein is associated with Zea mays 18 69978, Israel. plasmodesmata of onion and maize roots17, and a

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myosin VIII protein is localized in plasmodesmata in during plant growth6. Whether this developmental Arabidopsis thaliana, cress (Lepidium sativum) and regulation involves or is associated with maize root cells18. plasmodesmata cytoskeletal elements is unknown A centrin-like protein has been immunolocalized and awaits future investigations. to plasmodesmata of onion root tips, predominantly to the orifice region19. The involvement of calcium in the Pirating of the cytoskeleton in virus movement regulation of plasmodesmal function has been In animals, the cell-to-cell spread of viral infection suggested because centrin belongs to the calcium- occurs by means of endocytosis or by a fusion of the binding contractile protein family. Likewise, viral envelope with the plasma-membrane25. This is calreticulin (a calcium-sequestering protein) localizes not the case for plant viruses, which must circumvent to cortical ER, associated specifically with maize root the rigid cell wall by moving through plasmodesmata. apex plasmodesmata20. A calcium-dependent protein To successfully infect a plant, a virus must penetrate kinase is also associated with maize into a plant cell and replicate. It then moves from the plasmodesmata21. These results suggest that calcium initially infected cell to neighboring cells via is involved in regulating plasmodesmal permeability. plasmodesmata, and thereafter into the vascular Besides playing a structural role in plasmodesmata, transport system for systemic spread via the cytoskeletal elements might act in their regulation, phloem26. Given that the endogenous molecular and therefore in the control of the plasmodesmata- trafficking through plasmodesmata is restricted to mediated macromolecular trafficking. either small molecules or to proteins of <50 kDa, depending on cell species and developmental stage Regulation of plasmodesmata gating tissue6, the question arises as to how large structures, The permeability of plasmodesmata is dependent on such as plant viruses, gate open plasmodesmata to whether they are constricted or dilated7. Several abiotic increase the spread of viral infection? The answer is and biotic factors influence the plasmodesmal that virus-encoded non-structural proteins, termed permeability. In earlier investigations, evidence was movement proteins (MPs) mediate cell-to-cell virus presented that showed that transport through movement via plasmodesmata. plasmodesmata is reduced in the presence of high Numerous MPs have been reported to increase calcium concentrations. Moreover, plasmodesmata of plasmodesmal permeability and to mediate the maize cells rapidly closed, either when injected with transport of virions or viral nucleoproteins between calcium or as a result of cold, a treatment that induces cells. One of the most studied MPs is that of tobacco an increase in cytoplasmic calcium22. These mosaic virus (TMV), a plant RNA virus27. The MP of observations, concerning calcium sensitivity and the TMV (MPTMV) is able to bind to viral RNA to form a association of cytoskeletal components with ribonucleoprotein complex27. Also, during viral plasmodesmata, suggest that these calcium-sensitive infection, MPTMV is targeted to plasmodesmata cytoskeletal proteins might function in the regulation of increasing their permeability4. Several research plasmodesmal conductivity. The involvement of an groups have undertaken the characterization of host actin–myosin complex on plasmodesmal permeability is components that interact with viral MPs (Refs 28,29), supported by the observation that following treatment and have shown that a fusion between MPTMV and with cytochalasin D or as a result of microinjection of GFP colocalizes with components of the profilins (actin-binding proteins), treatments that cytoskeleton28,29 and ER-derived membranes9,30. result in the depolymerization of microfilaments, there Moreover, using in situ hybridization, TMV RNA has was an increase in the permeability of tobacco been shown to colocalize with both microtubules and mesophyll plasmodesmata23. By contrast, stabilization MPTMV (Ref. 30). In the presence of oryzalin, a of microfilaments following microinjection of phalloidin microtubule depolymerizing drug, the coalignment of had an opposite effect23. These data suggest that actin TMV RNA with microtubules was lost31. Likewise, constricts plasmodesmata, lowering their permeability cold treatment, which induces microtubule and that upon microfilament disruption depolymerization, dramatically altered the plasmodesmata dilate. Furthermore, the addition of the intracellular distribution of MPTMV and TMV RNA myosin ATPase inhibitor 2,3-butanedione 2-monoxime (Refs 30,31). Furthermore, the efficiency of leads to a constriction of plasmodesmata by stabilizing intercellular