Plasmodesmata

Abstract

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. Evidence suggests that small molecules can pass from cell to cell by passive diffusion and that this is controlled by regulation of the pore itself. This contributes to processes such as the transport of sugars between cells and tissues. Many endogenous plant proteins and ribonucleic acid (RNA)‐based signals also utilise plasmodesmata for cell‐to‐cell and long‐distance movement. Recent data suggests that plasmodesmata are tightly controlled during development and in response to environmental changes. There is increasing evidence that this regulation is controlled by proteins that have specific plasmodesmata‐associated functions in stimulus perception and signalling. In addition, many viruses exploit plasmodesmata for cell‐to‐cell spread during infection and their encoded viral movement proteins manipulate the pores to facilitate this process.

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 through 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 cytoplasmic 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 pathogen perception.
  • 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.
  • Groups of cells may be connected by plasmodesmata that share an SEL different to that 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; symplasm; cell‐to‐cell communication

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. Scale bar is 200 nm. (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. Scale bar is 100 nm. Robinson‐Beers and Evert 1991. With permission of Springer. (c) Comparison of simple and branched forms of plasmodesmata. In branched plasmodesmata, several adjacent plasmodesmal canals converge to form an enlarged central cavity.
Figure 2. 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 3. The observation of PD twins suggest that secondary PD formation occurs adjacent to existing PD. Figure (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). Figure (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 desmotubules giving rise to adjacent PD pores. In the lower model (b) the new secondary pore is formed by localised wall erosion as a new ER strand ‘drills’ through the wall to connect to the desmotubule of the original pore. Reproduced from Faulkner et al.2008 © American Society of Plant Biologists.
Figure 4. 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.
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References

Austefjord MW, Gerdes HH and Wang X (2014) Tunneling nanotubes: diversity in morphology and structure. Communicative & Integrative Biology 7: e27934.

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 United States of America 94: 14150–14155.

Benitez‐Alfonso Y, Cilia M, Thomas C, et al. (2009) Control of Arabidopsis meristem development by thioredoxin‐dependent regulation of intercellular transport. Proceedings of the National Academy of Sciences USA 106: 3615–3620.

Benitez‐Alfonso Y, Faulkner C, Pendle A, et al. (2013) Symplastic intercellular connectivity regulates lateral root patterning. Developmental Cell 26: 136–147.

Crawford KM and Zambryski PC (2000) Subcellular localization determines the availability of non‐targeted proteins to plasmodesmatal transport. 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.

Faulkner C, Petutschnig E, Benitez‐Alfonso Y, et al. (2013) LYM2‐dependent chitin perception limits molecular flux via plasmodesmata. Proceedings of the National Academy of Sciences USA 110: 9166–9170.

Fitzgibbon J, Beck M, Zhou J, et al. (2013) A developmental framework for complex plasmodesmata formation revealed by large‐scale imaging of the Arabidopsis leaf epidermis. Plant Cell 25: 57–70.

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.

Grison MS, Brocard L, Fouillen L, et al. (2015) Specific membrane lipid composition is important for plasmodesmata function in Arabidopsis. Plant Cell 27: 1228–1250.

Kankanala P, Czymmek K and Valent B (2007) Roles for rice membrane dynamics and plasmodesmata during biotrophic invasion by the blast fungus. Plant Cell 19: 706–724.

Khang CH, Berruyer R, Giraldo MC, et al. (2010) Translocation of Magnaporthe oryzae effectors into rice cells and their subsequent cell‐to‐cell movement. Plant Cell 22: 1388–1403.

knox K, Wang P, Kriechbaumer V et al. (2015) Putting the Squeeze on Plasmodesmata: A Role for Reticulons in Primary Plasmodesmata Formation. Plant Physiology 168: 1563–1572.

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.

Lee JY, Wang X, Cui W, et al. (2011) A plasmodesmata‐localized protein mediates crosstalk between cell‐to‐cell communication and innate immunity in Arabidopsis. Plant Cell 23: 3353–3373.

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.

Melnyk CW, Molnar A and Baulcombe DC (2011) Intercellular and systemic movement of RNA silencing signals. EMBO Journal 30: 3553–3563.

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.

Robinson‐Beers K and Evert RF (1991) Fine structure of plasmodesmata in mature leaves of sugarcane. Planta 184 (3): 307–318.

Ruan YL, Xu SM, White R and Furbank RT (2004) Genotypic and developmental evidence for the role of plasmodesmatal regulation in cotton fiber elongation mediated by callose turnover. Plant Physiology 136: 4104–4113.

Stahl Y, Grabowski S, Bleckmann A et al. (2013) Moderation of Arabidopsis root stemness by CLAVATA1 and ARABIDOPSIS CRINKLY4 receptor kinase complexes. Current Biology 23: 362–371.

Stonebloom S, Burch‐Smith T, Kim I et al. (2009) Loss of the plant DEAD‐box protein ISE1 leads to defective mitochondria and increased cell‐to‐cell transport via plasmodesmata. Proceedings of the National Academy of Sciences USA 106: 17229–17234.

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.

Thieme CJ, Rojas‐Triana M, Stecyk E, et al. (2015) Endogenous Arabidopsis messenger RNAs transported to distant tissues. Nature Plants 1: 15025.

Tilsner J, Linnik O, Louveaux M, et al. (2013) Replication and trafficking of a plant virus are coupled at the entrances of plasmodesmata. Journal of Cell Biology 7: 981–995.

Tian Q, Olsen L, Sun B et al. (2007) Subcellular localization and functional domain studies of DEFECTIVE KERNEL1 in maize and Arabidopsis suggest a model for aleurone cell fate specification involving CRINKLY4 and SUPERNUMERARY ALEURONE LAYER1. Plant Cell 19: 3127–3145.

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 movement in the Arabidopsis apex. Development 130: 3735–3745.

Xu XM, Wang J, Xuan Z, et al. (2011) Chaperonins facilitate KNOTTED1 cell‐to‐cell trafficking and stem cell function. Science 333: 1141–1144.

Further Reading

Brunkard JO, Runkel AM and Zambryski PC (2015) The cytosol must flow: intercellular transport through plasmodesmata. Current Opinion in Cell Biology 35: 13–20.

Heinlein M (2015) Plant virus replication and movement. Virology 479–480: 657–671.

Lee JY and Lu H (2011) Plasmodesmata: the battleground against intruders. Trends in Plant Science 16: 201–210.

Oparka KJ (ed) (2005) Plasmodesmata. Annual Plant Reviews. Oxford: Blackwell Publishing Ltd.

Otero S, Helariutta Y and Benitez‐Alfonso Y (2015) Symplastic communication in organ formation and tissue patterning. Current Opinion in Plant Biology 29: 21–28.

Roberts AG and Oparka KJ (2003) Plasmodesmata and the control of symplastic transport. Plant, Cell & Environment 26: 103–124.

Schulz A (2015) Diffusion or bulk flow: how plasmodesmata facilitate pre‐phloem transport of assimilates. Journal of Plant Research 128: 49–61.

Stahl Y and Faulkner C (2015) Receptor complex mediated regulation of symplastic traffic. Trends in Plant Science. DOI: 10.1016/j.tplants.2015.11.002.

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How to Cite close
Faulkner, Christine, and Oparka, Karl J(Aug 2016) Plasmodesmata. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0001681.pub3]