Skip to main content

Plasmodesmata: A History of Conceptual Surprises

  • Chapter
  • First Online:
Concepts in Cell Biology - History and Evolution

Part of the book series: Plant Cell Monographs ((CELLMONO,volume 23))

Abstract and Prologue

Since the initial postulate of plasmodesmata (PDs) and their function (Tangl 1879), three books have captured the progress in plasmodesmal (PD) research. The first (Gunning and Robards 1976) surveyed PD research extending over approximately 100 years. At the time of its publication, electron microscopy had confirmed the existence of previously putative intercellular cytoplasmic channels without a clear notion of the ultrastructure. PDs were no longer regarded as redundant evolutionary appendices, but solid evidence of their function was lacking. Over the years the hypothesis that higher plants were subdivided into symplasmic domains having some physiological role had been strengthened, but the significance of these domains remained uncertain. Exchange of low molecular weight solutes through PDs was a likely (but unproven) option, whereas passage of macromolecules was beyond the horizon of possibility at the time (Carr 1976).

Over two decades later, two other books (van Bel and van Kesteren 1999; Oparka 2005) illustrated the booming interest and progress in the preceding years. Doubts on issues put forward in the first book had been eliminated. Symplasmic domains were demonstrated to be of paramount importance for transport physiology (root transport, phloem transport) and developmental biology. The PD substructure had been assessed better and a number of components associated with PDs were identified. PDs turned out to be subject to strictly regulated constriction and dilation. The functional PD molecular exclusion limits were found to vary between the initially measured 1 kDa up to about 60 kDa. The latter values gave rise to the concept of macromolecular trafficking through PDs. As a result, new concepts on PD significance for short-distance and long-distance signaling emerged, including the key role of PDs in intercellular and long-distance transport of plant viruses.

This chapter is subdivided in line with the emergence of techniques that enabled new waves of experimental approaches in PD research. The discoveries that collectively led to the current concepts on PD structure and function are presented in chronological order. The emphasis is on the development of PD research rather than on the present state of the art. Therefore, recent research is discussed in less detail than work from the period before 2000.

Zur richtigen Deutung der dargestellten Befunde lässt sich auf Grund der gemachten Erfahrungen nur eine einzige Möglichkeit finden und diese entspricht der Auffassung, dass die Protoplasmakörper der inneren Zellen des Endosperms sich mit dünnen, in den feinen Verbindungskanälen verlaufenden Strängen unter einander in Verbindung setzen und so zu einer Einheit höherer Ordnung zusammentreten.

The statement of Eduard Tangl (1879) about the intimate interdependence of plant cells and the symplasm concept.

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 189.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 249.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 249.99
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

  • Amari K, Boutant E, Hofmann C, Schmitt-Keichinger C, Fernandez-Calvino L, Didier P, Lerich A, Mutterer J, Thomas CL, Heinlein M, Mély Y, Maule AJ, Ritzenthaler C (2010) A family of plasmodesmal proteins with receptor-like properties for plant viral movement proteins. PLoS Pathog 6:e1001119

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Amor Y, Haigler CH, Johnson S, Wainscott M, Delmer DP (1995) A membrane-associated form of sucrose synthase and its potential role in synthesis of cellulose and callose in plants. Proc Natl Acad Sci U S A 92:9353–9357

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • An Q-L, Hückelhoven R, Kogel K-H, van Bel AJE (2006a) Multivesicular bodies participate in a cell-wall associated defence response in barley leaves attacked by the pathogenic powdery mildew fungus. Cell Microbiol 8:1009–1019

    Article  CAS  PubMed  Google Scholar 

  • An Q-L, Ehlers K, Kogel K-H, van Bel AJE, Hückelhoven R (2006b) Multivesicular compartments proliferate in susceptible and resistant MLA12-barley plants in response to infection by the biotrophic powdery mildew fungus. New Phytol 172:563–576

    Article  CAS  PubMed  Google Scholar 

  • Aoki K, Suzui N, Fujimaki S, Dohmae N, Yonekura-Sakakibara K, Fujiwara T, Hayashi H, Yamaya T, Sakakibara H (2005) Destination-selective long-distance movement of phloem proteins. Plant Cell 17:1801–1814

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arisz WH (1958) Influence on inhibitors on the uptake and transport of chloride ions in leaves of Vallisneria spiralis. Acta Bot Neerl 7:1–32

    Article  CAS  Google Scholar 

  • Arisz WH (1960) Symplasmatischer Salztransport in Vallisneria-Blättern. Protoplasma 52:309–343

    Article  Google Scholar 

  • Arisz WH (1969) Intercellular polar transport and the role of plasmodesmata in coleoptiles and Vallisneria leaves. Acta Bot Neerl 18:14–38

    Article  CAS  Google Scholar 

  • Badelt K, White RG, Overall RL, Vesk M (1994) Ultrastructural specializations of the cell wall sleeve around plasmodesmata. Am J Bot 81:1422–1427

    Article  Google Scholar 

  • Balachandran S, Xiang Y, Schobert C, Thompson GA, Lucas WJ (1997) Phloem sap proteins from Cucurbita maxima and Ricinus communis have the capacity to travel cell to cell through plasmodesmata. Proc Natl Acad Sci U S A 94:14150–14155

    Article  CAS  PubMed  PubMed Central  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  CAS  PubMed  Google Scholar 

  • Baluska F, Cvrckova F, Kendrick-Jones J, Volkmann D (2001) Sink plasmodesmata as gateways for phloem unloading. Myosin VIII and calreticulin as molecular determinants of sink strength? Plant Physiol 126:39–46

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baron-Epel O, Hernandez D, Jiang L-W, Meiners S, Schindler M (1988) Dynamic continuity of cytoplasmic and membrane compartments between plant cells. J Cell Biol 106:715–721

    Article  CAS  PubMed  Google Scholar 

  • Barratt DH, Kolling K, Graf A, Pike M, Calder G, Findlay K, Zeeman SC, Smith AM (2011) Callose synthase GSL7 is necessary for normal phloem transport and inflorescence growth in Arabidopsis. Plant Physiol 155:328–341

    Article  CAS  PubMed  Google Scholar 

  • Bauer R (1930) Einführung in die experimentelle Vererbungslehre. Borntraeger, Berlin

    Google Scholar 

  • Beebe DU, Turgeon R (1992) Localization of galactinol, raffinose, and stachyose synthesis in Cucurbita pepo leaves. Planta 188:354–361

    Article  CAS  PubMed  Google Scholar 

  • Bell K, Oparka K (2011) Imaging plasmodesmata. Protoplasma 248:9–25

    Article  PubMed  Google Scholar 

  • Benitez-Alfonso Y, Cilia M, San Roman A, Thomas C, Maule A, Hearn S, Jackson D (2009) Control of Arabidopsis meristem development by thioredoxin-dependent regulation of intercellular transport. Proc Natl Acad Sci U S A 106:3615–3620

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Benitez-Alfonso Y, Faulkner C, Ritzenthaler C, Maule AJ (2010) Plasmodesmata gateways to local and systemic virus infection. Mol Plant-Microbe Interact 23:1403–1412

    Article  CAS  PubMed  Google Scholar 

  • Benitez-Alfonso Y, Faulkner C, Pendle A, Miyashima S, Helariutta Y, Maule A (2013) Symplastic intercellular connectivity regulates lateral root patterning. Dev Cell 26:136–147

    Article  CAS  PubMed  Google Scholar 

  • Besnard F, Refahi Y, Morin V, Marteaux B, Brunoud G, Chambrier P, Rozier F, Mirabet V, Legrand J, Lainé S, Thevenon E, Farcot E, Cellier C, Das P, Bishopp A, Dumas R, Parcy F, Helariutta Y, Boudaoud A, Godin C, Traas J, Guédon Y, Vernaix T (2014) Cytokinin signalling inhibitory fields provide robustness to phyllotaxis. Nature 505:417–421

    Article  CAS  PubMed  Google Scholar 

  • Bilska A, Sowinski P (2010) Closure of plasmodesmata in maize (Zea mays) at low temperature: a new mechanism for inhibition of photosynthesis. Ann Bot 106:675–686

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blackman LM, Overall RL (1998) Immunolocalisation of the cytoskeleton to plasmodesmata of Chara corallina. Plant J 15:733–741

    Article  Google Scholar 

  • Blackman LM, Boevink P, Santa Cruz S, Palukaitis P, Oparka KJ (1998) The movement protein of cucumber mosaic virus traffics into sieve elements in minor veins of Nicotiana clevelandii. Plant Cell 10:525–537

