Skip to main content

A model system for analyzing intercellular communication through plasmodesmata using moss protonemata and leaves

Journal of Plant Research volume 128, pages 63–72 (2015)Cite this article

Abstract

Plant growth, development, and environmental responses require the proper regulation of intercellular movement of signals and nutrients. For this, plants have specialized cytoplasmic channels, the plasmodesmata (PD), which allow the symplasmic movement of micro- and macromolecules between neighboring cells. Internal and external signals spatio-temporally regulate the movement of molecules through the PD to control plant development and environmental responses. Although some aspects of targeted movement of molecules have been revealed, the mechanisms of non-targeted, diffusible flow of molecules through PD, and its regulation and function, remain poorly understood, particularly at the cellular level. Previously, we developed a system to quantitatively analyze non-targeted movement of a photoconvertible fluorescent protein, Dendra2, at the single-cell level in the filamentous protonemata tissue of the moss Physcomitrella patens. In protonemata, one-dimensional intercellular communication can be easily observed and quantitatively analyzed at the cellular level. In this review, we describe how protonemata and leaves of P. patens can be used to study symplasmic movement through PD, and discuss how this system can help improve our understanding of PD regulation and function in development and environmental responses in plants.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

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

Fig. 1
Fig. 2
Fig. 3

References

  • Adam V, Nienhaus K, Bourgeois D, Nienhaus GU (2009) Structural basis of enhanced photoconversion yield in green fluorescent protein-like protein Dendra2. Biochemistry 48:4905–4915

    CAS  PubMed  Article  Google Scholar 

  • Ashton N, Grimsley N, Cove D (1979) Analysis of gametophytic development in the moss, Physcomitrella patens, using auxin and cytokinin resistant mutants. Planta 144:427–435

    CAS  PubMed  Article  Google Scholar 

  • Benitez-Alfonso Y (2014) Symplastic intercellular transport from a developmental perspective. J Exp Bot:eru067

  • 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

    CAS  PubMed  Article  Google Scholar 

  • Bilska A (2013) Regulation of intercellular transport through plasmodesmata under abiotic stresses. In: Sokolowska K, Pawel S (eds) Symplasmic transport in vascular plants. Springer, New York, pp 83–100

    Chapter  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

  • Burch-Smith TM, Zambryski PC (2012) Plasmodesmata paradigm shift: regulation from without versus within. Annu Rev Plant Biol 63:239–260

    CAS  PubMed  Article  Google Scholar 

  • Burch-Smith TM, Stonebloom S, Xu M, Zambryski PC (2011) Plasmodesmata during development: re-examination of the importance of primary, secondary, and branched plasmodesmata structure versus function. Protoplasma 248:61–74

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Carlsbecker A, Lee J-Y, Roberts CJ, Dettmer J, Lehesranta S, Zhou J, Lindgren O, Moreno-Risueno MA, Vatén A, Thitamadee S (2010) Cell signalling by microRNA165/6 directs gene dose-dependent root cell fate. Nature 465:316–321

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Chen H, Ahmad M, Rim Y, Lucas WJ, Kim JY (2013) Evolutionary and molecular analysis of Dof transcription factors identified a conserved motif for intercellular protein trafficking. New Phytol 198:1250–1260

    CAS  PubMed  Article  Google Scholar 

  • Chopra R, Kapur A (1989) Effect of abscisic acid and kinetin on protonemal differentiation in Timmiella anomala. Plant Sci 61:203–206

    CAS  Article  Google Scholar 

  • Christensen NM, Faulkner C, Oparka K (2009) Evidence for unidirectional flow through plasmodesmata. Plant Physiol 150:96–104

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Chudakov DM, Lukyanov S, Lukyanov KA (2007) Tracking intracellular protein movements using photoswitchable fluorescent proteins PS-CFP2 and Dendra2. Nat Protoc 2:2024–2032

    CAS  PubMed  Article  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

  • Cove D, Bezanilla M, Harries P, Quatrano R (2006) Mosses as model systems for the study of metabolism and development. Ann Rev Plant Biol 57:497–520

    CAS  Article  Google Scholar 

  • Crawford KM, Zambryski PC (1999) Plasmodesmata signaling: many roles, sophisticated statutes. Curr Opin Plant Biol 2:382–387

