[go: up one dir, main page]
Skip to main content
SpringerLink
Log in

Imaging plasmodesmata

  • Review Article
  • Published:
Protoplasma Aims and scope Submit manuscript

Abstract

At only 50 nm in diameter, plasmodesmata (PD) are below the limit of resolution of conventional light microscopy. Consequently, much of our current interpretation of the substructure of PD is derived from transmission electron microscopy. However, PD can be imaged with alternative techniques, including field emission scanning electron microscopy and ‘super-resolution’ imaging approaches such as 3D-structured illumination microscopy. This review considers the methods currently available for studying PD and focuses on the boundary between light- and electron-based imaging approaches.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Aaziz RD, Dinant A, Epel BL (2001) Plasmodesmata and plant cytoskeleton. Trends Plant Sci 6:326–330

    Article  CAS  PubMed  Google Scholar 

  • Abbe E (1873) Beitrage zur theorie das mikroskops und der mikroskopischen wahrnehmung. Arch Mikrosk Anat 9:413–468

    Article  Google Scholar 

  • Amari K, Boutant E, Hofmann C, Schmitt-Keichinger C, Fernandez-Calvino L, Dider P, Lerich A, Mutterer J, Thomas CL, Heinlein M, Mely Y, Maule AJ, Rizenthaler C (2010) A family of plasmodesmal proteins with receptor-like properties for plant viral movement proteins. PLoS Pathog 6:1–10

    Article  Google Scholar 

  • Andro R, Mizuno H, Miyawaki A (2004) Regulated fast reversible protein highlighting. Science 306:1370–1373

    Article  Google Scholar 

  • Axelrod D, Burghardt TP, Thompson R (1984) Total internal reflection fluorescence. Ann Rev Biophys Bioeng 13:247–268

    Article  CAS  Google Scholar 

  • Barlow PW, Hawes CR, Horne JC (1984) Structure of amyloplasts and endoplasmic reticulum in the root caps of Lepidium sativum and Zea mays observed after selective membrane staining and by high-voltage electron microscopy. Planta 160:363–371

    Article  CAS  PubMed  Google Scholar 

  • Bates M, Huang B, Dempsey GT, Zhuang X (2007) Multicolour super-resolution imaging with photo-switchable fluorescent probes. Science 317:1749–1753

    Article  CAS  PubMed  Google Scholar 

  • Betzig E, Patterson GH, Sougrat R, Lindwasser OW, Olenych S, Bonifacino JS, Davidson MW, Lippincott-Schwartz J, Hess HF (2006) Imaging intracellular fluorescent proteins at nanometer resolution. Science 313:1643–1645

    Article  Google Scholar 

  • Biteen JS, Thompson MA, Tselentis NK, Bowman GR, Shapiro L, Moerner WE (2008) Super-resolution imaging in live Caulobacter crescentus cells using photoswitchable EYFP. Nat Meth 5:947–949

    Article  CAS  Google Scholar 

  • Blackman LM, Overall RL (2001) Structure and function of plasmodesmata. Aust J Plant Physiol 28:709–727

    CAS  Google Scholar 

  • Chapman S, Oparka KJ, Roberts AG (2005) New tools for in vivo fluorescence tagging. Curr Opin Plant Biol 8:565–573

    Article  CAS  PubMed  Google Scholar 

  • Conchello J-A, Lichtman JW (2005) Optical sectioning microscopy. Nat Meth 2:920–931

    Article  CAS  Google Scholar 

  • Cortese K, Diaspro A, Tacchetti C (2009) Advanced correlative light/electron microscopy: current methods and new developments using Tokuyasu cryosections. J Histochem Cytochem 57:1103–1112

    Article  CAS  PubMed  Google Scholar 

  • Currier H (1957) Callose substance in plant cells. Amer J Bot 44:478–488

    Article  Google Scholar 

  • Ding B, Turgeon R, Parthasarathy MV (1992a) Substructure of freeze-substituted plasmodesmata. Protoplasma 169:28–41

    Article  Google Scholar 

  • Ding B, Haudenshield JS, Hull RJ, Wolf S, Beachy RN, Lucas WJ (1992b) Secondary plasmodesmata are specific sites of localization of the tobacco mosaic virus movement protein in transgenic tobacco plants. Plant Cell 4:915–928

