Skip to main content

Plasmodesmata and Noncell Autonomous Signaling in Plants

  • Chapter
  • First Online:
The Plant Plasma Membrane

Part of the book series: Plant Cell Monographs ((CELLMONO,volume 19))

Abstract

Plasmodesmata are fundamental intercellular communication channels in plants that are essential for coordination of physiological and developmental signaling processes across cellular boundaries. The fact that creation of these membranous structures is considered one of the most crucial factors in the evolution of higher plants clearly states their unparalleled significance in plant systems. Plasmodesmata are also unique in their structure, in that they establish an endomembrane as well as a cytoplasmic continuum throughout the whole plant body by forming cytoplasmic strands that are lined with plasma membrane externally and endoplasmic reticulum internally. These structures, when assembled during cytokinesis by entrapment of endoplasmic reticular strands in the expanding cell plate, are called primary plasmodesmata. It is remarkable that plant cells have acquired an additional mechanism to produce secondary plasmodesmata by de novo biosynthesis postcytokinetically across existing cell walls, which in essence is necessary to maintain or increase symplasmic connectivity between expanding cells. This process is thought to occur through cell wall loosening and membrane fusion followed by deposition of new cell wall materials around the nascent protoplasmic strands. Perhaps, it is one of the most fascinating discoveries in plant biology that plasmodesmata are highly dynamic channels with the capacity to dilate and facilitate macromolecular trafficking despite the physical constraint imposed by the surrounding cell wall. It is also this activity through which plasmodesmata can act as supracellular checkpoint over intercellular transfer of signaling or information molecules. Exciting future discoveries in plasmodesmal biology are expected to be made by uncovering the molecular composition, anatomy, and transport mechanism of this fascinating yet incredibly recalcitrant biological structure.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • AGI (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815

    Article  Google Scholar 

  • Atkins D, Hull R, Wells B, Roberts K, Moore P, Beachy RN (1991) The tobacco mosaic virus-30 k movement protein in transgenic tobacco plants is localized to plasmodesmata. J Gen Virol 72:209–211

    Article  PubMed  CAS  Google Scholar 

  • Baluska F, Samaj J, Napier R, Volkmann D (1999) Maize calreticulin localizes preferentially to plasmodesmata in root apex. Plant J 19:481–488

    Article  PubMed  CAS  Google Scholar 

  • Bernhardt C, Zhao M, Gonzalez A, Lloyd A, Schiefelbein J (2005) The bHLH genes GL3 and EGL3 participate in an intercellular regulatory circuit that controls cell patterning in the Arabidopsis root epidermis. Development 132:291–298

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Blackman LM, Harper JDI, Overall RL (1999) Localization of a centrin-like protein to higher plant plasmodesmata. Eur J Cell Biol 78:297–304

    Article  PubMed  CAS  Google Scholar 

  • Chen MH, Sheng JS, Hind G, Handa AK, Citovsky V (2000) Interaction between the tobacco mosaic virus movement protein and host cell pectin methylesterases is required for viral cell-to-cell movement. EMBO J 19:913–920

    Article  PubMed  CAS  Google Scholar 

  • Citovsky V (1999) Tobacco mosaic virus: a pioneer of cell-to-cell movement. Phil Trans R Soc Lond B Biol Sci 354:637–643

    Article  CAS  Google Scholar 

  • Cook ME, Graham LE, Botha CEJ, Lavin CA (1997) Comparative ultrastructure of plasmodesmata of Chara and selected bryophytes: toward an elucidation of the evolutionary origin of plant plasmodesmata. Am J Bot 84:1169–1178

    Article  PubMed  CAS  Google Scholar 

  • Cui H, Levesque MP, Vernoux T, Jung JW, Paquette AJ, Gallagher KL, Wang JY, Blilou I, Scheres B, Benfey PN (2007) An evolutionarily conserved mechanism delimiting SHR movement defines a single layer of endodermis in plants. Science 316:421–425

    Article  PubMed  CAS  Google Scholar 

  • Deom CM, Lapidot M, Beachy RN (1992) Plant-virus movement proteins. Cell 69:221–224

    Article  PubMed  CAS  Google Scholar 

  • Derossi D, Calvet S, Trembleau A, Brunissen A, Chassaing G, Prochiantz A (1996) Cell internalization of the third helix of the Antennapedia homeodomain is receptor-independent. J Biol Chem 271:18188–18193