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Böckenhoff A, Prior DAM, Grundler FMW, Oparka KJ (1996) Induction of phloem unloading in Arabidopsis thaliana roots by the parasitic nematode Heterodera schachtii. Plant Physiol 112:1421–1427

    Article  PubMed  PubMed Central  Google Scholar 

  • Bostwick DE, Dannenhoffer JM, Skaggs MI, Lister DM, Larkins BA, Thompson GA (1992) Pumpkin phloem lectin genes are specifically expressed in companion cells. Plant Cell 4:1539–1548

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Botha CEJ, Evert RF, Cross RHM, Marshall DJ (1982) The suberin lamella, an impermeable barrier in the bundle sheath cells of Themeda triandra Forsk. Protoplasma 112:1–8

    Article  Google Scholar 

  • Botha CEJ, Hartley BJ, Cross RHM (1993) The ultrastructure and computer-enhanced digital image analysis of plasmodesmata at the Kranz mesophyll-bundle sheath interface of Themeda triandra var. imberbis (Retz) A. Camus in conventionally-fixed leaf blades. Ann Bot 27:255–261

    Article  Google Scholar 

  • Botha CEJ, Cross RHM, Liu L (2005) Comparative structures of specialised monocotyledonous leaf blade plasmodesmata. In: Oparka KJ (ed) Plasmodesmata. Annual Plant Reviews 18. Blackwell, Oxford, pp 73–89

    Google Scholar 

  • Bowes BG (2001) Farbatlas Pflanzenanatomie: Formen, Gewebe, Strukturen. Blackwell Wissenschafts-Verlag, Berlin

    Google Scholar 

  • Brault V, Hersbach E, Rodriquez-Medina C (2011) Luteoviruses. doi: https://doi.org/10.1002/9780470015902.a0000751.p

  • Brinckmann E, Lüttge U (1974) Lichtabhängige Membranpotentialschwankungen und deren interzelluläre Weiterleitung bei panaschierten Photosynthesemutanten von Oenothera. Planta 119:47–57

    Article  CAS  PubMed  Google Scholar 

  • Brunkard JO, Zambryski PC (2017) Plasmodesmata enable multicellularity: new insights into their evolution, biogenesis, and functions in development and immunity. Curr Opin Cell Biol 35:76–83

    Article  Google Scholar 

  • Brunkard JO, Runkel AM, Zambryski PC (2013) Plasmodesmata dynamics are coordinated by intracellular signalling pathways. Curr Opin Plant Biol 16:614–620

    Article  CAS  PubMed  Google Scholar 

  • Burgoyne T, Patel S, Eden ER (2015) Calcium signalling at the ER membrane contact sites. Biochim Biophys Acta 1853:2012–2017

    Article  CAS  PubMed  Google Scholar 

  • Buvat R (1957) L’infrastructure des plasmodesmes et la continuité des cytoplasmes. C R Acad Sci Paris 245:198–201

    Google Scholar 

  • Cairns BG, Pasternak M, Wachter A, Corbett CS, Meyer A (2006) Maturation of Arabidopsis seeds is dependent on glutathione biosynthesis within the embryo. Plant Physiol 141:446–455

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Calderwood A, Kopriva S, Morris TJ (2016) Transcript abundance explains mRNA mobility data in Arabidopsis thaliana. Plant Cell 28:610–615

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carr DJ (1976) Plasmodesmata in growth and development. In: Gunning BES, Robards AW (eds) Intercellular communication in plants: studies on plasmodesmata. Springer, Berlin, pp 243–289

    Chapter  Google Scholar 

  • Chen X, Yao Q, Gao X, Jiang C, Harberd NP, Fu X (2016) Shoot-to-root mobile transcription factor HY5 coordinates plant carbon and nitrogen acquisition. Curr Biol 26:640–646

    Article  CAS  PubMed  Google Scholar 

  • Choi W-G, Hilleary R, Swanson SJ, Kim S-H, Gilroy S (2016) Rapid, long-distance electrical and calcium signalling in plants. Annu Rev Plant Biol 67:287–307

    Article  CAS  PubMed  Google Scholar 

  • Citovsky V, Wong ML, Shaw AL, Prasad BVV, Zambryski P (1992) Visualization and characterization of tobacco mosaic virus movement protein binding to single-stranded nucleic acids. Plant Cell 4:397–411

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cleland R, Fujiwara T, Lucas WJ (1994) Plasmodesmal-mediated cell-to-cell transport in wheat roots is modulated by anaerobic stress. Protoplasma 178:81–85

    Article  CAS  PubMed  Google Scholar 

  • Correns C (1909) Vererbungsversuche mit blass(gelb)grünen und buntblätterigen Sippen bei Mirabilis jalapa, Urtica pilufera, und Lunaria annua. Z Indukt Abstamm Vererbungsl 1:291–329

    Google Scholar 

  • Crawford KM, Zambryski P (2001) Non-targeted and targeted protein movement through plasmodesmata in leaves in different developmental and physiological states. Plant Physiol 125:1802–1812

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cronshaw J, Sabnis DD (1990) Phloem proteins. In: Behnke H-D, Sjolund RD (eds) Sieve elements. Comparative structure, induction and development. Springer, Berlin, pp 257–283

    Google Scholar 

  • Cui W, Lee J-Y (2016) Arabidopsis callose synthases CalS1/8 regulate plasmodesmal permeability during stress. Nat Plants 2:16034

    Article  CAS  PubMed  Google Scholar 

  • Currier HB, Strugger S (1956) Aniline blue and fluorescence microscopy of callose in bulb scales of Allium cepa L. Protoplasma 45:552–559

    Article  Google Scholar 

  • De Storme N, Geelen N (2014) Callose homeostasis at plasmodesmata: molecular regulators and developmental relevance. Front Plant Sci 5:138

    Article  PubMed  PubMed Central  Google Scholar 

  • Deeks MJ, Calcutt JR, Ingle EKS, Hawkins TJ, Chapman S, Richardson AC, Mentlak DA, Dixon MR, Cartwright F, Smertenko AP, Oparka K, Hussey PJ (2012) A superfamily of actin-binding proteins at the actin-membrane nexus of higher plants. Curr Biol 22:1595–1600

    Article  CAS  PubMed  Google Scholar 

  • Den Hollander PW, Kieper SN, Borst JW, van Lent JWM (2016) The role of plasmodesma-located proteins in tubule-guided transport is limited to the plasmodesmata. Arch Virol 161:2431–2440

    Article  CAS  Google Scholar 

  • Deom CM, Oliver MJ, Beachy RN (1987) The 30-kilodalton gene product of tobacco mosaic virus potentiates virus movement. Science 237:389–394

    Article  CAS  PubMed  Google Scholar 

  • Derrick PM, Barker H, Oparka KJ (1990) Effect of virus infection on symplastic transport of fluorescent tracers in Nicotiana clevelandii leaf epidermis. Planta 181:555–559

    Article  CAS  PubMed  Google Scholar 

  • Derrick PM, Barker H, Oparka KJ (1992) Increase in plasmodesmatal permeability during cell-to-cell spread of tobacco rattle virus from individually inoculated cells. Plant Cell 4:1405–1412

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  Google Scholar 

  • Ding B, Haudenshield JS, Willmitzer L, Lucas WJ (1993) Correlation between arrested secondary plasmodesmal development and onset of accelerated leaf senescence in yeast acid invertase transgenic tobacco plants. Plant J 4:179–189

    Article  CAS  PubMed  Google Scholar 

  • Ding B, Kwon M-O, 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 

  • Dominguez R, Holmes KC (2011) Actin structure and function. Annu Rev Biophys 40:169–186

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Duckett CM, Oparka KJ, Prior DAM, Dolan L, Roberts K (1994) Dye coupling in the root epidermis is progressively reduced during development. Development 120:3247–3255

    CAS  Google Scholar 

  • Ehlers K, Kollmann R (1996) Formation of branched plasmodesmata in regenerating Solanum nigrum protoplasts. Planta 199:126–138

    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 

  • Ehlers K, van Bel AJE (2010) Dynamics of plasmodesmal connectivity in successive interfaces of the cambial zone. Planta 231:371–385

    Article  CAS  PubMed  Google Scholar 

  • Ehlers K, Schulz M, Kollmann R (1996) Subcellular localization of ubiquitin in plant protoplasts and the function of ubiquitin in selective degradation of outer-wall plasmodesmata in regenerating protoplasts. Planta 199:139–151

    CAS  Google Scholar 

  • Ehlers K, Wang Y, Günther S, van Bel AJE (2004) Programming of plasmodesmal deployment and development. In: Scientific program and abstract. 5th International conference on plasmodesmata, Pacific Grove, p 26

