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Actin and Myosin VIII in Plant Cell-Cell Channels

  • Chapter
Cell-Cell Channels

Abstract

Plasmodesmata (PD) are cell-cell channels interconnecting all the cells of the plant body into a huge syncytium, which makes plants’ supracellular’ organisms. Recent studies have clearly revealed that both the targeting and gating of PD is highly regulated. Importantly, it is known that molecules below the size exclusion limits, such as auxin and calcium, cannot pass freely through plasmodesmata, strongly implicating a very effective sieve-like structure within PD. Even though the first PD-resident proteins emerge from recent molecular studies, the majority of these elusive proteins remain to be unveiled. Convincing evidence suggests that F-actin meshworks, supported by myosins of class VIII and perhaps also by ARP2/3 proteins and other actin-binding proteins, are components of gateable PD and potentially involved in sieve-like nature of these cell-cell channels. Interestingly, there are several structural and functional similarities between PD and nuclear pores. For example, homeodomain transcription factors are able to pass through both nuclear pores as well as PD via similar mechanisms. Some cells are also symplasmically isolated such as stomata and trichoblasts initiating root hairs, and root cap statocytes. The root cap statocytes and their PD are depleted in both F-actin and myosin VIII, implying that these cytoskeletal molecules are essential for transport through PD. Gravistimulation triggers the opening of a special subset of PD in the root cap statocytes suggesting that a physical force, such as gravity, is capable of targeting molecules/processes which regulate the gating of PD.

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References

  1. Lucas WJ, Lee J-Y. Plasmodesmata as a supracellular control network in plants. Nat Rev Mol Cell Biol 2004;5:712–726.

    Article  PubMed  CAS  Google Scholar 

  2. Huang Z, Andrianov VM, Han Y et al. Identification of Arabidopsis proteins that interact with cauliflower mosaic virus (CaMV) movement protein. Plant Mol Biol 2001;47:663–675.

    Article  PubMed  CAS  Google Scholar 

  3. Laporte C, Vetter G, Loudes AM et al. Involvement of the secretory pathway and the cytoskeleton in intracellular targeting and tubule assembly of Grapevine fan-leaf virus movement protein in tobacco BY-2 cells. Plant Cell 2003;15:2058–2075.

    Article  PubMed  CAS  Google Scholar 

  4. Escobar NM, Haupt S, Thow G et al. High-throughput viral expression of cDNA-green fluorescent protein fusions reveals novel subcellular addresses and identifies unique proteins that interacts with plasmodesmata. Plant Cell 2003;15:1507–1523.

    Article  PubMed  CAS  Google Scholar 

  5. Lu C, Zainal Z, Tucker GA et al. Developmental abnormalities and reduced fruit softening in tomato plants expressing an antisense Rab11 GTPase gene. Plant Cell 2001;13:1819–1833.

    Article  PubMed  CAS  Google Scholar 

  6. Más P, Beachy RN. Replication of tobacco mosaic virus on endoplasmic reticulum and role of the cytoskeleton and virus movement protein in intracellular distribution of viral RNA. J Cell Biol 1999;147:945–958.

    Article  PubMed  Google Scholar 

  7. Lee JY, Yoo BC, Rojas MR et al. Selective trafficking of noncell-autonomous proteins mediated by NtNCAPP1. Science 2003;299:392–396.

    Article  PubMed  CAS  Google Scholar 

  8. Velikanov GA, Volobueva OV, Khokhlova LP. The study of the hydraulic conductivity of the plasmodesmal transport channels by the pulse NMR method. Russ J Plant Phys 2001;48:375–383.

    Google Scholar 

  9. Volobueva OV, Velikanov GA, Baluska F. Regulation of intercellular water exchange in various zones of maize root under stresses. Russ J Plant Phys 2004; 51:676–683.

    Article  CAS  Google Scholar 

  10. Velikanov GA, Volobueva OV, Belova LP et al. Vacuolar symplast as a regulated pathway for water flows in plants. Russ J Plant Phys 2004;52:326–331.

    Article  Google Scholar 

  11. Kutsuna N, Hasezawa S. Dynamic organization of vacuolar and microtubule structures during cell cycle progression in synchronized tobacco BY-2 cells. Plant Cell Physiol 2002;43:965–973.

    Article  PubMed  CAS  Google Scholar 

  12. Kutsuna N, Kumagai F, Sato MH et al. Three-dimensional reconstruction of tubular structure of vacuolar membrane throughout mitosis in living tobacco cells. Plant Cell Physiol 2003;44:1045–1054.

