Abstract
Plant cells exchange developmental signals, distribute nutrients and ribonucleoprotein complexes through dynamic intercellular channels termed plasmodesmata (PD). Multidisciplinary investigations over the last decade have provided evidence that plasmodesmatal regulation is critical to various basic plant functions, such as development, host-pathogen interactions, and systemic RNA-silencing. This review highlights the cell-to-cell transport of micro- and macromolecules via PD during embryo and seedling growth.
Similar content being viewed by others
Literature cited
Atkins D, Hull R, Wells B, Roberts K, Moore R Beachy RN (1991) The tobacco mosaic virus 30K movement protein in transgenic tobacco plants is localized to plasmodesmata. J Gen Virol72: 209–211
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 Physiol126: 39–46
Baulcombe D (2002) RNA silencing. Curr Biol12: R82–84
Berleth T, Chatfield S (2002) Embryogenesis: Pattern formation from a single cell,In C Somerville, E Meyerowitz, eds, The Arabidopsis Book. American Society of Plant Biologists, Rockville, pp 1–22
Blackman LM, Harper JD, Overall RL (1999) Localization of a centrin-like protein to higher plant plasmodesmata. Eur J Cell Biol78: 297–304
Cilia ML, Jackson D (2004) Plasmodesmata form and function. Curr Opin Cell Biol16: 500–506
Cutler SR, Ehrhardt DW, Griffitts JS, Somerville CR (2000) Random CFP::cDNA fusions enable visualization of subcellular structures in cells ofArabidopsis at a high frequency. Proc Natl Acad Sci USA97: 3718–3723
Ding B, Itaya A, Qi Y (2003) Symplasmic protein and RNA traffic: Regulatory points and regulatory factors. Curr Opin Plant Biol6: 596–602
Duckett CM, Oparka KJ, Prior DAM, Dolan L, Roberts K (1994) Dye-coupling in the root epidermis ofArabidopsis is progressively reduced during development. Development120: 3247–3255
Erwee MG, Goodwin PB (1985) Symplast domains in extrastellar tissues ofEgeria densa Planch. Planta163: 9–19
Escobar NM, Haupt S, Thow G, Boevink P, Chapman S, Oparka K (2003) High throughput viral expression of cDNA-green fluorescent protein fusions reveals novel subcellular addresses and identifies unique proteins that interact with plasmodesmata. Plant Cell15: 1507–1523
Faulkner C, Brandom J, Maule A, Oparka K (2005a) Plasmodesmata 2004: Surfing the symplasm. Plant Physiol137: 607–610
Faulkner CR, Blackman LM, Cordwell SJ, Overall RL (2005b) Proteomic identification of putative plasmodesmatal proteins fromChara corallina. Proteomics5: 2866–2875
Ghoshroy S, Lartey R, Sheng J, Citovsky V (1997) Transport of proteins and nucleic acids through plasmodesmata. Annu Rev Plant Physiol Plant Mol Biol48: 27–50
Hake S (2001) Transcription factors on the move. Trends Genet17: 2–3
Heinlein M, Epel BL (2004) Macromolecular transport and signaling through plasmodesmata. Intl Rev Cytol235: 93–164
Johnston D, Nusslein-Volhard C (1992) The origin of pattern and polarity in theDrosophila embryo. Cell68: 201–219
Jurgens G, Mayer U (1994)Arabidopsis, In J Bard, ed, A Colour Atlas of Developing Embryos. Wolfe, London, pp 7–21
Kim I, Cho E, Crawford K, Hempel FD, Zambryski PC (2005b) Cell-to-cell movement of CFP during embryogenesis and early seedling development inArabidopsis. Proc Natl Acad Sci USA 102:2227–2231
Kim I, Hempel FD, Sha K, Pfluger J, Zambryski PC (2002) Identification of a developmental transition in plasmodesmatal function during embryogenesis inArabidopsis thaliana. Development129: 1261–1272
Kim I, Kobayashi K, Cho E, Zambryski PC (2005a) Subdomains for transport via plasmodesmata corresponding to the apical-basal axis are established duringArabidopsis embryogenesis. Proc Natl Acad Sci USA102: 11945–11950
Kim JY (2005) Regulation of short-distance transport of RNA and protein. Curr Opin Plant Biol8: 45–52
Kim JY, Yuan Z, Jackson D (2003; Developmental regulation and significance of KNOX protein trafficking inArabidopsis. Development130: 4351–4362
Kurata T, Okada K, Wada T (2005) Intercellular movement of transcription factors. Curr Opin Plant Biol8: 600–605
Kwiatkowska M (1999) Plasmodesmal coupling and cell differentiation in algae,In A van Bel, W van Kesteren, eds, Plasmodesmata: Structure, Function, Role in Cell Communication. Springer, Berlin, Heidelberg, New York, pp 205–224
Laux T, Wurschum T, Breuninger H (2004) Genetic regulation of embryonic pattern formation. Plant Cell16: S190–202
Lee JY, Taoka K, Yoo BC, Ben-Nissan G, Kim DJ, Lucas WJ (2005) Plasmodesmal-associated protein kinase in tobacco andArabidopsis recognizes a subset of non-cell-autonomous proteins. Plant Cell17: 2817–2831