    Google Scholar 

  • Epel BL, Kuckuck B, Kotlizky G, Shurtz S, Erlanger M, Yahalom A (1995) Isolation and characterization of plasmodesmata. Methods Cell Biol 50:237–253

    Article  CAS  PubMed  Google Scholar 

  • Erwee MG, Goodwin PB (1983) Characterization of the Egeria densa Planch. leaf symplast. Inhibition of cellular movement of fluorescent probes by group II ions. Planta 158:320–328

    Article  CAS  PubMed  Google Scholar 

  • Erwee MG, Goodwin PB (1984) Characterization of the Egeria densa Planch. leaf symplast response to plasmolysis, deplasmolysis and to aromatic amino acids. Protoplasma 122:162–168

    Article  CAS  Google Scholar 

  • Erwee MG, Goodwin PB, van Bel AJE (1985) Cell-cell communication in the leaves of Commelina cyanea and other plants. Plant Cell Environ 8:173–178

    Google Scholar 

  • Esau K (1963) Ultrastructure of differentiated cells in higher plants. Am J Bot 50:495–506

    Article  Google Scholar 

  • Esau K (1977) Anatomy of seed plants. Wiley, New York

    Google Scholar 

  • Esau K, Cronshaw J, Hoefert JJ (1967) Relation of the beet yellows virus to the phloem and to movement in the sieve tube. J Cell Biol 33:71–87

    Article  Google Scholar 

  • Evert RF (1990) Dicotyledons. In: Behnke H-D, Sjolund RD (eds) Sieve elements. Comparative structure, induction and development. Springer, Berlin, pp 103–137

    Google Scholar 

  • Faulkner C, Maule A (2011) Opportunities and successes in the search for plasmodesmal proteins. Protoplasma 248:27–38

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Faulkner CR, Blackman LM, Collings DA, Cordwell SJ, Overall RL (2009) Anti-tropomyosin antibodies co-localize with actin microfilaments and label plasmodesmata. Eur J Cell Biol 88:357–369

    Article  CAS  PubMed  Google Scholar 

  • Faulkner C, Petutschnig E, Benitez-Alfonso Y, Beck M, Robatzek S, Lipka V, Maule AJ (2013) Lym 2-dependent chitin perception limits molecular flux via plasmodesmata. Proc Natl Acad Sci 110:9166–9170

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fernandez-Calvino L, Faulkner C, Walshaw J, Saalbach G, Bayer E, Benitez-Alfonso Y, Maule A (2011) Arabidopsis plasmodesmal proteome. PLoS One 6:e18880

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fisher DG (1986) Ultrastructure, plasmodesmatal frequency, and solute concentration in green areas of variegated Coleus blumei Benth. leaves. Planta 169:141–152

    Article  CAS  PubMed  Google Scholar 

  • Fisher DB, Oparka KJ (1996) Post-phloem transport: principles and problems. J Exp Bot 47:1141–1154

    Article  CAS  PubMed  Google Scholar 

  • Fisher DB, Wang N (1995) Sucrose concentration gradients along the post-phloem transport pathway in the maternal tissues of developing grains. Plant Physiol 109:587–592

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fisher DB, Wu Y, MSB K (1992) Turnover of soluble proteins in the wheat sieve tube. Plant Physiol 100:1433–1441

    Article  CAS  PubMed  PubMed Central  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  PubMed Central  Google Scholar 

  • Foster TM, Lough TJ, Emerson SJ, Lee RH, Bowman JL, Foster RLS, Lucas WJ (2002) A surveillance system regulates selective entry of RNA into the shoot apex. Plant Cell 14:1497–1508

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fujiwara T, Giesman-Cookmeyer 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Furch ACU, Hafke JB, Schulz A, van Bel AJE (2007) Ca2+-mediated remote control of reversible sieve tube oocclusion in Vicia faba. J Exp Bot 58:2827–2838

    Article  CAS  PubMed  Google Scholar 

  • Furch ACU, van Bel AJE, Fricker MD, Felle HH, Fuchs M, Hafke JB (2009) Sieve element Ca2+ channels as relay stations between remote stimuli and sieve tube occlusion in Vicia faba. Plant Cell 21:2118–2132

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Furch ACU, Zimmermann MR, Will T, Hafke JB, van Bel AJE (2010) Remote-controlled stop of mass flow by biphasic occlusion in Cucurbita maxima. J Exp Bot 61:3697–3708

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gamalei YV (1989) Structure and function of leaf minor veins in trees and herbs. A taxonomic review. Trees 3:96–110

    Article  Google Scholar 

  • Gamalei YV, van Bel AJE, Pakhomova MV, Sjutkina AV (1994) Effects of temperature on the conformation of the endoplasmic reticulum and on starch accumulation in leaves with the symplasmic minor-vein configuration. Planta 194:443–453

    Article  CAS  Google Scholar 

  • Gaudioso-Pedraza R, Benitez-Alfonso Y (2014) A phylogenetic approach to study the origin and localization of plasmodesmata-localized glucosyl hydrolases family 17. Front Plant Sci 5:212

    Article  PubMed  PubMed Central  Google Scholar 

  • Geiger DR, Giaquinta RT, Sovonick SA, Fellows RJ (1973) Sugar distribution in sugar beet leaves in relation to phloem loading and translocation. Plant Physiol 52:585–589

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ghoshroy S, Lartey R, Sheng J, Citovsky V (1997) Transport of proteins and nucleic acids through plasmodesmata. Annu Rev Plant Physiol Plant Mol Biol 48:27–50

    Article  CAS  PubMed  Google Scholar 

  • Giaquinta RT (1983) Phloem loading of sucrose. Annu Rev Plant Physiol 34:347–387

    Article  CAS  Google Scholar 

  • Gicquaud C, Wong P (1994) Mechanism of interaction between actin and membrane lipids: a pressure-tuning infrared spectroscopy study. Biochem J 303:769–774

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gilroy S, Suzuki N, Miller G, Choi W-G, Toyota M, Devireddy AR, Mittler R (2014) A tidal wave of signals: calcium and ROS at the forefront of rapid systemic signalling. Trends Plant Sci 19:623–630

    Article  CAS  PubMed  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 

  • Goebel K (1897) Über Jugendformen von Pflanzen und deren künstliche Wiederhervorrufung. Sitzungsber der Math-Nat Klasse der königl bayer Akad Wiss zu München 26, pp 447–497

    Google Scholar 

  • Golecki B, Schulz A, Carstens-Behrens U, Kollmann R (1998) Evidence for graft transmission of structural phloem proteins or their precursors in heterografts of Cucurbitaceae. Planta 206:630–640

    Article  CAS  Google Scholar 

  • Goodwin PB (1976) Physiological and electrophysiological evidence for intercellular communication in plants symplasts. In: Gunning BES, Robards AW (eds) Intercellular communication plants: studies on plasmodesmata. Springer, Berlin, pp 121–129

    Chapter  Google Scholar 

  • Goodwin PB (1983) Molecular size limit for movement in the symplast of Elodea leaf. Planta 157:124–130

    Article  CAS  PubMed  Google Scholar 

  • Goodwin PB, Shepherd V, Erwee MG (1990) Compartmentation of fluorescent tracers injected into the epidermal cells of Egeria densa plants. Planta 181:129–136

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grison MS, Brocard L, Fouillen L, Nicolas W, Wewer V, Dörmann P, Nacir H, Benitez-Alfonso Y, Claverol S, Germain V, Boutté Y, Mongrand S, Bayer EM (2015) Specific membrane lipid composition is important for plasmodesmata function in Arabidopsis. Plant Cell 27:1228–1250

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gunning BES (1978) Age-related and origin-related control of the numbers of plasmodesmata of developing Azolla roots. Planta 143:181–190

    Article  CAS  PubMed  Google Scholar 

  • Gunning BES, Overall RL (1983) Plasmodesmata and cell-to-cell transport in plants. Bioscience 33:260–265

    Article  CAS  Google Scholar 

  • Gunning BES, Robards AW (1976) Intercellular communication plants: studies on plasmodesmata. Springer, Berlin

    Book  Google Scholar 

  • Gupton SL, Anderson KL, Kole TP, Fisher RS, Ponti A, Hitchcock-Degregori SE, Damaser G, Fowler VM, Wirtz D, Hanein D, Waterman-Storer CM (2005) Cell migration without a lamellopodium: translation of actin dynamics into cell movement mediated by tropomyosin. J Cell Biol 168:619–631