    Article  PubMed  CAS  Google Scholar 

  13. Lucas WJ, Bouche-Pillon S, Jackson DP et al. Selective trafficking of KNOTTED1 homeodomain protein and its mRNA through plasmodesmata. Science 1995;270:1980–1983.

    Article  PubMed  CAS  Google Scholar 

  14. Wu X, Dinneny JR, Crawford KM et al. Modes of intercellular transcription factor movement in the Arabidopsis apex. Development 2003;130:3735–3745.

    Article  PubMed  CAS  Google Scholar 

  15. Gallagher KL, Paquette AJ, Nakajima K et al. Mechanisms regulating SHORT-ROOT intercellular movement. Curr Biol 2004;14:1847–1851.

    Article  PubMed  CAS  Google Scholar 

  16. Nakajima K, Sena G, Nawy T et al. Intercellular movement of the putative transcription factor SHR in root patterning. Nature 2001;413:307–311.

    Article  PubMed  CAS  Google Scholar 

  17. Sena G, Jung JW, Benfey PN. A broad competence to respond to SHORT-ROOT revealed by tissue-specific ectopic expression. Development 2004;131:2817–2826.

    Article  PubMed  CAS  Google Scholar 

  18. Kawakami S, Watanabe Y, Beachy RN. Tobacco mosaic virus infection spreads cell to cell as intact replication complexes. Proc Natl Acad Sci USA 2004;101:6291–6296.

    Article  PubMed  CAS  Google Scholar 

  19. Rustom A, Saffrich R, Markovic I et al. Nanotubular highways for intercellular organelle transport. Science 2004;303:1007–1010.

    Article  PubMed  CAS  Google Scholar 

  20. Baluska F, Hlavacka A, Volkmann D et al. Getting connected: Actin-based cell-to-cell channel in plants and animals. Trends Cell Biol 2004;14:404–408.

    Article  PubMed  CAS  Google Scholar 

  21. Zhu D, Tan KS, Zhang X et al. Hydrogen peroxide alters membrane and cytoskeleton properties and increases intercellular connections in astrocytes. J Cell Sci 2005;118:3695–3703.

    Article  PubMed  CAS  Google Scholar 

  22. White RG, Badelt K, Overall RL et al. Actin associated with plasmodesmata. Protoplasma 1994;180:169–184.

    Article  CAS  Google Scholar 

  23. Overall RL, Blackman LM. A model of the macromolecular structure of plasmodesmata. Trends Plant Sci 1996;1:307–311.

    Google Scholar 

  24. Blackman LM, Overall RL. Immunolocalisation of the cytoskeleton to plasmodesmata of Chara corallina. Plant J 1998;14:733–741.

    Article  CAS  Google Scholar 

  25. Radford JE, White RG. Localization of myosin-like protein to plasmodesmata. Plant J 1998;14:743–750.

    Article  PubMed  CAS  Google Scholar 

  26. Reichelt S, Knight AE, Hodge TP et al. Characterisation of the unconventional myosin VIII in plant cells and its localization at the post-cytokinetic cell wall. Plant J 1999;19:555–568.

    Article  PubMed  CAS  Google Scholar 

  27. Baluska F, Cvrckova F, Kendrick-Jones J et al. Sink plasmodesmata as gateways for phloem un loading: Myosin VIII and calreticilin as molecular determinants of sink strenght. Plant Physiol 2001;126:39–47.

    Article  PubMed  CAS  Google Scholar 

  28. Baluska F, Samaj J, Hlavacka A et al. Myosin VIII and F-actin enriched plasmodesmata in maize root inner cortex cells accomplish fluid-phase endocytosis via an actomyosin-dependent process. J Exp Bot 2004;55:463–473.

    Article  PubMed  CAS  Google Scholar 

  29. Chaffey NJ, Barlow PW. The cytoskeleton facilitates a three-dimensional symplasmic continuum in the long-lived ray and axial parenchyma cells of angiosperm trees. Planta 2001;213:811–823, (Erratum: Planta 2001;214, 330–331).

    Article  PubMed  CAS  Google Scholar 

  30. Nemec B. Die Reizleitung und die Reizleitenden Strukturen bei den Pflanzen. Jena: Verlag von Gustaf Fischer, 1901.

    Google Scholar 

  31. Volkmann D, Mori T, Tirlapur UK et al. Unconventional myosins of the plant-specific class VIII: Endocytosis, cytokinesis, plasmodesmata/pit-fields, and cell-to-cell coupling. Cell Biol Int 2003;27:289–291.