    Article  CAS  PubMed  Google Scholar 

  • Donnert G, Keller J, Wurm CA, Rizzoli SO, Westphal V, Schonle A, Jahn R, Jakobs S, Eggeling C, Hell SW (2007) Two-color far-field fluorescence. Nanoscopy Biophys J 92:L67–L69

    Article  CAS  Google Scholar 

  • Ehlers K, Kollmann R (2001) Primary and secondary plasmodesmata: structure, origin and functioning. Protoplasma 216:1–30

    Article  CAS  PubMed  Google Scholar 

  • Epel B (2009) Plant viruses spread by diffusion on ER-associated movement-protein-rafts through plasmodesmata gated by viral induced host beta-1, 3-glucanases. Semin Cell Dev Biol 20:1074–1081

    Article  CAS  PubMed  Google Scholar 

  • Epel BL, Padgett HS, Heinlein M, Beachy RN (1996) Plant virus dynamics probed with GFP–protein fusion. Gene 173:75–79

    Article  CAS  PubMed  Google Scholar 

  • Esau K, Thorsch J (1985) Sieve plate pores and plasmodesmata, the communication channels of the symplast—ultrastructural aspects and developmental relations. Amer J Bot 72:1641–1653

    Article  Google Scholar 

  • Escobar NM, Haupt S, Thow G, Boevink P, Chapman S, Oparka K (2003) High-throughput viral expression of cDNA–green fluorescent protein fusions reveals novel subcellular addresses and identifies unique proteins that interact with plasmodesmata. Plant Cell 15:1507–1523

    Article  CAS  PubMed  Google Scholar 

  • Evert RF, Mierzwa RJ (1989) The cell wall–plasmalemma interface in sieve tubes of barley. Planta 177:24–34

    Article  Google Scholar 

  • Faulkner C, Akman OE, Bell K, Jeffree C, Oparka K (2008) Peeking into pit fields: a multiple twinning model of secondary plasmodesmata formation in tobacco. Plant Cell 20:1504–1518

    Article  CAS  PubMed  Google Scholar 

  • Fitzgibbon J, Bell K, King E, Oparka K (2010) Super-resolution imaging of plasmodesmata using three-dimensional structured illumination microscopy. Plant Physiol 153:1453–1463

    Article  CAS  PubMed  Google Scholar 

  • Fridborg I, Grainger J, Page A, Coleman M, Findlay K, Angell S (2003) TIP, a novel host factor linking callose degradation with the cell-to-cell movement of potato virus X. Mol Plant Microb Interact 16:132–140

    Article  CAS  Google Scholar 

  • Geipmans BNG, Adams SR, Ellisman MH, Tsein RY (2006) The fluorescent toolbox for assessing protein location and function. Science 312:217–224

    Article  Google Scholar 

  • Gilkey JC, Staehelin LA (1986) Advances in ultrarapid freezing for the preservation of cellular ultrastructure. J Electron Microsc Tech 3:177–210

    Article  Google Scholar 

  • Glockmann C, Kollmann R (1996) Structure and development of cell connections in the phloem of Metasequoia glyptostroboides needles. I. Ultrastructural aspects of modified primary plasmodesmata in Strasburger cells. Protoplasma 193:191–203

    Article  Google Scholar 

  • Grabenbauer M, Geerts WJ, Fernandez-Rodriguez J, Hoenger A, Koster AJ, Nilsson T (2005) Correlative microscopy and electron tomography of GFP through photooxidation. Nat Meth 2:857–862

    Article  CAS  Google Scholar 

  • Guenoune-Gelbart D, Elbaum M, Sagi G, Levy A, Epel BL (2008) Tobacco mosaic virus (TMV) replicase and movement protein function synergistically in facilitating TMV spread by lateral diffusion in the plasmodesmal desmotubule of Nicotiana benthamiana. Mol Plant Microb Interact 21:335–345

    Article  CAS  Google Scholar 

  • Gustafsson MGL (2000) Surpassing the lateral resolution limit by a factor of two using structured illumination microscopy. J Microsc 198:82–87