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guseman JM, Lee JS, Bogenschutz NL, Peterson KM, Virata RE, Xie B, Kanaoka MM, Hong Z, Torrii K (2010) Dysregulation of cell-to-cell connectivity and stomatal patterning by loss-of-function mutation in Arabidopsis CHORUS (GLUCOSE-SYNTHASE LIKE 8). Development 137:1731–1741

    Article  CAS  PubMed  Google Scholar 

  • Hafke JB, van Amerongen J-K, Kelling F, Furch ACU, Gaupels F, van Bel AJE (2005) Thermodynamic battle for photosynthate acquisition between sieve tubes and adjoining parenchyma in transport phloem. Plant Physiol 138:1527–1537

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hafke JB, Furch ACU, Fricker MD, van Bel AJE (2009) Forisome dispersion in Vicia faba is triggered by Ca2+ hotspots created by the concerted action of diverse Ca2+ channels in sieve elements. Plant Signal Behav 4:968–972

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ham B-K, Lucas WJ (2017) Phloem-mobile RNAs as systemic signalling agents. Annu Rev Plant Biol 68:173–195. https://doi.org/10.1146/annurev-arplant-042916-041139

    Article  CAS  PubMed  Google Scholar 

  • Haraguchi T, Tominaga M, Matsumoto R, Sato K, Nakano A, Yamamoto K, Ito K (2014) Molecular characterization and subcellular localization of Arabidopsis class VIII myosin, AT M1. J Biol Chem 289:12343–12355

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hedrich E, Salvador-Retacala V, Dreyer I (2016) Electrical wiring and long-distance plant communication. Trends Plant Sci 21:376–387

    Article  CAS  PubMed  Google Scholar 

  • Heinlein M, Padgett HS, Gens JS, Pickard BG, Casper SJ, Epel BL, Beachy RN (1998) Changing patterns of localization of the tobacco mosaic virus movement protein and replicase to the endoplasmic reticulum and microtubules during infection. Plant Cell 10:1107–1120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Henne WM, Liou J, Emr SD (2015) Molecular mechanisms of inter-organelle ER-PM contact sites. Curr Opin Cell Biol 35:123–130

    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 

  • Higashi-Fujime S, Nakamura A (2009) Cell and molecular biology of the fastest myosins. Int Rev Cell Mol Biol 276:301–347

    Article  PubMed  CAS  Google Scholar 

  • Holdaway-Clarke TL, Walker NA, Overall RL (1996) Measurement of the electrical resistance of plasmodesmata and membranes of corn suspension-culture cells. Planta 199:537–544

    Article  Google Scholar 

  • Holdaway-Clarke TL, Walker NA, Hepler PK, Overall RL (2000) Physiological elevations in cytoplasmic free calcium by cold or ion injection result in transient closure of higher plant plasmodesmata. Planta 210:329–335

    Article  CAS  PubMed  Google Scholar 

  • Hong Z-L, Zhang Z-M, Olson JM, Verma DPS (2001) A novel UDP-glucose transferase is part of the callose synthase complex and interacts with phragmoplastin at the forming cell plate. Plant Cell 13:769–779

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Imlau A, Truernit E, Sauer N (1999) Cell-to-cell and long-distance trafficking of the green fluorescent protein in the phloem and symplasmic unloading of the protein into sink tissue. Plant Cell 11:309–322

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Itaya A, Woo Y-M, Masuta C, Bao Y, Nelson RS, Ding B (1998) Developmental regulation of intercellular protein trafficking through plasmodesmata in tobacco leaf epidermis. Plant Physiol 118:373–385

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Itaya A, Liang G, Woo Y-M, Nelson RS, Ding B (2000) Nonspecific intercellular protein trafficking probed by green-fluorescent protein in plants. Protoplasma 213:165–175

    Article  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 

  • Jaeger KA, Wigge FT (2007) FT protein acts as a long-range signal in Arabidopsis. Curr Biol 17:1050–1054

    Article  CAS  PubMed  Google Scholar 

  • Jo Y, Cho W-K, Rim Y, Moon J, Chen X-Y, Chu H, Kim C-Y, Park Z-Y, Lucas WJ, Kim J-Y (2010) Plasmodesmal receptor-like kinases identified through analysis of rice cell wall extracted proteins. Protoplasma 248:191–203

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jones MGK (1976) The origin and development of plasmodesmata. In: Gunning BES, Robards AW (eds) Intercellular communication plants: studies on plasmodesmata. Springer, Berlin, pp 81–105

    Chapter  Google Scholar 

  • Kauss H (1987) Some aspects of calcium-dependent regulation in plant metabolism. Annu Rev Plant Physiol 38:47–72

    Article  CAS  Google Scholar 

  • Kempers R, van Bel AJE (1997) Symplasmic connections between sieve element and companion cell in the stem phloem of Vicia faba L. have a molecular exclusion limit of at least 10 kDa. Planta 201:195–201

    Article  CAS  Google Scholar 

  • Kempers R, Prior DAM, van Bel AJE, Oparka KJ (1993) Plasmodesmata between sieve element and companion cell of extrafascicular stem phloem of Cucurbita maxima permit passage of 3 kDa fluorescent probes. Plant J 4:567–575

    Article  Google Scholar 

  • Kempers R, Ammerlaan A, van Bel AJE (1998) Symplasmic constriction and ultrastructural features of the sieve element/companion cell complex in the transport phloem of apoplasmatically and symplasmatically phloem loading species. Plant Physiol 116:271–278

    Article  CAS  PubMed Central  Google Scholar 

  • Kempers R, Prior DAM, Oparka KJ, Knoblauch M, van Bel AJE (1999) Integration of controlled pressure microinjection, iontophoresis, and membrane potential measurement. Plant Biol 1:61–67

    Article  Google Scholar 

  • Kikuyama M, Hara R, Shimada K, Yamamoto K, Hiramoto Y (1992) Intercellular transport of macromolecules in Nitella. Plant Cell Physiol 33:413–417

    CAS  Google Scholar 

  • Kim M, Canio W, Kessler S, Sinha S (2001) Developmental changes due to long-distance movement of a homeobox fusion transcript in tomato. Science 293:287–289

    Article  CAS  PubMed  Google Scholar 

  • Kim I, Hempel FD, Sha K, Pfluger J, Zambryski PC (2002) Identification of a developmental transition in plasmodesmatal function during embryogenesis in Arabidopsis thaliana. Development 129:1261–1272

    CAS  PubMed  Google Scholar 

  • Kim I, Cho E, Crawford K, Hempel FD, Zambryski PC (2005) Cell-to-cell movement of GFP during embryogenesis and early seedling development in Arabidopsis. Proc Natl Acad Sci U S A 102:2227–2231

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Knox K, Wang P, Kriechbaumer V, Tilsner J, Frigerio L, Sparkes I, Hawes C, Oparka KJ (2015) Putting the squeeze on PDs – a role for RETICULONS in primary plasmodesmata formation. Plant Physiol 168:1563–1572

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kollmann R, Schumacher W (1963) Über die Feinstruktur des Phloems von Metasquoia glyptostroboides und seine jahreszeitliche Änderungen. IV. Weitere Beobachtungen zum Feinbau der Plasmabrücken in den Siebzellen. Planta 60:360–389

    Article  Google Scholar 

  • Kollmann R, Glockmann C (1985) Studies on graft unions. I Plasmodesmata between cell belonging to different unrelated taxa. Protoplasma 124:224–235

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Kollmann R, Glockmann C (1999) Multimorphology and nomenclature of plasmodesmata in higher plants. In: van Kesteren WJP (ed) van Bel AJE. Springer, Berlin, pp 149–174

    Google Scholar 

  • Kollmann R, Yang S, Glockmann C (1985) Studies on graft unions. II. Continuous and half plasmodesmata in different regions of the graft interface. Protoplasma 126:19–29

    Article  Google Scholar 

  • Kong L, Sun M, Xie Y, Wang F, Zhao Z (2015) Photochemical and antioxidative responses of the glume and flag leaf to seasonal senescence in wheat. Front Plant Sci 6:358

    PubMed  PubMed Central  Google Scholar 

  • Kooiman P (1960) On the occurrence of amyloids in plant seeds. Acta Bot Neerl 2:208–219

    Article  Google Scholar 

  • Kotlizky G, Shurtz S, Yahalom A, Malik Z, Traub O, Epel BL (1992) An improved procedure for the isolation of plasmodesmata embedded in clean maize cell walls. Plant J 2:623–630

    Article  Google Scholar 

  • Kragler F, Lucas WJ, Monzer J (1998) Plasmodesmata: dynamics, domains and patterning. Ann Bot 81:1–10