    CAS  PubMed  Article  Google Scholar 

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

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Dashevskaya S, Kopito RB, Friedman R, Elbaum M, Epel BL (2008) Diffusion of anionic and neutral GFP derivatives through plasmodesmata in epidermal cells of Nicotiana benthamiana. Protoplasma 234:13–23

    CAS  PubMed  Article  Google Scholar 

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

    PubMed Central  PubMed  Article  Google Scholar 

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

    Article  Google Scholar 

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

    CAS  Google Scholar 

  • Duckett JG, Schmid AM, Ligrone R (1998) Protonemal morphogenesis. In: Bates JW, Ashton NW, Duckett JG (eds) Bryology for the Twenty-first Century. Maney, Leeds, pp 223–246

    Google Scholar 

  • Durbak A, Yao H, McSteen P (2012) Hormone signaling in plant development. Curr Opin Plant Biol 15:92–96

    CAS  PubMed  Article  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

  • Epel BL, Erlanger MA (1991) Light regulates symplastic communication in etiolated corn seedlings. Physiol Plant 83:149–153

    CAS  Article  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

  • Faulkner C, Petutschnig E, Benitez-Alfonso Y, Beck M, Robatzek S, Lipka V, Maule AJ (2013) LYM2-dependent chitin perception limits molecular flux via plasmodesmata. Proc Natl Acad Sci USA 110:9166–9170

    CAS  PubMed Central  PubMed  Article  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

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Furuta K, Lichtenberger R, Helariutta Y (2012) The role of mobile small RNA species during root growth and development. Curr Opin Cell Biol 24:211–216

    CAS  PubMed  Article  Google Scholar 

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

    PubMed Central  PubMed  Article  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

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Goode JA, Stead AD, Duckett JG (1993) Redifferentiation of moss protonemata: an experimental and immunofluorescence study of brood cell formation. Canad J Bot 71:1510–1519

    Article  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

  • Han X, Hyun TK, Zhang M, Kumar R, E-J Koh, Kang B-H, Lucas WJ, Kim J-Y (2014) Auxin-callose-mediated plasmodesmal gating is essential for tropic auxin gradient formation and signaling. Dev Cell 28:132–146

    CAS  PubMed  Article  Google Scholar 

  • Harrison CJ, Roeder AH, Meyerowitz EM, Langdale JA (2009) Local cues and asymmetric cell divisions underpin body plan transitions in the moss Physcomitrella patens. Curr Biol 19:461–471

    CAS  PubMed  Article  Google Scholar 

  • Heidstra R, Sabatini S (2014) Plant and animal stem cells: similar yet different. Nat Rev Mol Cell Biol 15:301–312

    CAS  PubMed  Article  Google Scholar 

  • Hisanaga T, Miyashima S, Nakajima K (2014) Small RNAs as positional signal for pattern formation. Curr Opin Plant Biol 21:37–42

    CAS  PubMed  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

    CAS  PubMed  Article  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 symplastic unloading of the protein into sink tissues. Plant Cell 11:309–322

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Ito K, Ren J, Fujita T (2014) Conserved function of Rho-related Rop/RAC GTPase signaling in regulation of cell polarity in Physcomitrella patens. Gene 544:241–247

    CAS  PubMed  Article  Google Scholar 

  • Khandelwal A, Cho S, Marella H, Sakata Y, Perroud PF, Pan A, Quatrano R (2010) Role of ABA and ABI3 in desiccation tolerance. Science 327:546–546

  • Kim I, Zambryski PC (2005) Cell-to-cell communication via plasmodesmata during Arabidopsis embryogenesis. Curr Opin Plant Biol 8:593–599

    CAS  PubMed  Article  Google Scholar 

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

    CAS  PubMed Central  PubMed  Article  Google Scholar 

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

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Kitagawa M, Fujita T (2013) Quantitative imaging of directional transport through plasmodesmata in moss protonemata via single-cell photoconversion of Dendra2. J Plant Res 126:577–585

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Kofuji R, Hasebe M (2014) Eight types of stem cells in the life cycle of the moss Physcomitrella patens. Curr Opin Plant Biol 17:13–21

    PubMed  Article  Google Scholar 

  • Kong D, Karve R, Willet A, Chen M-K, Oden J, Shpak ED (2012) Regulation of plasmodesmatal permeability and stomatal patterning by the glycosyltransferase-like protein KOBITO1. Plant Physiol 159:156–168

