Skip to main content
Log in

Dynamics of plasmodesmal connectivity in successive interfaces of the cambial zone

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Frequency, density and branching of plasmodesmata were counted in successive tangential and transverse walls in the cambial zone of tomato stems in order to examine development of the plasmodesmal network in a chronological order. Coincident with progress of cell development, plasmodesmal connectivity increased, both at the xylem- and phloem-side. In transverse walls, the number of secondary plasmodesmata enhanced considerably. The same held for tangential walls, with a superimposed plasmodesmal doubling during the first phase of phloem development. This plasmodesmal doubling was interpreted to result from the deposition of wall material between branched plasmodesmal strands. Structural plasmodesmal development was correlated with production of hydroxyl radicals which control local cell wall alterations. Successive phases of plasmodesmal deployment and modification were distinguished which may coincide with differential functional capacities as documented by intracellular injection of fluorochromes. Diffusion-driven symplasmic transport appeared to be transiently interrupted during cell maturation.

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

Access this article

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11

Similar content being viewed by others

Abbreviations

ER:

Endoplasmic reticulum

PD(s):

Plasmodesma(ta)

LYCH:

Lucifer Yellow

SEL:

Basal size exclusion limit

TEM:

Transmission-electron microscopy

References

  • Barceló AR (2005) Xylem parenchyma cells deliver the H2O2 necessary for lignification in differentiating xylem vessels. Planta 220:747–756

    Article  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 USA 106:3615–3620

    Article  CAS  PubMed  Google Scholar 

  • Bergmans ACJ, de Boer AD, Derksen JWM, van der Schoot C (1997) The symplasmic coupling of L2-cells diminishes in early floral development of Iris. Planta 203:245–252

    Article  CAS  Google Scholar 

  • Bestwick CS, Brown IR, Bennett MHR, Mansfield JW (1997) Localization of hydrogen peroxide accumulation during the hypersensitive reaction of lettuce cells to Pseudomonas syringae pv phaseolicola. Plant Cell 9:209–221

    Article  CAS  PubMed  Google Scholar 

  • Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6:850–861

    Article  CAS  PubMed  Google Scholar 

  • Ding B, Itaya A (2007) Control of directional macromolecular trafficking across specific cellular boundaries: a key to integrative plant biology. J Integr Plant Biol 49:1227–1234

    Article  CAS  Google Scholar 

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

    Article  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 (1999) The physiological and developmental consequences of plasmodesmal connectivity. In: van Bel AJE, van Kesteren WJP (eds) Plasmodesmata. Structure, function, role in cell communication. Springer, Berlin, pp 243–260

    Google Scholar 

  • Ehlers K, Knoblauch M, van Bel AJE (2000) Ultrastructural features of well-preserved and injured sieve elements. Minute clamps keep the phloem transport conduits free for mass flow. Protoplasma 214:80–92

    Article  Google Scholar 

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

  • Evert RF (ed) (2006) Esau′s plant anatomy: meristems, cells, and tissues of the plant body: their structure, function, and development, 3rd edn. Wiley, Hoboken

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

    Article  CAS  PubMed  Google Scholar 

  • Gisel A, Hempel FD, Barella S, Zambryski P (2002) Leaf-to-shoot apex movement of symplastic tracer is restricted coincident with flowering in Arabidopsis. Proc Natl Acad Sci USA 99:1713–1717

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Hafke JB, van Amerongen JK, 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  Google Scholar 

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

    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 

  • Hu J, Shibata Y, Voss C, Shemesh T, Li Z, Coughlin M, Kozlov MM, Rapoport TA, Prinz WA (2008) Membrane proteins of the endoplasmic reticulum induce high-curvature tubules. Science 319:1247–1250

    Article  CAS  PubMed  Google Scholar 

  • Imaichi R, Hiratsuka R (2007) Evolution of shoot apical meristem structures in vascular plants with respect to the plasmodesmatal network. Am J Bot 94:1911–1921

    Article  Google Scholar 

  • Itaya A, Woo YM, 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  Google Scholar 

  • Itaya A, Ma F, Qi Y, Matsuda Y, Zhu Y, Liang G, Ding B (2002) Plasmodesma-mediated selective protein traffic between “symplasmically-isolated” cells probed by a viral movement protein. Plant Cell 14:2071–2083

    Article  CAS  PubMed  Google Scholar 

  • Jackson D (2005) Transcription factor movement through plasmodesmata. In: Oparka KJ (ed) Plasmodesmata. Blackwell Publishing, Oxford, pp 113–134

    Chapter  Google Scholar 

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

    Google Scholar 

  • Kempers R, Prior DAM, Oparka KJ, Knoblauch M, van Bel AJE (1999) Integration of controlled intracellular pressure microinjection, iontophoresis, and membrane potential measurement. Plant Biol 1:61–77

    Article  Google Scholar 

  • Kim I, Kobayashi K, Cho E, Zambryski PC (2005) Subdomains for transport via plasmodesmata corresponding to the apical-basal axis are established during Arabidopsis embryogenesis. Proc Natl Acad Sci USA 102:11945–11950

    Article  CAS  PubMed  Google Scholar 

  • Knoblauch M (2001) Microinjection. In: Hawes CR, Satiat-Jeunemaitre B (eds) Plant cell biology: practical approach. Oxford University Press, Cambridge, pp 143–158

    Google Scholar 

  • Kobayashi K, Kim I, Cho E, Zambryski P (2005) Plasmodesmata and plant morphogenesis. In: Oparka KJ (ed) Plasmodesmata. Blackwell Publishing, Oxford, pp 90–112

    Chapter  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 

  • Kragler F (2005) Plasmodesmata: protein transport signals and receptors. In: Oparka KJ (ed) Plasmodesmata. Blackwell Publishing, Oxford, pp 53–72