    Article  Google Scholar 

  • Kriechbaumer V, Botchway SW, Slade SE, Knox K, Frigerio L, Oparka K, Hawes C (2015) Reticulomics: protein-protein interaction studies with two plasmodesmata-localized reticulon family proteins identify binding partners enriched at plasmodesmata, endoplasmic reticulum, and the plasma membrane. Plant Physiol 169:1933–1945

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kühn C, Franceschi VR, Schulz A, Lemoine R, Frommer WB (1997) Macromolecular trafficking indicated by localization and turnover of sucrose transporters in enucleate sieve elements. Science 275:1298–1300

    Article  PubMed  Google Scholar 

  • Kumar R, Kumar D, Hyun TK, Kim J-Y (2015) Players at plasmodesmal nanochannels. J Plant Biol 58:75–86

    Article  CAS  Google Scholar 

  • Kwiatkowska M, Maszewski J (1986) Changes in the occurrence and ultrastructure of plasmodesmata in antheridia of Chara vulgaris L. during different stages of spermatogenesis. Protoplasma 132:179–188

    Article  Google Scholar 

  • Lahiri S, Toulmay A, Prinz WA (2015) Membrane contact sites, gateways for lipid homeostasis. Curr Opin Cell Biol 32:82–87

    Article  CAS  Google Scholar 

  • Lapidot M, Gafny R, Ding B, Wolf S, Lucas WJ, Beachy RN (1993) A dysfunctional movement protein of tobacco mosaic virus that partially modifies the plasmodesmata and limits virus spread in transgenic plants. Plant J 4:959–970

    Article  CAS  Google Scholar 

  • Lazzaro MD, Thomson WW (1996) The vacuolar tubular continuum in living trichomes of living chickpea (Cicer arietinum) provides a rapid means of solute delivery. Protoplasma 193:181–190

    Article  Google Scholar 

  • Lecourieux D, Ranjeva R, Pugin A (2006) Calcium in plant defence-signalling pathways. New Phytol 171:249–269

    Article  CAS  PubMed  Google Scholar 

  • Lee J-Y, Cui W (2009) Non-cell autonomous RNA trafficking and long-distance signalling. J Plant Biol 52:10–18

    Article  CAS  Google Scholar 

  • Lee J-Y, Lu H (2011) Plasmodesmata: the battleground against intruders. Trends Plant Sci 16:201–210

    Article  CAS  PubMed  Google Scholar 

  • Lee J-Y, Wang X, Cui W, Sager R, Modla S, Czymmek K, Zybaliov B, van Wijk K, Zhang C, Lu H, Lakshaman V (2011) A plasmodesmata-localized protein mediates crosstalk between cell-to-cell communication and innate immunity in Arabidopsis. Plant Cell 23:3353–3373

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee H, Sparkes I, Gattolin S, Dzimitrowitz N, Roberts LM, Hawes C, Frigerio L (2013) An Arabidopsis reticulon and the atlastin homologue THD3-like 2 act together in shaping the tubular endoplasmic reticulum. New Phytol 197:481–489

    Article  CAS  PubMed  Google Scholar 

  • Levy A, Epel BL (2009) Cytology of the (1,3)-β-glucan (callose) in plasmodesmata and sieve plate pores. In: Basic A, Fincher GB, Stone BA (eds) Chemistry, biochemistry and biology of (1-3)-beta-glucans and related polysaccharides. Academic Press, London, pp 439–463

    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  CAS  PubMed  Google Scholar 

  • Levy A, Zheng J-Y, Lazarowitz SG (2015) Synaptotagmin SYT a forms ER-plasma membrane junctions that are recruited to plasmodesmata for plant virus movement. Curr Biol 25:1–8

    Article  CAS  Google Scholar 

  • Lew RR (1996) Pressure regulation of the electrical properties of growing Arabidopsis thaliana L. root hairs. Plant Physiol 112:1089–1100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lewis JD, Lazarowitz SG (2010) Arabidopsis synaptotagmin SYTA regulates endocytosis and virus movement protein cell-to-cell transport. Proc Natl Acad Sci U S A 107:2491–2496

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li C, Gu M, Shi N, Zhang H, Yang X, Osman T, Liu Y, Wang H, Vatush M, Jackson S, Hong Y (2011a) Mobile FT mRNA contributes to the systemic florigenic signalling in floral induction. Sci Rep 1:73

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Li W, Zhao Y, Liu C, Yao G, Wu S, Hou C, Zhang M, Wang D (2011b) Callose deposition at plasmodesmata is a critical factor in restricting cell-to-cell movement of Soybean mosaic virus. Plant Cell Rep 31:905–916

    Article  CAS  PubMed  Google Scholar 

  • Lim G-H, Shine MB, De Lorenzo L, Yu K, Cui W, Navarre D, Hunt AG, Lee J-Y, Kachroo A, Kachroo P (2016) Plasmodesmata localizing proteins regulate transport and signalling during systemic acquired immunity in plants. Cell Host Microbe 19:541–549

    Article  CAS  PubMed  Google Scholar 

  • Lopez-Saez JF, Gimenez-Martin G, Risueno MC (1966) Fine structure of the plasmodesm. Protoplasma 61:81–84

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Lucas WJ, Bouché-Pillon S, Jackson DP, Nguyen L, Baker L, Ding B, Hake S (1995) Selective trafficking of KNOTTED1 homeodomain protein and its mRNA through plasmodesmata. Science 270:190–193

    Article  Google Scholar 

  • Lucas WJ, Ham B-K, Kim J-Y (2009) Plasmodesmata – bridging the gap between neighbouring plant cells. Trends Cell Biol 19:495–503

    Article  CAS  PubMed  Google Scholar 

  • Lucas WJ, Yoo BC, Kragler F (2001) RNA as a long-distance information molecule in plants. Nat Rev Mol Cell Biol 2:849–857

    Article  CAS  PubMed  Google Scholar 

  • Maule AJ, Benitez-Alfonso Y, Faulkner C (2011) Plasmodesmata – membrane tunnels with attitude. Curr Opin Plant Biol 14:1–8

    Article  CAS  Google Scholar 

  • McLean BG, Waigmann E, Citovsky V, Zambryski P (1993) Cell-to-cell movement of plant viruses. Trends Microbiol 1:105–109

    Article  CAS  PubMed  Google Scholar 

  • McLean BG, Zupan J, Zambryski PC (1995) Tobacco mosaic virus movement protein associates with the cytoskeleton in tobacco cells. Plant Cell 7:2101–2114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McLean BG, Hempel FD, Zambryski PC (1997) Plant intercellular communication via plasmodesmata. Plant Cell 9:1043–1054

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McMahon HT, Boucrot E (2015) Membrane curvature at a glance. J Cell Sci 128:1065–1070

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meiners S, Schindler M (1989) Characterization of a connexin homologue in cultured soybean cells and diverse plant organs. Planta 179:148–155

    Article  CAS  PubMed  Google Scholar 

  • Meiners S, Xu A, Schindler M (1991) Gap junction protein homologue from Arabidopsis thaliana: evidence for connexons in plants. Proc Natl Acad Sci U S A 88:4119–4122

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mercer FV (1956) Cytology and the electron microscope. Proc Linnean Soc NSW 81:4–19

    Google Scholar 

  • Mezitt LA, Lucas WJ (1996) Plasmodesmal cell-to-cell transport of proteins and nucleic acids. Plant Mol Biol 32:251–273

    Article  CAS  PubMed  Google Scholar 

  • Monzer J, Kloth S (1991) The preparation of plasmodesmata from plant tissue homogenates: access to the biochemical characterization of plasmodesmata-related proteins. Bot Acta 104:82–84

    Article  CAS  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 

  • Mumm P, Wolf T, Fromm J, Roelfsema RG, Marten I (2011) Cell type-specific regulation of ion channels within the maize stomatal complex. Plant Cell Physiol 52:1365–1375

    Article  CAS  PubMed  Google Scholar 

  • Münch E (1930) Die Stoffbewegungen in der Pflanze. Gustav Fischer, Jena

    Google Scholar 

  • Mushegian AR, Koonin EV (1993) The proposed plant connexin is a protein kinase-like protein. Plant Cell 5:998–999

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nakamura S, Hayashi H, Mori S, Chino M (1993) Protein phosphorylation in the sieve tubes of rice plants. Plant Cell Physiol 34:927–933

    CAS  Google Scholar 

  • Niehl A, Heinlein M (2011) Cellular pathways for viral transport through plasmodesmata. Protoplasma 248:75–99