TMV RNA spread at high temperatures microfilaments and preventing their (32°C versus 22°C) positively correlates with the depolymerization24. This result is consistent with a association of MPTMV to microtubules32. Further putative role of myosin, in association with actin, in the evidence implicating microtubules in TMV RNA control of the plasmodesmal permeability17. movement was provided recently by the identification In other respects, the permeability of of a conserved sequence motif in tobamovirus MP that plasmodesmata is developmentally regulated. For shares similarity with a region in tubulins that is example, the down-regulation of the plasmodesmal thought to mediate lateral contacts between permeability accompanying the sink-to-source microtubule protofilaments33. Point mutations in this transition probably has important implications on the motif confer temperature sensitivity to microtubule control of intercellular movement of macromolecules association and to viral RNA intercellular-transport

http://plants.trends.com Review TRENDS in Plant Science Vol.6 No.7 July 2001 329 functions of MPTMV, indicating that MP-interacting employment of multiple staining methods exploiting microtubules are functionally involved in the spread of GFP fluorescent variants to simultaneously probe for TMV RNA to plasmodesmata33. A model was proposed MP, microtubules and microfilaments. Another suggesting that MPTMV functions in intracellular interesting issue is whether the microtubule- transport by mimicking tubulin assembly surfaces, dependent TMV RNA movement towards thus enabling it to propel TMV RNA by a dynamic plasmodesmata follows similar pathways process driven by microtubule polymerization33. encountered in the intracellular mRNA movement MPTMV has also been shown to associate with along the cytoskeleton network. microfilaments29. However, the involvement of microfilaments in intracellular and intercellular Intracellular mRNA movement: plants like animals? TMV RNA movement is unclear. Because Subcellular protein sorting and distribution are microfilaments are associated with plasmodesmata accomplished both by the positioning of proteins and and involved in the regulation of the plasmodesmal mRNA in the cytoplasm. In specialized cells, specific permeability, and because a transport vehicle is mRNA localization enables the synthesis and essential for viral RNA movement through concentration of specific proteins at subcellular sites plasmodesmata, one could speculate that where they are required10,11. The role of the cytoskeleton microfilaments are involved in this transport function in intracellular transport, targeting and anchoring of through plasmodesmata. mRNA to functional sites is well established in animals It has been proposed that ER inclusion bodies and yeast. Using specific cytoskeleton-depolymerizing represent sites of viral replication and protein drugs, microfilaments and microtubules have been synthesis, as virus ‘factories’ sites30. A recent report shown to be involved in mRNA localization in small presented data suggesting that intercellular TMV (e.g. myoblasts) and large (e.g. neurons) cell types, RNA movement is not dependent on the respectively. In some cells, such as Drosophila and accumulation of MPTMV on ER-derived inclusion Xenopus oocytes, both microtubules and microfilaments bodies34. It was proposed that the crucial step are involved. The significance of this differential involves the redistribution of MPTMV and viral RNA requirement is unclear11. from these ‘factory sites’ to microtubules that are Because of the viscosity of the cytoplasm, only involved in targeting the viral ribonucleoprotein small mRNAs can freely and randomly diffuse. By complex towards plasmodesmata32,34. By contrast, contrast, the positioning of large mRNA-protein others have proposed that the cortical ER plays a role complexes needs active processes. This active during the translocation step of TMV RNA through intracellular mRNA transport relies on cytoskeleton plasmodesmata9. This model is based on the finding proteins such as kinesin, myosin and tropomyosin10. that MPTMV is an integral ER membrane protein and Several cytoskeleton-associated proteins, as well as that ER membranes traverse plasmodesmata9. This translational factors and ribosomes, specifically bind model requires the involvement of cytoskeletal to cytoplasmic, moving mRNA, to form ‘granules’ of components as vehicles for ER movement. mRNAs that are then translocated along the In the case of animal viruses, the cytoskeleton has cytoskeleton network10,11. It has been suggested that been described as being involved in the intracellular during mRNA localization, microtubules serve as the trafficking of numerous animal viruses or of viral tracks for long-distance movement, whereas proteins25. In animal and yeast cells, the involvement microfilaments direct local movement as well as of cytoskeletal elements