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Kubo M, Imai A, Nishiyama T, Ishikawa M, Sato Y, Kurata T, Hiwatashi Y, Reski R, Hasebe M (2013) System for stable β-estradiol-inducible gene expression in the moss Physcomitrella patens. PLoS One 8:e77356

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Lee J-Y (2014) New and old roles of plasmodesmata in immunity and parallels to tunneling nanotubes. Plant Sci 221:13–20

    PubMed  Article  Google Scholar 

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

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Lew RR (2005) Mass flow and pressure-driven hyphal extension in Neurospora crassa. Microbiology 151:2685–2692

    CAS  PubMed  Article  Google Scholar 

  • Lew RR (2011) How does a hypha grow? The biophysics of pressurized growth in fungi. Nat Rev Microbiol 9:509–518

    CAS  PubMed  Article  Google Scholar 

  • Liarzi O, Epel BL (2005) Development of a quantitative tool for measuring changes in the coefficient of conductivity of plasmodesmata induced by developmental, biotic, and abiotic signals. Protoplasma 225:67–76

    CAS  PubMed  Article  Google Scholar 

  • Liesche J, Schulz A (2012a) In vivo quantification of cell coupling in plants with different phloem-loading strategies. Plant Physiol 159:355–365

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Liesche J, Schulz A (2012b) Quantification of plant cell coupling with three-dimensional photoactivation microscopy. J Microsc 247:2–9

    CAS  PubMed  Article  Google Scholar 

  • Martens HJ, Hansen M, Schulz A (2004) Caged probes: a novel tool in studying symplasmic transport in plant tissues. Protoplasma 223:63–66

    CAS  PubMed  Article  Google Scholar 

  • Minami A, Nagao M, Arakawa K, Fujikawa S, Takezawa D (2003) Abscisic acid-induced freezing tolerance in the moss Physcomitrella patens is accompanied by increased expression of stress-related genes. J Plant Physiol 160:475–483

    CAS  PubMed  Article  Google Scholar 

  • Miyashima S, Koi S, Hashimoto T, Nakajima K (2011) Non-cell-autonomous microRNA165 acts in a dose-dependent manner to regulate multiple differentiation status in the Arabidopsis root. Development 138:2303–2313

    CAS  PubMed  Article  Google Scholar 

  • Moore-Gordon CS, Cowan AK, Bertling I, Botha CEJ, Cross RHM (1998) Symplastic solute transport and avocado fruit development: a decline in cytokinin/ABA ratio is related to appearance of the Hass small fruit variant. Plant Cell Physiol 39:1027–1038

    CAS  Article  Google Scholar 

  • Oparka K, Boevink P (2005) Techniques for imaging intercellular transport. In: Oparka KJ (ed) Plasmodesmata annual plant reviews, vol 18. Blackwell, Oxford, pp 241–262

    Chapter  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, Roberts AG, Boevink P, Santa Cruz S, Roberts L, 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

    CAS  PubMed  Article  Google Scholar 

  • Overall RL, Liu DY, Barton DA (2013) Plasmodesmata: new perspectives on old questions. In: Sokolowska K, Pawel S (eds) Symplasmic transport in vascular plants. Springer, New York, pp 217–244

    Chapter  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

    CAS  PubMed  Article  Google Scholar 

  • Pillitteri LJ, Torii KU (2012) Mechanisms of stomatal development. Ann Rev Plant Biol 63:591–614

    CAS  Article  Google Scholar 

  • Piršelová B, Mistríková V, Libantová J, Moravčíková J, Matušíková I (2012) Study on metal-triggered callose deposition in roots of maize and soybean. Biologia 67:698–705

    Article  Google Scholar 

  • Pressel S, Ligrone R, Duckett JG (2006) Effects of de-and rehydration on food-conducting cells in the moss Polytrichum formosum: a cytological study. Ann Bot 98:67–76

    PubMed Central  PubMed  Article  Google Scholar 

  • Pressel S, Ligrone R, Duckett JG (2008) Cellular differentiation in moss protonemata: a morphological and experimental study. Ann Bot 102:227–245

    PubMed Central  PubMed  Article  Google Scholar 

  • Radford JE, White RG (2011) Inhibitors of myosin, but not actin, alter transport through Tradescantia plasmodesmata. Protoplasma 248:205–216