    Article  CAS  PubMed  Google Scholar 

  • Niyogi KK, Wolosiuk RA, Malkin RA (2015) Photosynthesis. In: Buchanan BB, Gruissem W, Jones TL (eds) Biochemistry and molecular biology of plants. Wiley, Chichester, pp 508–566

    Google Scholar 

  • Ohana P, Benziman M, Delmer DP (1993) Stimulation of callose synthesis in vitro correlates with changes in intracellular distribution of the callose synthase activator β-furfuryl-β-glucoside. Plant Physiol 101:187–191

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Olesen P (1979) The neck constriction in plasmodesmata. Evidence for a peripheral sphincter-like structure revealed by fixation with tannic acid. Planta 144:349–358

    Article  CAS  PubMed  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 (2005) Plasmodesmata. Blackwell, Oxford

    Book  Google Scholar 

  • Oparka KJ, Prior DAM (1992) Direct evidence for pressure-generated closure of plasmodesmata. Plant J 2:741–750

    Article  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 

  • Oparka KJ, Prior DAM, Santa Cruz S, Padgett HS, Beachy RN (1997) Gating of epidermal plasmodesmata is restricted to the leading edge of expanding infection sites of tobacco mosaic virus (TMV). Plant J 12:781–789

    Article  CAS  PubMed  Google Scholar 

  • Oparka KJ, Roberts AG, Boevink P, Santa Cruz S, Roberts IM, Pradel KS, Imlau A, Kotlizky G, Sauer N, Epel B (1999) Simple, but not branched, plasmodesmata allow the nonspecific trafficking of proteins in developing tobacco leaves. Cell 97:743–754

    Article  CAS  PubMed  Google Scholar 

  • Otero S, Helariutta Y, Benitez-Alfonso Y (2016) Symplastic communication in organ formation and tissue patterning. Curr Opin Plant Biol 29:21–28

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Overall RL, Wolfe J, Gunning BES (1982) Intercellular communication in Azolla roots L. I. Ultrastructure of the plasmodesmata. Protoplasma 111:134–150

    Article  Google Scholar 

  • Palevitz BA, Hepler PK (1985) Changes in dye coupling of stomatal cells of Allium and Commelina demonstrated by microinjection of Lucifer Yellow. Planta 164:473–479

    Article  CAS  PubMed  Google Scholar 

  • Patrick JW (1997) Phloem unloading: sieve element unloading and post-phloem transport. Annu Rev Plant Physiol Plant Mol Biol 48:191–222

    Article  CAS  PubMed  Google Scholar 

  • Patrick JW, Offler CE (1995) Post-sieve element transport of sucrose in developing seeds. Aust J Plant Physiol 22:681–702

    Article  CAS  Google Scholar 

  • Patrick JW, Offler CE (1996) Post-sieve element transport of photoassimilates in sink regions. J Exp Bot 47:1165–1177

    Article  CAS  PubMed  Google Scholar 

  • Patrick JW, Offler CE (2001) Compartmentation of transport and transfer events in developing seeds. J Exp Bot 52:551–564

    Article  CAS  PubMed  Google Scholar 

  • Patrick JW, Tyerman SD, van Bel AJE (2015) Long-distance transport. In: Buchanan BB, Gruissem W, Jones TL (eds) Biochemistry and molecular biology of plants. Wiley, Chichester, pp 658–710

    Google Scholar 

  • Paultre DSG, Gustin M-P, Molnar A, Oparka KJ (2016) Lost in transit: long-distance trafficking and phloem unloading of protein signals in Arabidopsis homografts. Plant Cell 28:2016–2025

    Article  CAS  PubMed Central  Google Scholar 

  • Perbal M-C, Haughn G, Saedler H, Schwarz-Sommer 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

    CAS  PubMed  Google Scholar 

  • Perez-Sancho J, Vanneste S, Lee E, McFarlane H, Esteban de Valle A, Valpuesta V, Friml J, Botella MA, Rosada A (2015) The Arabidopsis SYT 1 is enriched in ER-PM contact sites and confers cellular resistance to mechanical stresses. Plant Physiol 168:132–143

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peter BJ, Kent HM, Mills IG, Vallis Y, Butler PJ, Evans PR, McMahon HT (2004) BAR domains as sensor of membrane curvature. Science 303:495–499

    Article  CAS  PubMed  Google Scholar 

  • Peter KA, Gildow F, Palukaitis P, Grey SM (2009) The C-terminus of the polerovirus p5 readthrough domain limits virus infection to the phloem. J Virol 83:5419–5429

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Porter KR, Machado RD (1960) Studies on the endoplasmic reticulum IV. Its form and distribution during mitosis in cells of onion root tip. J Biophys Biochem Cytol 7:167–180

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Radford JE, White RG (1998) Localisation of a myosin-like protein to plasmodesmata. Plant J 14:743–760

    Article  CAS  PubMed  Google Scholar 

  • Radford JE, Vesk M, Overall RL (1998) Callose deposition at plasmodesmata. Protoplasma 201:30–37

    Article  CAS  Google Scholar 

  • Raffaele S, Bayer E, Lafarge D, Cluzet S, German RS, Boubekeur T, Leborgne-Castel N, Carde JP, Lherminier J, Noirot E, Satiat-Jeunemaître B, Laroche-Traineau J, Moreau P, Ott T, Maule AJ, Reymond P, Simon-Plas F, Farmer EE, Bessoule J-J, Mongrand S (2009) Remorin, a Solanaceae protein resident in membrane rafts and plasmodesmata, impairs potato X virus movement. Plant Cell 21:1541–1555

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reichelt S, Knight AE, Hodge TP, Baluska F, Samaj J, Volkmann D, Kendrick-Lones J (1999) Characterization of the unconventional myosin VIII in plant cells and its localization at the post-kinetic cell wall. Plant J 19:555–567

    Article  CAS  PubMed  Google Scholar 

  • Rhodes JD, Thain JF, Wildon DC (1996) The pathway for systemic electrical signal conduction in the wounded tomato plant. Planta 200:50–57

    Article  CAS  Google Scholar 

  • Rinne PL, Welling A, Vahala J, Ripel L, Ruonala R, Kangasjarvi J, van der Schoot C (2011) Chilling of dormant buds hyperinduces FLOWERING LOCUS T and recruits GA-inducible 1,3-beta-glucanases to reopen signal conduits and release dormancy in Populus. Plant Cell 23:130–146

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  Google Scholar 

  • Robards AW (1968b) A new interpretation of the plasmodesmatal ultrastructure. Planta 82:200–210

    Article  CAS  PubMed  Google Scholar 

  • Robards AW (1976) Plasmodesmata in higher plants. In: Gunning BES, Robards AW (eds) Intercellular communication in plants: studies on plasmodesmata. Springer, Berlin, pp 15–57

    Chapter  Google Scholar 

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

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

    CAS  PubMed  Google Scholar 

  • Ruan Y-L, Llewellyn DJ, Furbank RT (2001) The control of single-cell cotton fiber elongation by developmentally reversible gating of plasmodesmata and coordinated expression of sucrose and K+ transporters and expansin. Plant Cell 13:47–60

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ruan Y-L, S-M X, White R, Furbank RT (2004) Genotypic and developmental evidence for the role of plasmodesmatal regulation in cotton fiber elongation mediated by callose turnover. Plant Physiol 136:4104–4113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rüping B, Ernst AM, Jekat SB, Nordzieke S, Reineke AR, Müller B, Bornberg-Bauer E, Prüfer D, Noll GA (2010) Molecular and phylogenetic characterization of the sieve element occlusion family in Fabaceae and non-Fabaceae plants. BMC Plant Biol 10:219

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Saez JC, Berthoud VM, Branes MC, Martinez AD, Beyer EC (2003) Plasma membrane channels formed by connexins. Physiol Rev 83:1359–1400

    Article  CAS  PubMed  Google Scholar 

  • Sager R, Lee J-Y (2014) Plasmodesmata in integrated cell signalling: insights from developmental and environmental signals and stresses. J Exp Bot 65:6337–6358

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sagi G, Katz A, Guenoune-Gelbart D, Epel BL (2005) Class 1 reversibly glycosylated polypeptides are plasmodesmal-associated proteins delivered to plasmodesmata via the Golgi apparatus. Plant Cell 17:1788–1800

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sakuth T, Schobert C, Pecsvaradi A, Eichholz E, Komor E, Orlich G (1993) Specific proteins in the sieve-tube exudate of Ricinus communis L. seedlings: separation, characterization and in-vivo labelling. Planta 191:207–213

    Article  CAS  Google Scholar 

  • Schenk E (1972) Quantitative studies on translocation in Sagittaria graminea Michx leaves. A new method of measurement. Acta Bot Neerl 21:231–234