in the intracellular transport mRNA anchoring10. These models probably hold true of cellular vesicles12 and mRNAs11 is well for plants as well. Such a model for plants is documented. Similarly TMV, by means of MPTMV, supported by the report that in Arabidopsis thaliana, appears to exploit (and probably mimic) the existing profilin and its mRNA are accumulated at growing host cytoskeleton network for intracellular root hair tips36. It has been suggested that this trafficking. Other viral MPs have not been reported to localization is essential for active installation of the accumulate to detectable levels on cytoskeletal actin-dependent tip growth machinery. Clearly, elements35. It is not known whether the MPTMV case is further investigations are required to understand the unique or if the lack of detection is because the MP mRNA positioning process in plants. accumulate at low undetectable levels. Kinetic In the past few years, significant efforts have shed considerations predict that there will be no detectable light on viral RNA intracellular movement. The viral accumulation of MP with cytoskeletal components if system might represent an excellent and convenient there is a rate-limiting step before association with model for understanding processes involved in mRNA the cytoskeletal elements. A clarification of this movement and positioning in plants. discrepancy will require a time-course systematic examination of infection sites of other virus groups Conclusion and future prospects performed under different temperature conditions Over the past decade, tremendous progress has been and with cytoskeleton inhibitors. Such a study would made in understanding plasmodesmal structure and encompass using not only wild type but also function. By contrast, compositional analysis of dysfunctional MP mutants and would require the plasmodesmata is in its infancy because it is difficult http://plants.trends.com 330 Review TRENDS in Plant Science Vol.6 No.7 July 2001

to obtain pure plasmodesmata cell wall fractions. unanswered. What elements and mechanisms are However, recent improvements in isolation involved in the interaction between MP, microtubules techniques, in addition to immuno-based studies, have and viral RNA? What other cytoskeletal (i.e. other shed light on preliminary plasmodesmal composition. than microtubules and microfilaments) components These findings indicate a close relationship between are involved in targeting viral RNA (or cellular plasmodesmata and the cytoskeleton. In this respect, macromolecules) to plasmodesmata? Interestingly, selection and screening protocols need to be developed plasmodesmata as well as the plant cytoskeleton are to obtain specific plasmodesmal mutants that could also involved in defense reactions against other serve in the exploration of the function and regulation pathogen invasions2,37. This raises the question as to of each identified plasmodesmal gene. the precise link between plasmodesmata and the The involvement of the cytoskeleton in the cytoskeleton during the plant response to invading intracellular movement of membranous organelles and pathogens. mRNA in animal and yeast systems has been well With the development of multiple fluorescent documented. By contrast, in plants, only minimal effort probes for the various subcellular compartments and has been addressed to this important cellular process. cytoskeletal elements, and with the rapid Recent research showing that intracellular TMV development of proteomics we should be able to study Acknowledgements movement is cytoskeleton-assisted could represent a protein complexes and protein modifications as well We are grateful to our valuable system to unravel the intracellular trafficking as protein–protein interaction that occur in the colleagues Jean- of macromolecules in plants. Likewise, the plasmodesmata-mediated trafficking. The Christophe Palauqui, Miguel Freire and identification of plant cytoskeleton mutants defective in exploitation of these new powerful tools should enable Laurent Bigarré for their either intracellular or intercellular movement should rapid progress in our understanding of plasmodesmal comments on the enlighten this little-understood process in plants. structure and function and of how viruses exploit and manuscript. This work is supported by an AFIRST Significant questions about the relationship mimic the host trafficking machinery for intracellular program between plasmodesmata and the cytoskeleton remain and intercellular movement.