    Article  PubMed  CAS  Google Scholar 

  32. Wojtaszek P, Anielska-Mazur A, Gabrys H et al. Recruitment of myosin VIII towards plastid surfaces is root-cap specific and provides the evidence for actomyosin involvement in root osmosensing. Funct Plant Biol 2005;32:1–16.

    Article  Google Scholar 

  33. Van Gestel K, Siegers H, von Witsch M et al. Immunological evidence for the presence of plant homologues of the actin related protein Arp3 in tobacco and maize: Subcellular localization to actin-enriched pit fields an emerging root hairs. Protoplasma 2003;222:45–52.

    Article  PubMed  Google Scholar 

  34. Tseng Y, Kole TP, Le JSH et al. How actin crosslinking and bundling proteins cooperate to generate an enhanced cell mechanical response. Biochem Biophys Res Comm 2005;334:183–192.

    Article  PubMed  CAS  Google Scholar 

  35. Weaver AM. Cytoskeletal interactions with the outside world. Dev Cell 2005;9:35–38.

    Article  PubMed  CAS  Google Scholar 

  36. Tirlapur UK, König K. Technical advance: Near-infrared femtosecond laser pulses as a novel noninvasive means for dye-permeation and 3D imaging of localised dye-coupling in the Arabidopsis root meristem. Plant J 1999;20:363–370.

    PubMed  CAS  Google Scholar 

  37. Tirlapur UK, König K. Femtosecond near-infrared laser pulses as a versatile noninvasive tool for intra-tissue nanoprocessing in plants without compromising viability. Plant J 2002;31:365–374.

    Article  PubMed  Google Scholar 

  38. Ueki S, Citovsky V. Control improves with age: Intercellular transport in plant embryos and adults. Proc Natl Acad Sci USA 2005;102:1817–1818.

    Article  PubMed  CAS  Google Scholar 

  39. Epel BL, Erlanger MA. Light regulates symplastic communication in etiolated corn seedlings. Physiol Plant 1991;83:149–153.

    Article  CAS  Google Scholar 

  40. Barlow PW. The root cap: Cell dynamics, cell differentiation and cap function. J Plant Growth Regul 2003;21:261–286.

    Article  Google Scholar 

  41. Hawes MC, Brigham LA, Wen F et al. Function of root border cells in plant health: Pioneers in the rhizosphere. Annu Rev Phytopathol 1998;36:311–327.

    Article  PubMed  CAS  Google Scholar 

  42. Baluska F, Barlow PW, Volkmann D. Actin and myosin VIII in developing root cells. In: Staiger CJ, Baluska F, Volkmann D, Barlow PW, eds. Actin: A Dynamic Framework for Multiple Plant Cell Functions. Dordrecht, The Netherlands: Kluwer Academic Publishers, 2000:457–476.

    Google Scholar 

  43. Baluska F, Samaj J, Wojtaszek P et al. Cytoskeleton — plasma membrane — cell wall continuum in plants: Emerging links revisited. Plant Physiol 2003;133:482–491.

    Article  PubMed  CAS  Google Scholar 

  44. Oparka KJ, Prior DAM. Direct evidence for pressuregenerated closure of plasmodesmata. Plant J 1992;2:741–750.

    Google Scholar 

  45. Lee JY, Yoo BC, Lucas WJ. Parallels between nuclear-pore and plasmodesmal trafficking of information molecules. Planta 2000;210:177–178.

    Article  PubMed  CAS  Google Scholar 

  46. Prochiantz A, Joliot A. Can transcription factors function as cell-cell signalling molecules? Nat Rev Mol Cell Biol 2003;4:814–819.

    PubMed  CAS  Google Scholar 

  47. Maizel A. Cell-cell movements of transcription factors in plants. In: Baluska F, Volkmann D, Barlow PW, eds. Cell-Cell Channels. Georgetown: Landes Bioscience, 2006:176–182.

    Google Scholar 

  48. Tassetto M, Maizel A, Osorio J et al. Plant and animal homeodomains use convergent mechanisms for intercellular transfer. EMBO Rep 2005;6:885–890.

    Article  PubMed  CAS  Google Scholar 

  49. Baluska F, Volkmann D, Barlow PW. Cell bodies in a cage. Nature 2004b;428:371.

    Article  PubMed  CAS  Google Scholar 

  50. Baluska F, Volkmann D, Barlow PW. Eukaryotic cells and their cell bodies: Cell theory revisited. Ann Bot 2004c;94:9–32.