    Article  PubMed  CAS  Google Scholar 

  • Ding B (1997) Cell-to-cell transport of macromolecules through plasmodesmata: a novel signaling pathway in plants. Trends Cell Biol 7:5–9

    Article  PubMed  CAS  Google Scholar 

  • Ding B (1998) Intercellular protein trafficking through plasmodesmata. Plant Mol Biol 38:279–310

    Article  PubMed  CAS  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

    PubMed  CAS  Google Scholar 

  • Ding B, Kwon MO, Warnberg L (1996) Evidence that actin filaments are involved in controlling the permeability of plasmodesmata in tobacco mesophyll. Plant J 10:157–164

    Article  Google Scholar 

  • Dolan L (2006) Positional information and mobile transcriptional regulators determine cell pattern in the Arabidopsis root epidermis. J Exp Bot 57:51–54

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Franceschi VR, Ding B, Lucas WJ (1994) Mechanism of plasmodesmata formation in Characean algae in relation to evolution of intercellular communication in higher-plants. Planta 192:347–358

    Article  Google Scholar 

  • Fujiwara T, Giesmancookmeyer D, Ding B, Lommel SA, Lucas WJ (1993) Cell-to-cell trafficking of macromolecules through plasmodesmata potentiated by the red-clover necrotic mosaic-virus movement protein. Plant Cell 5:1783–1794

    PubMed  CAS  Google Scholar 

  • Gallagher KL, Paquette AJ, Nakajima K, Benfey PN (2004) Mechanisms regulating SHORT-ROOT intercellular movement. Curr Biol 14:1847–1851

    Article  PubMed  CAS  Google Scholar 

  • Grabski S, Defeijter AW, Schindler M (1993) Endoplasmic-reticulum forms a dynamic continuum for lipid diffusion between contiguous soybean root-cells. Plant Cell 5:25–38

    PubMed  CAS  Google Scholar 

  • Graham LE, Cook ME, Busse JS (2000) The origin of plants: body plan changes contributing to a major evolutionary radiation. Proc Natl Acad Sci USA 97:4535–4540

    Article  PubMed  CAS  Google Scholar 

  • Guimil S, Dunand C (2006) Patterning of Arabidopsis epidermal cells: epigenetic factors regulate the complex epidermal cell fate pathway. Trends Plant Sci 11:601–609

    Article  PubMed  CAS  Google Scholar 

  • Haywood V, Kragler F, Lucas WJ (2002) Plasmodesmata: pathways for protein and ribonucleoprotein signaling. Plant Cell 14:S303–S325

    PubMed  CAS  Google Scholar 

  • Heinlein M (2002) Plasmodesmata: dynamic regulation and role in macromolecular cell-to-cell signaling. Curr Opin Plant Biol 5:543–552

    Article  PubMed  CAS  Google Scholar 

  • Heinlein M, Epel BL (2004) Macromolecular transport and signaling through plasmodesmata. Int Rev Cytol 235:93–164

    Article  PubMed  CAS  Google Scholar 

  • Helariutta Y, Fukaki H, Wysocka-Diller J, Nakajima K, Jung J, Sena G, Hauser MT, Benfey PN (2000) The SHORT-ROOT gene controls radial patterning of the Arabidopsis root through radial signaling. Cell 101:555–567

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Ishida T, Kurata T, Okada K, Wada T (2008) A genetic regulatory network in the development of trichomes and root hairs. Annu Rev Plant Biol 59:365–386

    Article  PubMed  CAS  Google Scholar 

  • Jackson D (2001) The long and the short of it: signaling development through plasmodesmata. Plant Cell 13:2569–2572

    PubMed  CAS  Google Scholar 

  • Jackson D, Veit B, Hake S (1994) Expression of maize Knotted1 related homeobox genes in the shoot apical meristem predicts patterns of morphogenesis in the vegetative shoot. Development 120:405–413

    CAS  Google Scholar 

  • Karol KG, McCourt RM, Cimino MT, Delwiche CF (2001) The closest living relatives of land plants. Science 294:2351–2353