    Article  CAS  Google Scholar 

  • Schleiden MJ (1838) Beiträge zur Phytogenesis. Müller’s Archiv für Anatomie, Physiol. u. wiss. Medizin 5:136–176

    Google Scholar 

  • Schobert C, Groβmann P, Gottschalk M, Komor E, Pecsvaradi A, zur Nieden U (1995) Sieve-tube exudate from Ricinus communis L. seedlings contains ubiquitin and chaperones. Planta 196:205–210

    Article  CAS  Google Scholar 

  • Schreiber L (2010) Transport barriers made of cutin, suberin and associated waxes. Trends Plant Sci 15:546–553

    Article  CAS  PubMed  Google Scholar 

  • Schulz A (1992) Living cells of conifers as visualized by confocal, laser-scanning microscopy. Protoplasma 166:153–164

    Article  Google Scholar 

  • Schulz A (1994) Phloem transport and differential unloading in pea seedlings after source and sink manipulation. Planta 192:239–248

    Article  CAS  Google Scholar 

  • Schulz A (1995) Plasmodesmal widening accompanies the short-term increase in symplastic phloem unloading in pea root tips under osmotic stress. Protoplasma 188:23–37

    Article  Google Scholar 

  • Schulz A (1999) Physiological control of plasmodesmal gating. In: van Kesteren WJP (ed) van Bel AJE. Springer, Berlin, pp 173–204

    Google Scholar 

  • Schulz A (2017) Long-distance trafficking: lost in transit or stopped at the gate? Plant Cell 29:426–430

    Article  PubMed  PubMed Central  Google Scholar 

  • Schumacher W (1936) Untersuchungen über die Wanderung des Fluoresceins in den Haaren von Cucurbita pepo. Jb Wiss Bot 82:507–533

    CAS  Google Scholar 

  • Schwann J (1839) Mikroskopische Untersuchungen über die Übereinstimmung in der Struktur und dem Wachstum der Thiere und Pflanzen. Verlag der Sander’schen Buchhandlung, Berlin

    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  PubMed Central  Google Scholar 

  • Sinha N, Hake S (1990) Mutant characters of Knotted maize leaves are determined in the innermost tissue layers. Dev Biol 141:203–210

    Article  CAS  PubMed  Google Scholar 

  • Spanswick RM, Costerton JWF (1967) Plasmodesmata in Nitella translucens: structure and electrical resistance. J Cell Sci 2:451–464

    CAS  PubMed  Google Scholar 

  • Srivastava LM, Singh AP (1972) Stomatal structure in corn leaves. J Ultrastruct Res 39:345–363

    Article  CAS  PubMed  Google Scholar 

  • Stadler R, Wright KM, Lauterbach C, Amon G, Gahrtz M, Feuerstein A, Oparka KJ, Sauer N (2005) Expression of GFP-fusions in Arabidopsis companion cells reveals non-specific protein trafficking into sieve elements and identifies a novel post-phloem domain in roots. Plant J 41:319–331

    Article  CAS  PubMed  Google Scholar 

  • Staiger CJ, Sheahan MB, Khurana P, Wang X, McCurdy DW, Bianchoin L (2009) Actin filament dynamics are dominated by rapid growth and severing activity in the Arabidopsis cortical array. J Cell Biol 184:269–280

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Strasburger E (1901) Über Plasmaverbindungen pflanzlicher Zellen. J Wiss Bot 36:493–610

    Google Scholar 

  • Strugger S (1957) Der elektronenmikroskopische Nachweis von Plasmodesmen mit Hilfe der Uranylimprägnierung an Wurzelsystemen. Protoplasma 48:365–367

    Article  Google Scholar 

  • Tangl E (1879) Über offenen Communicationen zwischen den Zellen des Endosperms einiger Samen. Jb Wiss Bot 12:170–190

    Google Scholar 

  • Terry BR, Robards AW (1987) Hydrodynamic radius alone governs the mobility of molecules through plasmodesmata. Planta 171:145–157

    Article  CAS  PubMed  Google Scholar 

  • Thomas CL, Bayer E, Ritzenthaler C, Fernandez-Calvino L, Maule AJ (2008) Specific targeting of a plasmodesmal protein affecting cell-to-cell communication. PLoS Biol 6:e7

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Thomson WW, Platt-Aloia K (1985) The ultrastructure of the plasmodesmata of the salt glands of Tamarix as revealed by transmission and freeze-fracture electron microscopy. Protoplasma 125:13–23

    Article  Google Scholar 

  • Tilney LG, Cooke TJ, Connelly PS, Tilney MS (1991) The structure of plasmodesmata as revealed by plasmolysis, detergent extraction and protease digestion. J Cell Biol 112:739–747

    Article  CAS  PubMed  Google Scholar 

  • Tilsner J, Amari K, Torrance L (2011) Plasmodesmata viewed as specialised membrane adhesion sites. Protoplasma 248:39–60

    Article  CAS  PubMed  Google Scholar 

  • Tilsner JT, Nicolas W, Rosado A, Bayer EM (2016) Staying tight: plasmodesmal membrane contact sites and control of cell-to-cell connectivity in plants. Annu Rev Plant Biol 67:537–564

    Article  CAS  Google Scholar 

  • Todokoro Y, Yumen I, Fukushima K, Kang SW, Park JS, Kohno T, Wakamatsu K, Akutsu H, Fujiwara T (2006) Structure of tightly-bound mastoparan-X, a G protein activating peptide, determined by solid-state NMR. Biophys J 91:1368–1379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tolley N, Sparkes I, Craddock CP, Eastmond PJ, Runions J, Hawes C, Frigerio L (2010) Transmembrane domain length is responsible for the ability of a plant reticulon to shape endoplasmic reticulum tubules in vivo. Plant J 64:411–418

    Article  CAS  PubMed  Google Scholar 

  • Townsend CO (1897) Der Einfluss des Zellkernes auf die Bildung der Zellhaut. Jb Wiss Bot 30:484–510

    Google Scholar 

  • Tucker EB (1982) Translocation in the staminal hairs of Setcreasea purpurea. A study of cell ultrastructure and cell-to-cell passage of molecular probes. Protoplasma 113:193–201

    Article  CAS  Google Scholar 

  • Tucker EB (1988) Inositol bisphosphate and inositol trisphosphate inhibit cell-to-cell passage of carboxyfluorescein in staminal hairs of Setcreasea purpurea. Planta 174:358–363

    Article  CAS  PubMed  Google Scholar 

  • Tucker EB (1990) Calcium-loaded 1,2-bis(2-aminophenoxy)ethane-N,N,N’,N’-tetraacetic acid blocks cell-to-cell diffusion of carboxyfluorescein in staminal hairs of Setcreasea purpurea. Planta 182:34–38

    Article  CAS  PubMed  Google Scholar 

  • Tucker EB (1993) Azide treatment enhances cell-to-cell diffusion in staminal hairs of Setcreasea purpurea. Protoplasma 174:45–49

    Article  CAS  Google Scholar 

  • Tucker EB, Boss WF (1996) Mastoparan-induced intracellular Ca2+ fluxes may regulate cell-to-cell communication in plants. Plant Physiol 111:459–467

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tucker EB, Tucker JE (1993) Cell-to-cell diffusion selectivity in staminal hairs of Setcreasea purpurea. Protoplasma 174:36–44

    Article  Google Scholar 

  • Tucker J, Mauzerall D, Tucker EB (1989) Symplastic transport of carboxyfluorescein in staminal hairs of Setcreasea purpurea is diffusive and includes loss to the vacuole. Plant Physiol 90:1143–1147

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Turgeon R (1991) Symplastic phloem loading and source sink transition in leaves; a model. In: Bonnemain J-L, Delrot S, Lucas WJ, Dainty J (eds) Recent advances in phloem transport and assimilate compartmentation. Ouest Editions, Nantes, pp 18–22

    Google Scholar 

  • Turnbull CGN, Booker JP, Leyser HMO (2002) Micrografting techniques for testing long-distance signalling in Arabidopsis. Plant J 32:255–262

    Article  CAS  PubMed  Google Scholar 

  • Turner A, Wells B, Roberts K (1994) Plasmodesmata of root tips: structure and composition. J Cell Sci 107:3351–3361

    CAS  PubMed  Google Scholar 

  • Vaquero C, Turner AP, Demangeat G, Sanz A, Serra MT, Roberts K, Garcia-Luque L (1994) The 3a protein from cucumber mosaic virus increases the gating capacity of plasmodesmata in transgenic tobacco plants. J Gen Virol 75:3193–3197