    Article  PubMed  CAS  Google Scholar 

  51. Baluska F, Volkmann D, Barlow PW. Cell-cell channels and their implications for Cell Theory. In: Baluska F, Volkmann D, Barlow PW, eds. Cell-Cell Channels. Georgetown: Landes Bioscience, 2006:1–18.

    Google Scholar 

  52. Baluska F, Samaj J, Napier R et al. Maize calreticulin localizes preferentially to plasmodesmata in root apices. Plant J 1999;19:481–488.

    Article  PubMed  CAS  Google Scholar 

  53. Laporte C, Vetter G, Loudes AM et al. Involvement of the secretory pathway and the cytoskeleton in intracellular targeting and tubule assembly of Grapevine fanleaf virus movement protein in to bacco BY-2 cells. Plant Cell 2003;15:2058–2075.

    Article  PubMed  CAS  Google Scholar 

  54. Chen M-H, Tian G-W, Gafni Y et al. Effects of calreticulin on viral cell-to-cell movement. Plant Physiol 2005;138:1866–1876.

    Article  PubMed  CAS  Google Scholar 

  55. Holaska JM, Black BE, Rastinejad F et al. Ca2+-dependent nuclear export mediated by calreticulin. Mol Cell Biol 2002;22:6286–6297.

    Article  PubMed  CAS  Google Scholar 

  56. Schindler M, Jiang L-W. Nuclear actin and myosin as control elements in nucleocytoplasmic transport. J Cell Biol 1986;102:859–862.

    Article  PubMed  CAS  Google Scholar 

  57. Berrios M, Fisher PA, Matz EC. Localization of a myosin heavy chain-like polypeptide to Drosophila nuclear pore complexes. Proc Natl Acad Sci USA 1991;88:219–233.

    Article  PubMed  CAS  Google Scholar 

  58. Tonini R, Grohovaz F, Laporta CAM et al. Gating mechanism of the nuclear pore complex channel in isolated neonatal and adult mouse liver nuclei. FASEB J 1999;13:1395–1403.

    PubMed  CAS  Google Scholar 

  59. Kiseleva E, Drummond SP, Goldberg MW et al. Actin-and protein-4.1-containing filaments link nuclear pore complexes to subnuclear organelles in Xenopus oocyte nuclei. J Cell Sci 2004;117:2481–2490.

    Article  PubMed  CAS  Google Scholar 

  60. Green DM, Johnson CP, Hagan H et al. The C-terminal domain of myosin-like protein 1 (Mlp1p) is a docking site for heterogeneous nuclear ribonucleoproteins that are required for mRNA export. Proc Natl Acad Sci USA 2003;100:1010–1015.

    Article  PubMed  CAS  Google Scholar 

  61. Minakhina S, Myers R, Druzhinina M et al. Crosstalk between the actin cytoskeleton and Ran-mediated nuclear transport. BMC Cell Biol 2005;6:32.

    Article  PubMed  Google Scholar 

  62. Patel S, Rose A, Meulia T et al. Arabidopsis WPP-domain proteins are developmentally associated with the nuclear envelope and promote cell division. Plant Cell 2004;16:3260–3273.

    Article  PubMed  CAS  Google Scholar 

  63. Jeong SY, Rose A, Joseph J et al. Plant-specific mitotic targeting of RanGAP requires a functional WPP domain. Plant J 2005;42:270–282.

    Article  PubMed  CAS  Google Scholar 

  64. Baluska F, Liners F, Hlavacka A et al. Cell wall pectins and xyloglucans are internalized into dividing root cells and accumulate within cell plates during cytokinesis. Protoplasma 2005;225:141–155.

    Article  PubMed  CAS  Google Scholar 

  65. Samaj J, Read ND, Volkmann D et al. The endocytic network in plants. Trends Cell Biol 2005;15:425–433.

    Article  PubMed  CAS  Google Scholar 

  66. Haupt S, Cowan GH, Ziegler A et al. Two plant-viral movement proteins traffic in the endocytic recycling pathway. Plant Cell 2005;17:164–181.

    Article  PubMed  CAS  Google Scholar 

  67. Oparka KJ. Getting the message across: How do plant cells exchange macromolecular complexes? Trends Plant Sci 2004;9:33–41.

    Article  PubMed  CAS  Google Scholar 

  68. Devos D, Dokudovskaya S, Alber F et al. Components of coated vesicles and nuclear pore com plexes share a common molecular architecture. PloS Biol 2004;2:2085–2093.