Lee JY, Yoo BC, Rojas MR, Gomez-Ospina N, Staehelin LA, Lucas WJ (2003) Selective trafficking of non-cell-autonomous proteins mediated by NtNCAPP1. Science299: 392–396
Lucas WJ, Lee JY (2004) Plasmodesmata as a supracellular control network in plants. Nat Rev Mol Cell Biol5: 712–726
Mansfield SG, Briarty LG (1991) Early embryogenesis inArabidopsis thaliana: II. The developing embryo. Can J Bot69: 461–476
McLean BG, Hempel FD, Zambryski PC (1997) Plant intercellular communication via plasmodesmata. Plant Cell9: 1043–1054
Nakajima K, Sena G, Nawy T, Benfey PN (2001) Intercellular movement of the putative transcription factor SHR in root patterning. Nature413: 307–311
Oparka KJ (2004) Getting the message across: How do plant cells exchange macromolecular complexes? Trends Plant Sci9: 33–41
Oparka KJ, Duckett CM, Prior DAM, Fisher DB (1994) Real-time imaging of phloem unloading in the root tip ofArabidopsis. Plant J6: 759–766
Poethig R, Coe E, Johri M (1986) Cell lineage patterns in maize embryogenesis: A clonal analysis. Dev Biol117: 392–404
Provencher LM, Miao L, Sinha N, Lucas WJ (2001) Sucrose export defectivel encodes a novel protein implicated in chloroplast-to-nucleus signaling. Plant Cell13: 1127–1141
Roberts AG (2005) Plasmodesmal structure and development,In KJ Oparka, ed, Plasmodesmata. Blackwell, Oxford, pp 1–32
Russin WA, Evert RF, Vanderveer PJ, Sharkey TD, Briggs SP (1996) Modification of a specific class of plasmodesmata and loss of sucrose export ability in thesucrose export defective 7 maize mutant. Plant Cell8: 645–658
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 Cell17: 1788–1800
Saulsberry A, Martin PR, O’Brien T, Sieburth LE, Pickett FB (2002) The induced sectorArabidopsis apical embryonic fate map. Development129: 3403–3410
Scheres B, Wolkenfelt H, Willemsen V, Terlouw M, Lawson E, Dean C, Weisbeek P (1994) Embryonic origin of theArabidopsis primary root and root meristem initials. Development120: 2475–2487
Stadler R, Lauterbach C, Sauer N (2005a) Cell-to-cell movement of green fluorescent protein reveals post-phloem transport in the outer integument and identifies symplastic domains inArabidopsis seeds and embryos. Plant Physiol139: 701–712
Stadler R, Wright KM, Lauterbach C, Amon G, Gahrtz M, Feuerstein A, Oparka KJ, Sauer N (2005b) Expression of GFP-fusions inArabidopsis companion cells reveals non-specific protein trafficking into sieve elements and identifies a novel post-phloem domain in roots. Plant J41: 319–331
Tilney LG, Cooke TJ, Connelly PS, Tilney MS (1990) The distribution of plasmodesmata and its relationship to morphogenesis in fern gametophytes. Development110: 1209–1221
Tomenius K, Clapham D, Meshi T (1987) Localization by immunogold cytochemistry of the virus coded 30 kD protein in plasmodesmata of leaves infected with tobacco mosaic virus. Virology160: 363–371
van der Schoot C, Deitrich MA, Storms M, Verbeke JA, Lucas WJ (1995) Establishment of a cell-to-cell communication pathway between separate carpels during gynoecium development. Planta195: 450–455
van der Schoot C, Rinne P (1999) The symplastic organization of the shoot apical meristem,In A van Bel, W van Kesteren, eds, Plasmodesmata: Structure, Function, Role in Cell Communication. Springer, Berlin, Heidelberg, New York, pp 357
van der Schoot C, van Bel A (1990) Mapping membrane potential differences and dye-coupling in internodal tissues of tomato(Solarium lycopersicum L). Planta182: 9–21
Voinnet O (2002) RNA silencing: small RNAs as ubiquitous regulators of gene expression. Curr Opin Plant Biol5: 444–451
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, inArabidopsis root epidermal cell differentiation. Development129: 5409–5419
Wolpert L (2002) Principles of Development. Oxford University Press, New York
Wu X, Dinneny JR, Crawford KM, Rhee Y, Citovsky V, Zambryski PC, Weigel D (2003) Modes of intercellular transcription factor movement in theArabidopsis apex. Development130: 3735–3745
Wu X, Weigel D, Wigge PA (2002) Signaling in plants by intercellular RNA and protein movement. Genes Dev16: 151–158
Zambryski P (2004) Cell-to-cell transport of proteins and fluorescent tracers via plasmodesmata during plant development. J Cell Biol164: 165–168
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Kim, I. Cell-to-cell transport of macromolecules during early plant development. J. Plant Biol. 50, 266–273 (2007). https://doi.org/10.1007/BF03030654
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF03030654