References 14 Epel, B.L. et al. (1996) A 41 kDa protein isolated Plant Sci. 1, 260–268 1 Kost, B. et al. (1999) Cytoskeleton in plant from maize mesocotyl cell walls immunolocalizes 27 Citovsky, V. (1999) Tobacco mosaic virus: a pioneer development. Curr. Opin. Plant Biol. to plasmodesmata. Protoplasma 191, 70–78 of cell-to-cell movement. Philos. Trans. R. Soc. 2, 462–470 15 White, R.G. et al. (1994) Actin associated with Lond. B. Biol. 354, 637–643 2 Staiger, C.J. (2000) Signalling to the actin plasmodesmata. Protoplasma 180, 169–184 28 Heinlein, M. et al. (1995) Interaction of cytoskeleton in plants. Annu. Rev. Plant. Physiol. 16 Blackman, L.M. and Overall, R.L. (1998) tobamovirus movement proteins with the plant Plant Mol. Biol. 51, 257–288 Immunolocalisation of the cytoskeleton to cytoskeleton. Science 270, 1983–1985 3 Epel, B.L. (1994) Plasmodesmata: composition, plasmodesmata of Chara corallina. Plant J. 29 McLean, B.G. et al. (1995) Tobacco mosaic virus structure and trafficking. Plant Mol. Biol. 14, 733–741 movement protein associates with the 26, 1343–1356 17 Radford, J.E. and White, R.G. (1998) Localization cytoskeleton in tobacco plants. Plant Cell 4 Ding, B. (1998). Intercellular protein trafficking of a myosin-like protein to plasmodesmata. Plant 7, 2101–2114 through plasmodesmata. Plant Mol. Biol. J. 14, 743–750 30 Mas, P. and Beachy, R.N. (1999) Replication of 38, 279–310 18 Reichelt, S. et al. (1999) Characterization of the tobacco mosaic virus on endoplasmic reticulum 5 Lucas, W.J. (1999) Plasmodesmata and cell-to-cell unconventional myosin VIII in plant cells and its and role of the cytoskeleton and virus movement transport of proteins and nucleoprotein localization at the post-cytokinetic cell wall. Plant protein in intracellular distribution of viral RNA. complexes. J. Exp. Bot. 50, 979–987 J. 19, 555–567 J. Cell Biol. 147, 945–958 6 Oparka, K.J. et al. (1999) Simple, but not 19 Blackman, L.M. et al. (1999) Localization of a 31 Mas, P. and Beachy, R.N. (2000) Role of branched, plasmodesmata allow the nonspecific centrin-like protein to higher plant microtubules in the intracellular distribution of trafficking of proteins in developing tobacco plasmodesmata. Eur. J. Cell. Biol. 78, 297–304 tobacco mosaic virus movement protein. Proc. leaves. Cell 97, 743–754 20 Baluska, F. et al. (1999) Maize calreticulin Natl. Acad. Sci. U. S. A. 97, 12345–12349 7 Crawford, K.M. and Zambryski, P.C. (2000) localizes preferentially to plasmodesmata in root 32 Boyko, V. et al. (2000) Cell-to-cell movement of Subcellular localization determines the apex. Plant J. 19, 481–488 TMV RNA is temperature-dependent and availability of non-targeted proteins to 21 Yahalom, A. et al. (1998) A calcium-dependent corresponds to the association of movement plasmodesmatal transport. Curr. Biol. protein kinase is associated with maize mesocotyl protein with microtubules. Plant J. 22, 315–325 10, 1032–1040 plasmodesmata. J. Plant Physiol. 153, 354–362 33 Boyko, V. et al. (2000) Function of microtubules in 8 Kragler, F. et al. (2000) Peptide antagonists of the 22 Holdaway-Clarke, T.I. et al. (2000) Physiological intercellular transport of plant virus RNA. Nat. plasmodesmal macromolecular trafficking elevation in cytoplasmic free calcium by cold or Cell. Biol. 2, 826–832 pathway. EMBO J. 19, 2856–2868 ion injection result in transient closure of higher 34 Boyko, V. et al. (2000) Cellular targets of 9 Reichel, C. et al. (1999) The role of the ER and plant plasmodesmata. Plant J. 210, 329–335 functional and dysfunctional mutants of Tobacco cytoskeleton in plant viral trafficking. Trends 23 Ding, B. et al. (1996) Evidence that actin mosaic virus movement protein fused to green Plant Sci. 4, 458–462 filaments are involved in controlling the fluorescent protein. J. Virol. 74, 11339–11346 10 Bassel, G. and Singer, R.H. (1997) mRNA and permeability of plasmodesmata in tobacco 35 Lazarowitz, S.G. and Beachy, R.N. (1999) Viral cytoskeletal filaments. Curr. Opin. Cell. Biol. mesophyll. Plant J. 10, 157–164 movement proteins as probes for intracellular and 9, 109–115 24 Samaj, J. et al. (2000) Effects of myosin ATPase intercellular trafficking in plants. Plant Cell 11, 11 Jansen, R.P. (1999) RNA-cytoskeletal association. inhibitor 2,3-butanedione 2-monoxime on 535–548 FASEB J. 13, 455–466 distributions of myosins, F-actin, microtubules, 36 Baluska, F. et al. (2000) Root hair formation: 12 Kamal, A. and Goldstein, L.S.B. (2000) and cortical endoplasmic reticulum in maize root F-actin-dependent tip growth is initiated by local Connecting vesicle transport to the cytoskeleton. apices. Plant Cell Physiol. 41, 571–582 assembly of profilin-supported F-actin Curr. Opin. Cell. Biol. 12, 503–508 25 Ploubidou, A. and Way, M. (2001) Viral transport meshworks accumulated within expansin- 13 Yahalom, A. et al. (1991) Maize mesocotyl and the cytoskeleton. Curr. Opin. Cell. Biol. enriched bulges. Dev. Biol. 227, 618–632 plasmodesmata proteins cross-react with 13, 97–105 37 Murillo, I. et al. (1997) The maize pathogenesis- connexin gap junction protein antibodies. Plant 26 Gilbertson, R.L. and Lucas, W.J. (1996) How do related PRms protein localizes to plasmodesmata Cell 3, 407–417 viruses traffic on the ‘vascular highway’? Trends in maize radicles. Plant Cell 9, 145–156

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