    Article  PubMed  CAS  Google Scholar 

  • Kim JY, Yuan ZA, Cilia M, Khalfan-Jagani Z, Jackson D (2002) Intercellular trafficking of a KNOTTED1 green fluorescent protein fusion in the leaf and shoot meristem of Arabidopsis. Proc Natl Acad Sci USA 99:4103–4108

    Article  PubMed  CAS  Google Scholar 

  • Kim JY, Yuan Z, Jackson D (2003) Developmental regulation and significance of KNOX protein trafficking in Arabidopsis. Development 130:4351–4362

    Article  PubMed  CAS  Google Scholar 

  • Kim JY, Rim Y, Wang J, Jackson D (2005) A novel cell-to-cell trafficking assay indicates that the KNOX homeodomain is necessary and sufficient for intercellular protein and mRNA trafficking. Genes Dev 19:788–793

    Article  PubMed  CAS  Google Scholar 

  • Kollmann R, Glockmann C (1991) Studies on graft unions. 3. On the mechanism of secondary formation of plasmodesmata at the graft interface. Protoplasma 165:71–85

    Article  Google Scholar 

  • Kurata T, Okada K, Wada T (2005a) Intercellular movement of transcription factors. Curr Opin Plant Biol 8:600–605

    Article  PubMed  CAS  Google Scholar 

  • Kurata T, Ishida T, Kawabata-Awai C, Noguchi M, Hattori S, Sano R, Nagasaka R, Tominaga R, Koshino-Kimura Y, Kato T, Sato S, Tabata S, Okada K, Wada T (2005b) Cell-to-cell movement of the CAPRICE protein in Arabidopsis root epidermal cell differentiation. Development 132:5387–5398

    Article  PubMed  CAS  Google Scholar 

  • Kwak SH, Schiefelbein J (2006) The role of the SCRAMBLED receptor-like kinase in patterning the Arabidopsis root epidermis. Dev Biol 302:118–131

    Article  PubMed  Google Scholar 

  • Lee JY, Yoo BC, Lucas WJ (2000) Parallels between nuclear-pore and plasmodesmal trafficking of information molecules. Planta 210:177–187

    Article  PubMed  CAS  Google Scholar 

  • Lee JY, Yoo BC, Rojas MR, Gomez-Ospina N, Staehelin LA, Lucas WJ (2003) Selective trafficking of non-cell-autonomous proteins mediated by NtNCAPP1. Science 299:392–396

    Article  PubMed  CAS  Google Scholar 

  • Lee JY, Taoka K, Yoo BC, Ben-Nissan G, Kim DJ, Lucas WJ (2005) Plasmodesmal-associated protein kinase in tobacco and Arabidopsis recognizes a subset of non-cell-autonomous proteins. Plant Cell 17:2817–2831

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Lucas WJ, Lee JY (2004) Plasmodesmata as a supracellular control network in plants. Nat Rev Mol Cell Biol 5:712–726

    Article  PubMed  CAS  Google Scholar 

  • Lucas WJ, Wolf S (1993) Plasmodesmata: the intercellular organelles of green plants. Trends Cell Biol 3:308–315

    Article  PubMed  CAS  Google Scholar 

  • Lucas WJ, Ding B, Vanderschoot C (1993) Plasmodesmata and the supracellular nature of plants. New Phytol 125:435–476

    Article  Google Scholar 

  • Lucas WJ, Bouchepillon S, Jackson DP, Nguyen L, Baker L, Ding B, Hake S (1995) Selective trafficking of Knotted1 homeodomain protein and its messenger-RNA through plasmodesmata. Science 270:1980–1983

    Article  PubMed  CAS  Google Scholar 

  • Maizel A, Tassetto M, Filhol O, Cochet C, Prochiantz A, Joliot A (2002) Engrailed homeoprotein secretion is a regulated process. Development 129:3545–3553

    PubMed  CAS  Google Scholar 

  • Martens HJ, Roberts AG, Oparka KJ, Schulz A (2006) Quantification of plasmodesmatal endoplasmic reticulum coupling between sieve elements and companion cells using fluorescence redistribution after photobleaching. Plant Physiol 142:471–480

    Article  PubMed  CAS  Google Scholar 

  • Maule AJ (2008) Plasmodesmata: structure, function and biogenesis. Curr Opin Plant Biol 11(6):680–686