    Article  CAS  Google Scholar 

  69. Uemura T, Ueda T, Ohniwa RL et al. Systematic analysis of SNARE molecules in Arabidopsis: Dissection of the post-Golgi network in plant cells. Cell Struct Funct 2004;29:49–65.

    Article  PubMed  CAS  Google Scholar 

  70. Chaffey NJ, Harris N. Plasmatubules: Fact or artefact? Planta 1985;165:185–190.

    Article  Google Scholar 

  71. Samaj J, Peters M, Volkmann D et al. Effects of myosin ATPase inhibitor 2,3-butanedione monoxime on distributions of myosins, F-actin, microtubules, and cortical endoplasmic reticulum in maize root apices. Plant Cell Physiol 2000;41:571–582.

    PubMed  CAS  Google Scholar 

  72. Chaffey NJ. Introduction. In: Chaffey NJ, ed. Wood Formation in Trees: Cell and Molecular Biology Techniques. London: Taylor and Francis, 2002a:1–8.

    Google Scholar 

  73. Chaffey NJ, Barlow PW. Myosin, microtubules, and microfilaments: Cooperation between cytoskeletal components during cambial cell division and secondary vascular differentiation in trees. Planta 2002;214:526–436.

    Article  PubMed  CAS  Google Scholar 

  74. Radford JE, Vesk M, Overall RL. Callose deposition at plasmodesmata. Protoplasma 1998;201:30–37.

    Article  CAS  Google Scholar 

  75. Sauter JJ, Kloth S. Plasmodesmatal frequency and radial translocation rates in ray cells of poplar (Populus x canadensis Moench ‘robusta’). Planta 1986;168:377–380.

    Article  Google Scholar 

  76. Chaffey NJ. An introduction to the problems of working with trees. In: Chaffey NJ, ed. Wood Formation in Trees: Cell and Molecular Biology Techniques. London: Taylor and Francis, 2002b:9–16.

    Google Scholar 

  77. Onfelt B, Nedvetzki S, Yanagi K et al. Cutting Edge: Membrane nanotubes connect immune cells. J Immunol 2004;173:1511–1513.

    PubMed  Google Scholar 

  78. Vidulescu C, Clejan S, O’Connor KC. Vesicle traffic through intercellular bridges in DU 145 human prostate cancer cells. J Cell Mol Med 2004;8:388–396.

    Article  PubMed  Google Scholar 

  79. Koyanagi M, Brandes RP, Haendeler J et al. Cell-to-cell connection of endothelial progenitor cells with cardiac myocytes by nanotubes: A novel mechanism for cell fate changes? Circ Res 2005;96:1039–1041.

    Article  PubMed  CAS  Google Scholar 

  80. Watkins SC, Salter RD. Functional connectivity between immune cells mediated by tunneling nanotubules. Immunity 2005;23:309–318.

    Article  PubMed  CAS  Google Scholar 

  81. Hsiung F, Ramirez-Weber F-A, Iwaki DD et al. Dependence of Drosophila wing imaginal disc cytonemes on Decapentaplegic. Nature 2005;437:560–563.

    Article  PubMed  CAS  Google Scholar 

  82. Voigt B, Timmers T, Samaj J et al. GFP-FABD2 fusion construct allows in vivo visualization of the dynamic actin cytoskeleton in all cells of Arabidopsis seedlings. Eur J Cell Biol 2005;84:595–608.

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Institute of Cellular and Molecular Botany, University of Bonn, Kirschallee 1, 53115, Bonn, Germany

    Jozef Samaj, Andrej Hlavacka & Diedrik Menzel

  2. Department of Biology, Bath Spa University, Newton St. Loe, UK

    Nigel Chaffey

  3. Department of Engineering Science, University of Oxford, Oxford, UK

    Uday Tirlapur & Zhan Feng Cui

  4. Max Planck Institute for Plant Breeding Research, Cologne, Germany

    Jan Jasik

  5. Institute of Cellular and Molecular Botany, Rheinische Friedrich-Wilhelms University of Bonn, Bonn, Germany

    Dieter Volkmann & Frantisek Baluska

  6. Institute of Plant Genetics and Biotechnology, Slovak Academy of Sciences, Akademicka 2, SK-950 07, Nitra, Slovak Republic

    Jozef Samaj

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  1. Jozef Samaj
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Samaj, J. et al. (2006). Actin and Myosin VIII in Plant Cell-Cell Channels. In: Cell-Cell Channels. Springer, New York, NY. https://doi.org/10.1007/978-0-387-46957-7_8

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