Plasmodesmata

Christine R Faulkner, University of Edinburgh, Edinburgh, UK
Karl J Oparka, University of Edinburgh, Edinburgh, UK

Published online: September 2009

DOI: 10.1002/9780470015902.a0001681.pub2

Plasmodesmata are plasma membrane-lined pores that span the adjoining walls of plant cells. They permit the intercellular passage of molecules and signals and play a central role in plant physiology and development. Plasmodesmata are also conduits through which viral genomes spread during infection, and many viruses encode movement proteins that modify plasmodesmata, facilitating the intercellular trafficking of macromolecules. Recent evidence suggests that many endogenous plant proteins and systemic ribonucleic acid (RNA)-based signals also utilize plasmodesmata for cell-to-cell and long-distance movement. It appears that the substructural morphology of plasmodesmata is central to their role in cell-to-cell communication, allowing them to function as controllable ‘valves’ that regulate the intercellular passage of molecules.

Key Concepts

  • Plant cells are connected to each other by cytoplasmic bridges called plasmodesmata. The continuous interconnected cytoplasm in plants is referred to as the symplasm.
  • A tube of endoplasmic reticulum passes though plasmodesmata and connects the endoplasmic reticulum of neighbouring cells, thus providing endomembrane continuity between cells.
  • Primary plasmodesmata are formed at cytokinesis when strands of endoplasmic reticulum are trapped between fusing vesicles in the developing cell wall.
  • Secondary plasmodesmata are formed across existing cell walls, including those at graft unions, and usually arise immediately adjacent to existing plasmodesmata.
  • Molecules smaller than the size exclusion limit (SEL) of plasmodesmata are able to move freely through the cytolplasmic channel of plasmodesmata by simple diffusion.
  • The SEL of plasmodesmata may increase or decrease to allow changes in plasmodesmatal conductance. This may occur under different conditions, for example, in response to intracellular factors such as cytoplasmic calcium levels or in response to changes in turgor pressure between cells.
  • Some endogenous proteins and some movement proteins encoded by plant viruses are able to increase the SEL of plasmodesmata to facilitate their own passage into neighbouring cells. This enables these proteins to function in cells in which they are not normally expressed.
  • Regions of cells may be connected by plasmodesmata that share an SEL different to the SEL of neighbouring cells. These regions of cells are called symplasmic domains.
  • Some proteins and RNA molecules pass into the plant's translocation stream and move over long distances. These macromolecules traffic through the plasmodesmata that join sieve elements (SE) and companion cells within the phloem. These macromolecules may have a site of action distant to their site of expression and synthesis.