    Article  PubMed  CAS  Google Scholar 

  • Meiners S, Xu AD, Schindler M (1991) Gap junction protein homolog from Arabidopsis thaliana – evidence for connexins in plants. Proc Natl Acad Sci USA 88:4119–4122

    Article  PubMed  CAS  Google Scholar 

  • Murillo I, Cavallarin L, SanSegundo B (1997) The maize pathogenesis-related PRms protein localizes to plasmodesmata in maize radicles. Plant Cell 9:145–156

    PubMed  CAS  Google Scholar 

  • Nakajima K, Sena G, Nawy T, Benfey PN (2001) Intercellular movement of the putative transcription factor SHR in root patterning. Nature 413:307–311

    Article  PubMed  CAS  Google Scholar 

  • Noueiry AO, Lucas WJ, Gilbertson RL (1994) Two proteins of a plant DNA virus coordinate nuclear and plasmodesmal transport. Cell 76:925–932

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Overall RL, Wolfe J, Gunning BES (1982) Inter-cellular communication in Azolla roots. 1. Ultrastructure of plasmodesmata. Protoplasma 111:134–150

    Article  Google Scholar 

  • Perbal MC, Haughn G, Saedler H, SchwarzSommer Z (1996) Non-cell-autonomous function of the Antirrhinum floral homeotic proteins DEFICIENS and GLOBOSA is exerted by their polar cell-to-cell trafficking. Development 122:3433–3441

    PubMed  CAS  Google Scholar 

  • Pouwels J, Van der Krogt GNM, Van Lent J, Bisseling T, Wellink J (2002) The cytoskeleton and the secretory pathway are not involved in targeting the cowpea mosaic virus movement protein to the cell periphery. Virol 297:48–56

    Article  CAS  Google Scholar 

  • Pouwels J, Kornet N, van Bers N, Guighelaar T, van Lent J, Bisseling T, Wellink J (2003) Identification of distinct steps during tubule formation by the movement protein of Cowpea mosaic virus. J Gen Virol 84:3485–3494

    Article  PubMed  CAS  Google Scholar 

  • Pouwels J, van der Velden T, Willemse J, Borst JW, van Lent J, Bisseling T, Wellink J (2004) Studies on the origin and structure of tubules made by the movement protein of Cowpea mosaic virus. J Gen Virol 85:3787–3796

    Article  PubMed  CAS  Google Scholar 

  • Prochiantz A, Joliot A (2003) Can transcription factors function as cell–cell signalling molecules? Nat Rev Mol Cell Biol 4:814–819

    Article  PubMed  CAS  Google Scholar 

  • Radford JE, White RG (1998) Localization of a myosin-like protein to plasmodesmata. Plant J 14:743–750

    Article  PubMed  CAS  Google Scholar 

  • Robards AW (1968) Desmotubule – a plasmodesmatal substructure. Nature 218:784

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Rustom A, Saffrich R, Markovic I, Walther P, Gerdes HH (2004) Nanotubular highways for intercellular organelle transport. Science 303:1007–1010

    Article  PubMed  CAS  Google Scholar 

  • Schellmann S, Schnittger A, Kirik V, Wada T, Okada K, Beermann A, Thumfahrt J, Jurgens G, Hulskamp M (2002) TRIPTYCHON and CAPRICE mediate lateral inhibition during trichome and root hair patterning in Arabidopsis. EMBO J 21:5036–5046

    Article  PubMed  CAS  Google Scholar 

  • Schmitz K, Kuhn R (1982) Fine-structure, distribution and frequency of plasmodesmata and pits in the cortex of Laminaria-Hyperborea and Laminaria-Saccharina. Planta 154:385–392

    Article  Google Scholar 

  • Seagull RW (1983) Differences in the frequency and disposition of plasmodesmata resulting from root cell elongation. Planta 159:497–504

    Article  Google Scholar 

  • Sessions A, Yanofsky MF, Weigel D (2000) Cell–cell signaling and movement by the floral transcription factors LEAFY and APETALA1. Science 289:779–781

    Article  PubMed  CAS  Google Scholar 

  • Taoka K, Ham BK, Xoconostle-Cazares B, Rojas MR, Lucas WJ (2007) Reciprocal phosphorylation and glycosylation recognition motifs control NCAPP1 interaction with pumpkin phloem proteins and their cell-to-cell movement. Plant Cell 19:1866–1884