    Article  CAS  PubMed  Google Scholar 

  • Gustafsson MGL (2005) Nonlinear structured-illumination microscopy: wide-field fluorescence imaging with theorectically unlimited resolution. Proc Natl Acad Sci USA 2:13081–13086

    Article  Google Scholar 

  • Gustafsson MGL, Agard DA, Sedat JW (1999) I5M: 3D widefield light microscopy with better than 100 nm axial resolution. J Microsc 195:10–16

    Article  CAS  PubMed  Google Scholar 

  • Habuchi S, Ando R, Dedecker P, Verheijen W, Mizuno H, Miyawaki A, Hofkens J (2005) Reversible single-molecule photoswitching in the GFP-like fluorescent protein dronpa. Proc Natl Acad Sci USA 102:9511–9516

    Article  CAS  PubMed  Google Scholar 

  • Hawes C (1994) Electron microscopy. In: Harris N, Oparka KJ (eds) Plant cell biology: a practical approach. IRL, Oxford, pp 69–96

    Google Scholar 

  • Hein BH, Willig KI, Wurm CA, Westphal V, Jakobs S, Hell SW (2010) Stimulated emission depletion nanoscopy of living cells using SNAP-tag fusion proteins. Biophys J 98:158–163

    Article  CAS  PubMed  Google Scholar 

  • Hell SW, Stelzer EHK (1994) Confocal microscopy with an increased detection aperture: type-B 4Pi confocal microscopy. Opt Lett 19:222–224

    Article  CAS  PubMed  Google Scholar 

  • Hepler PK (1982) Endoplasmic reticulum in the formation of the cell plate and plasmodesmata. Protoplasma 111:121–133

    Article  Google Scholar 

  • Huang B (2010) Super-resolution optical microscopy: multiple choices. Curr Opin In Chem Biol 14:10–14

    Article  CAS  Google Scholar 

  • Huang B, Wang W, Bates M, Zhuang X (2008) Three-dimensional super-resolution imaging by stochastic optical reconstruction microscopy. Science 319:810–813

    Article  CAS  PubMed  Google Scholar 

  • Huang B, Bates M, Zhuang XW (2009) Super-resolution fluorescence microscopy. Ann Rev Biochem 78:993–1016

    Article  CAS  PubMed  Google Scholar 

  • Iglesias VA, Meins F Jr (2000) Movement of plant viruses is delayed in a β-1, 3-glucanase-deficient mutant showing a reduced plasmodesmatal size exclusion limit and enhanced callose deposition. Plant J 21:157–166

    Article  CAS  PubMed  Google Scholar 

  • Klar TA, Hell SW (1999) Subdiffraction resolution in far-field fluorescence microscopy. Opt Lett 24:954–956

    Article  CAS  PubMed  Google Scholar 

  • Koster AJ, Klumperman J (2003) Electron microscopy in cell biology: integrating structure and function. Nat Cell Biol 4 (Supplement):SS6–SS10

    Google Scholar 

  • Levy A, Erlanger M, Rosenthal M, Epel B (2007) A plasmodesmata-associated β-1, 3-glucanase in Arabidopsis. Plant J 49:669–682

    Article  CAS  PubMed  Google Scholar 

  • Lippincott-Schwartz J, Patterson GH (2009) Photoactivatable fluorescent proteins for diffraction-limited and super-resolution imaging. Trends Cell Biol 19:555–565

    Article  CAS  PubMed  Google Scholar 

  • Liu DYT, Kuhlmey BT, Smith PMC, Day DA, Faulkner CR, Overall RL (2008) Reflection across plant cell boundaries in confocal laser scanning microscopy. J Microsc 231:349–357

    Article  CAS  PubMed  Google Scholar 

  • Lucas WJ (2006) Plant viral movement proteins: agents for cell-to-cell trafficking of viral genomes. Virology 344:169–184

    Article  CAS  PubMed  Google Scholar 

  • Maillet M (1959) Modification de la technique de Champy au tetraoxyde d’osmium-iodure de K. Resultats de son application a l’etude des fibres nerveuses. C R Soc Biol 153:939–941