    Chapter  Google Scholar 

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

    Article  Google Scholar 

  • Krull R (1960) Untersuchungen über den Bau und die Entwicklung der Plasmodesmen im Rindenparenchym von Viscum album. Planta 55:598–629

    Article  Google Scholar 

  • Lachaud S, Catesson AM, Bonnemain JL (1999) Structure and functions of the vascular cambium. CR Acad Sci Paris Life Sci 322:633–650

    CAS  Google Scholar 

  • Liszkay A, Kenk B, Schopfer P (2003) Evidence for the involvement of cell wall peroxidase in the generation of hydroxyl radicals mediating extension growth. Planta 217:658–667

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Oparka K, Boevink P (2005) Techniques for imaging intercellular transport. In: Oparka KJ (ed) Plasmodesmata. Blackwell Publishing, Oxford, pp 241–262

    Chapter  Google Scholar 

  • Oparka KJ, Roberts AG (2001) Plasmodesmata. A not so open-and-shut case. Plant Physiol 125:123–126

    Article  CAS  PubMed  Google Scholar 

  • Oparka KJ, Roberts AG, Boevink P, Santa Cruz S, Roberts IM, Pradel KS, Imlau A, Kotlitzky 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 

  • Ormenese S, Havelange A, Bernier G, van der Schoot C (2002) The shoot apical meristem of Sinapis alba L. expands its central symplasmic field during the floral transition. Planta 215:67–78

    Article  CAS  PubMed  Google Scholar 

  • Passardi F, Penel C, Dunand C (2004) Performing the paradoxical: how plant peroxidases modify the cell wall. Trends Plant Sci 9:534–540

    Article  CAS  PubMed  Google Scholar 

  • Rinne PL, Kaikuranta PM, van der Schoot C (2001) The shoot apical meristem restores its symplasmic organization during chilling-induced release from dormancy. Plant J 26:249–264

    Article  CAS  PubMed  Google Scholar 

  • Roberts AG (2005) Plasmodesmal structure and development. In: Oparka KJ (ed) Plasmodesmata. Blackwell Publishing, Oxford, pp 1–32

    Chapter  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Ruiz-Medrano R, Xoconostle-Cazares B, Kragler F (2004) The plasmodesmatal transport pathway for homeotic proteins, silencing signals and viruses. Curr Opin Plant Biol 7:641–650

    Article  CAS  PubMed  Google Scholar 

  • Schopfer P (2006) Biomechanics of plant growth. Am J Bot 93:1415–1425

    Article  Google Scholar 

  • Schweikert C, Liszkay A, Schopfer P (2000) Scission of polysaccharides by peroxidase-generated hydroxyl-radicals. Phytochemistry 53:565–570

    Article  CAS  PubMed  Google Scholar 

  • Sowiński P, Bilska A, Barańska K, Fronk J, Kobus P (2007) Plasmodesmata density in vascular bundles in leaves of C4 grasses grown at different light conditions in respect to photosynthesis and photosynthate export efficiency. Environ Exp Bot 61:74–84

    Article  Google Scholar 

  • Stadler R, Lauterbach C, Sauer N (2005) Cell-to-cell movement of green fluorescent protein reveals post-phloem transport in the outer integument and identifies symplastic domains in Arabidopsis seeds and embryos. Plant Physiol 139:701–712

    Article  CAS  PubMed  Google Scholar 

  • Thordal-Christensen H, Zhang Z, Wei Y, Collinge DB (1997) Subcellular localization of H2O2 in plants: H2O2 accumulation in papillae and hypersensitive response during the barley–powdery mildew interaction. Plant J 11:1187–1194

    Article  CAS  Google Scholar 

  • van Bel AJE, Ehlers K (2000) Symplasmic organization of the transport phloem and the implications for photosynthate transfer to the cambium. In: Savidge RA, Barnett JR, Napier R (eds) Cell and molecular biology of wood formation. BIOS, Oxford, pp 85–99

    Google Scholar 

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

    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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Voeltz GK, Prinz WA, Shibata Y, Rist JM, Rapoport TA (2006) A class of membrane proteins shaping the tubular endoplasmic reticulum. Cell 124:573–586

    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

    Article  CAS  PubMed  Google Scholar 

  • Zambryski P (2004) Cell-to-cell transport of proteins and fluorescent tracers via plasmodesmata during plant development. J Cell Biol 162:165–168

    Article  Google Scholar 

  • Zhu T, Lucas WJ, Rost TL (1998a) Directional cell-to-cell communication in the Arabidopsis root apical meristem I. An ultrastructural and functional analysis. Protoplasma 203:35–47

    Article  Google Scholar 

  • Zhu T, O′Quinn RL, Lucas WJ, Rost TL (1998b) Directional cell-to-cell communication in the Arabidopsis root apical meristem II. Dynamics of plasmodesmal formation. Protoplasma 204:84–93

    Article  Google Scholar 

Download references

Acknowledgments

This work was supported by grants of the Deutsche Forschungsgemeinschaft (BE 1925/4-1, 4-2). Microinjections were performed by L. Ait-Hsiko (2002, Diploma-Thesis, University of Giessen). For TEM, the equipment of the Zentrale Biotechnische Betriebseinheit, University of Giessen was used. We thank PD Dr. Günter Lochnit, University of Giessen for his help with the MALDI-TOF–MS analysis.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Katrin Ehlers.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ehlers, K., van Bel, A.J.E. Dynamics of plasmodesmal connectivity in successive interfaces of the cambial zone. Planta 231, 371–385 (2010). https://doi.org/10.1007/s00425-009-1046-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-009-1046-8

Keywords

Navigation