    Article  PubMed  CAS  Google Scholar 

  • Tassetto M, Maizel A, Osorio J, Joliot A (2005) Plant and animal homeodomains use convergent mechanisms for intercellular transfer. EMBO Rep 6:885–890

    Article  PubMed  CAS  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 

  • Vanlent J, Storms M, Vandermeer F, Wellink J, Goldbach R (1991) Tubular structures involved in movement of Cowpea mosaic-virus are also formed in infected Cowpea protoplasts. J Gen Virol 72:2615–2623

    Article  Google Scholar 

  • Volkmann D, Mori T, Tirlapur UK, Konig K, Fujiwara T, Kendrick-Jones J, Baluska F (2003) Unconventional myosins of the plant-specific class VIII: endocytosis, cytokinesis, plasmodesmata/pit-fields, and cell-to-cell coupling. Cell Biol Int 27:289–291

    Article  PubMed  CAS  Google Scholar 

  • Wada T, Kurata T, Tominaga R, Koshino-Kimura Y, Tachibana T, Goto K, Marks MD, Shimura Y, Okada K (2002) Role of a positive regulator of root hair development, CAPRICE, in Arabidopsis root epidermal cell differentiation. Development 129:5409–5419

    Article  PubMed  CAS  Google Scholar 

  • Waigmann E, Zambryski P (1995) Tobacco mosaic virus movement protein-mediated protein transport between trichome cells. Plant Cell 7:2069–2079

    PubMed  CAS  Google Scholar 

  • Waigmann E, Lucas WJ, Citovsky V, Zambryski P (1994) Direct functional assay for tobacco mosaic virus cell-to-cell movement protein and identification of a domain involved in increasing plasmodesmal permeability. Proc Natl Acad Sci USA 91:1433–1437

    Article  PubMed  CAS  Google Scholar 

  • Waigmann E, Chen MH, Bachmaier R, Ghoshroy S, Citovsky V (2000) Regulation of plasmodesmal transport by phosphorylation of tobacco mosaic virus cell-to-cell movement protein. EMBO J 19:4875–4884

    Article  PubMed  CAS  Google Scholar 

  • Wellink J, Vanlent JWM, Verver J, Sijen T, Goldbach RW, Vankammen AB (1993) The cowpea mosaic-virus mRNA-encoded 48-kilodalton protein is responsible for induction of tubular structures in protoplasts. J Virol 67:3660–3664

    PubMed  CAS  Google Scholar 

  • White RG, Badelt K, Overall RL, Vesk M (1994) Actin associated with plasmodesmata. Protoplasma 180:169–184

    Article  CAS  Google Scholar 

  • Wolf S, Lucas WJ (1994) Virus movement proteins and other molecular probes of plasmodesmal function. Plant Cell Environ 17:573–585

    Article  CAS  Google Scholar 

  • Wolf S, Deom CM, Beachy RN, Lucas WJ (1989) Movement protein of tobacco mosaic-virus modifies plasmodesmatal size exclusion limit. Science 246:377–379

    Article  PubMed  CAS  Google Scholar 

  • Wolf S, Deom CM, Beachy R, Lucas WJ (1991) Plasmodesmatal function is probed using transgenic tobacco plants that express a virus movement protein. Plant Cell 3:593–604

    PubMed  CAS  Google Scholar 

  • Zambryski P, Crawford K (2000) Plasmodesmata: gatekeepers for cell-to-cell transport of developmental signals in plants. Ann Rev Cell Dev Biol 16:393–421

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We apologize to all our colleagues whose important work could not be cited in this review, or be cited indirectly through other references, due to space limitations. Special thanks go to Shannon Modla for producing micrographs of plasmodesmata. This work was supported by the National Science Foundation (MCB 0445626 to J.-Y. L.) and National Institutes of Health COBRE (P20 RR15588 to J.-Y. L.).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jung-Youn Lee .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2011 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Lee, JY., Cho, S.K., Sager, R. (2011). Plasmodesmata and Noncell Autonomous Signaling in Plants. In: Murphy, A., Schulz, B., Peer, W. (eds) The Plant Plasma Membrane. Plant Cell Monographs, vol 19. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-13431-9_4

Download citation

Publish with us

Policies and ethics