    Article  CAS  PubMed  Google Scholar 

  • Van Bel AJE (1993) The transport phloem. Specifics of its functioning. Prog Bot 54:134–150

    Google Scholar 

  • Van Bel AJE (2003) The phloem, a miracle of ingenuity. Plant Cell Environ 26:125–149

    Article  Google Scholar 

  • Van Bel AJE, Ehlers K (2005) Electrical signalling via plasmodesmata. In: Oparka KJ (ed) Plasmodesmata. Annual Plant Reviews, vol 18. Blackwell, Oxford, pp 263–278

    Google Scholar 

  • Van Bel AJE, Kempers R (1990) Symplastic isolation of the sieve element-companion cell complex in the phloem of Ricinus communis and Salix alba stems. Planta 183:69–76

    Google Scholar 

  • Van Bel AJE, Oparka KJ (1995) On the validity of plasmodesmograms. Bot Acta 108:174–182

    Article  Google Scholar 

  • Van Bel AJE, van Kesteren WJP (1999) Plasmodesmata. Structure, function, role in cell communication. Springer, Berlin

    Google Scholar 

  • Van Bel AJE, van Rijen HVM (1994) Microelectrode-recorded development of the symplasmic autonomy of the sieve element/companion cell complex in the stem phloem of Lupinus luteus L. Planta 192:165–175

    Google Scholar 

  • Van Bel AJE, van Kesteren WJP, Papenhuijzen C (1988) Ultrastructural indications for coexistence of symplastic and apoplastic phloem loading in Commelina benghalensis leaves. Differences in ontogenic development, spatial arrangement and symplastic connections of the two sieve tubes in the minor vein. Planta 176:159–172

    Article  PubMed  Google Scholar 

  • Van Bel AJE, Furch ACU, Hafke JB, Knoblauch M, Patrick JW (2011) (Questions)n on phloem biology: 2. Mass flow, molecular hopping, distribution patterns and macromolecular signalling. Plant Sci 181:325–330

    Article  PubMed  CAS  Google Scholar 

  • Van Bel AJE, Furch ACU, Will T, Buxa SV, Musetti R, Hafke JB (2014) Spread the news: systemic dissemination and local impact of Ca2+ signals along the phloem pathway. J Exp Bot 65:1761–1787

    Article  PubMed  CAS  Google Scholar 

  • Van den Biggelaar JAM, Kühtreiber WM, Serras F, Dorresteijn A, Beekhuizen H, Schaap D (1986) Analysis of cell communication mechanisms involved in the induction of the stem cell of the mesodermal bands in embryos of Patella vulgata Mollusca. Acta Histochem 32:29–33

    Google Scholar 

  • Van der Schoot C, van Bel AJE (1990) Mapping membrane potential differences and dye-coupling in internodal tissues of tomato (Solanum lycopersicon L.) Planta 182:9–21

    Article  PubMed  Google Scholar 

  • Van Gestel K, Slegers H, von Witsch M, Samaj J, Baluska F, Verbelen J-P (2003) 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 and emerging root hairs. Protoplasma 222:45–52

    Article  PubMed  CAS  Google Scholar 

  • Van Lent J, Wellink J, Goldbach R (1990) Evidence for the involvement of the 58K and 48K proteins in the intercellular movement of cowpea mosaic virus. J Gen Virol 71:219–223

    Article  Google Scholar 

  • Vaten A, Dettmer J, Wu S, Stierhof YD, Miyashima S, Yadav ST, Roberts CT, Campillo A, Bulone V, Lichtenberger R, Lehesranta S, Mähönen AP, Kim J-Y, Jokalito E, Sauer N, Scheres B, Nakajima K, Carlsbecker A, Gallagher L, Helariutta Y (2011) Callose biosynthesis regulates symplastic trafficking during root development. Dev Cell 21:1144–1155

    Article  CAS  PubMed  Google Scholar 

  • Viola R, Roberts AG, Haupt S, Gazzani S, Hancock RD, Marmiroli N, Machray GC, Oparka KJ (2001) Tuberization in potato involves a swirh from apoplastic to symplastic phloem unloading. Plant Cell 13:385–398

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vodeneev VA, Sherstneva ON, Surova LM, Semina MM, Katicheva LA, Sukhov VS (2016) Age-dependent changes of photosynthetic responses induced by electrical signals in wheat seedlings. Russ J Plant Physiol 63:861–868

    Article  CAS  Google Scholar 

  • Volk GM, Turgeon R, Beebe DU (1996) Secondary plasmodesmata formation in the minor-vein phloem of Cucumis melo L. and Cucurbita pepo L. Planta 199:425–432

    Article  Google Scholar 

  • Waigmann E, Turner A, Peart J, Roberts K, Zambryski P (1997) Ultrastructural analysis of leaf trichome plasmodesmata reveals major differences from mesophyll plasmodesmata. Planta 203:75–84

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang N, Fisher DB (1994) Monitoring phloem unloading and post-phloem transport by microperfusion of attached wheat grains. Plant Physiol 104:7–16

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang X, Sager R, Cui W, Zhang C, Lu H, Lee J-Y (2013) Salicylic acid regulates plasmodesmata closure during innate immunity responses in Arabidopsis. Plant Cell 25:2315–2329

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wanner G (2004) Mikroskopisch-Botanisches Praktikum. Thieme, Stuttgart

    Google Scholar 

  • Whaley WG, Mollenhauer HH, Leech JH (1960) The ultrastructure of the meristematic cell. Am J Bot 47:401–449

    Article  Google Scholar 

  • White RG, Barton DA (2011) The cytoskeleton in plasmodesmata: a role in intercellular transport? J Exp Bot 62:5249–5266

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Wille AC, Lucas WJ (1984) Ultrastructural and histochemical studies on guard cells. Planta 160:129–142

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Wright KM, Oparka KJ (1994) Physicochemical properties alone do not predict the movement and compartmentation of fluorescent xenobiotics. J Exp Bot 45:35–44

    Article  CAS  Google Scholar 

  • Wright KM, Oparka KJ (1997) Metabolic inhibitors induce symplastic movement of solutes from the transport phloem of Arabidopsis roots. J Exp Bot 48:1807–1814

    Article  CAS  Google Scholar 

  • Wu S, Gallagher KL (2012) Transcription factors on the move. Curr Opin Plant Biol 15:645–651

    Article  CAS  PubMed  Google Scholar 

  • Xie L, Shang W, Liu C, Zhang Q, Sunter G, Hong J, Zhou X (2016) Mutual association of Broad bean wilt virus 2 VP37-derived tubules and plasmodesmata obtained from cytosolic observation. Sci Rep 6:21552

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yahalom A, Warmbrodt RD, Laird DW, Traub O, Revel J-P, Willecke K, Epel BL (1991) Maize mesocotyl plasmodesmata proteins cross-react with connexin gap junction protein antibodies. Plant Cell 3:407–417

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang S, Xiang G, Zhang S, Lou C (1992) Electrical resistance as a measure of graft union. J Plant Physiol 141:98–104

    Article  Google Scholar 

  • Zavaliev R, Ueki S, Epel BL, Citovsky V (2011) Biology of callose (β-1,3-glucan) turnover at plasmodesmata. Protoplasma 248:117–130

    Article  CAS  PubMed  Google Scholar 

  • Zavaliev R, Levy A, Gera A, Epel BL (2013) Subcellular dynamics and role of Arabidopsis β-1,3-glucanases in cell-to-cell movement of tobamoviruses. Mol Plant-Microbe Interact 26:1016–1030

    Article  CAS  PubMed  Google Scholar 

  • Zhang WH, Tyerman SD (1997) Effect of low oxygen concentration on the electrical properties of cortical cells of wheat roots. J Plant Physiol 150:567–572

    Article  CAS  PubMed  Google Scholar 

  • Zhang X-Y, Wang X-Y, Wang X-F, Xia G-H, Pan Q-H, Fan R-C, F-Q W, X-C Y, Zhang D-P (2006) A shift of phloem unloading from symplasmic to apoplasmic pathway is involved in developmental onset of ripening in grape berry. Plant Physiol 142:220–232

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

Linguistic correction of the manuscript by Dr. Daniel T. van Bel is gratefully acknowledged.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Aart J. E. van Bel .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer International Publishing AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

van Bel, A.J.E. (2018). Plasmodesmata: A History of Conceptual Surprises. In: Sahi, V., Baluška, F. (eds) Concepts in Cell Biology - History and Evolution. Plant Cell Monographs, vol 23. Springer, Cham. https://doi.org/10.1007/978-3-319-69944-8_11

Download citation

Publish with us

Policies and ethics