Keywords: plants; plasmodesmata; intercellular transport; virus movement

Figure 1. Ultrastructure of plasmodesmata. (a) Plasmodesmata in longitudinal section appear as elongated pores that traverse the cell wall. Note the central desmotubule, an endoplasmic reticulum-derived structure that facilitates endomembrane continuity between cells. The plasmodesmata shown also have a prominent neck constriction at the entrance to the pore. (b) Plasmodesmata in transverse section. Here the plasmodesmata appear as circular, plasma membrane-lined pores. The desmotubule is seen in the centre of the pore. Reproduced with permission from Robinson-Beers K and Evert RF (1991). Fine structure of plasmodesmata in mature leaves of sugarcane. Planta 184(3): 307–318.
Figure 2. Comparison of simple and branched forms of plasmodesmata. In branched plasmodesmata, several adjacent plasmodesmal canals converge to form an enlarged central cavity.
Figure 3. Diagrammatic representation of a simple plasmodesma. Small molecules pass through the cytoplasmic sleeve separating the desmotubule from the plasma membrane. Globular proteins line the plasma membrane and desmotubule, and are linked by spoke-like extensions.
Figure 4. The observation of PD twins suggest secondary PD formation occurs adjacent to existing PD. (a) shows PD twins observed in face view in the basal cell wall of a fractured tobacco trichome imaged by field emission scanning electron microscopy (FESEM). (b) depicts two alternative models for how these PD twins might be formed during cell wall expansion. In the upper model (A) a second desmotubule is inserted into the enlarging PD pore to produce a transitory structure that contains two desmotubules. New wall is then deposited between the two demotubules giving rise to adjacent PD pores. In the lower model (B) the new secondary pore is formed by localized wall erosion as a new ER strand ‘drills’ through the wall to connect to the desmotubule of the original pore. Reproduced from www.plantcell.org. Copyright American Society of Plant Biologists.
Figure 5. Diagrammatic representation of the movement of the Tobacco mosaic virus (TMV) genome through plasmodesmata. The viral RNA is trafficked through the ‘gated’ plasmodesmal pore, together with the viral movement protein, as a linear ribonucleoprotein complex.
close
 References
    Balachandran S, Xiang Y, Scobert C, Thompson G and Lucas WJ (1997) Phloem sap proteins from Cucurbita maxima and Ricinus communis have the capacity to traffic cell to cell through plasmodesmata. Proceedings of the National Academy of Sciences of the USA 94: 14150–14155.
    Brosnan CA, Mitter N, Christie M et al. (2007) Nuclear gene silencing directs reception of long-distance mRNA silencing in Arabidopsis. Proceedings of the National Academy of Sciences of the USA 104: 14741–14746.
    Crawford KM and Zambryski PC (2000) Characterisation of two forms of plant intercellular protein movement: subcellular address controls cell-to-cell transportability. Current Biology 10: 1032–1040.
    Duckett CM, Oparka KJ, Prior DAM, Dolan L and Roberts K (1994) Dye-coupling in the root epidermis of Arabidopsis is progressively reduced during development. Development 120: 3247–3255.
    Erwee MG and Goodwin PB (1985) Symplast domains in extrastelar tissues of Egeria densa Planch. Planta 163: 9–19.
    Faulkner C, Akman OE, Bell K et al. (2008) Peeking into pit fields: a multiple twinning model of secondary plasmodesmata formation in tobacco. Plant Cell 20(6): 1504–1518. Epub 30 Jun 2008.
    Goshroy S and Citovsky V (1997) Transport of proteins and nucleic acids through plasmodesmata. Annual Review of Plant Physiology and Plant Molecular Biology 48: 27–50.
    Kim Z, Hempel FD, Sha K, Pfluger J and Zambryski P (2002) Identification of a developmental transition in plasmodesmatal function during embryogenesis in Arabidopsis thaliana. Development 129: 1261–1272.
    Kobayashi K, Otegui MS, Krishnakumar S, Mindrinos M and Zambryski P (2007) INCREASED SIZE EXCLUSION LIMIT2 encodes a putative DEVH box RNA helicase involved in plasmodesmata function during Arabidopsis embryogenesis. Plant Cell 19: 1885–1897.
    book Kollmann R and Glockmann C (1999) "Multimorphology and nomenclature of plasmodesmata in higher plants". In: Van Bel AJE and van Kesteren WJP (eds) Plasmodesmata structure, function, role in cell communication. Berlin: Springer.
    Liarzi O and Epel BL (2005) Development of a quantitative tool for measuring changes in the coefficient of conductivity of plasmodesmata induced by developmental, biotic, and abiotic signals. Protoplasma 225: 67–76.
    Lucas WJ (2006) Viral movement proteins: agents for cell-to-cell trafficking of viral genomes. Virology 344: 169–184.
    Lucas WJ, Bouche-Pillon S, Jackson DP et al. (1995) Selective trafficking of KNOTTED1 homeodomain protein and its mRNA through plasmodesmata. Science 270: 1980–1983.
    Oparka KJ, Roberts AG, Boevink P et al. (1999) Simple, but not branched, plasmodesmata allow the non-specific trafficking of proteins in developing tobacco leaves. Cell 97: 743–754.
    Oparka KJ and Turgeon R (1999) Sieve elements and companion cells – traffic control centers of the phloem. Plant Cell 11: 739–750.
    Overall RL and Blackman LM (1996) A model of the macromolecular structure of plasmodesmata. Trends in Plant Science 1: 307–311.
    Tassetto M, Maizel A, Osorio J and Jolio A (2005) Plant and animal homeodomains use convergent mechanisms for intercellular transfer. Embo Reports 6: 885–890.
    Terry BR and Robards AW (1987) Hydrodynamic radius alone governs the mobility of molecules through plasmodesmata. Planta 171: 145–171.
    Thomas C, Bayer EM, Ritzenthaler C, Fernandez-Cavino L and Maule AJ (2008) Specific targeting of a plasmodesmal protein affecting cell-to-cell communication. PLoS Biology 6: e7.
    Voinnet O (2005) Induction and suppression of RNA silencing: insights from viral infections. Nature Reviews Genetics 6: 206–220.
    Wille AC and Lucas WJ (1984) Ultrastructural and histochemical studies on guard cells. Planta 186: 2–12.
    Wolf S, Deom CM, Beachy RN and Lucas WJ (1989) Movement protein of tobacco mosaic virus modifies plasmodesmatal size exclusion limit. Science 246: 377–379.
    Wu X, Dinnemy JR, Crawford KM et al. (2003) Modes of intercellular transcription factor movemrent in the Arabidopsis apex. Development 130: 3735–3745.
 Further Reading
    Ding B (1997) Cell-to-cell transport of macromolecules through plasmodesmata: a novel signalling pathway in plants. Trends in Cell Biology 7: 5–9.
    Gilbertson RL and Lucas WJ (1996) How do viruses traffic on the vascular highway? Trends in Plant Science 1: 260–268.
    Jackson D and Hake S (1997) Morphogenesis on the move: cell-to-cell trafficking of plant regulatory proteins. Current Opinion in General Development 7: 495–500.
    Lucas WJ, Ding B and van der Schoot C (1993) Plasmodesmata and the supracellular nature of plants. New Phytologist 125: 435–476.
    book Oparka KJ (ed.) (2005) Plasmodesmata. Annual Plant Reviews. Oxford: Blackwell Publishing Ltd.

Related Sub-Topics:

Plant Development | General Plant Science | Cellular Transport | Intracellular and Extracellular Signalling | Cell Compartments and Cellular Organelles | Plant Disease
Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

Article Title: Plasmodesmata
 
How to Cite close
Faulkner, Christine R, and Oparka, Karl J(Sep 2009) Plasmodesmata. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0001681.pub2]