    CAS  Google Scholar 

  • Maranto AR (1982) Neuronal mapping: a photooxidation reaction makes lucifer yellow useful for electron microscopy. Science 217:953–955

    Article  CAS  PubMed  Google Scholar 

  • Maule AJ (2008) Plasmodesmata:structure, function and biogenesis. Curr Opin Plant Biol 11:680–686

    Article  CAS  PubMed  Google Scholar 

  • McIntosh R, Nicastro D, Mastronarde D (2005) New views of cells in 3D: an introduction to electron microscopy. Trends Cell Biol 15:43–51

    Article  CAS  PubMed  Google Scholar 

  • Meisslitzer-Ruppitsch C, Rohrl C, Neumuller J, Pavelka M, Ellinger A (2009) Photooxidation technology for correlated light and electron microscopy. J Microsc 235:322–335

    Article  CAS  PubMed  Google Scholar 

  • Moore PJ, Fenczik CA, Deom CM, Beachy RN (1992) Developmental changes in plasmodesmata in transgenic tobacco expressing the movement protein of tobacco mosaic virus. Protoplasma 170:115–127

    Article  Google Scholar 

  • Moreno N, Bougourd S, Haselhoff J, Feijo JA (2006) Imaging plant cells. In: Pawley JP (ed) Handbook of biological confocal microscopy, 3rd edn. Springer, New York, pp 769–787

    Chapter  Google Scholar 

  • Mullendore DL, Windt CW, Van As H, Knoblauch M (2010) Sieve tube geometry in relation to phloem flow. Plant Cell 22:579–593

    Article  CAS  PubMed  Google Scholar 

  • Olesen P (1979) The neck constriction in plasmodesmata. Planta 144:349–358

    Article  Google Scholar 

  • Oparka KJ (2004) Getting the message across: how do plant cells exchange macromolecular complexes? Trends Plant Sci 9:33–41

    Article  CAS  PubMed  Google Scholar 

  • Oparka KJ, Read ND (1994) The use of fluorescent probes for studies of living plant cells, Plant cell biology: a practical approach. IRL, Oxford, pp 27–50

    Google Scholar 

  • Oparka KJ, Prior DAM, Crawford JW (1994) Behaviour of plasma membrane, cortical ER and plasmodesmata during plasmolysis of onion epidermal cells. Plant Cell Environ 17:163–171

    Article  Google Scholar 

  • Patterson GH, Davidson M, Manley S, Lippincott-Schwartz J (2010) Super-resolution imaging using single-molecule localization. Annu Rev Phys Chem 61:345–367

    Article  CAS  PubMed  Google Scholar 

  • Pellegrino de Iraldi A (1977) Significance of the Maillet method (ZIO) for cytochemical studies of subcellular structures. Experientia 33:1–10

    Article  CAS  Google Scholar 

  • Perinetti G, Muller T, Spaar A, Polishchuk R, Luini A, Egner A (2009) Correlation of 4Pi and electron microscopy to study transport through single Golgi stacks in living cells with super resolution. Traffic 10:379–391

    Article  CAS  PubMed  Google Scholar 

  • Ritzenthaler C, Finlay K, Roberts K, Maule AJ (2000) Rapid detection of plasmodesmata in purified cell walls. Protoplasma 211:165–171

    Article  Google Scholar 

  • Robards AW, Lucas WJ (1990) Plasmodesmata. Annu Rev Plant Physiol 41:369–419

    Article  Google Scholar 

  • Roberts AG (2005) Plasmodesmal structure and development. In: Oparka KJ (ed) Plasmodesmata. Blackwell, Oxford, pp 1–23

    Chapter  Google Scholar 

  • Roberts IM, Boevink P, Roberts AG, Sauer N, Reichel C, Oparka KJ (2001) Dynamic changes in the frequency and architecture of plasmodesmata during the sink-source transition in tobacco leaves. Protoplasma 218:31–44

    Article  CAS  PubMed  Google Scholar 

  • Robinson JM, Takizawa T (2009) Correlative fluorescence and electron microscopy in tissues: immunocytochemistry. J Microsc 235:259–272

    Article  CAS  PubMed  Google Scholar 

  • Robinson-Beers K, Evert RF (1991) Fine structure of plasmodesmata in mature leaves of sugarcane. Planta 184:307–318

    Google Scholar 

  • Schermelleh L, Carlton PM, Haase S, Shao L, Winoto L, Kner P, Burke B, Cardoso MC, Agard DA, Gustafsson MGL, Leonhardt H, Sedat JW (2008) Subdiffraction multicolor imaging of the nuclear periphery with 3D structured illumination microscopy. Science 320:1332–1336

    Article  CAS  PubMed  Google Scholar 

  • Schmidt R, Wurm CA, Jakobs S, Engelhardt J, Egner A, Hell SW (2008) Spherical nanosized focal spot unravels the interior of cells. Nat Meth 5:539–544

    Article  CAS  Google Scholar 

  • Simpson C, Thomas C, Findlay K, Bayer E, Maule AJ (2009) An Arabidopsis GPI-anchor plasmodesmal neck protein with callose binding activity and potential to regulate cell-to-cell trafficking. Plant Cell 21:581–594

    Article  CAS  PubMed  Google Scholar 

  • Stemmer A, Beck M, Fiolka R (2008) Widefield fluorescence microscopy with extended resolution. Histochem Cell Biol 130:807–817

    Article  CAS  PubMed  Google Scholar 

  • Thomas CL, Bayer EM, Ritzenthaler C, Fernandez-Calvino L, Maule AJ (2008) Specific targeting of a plasmodesmal protein affecting cell-to-cell communication. PLoS Biol 6:180–190

    Article  CAS  Google Scholar 

  • Tilsner J, Oparka KJ (2010) Tracking the green invaders: advances in imaging virus infection in plants. Biochem J 430:21–37

    Article  CAS  PubMed  Google Scholar 

  • Tilsner J, Amari K, Torrance L (2010) Plasmodesmata viewed as specialised membrane adhesion sites. Protoplasma. doi:10.1007/s00709-010-0217-6

  • Tomenius K, Clapham D, Meshi T (1987) Localization by immunogold cytochemistry of the virus-coded 30K protein in plasmodesmata of leaves infected with tobacco mosaic virus. Virology 160:363–371

    Article  CAS  PubMed  Google Scholar 

  • Vesk M, Dibbayawan TP, Vesk PA, Egan EA (2000) Field emission scanning electron microscopy of plant cells. Protoplasma 210:138–155

    Article  Google Scholar 

  • Vogel F, Hofius D, Sonnewald U (2007) Intracellular trafficking of potato leaf roll virus movement protein in transgenic Arabidopsis. Traffic 8:1205–1214

    Article  CAS  PubMed  Google Scholar 

  • Westphal V, Rizzoli SO, Lauterbach MA, Kamin D, Jahn R, Hell SW (2008) Video-rate far-field optical nanoscopy dissects synaptic vesicle movement. Science 320:246–249

    Article  CAS  PubMed  Google Scholar 

  • White DL, Mazurkiewicz JE, Barrnett RJ (1979) A chemical mechanism for tissue staining by osmium tetroxide-ferrocyanide mixtures. J Histochem Cytochem 27:1084–1091

    CAS  PubMed  Google Scholar 

  • White J, Amos W, Fordham M (1987) An evaluation of confocal versus conventional imaging of biological structures by fluorescence light microscopy. J Cell Biol 105:41–48

    Article  CAS  PubMed  Google Scholar 

  • Willig KI, Kellner RR, Medda R, Hein B, Jakobs S, Hell SW (2006) Nanoscale resolution in GFP-based microscopy. Nat Meth 9:721–723

    Article  Google Scholar 

Download references

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. Institute of Molecular Plant Sciences, University of Edinburgh, Mayfield Road, Edinburgh, EH9 3JR, UK

    Karen Bell & Karl Oparka

Authors
  1. Karen Bell
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Karl Oparka
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Karl Oparka.

Additional information

Handling Editor: Manfred Heinlein

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bell, K., Oparka, K. Imaging plasmodesmata. Protoplasma 248, 9–25 (2011). https://doi.org/10.1007/s00709-010-0233-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-010-0233-6

Keywords

Search

Navigation