    CAS  PubMed  Article  Google Scholar 

  • Rensing SA, Lang D, Zimmer AD, Terry A, Salamov A, Shapiro H, Nishiyama T, Perroud PF, Lindquist EA, Kamisugi Y, Tanahashi T, Sakakibara K, Fujita T, Oishi K, Shin IT, Kuroki Y, Toyoda A, Suzuki Y, Hashimoto S, Yamaguchi K, Sugano S, Kohara Y, Fujiyama A, Anterola A, Aoki S, Ashton N, Barbazuk WB, Barker E, Bennetzen JL, Blankenship R, Cho SH, Dutcher SK, Estelle M, Fawcett JA, Gundlach H, Hanada K, Heyl A, Hicks KA, Hughes J, Lohr M, Mayer K, Melkozernov A, Murata T, Nelson DR, Pils B, Prigge M, Reiss B, Renner T, Rombauts S, Rushton PJ, Sanderfoot A, Schween G, Shiu SH, Stueber K, Theodoulou FL, Tu H, Van de Peer Y, Verrier PJ, Waters E, Wood A, Yang L, Cove D, Cuming AC, Hasebe M, Lucas S, Mishler BD, Reski R, Grigoriev IV, Quatrano RS, Boore JL (2008) The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319:64–69

    CAS  PubMed  Article  Google Scholar 

  • Rinne PLH, 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

    CAS  PubMed  Article  Google Scholar 

  • Rivas-San Vicente M, Plasencia J (2011) Salicylic acid beyond defence: its role in plant growth and development. J Exp Bot 62:3321–3338

    CAS  PubMed  Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Ruan YL, Llewellyn DJ, Furbank RT (2001) The control of single-celled 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 Central  PubMed  Google Scholar 

  • Sakakibara K, Nishiyama T, Deguchi H, Hasebe M (2008) Class 1 KNOX genes are not involved in shoot development in the moss Physcomitrella patens but do function in sporophyte development. Evol Dev 10:555–566

    CAS  PubMed  Article  Google Scholar 

  • Salmon MS, Bayer EM (2012) Dissecting plasmodesmata molecular composition by mass spectrometry-based proteomics. Front Plant Sci 3

  • Schaefer DG, Zryd JP (1997) Efficient gene targeting in the moss Physcomitrella patens. Plant J 11:1195–1206

    CAS  PubMed  Article  Google Scholar 

  • Schlereth A, Möller B, Liu W, Kientz M, Flipse J, Rademacher EH, Schmid M, Jürgens G, Weijers D (2010) MONOPTEROS controls embryonic root initiation by regulating a mobile transcription factor. Nature 464:913–916

    CAS  PubMed  Article  Google Scholar 

  • Schnepf E, Reinhard C (1997) Brachycytes in Funaria protonemate: induction by abscisic acid and fine structure. J Plant Physiol 151:166–175

    CAS  Article  Google Scholar 

  • Schnepf E, Sawidis T (1991) Filament disruption in Funaria protonemata: occlusion of plasmodesmata. Bot Acta 104:98–102

    Article  Google Scholar 

  • Schuette S, Wood AJ, Geisler M, Geisler-Lee J, Ligrone R, Renzaglia KS (2009) Novel localization of callose in the spores of Physcomitrella patens and phylogenomics of the callose synthase gene family. Ann Bot 103:749–756

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Schulz A (1995) Plasmodesmal widening accompanies the short-term increase in symplasmic phloem unloading in pea root-tips under osmotic-stress. Protoplasma 188:22–37

    Article  Google Scholar 

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

    CAS  Article  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

    CAS  PubMed  Article  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

    CAS  PubMed  Article  Google Scholar 

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

    CAS  Article  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

    CAS  PubMed Central  PubMed  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 JE, 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

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Uenaka H, Wada M, Kadota A (2005) Four distinct photoreceptors contribute to light-induced side branch formation in the moss Physcomitrella patens. Planta 222:623–631

    CAS  PubMed  Article  Google Scholar 

  • van der Schoot C, Rinne PLH (2011) Dormancy cycling at the shoot apical meristem: transitioning between self-organization and self-arrest. Plant Sci 180:120–131

    PubMed  Article  Google Scholar 

  • Vatén A, Dettmer J, Wu S, Stierhof Y-D, Miyashima S, Yadav SR, Roberts CJ, Campilho A, Bulone V, Lichtenberger R (2011) Callose biosynthesis regulates symplastic trafficking during root development. Dev Cell 21:1144–1155

    PubMed  Article  Google Scholar 

  • Waigmann E, Zambryski P (2000) Trichome plasmodesmata: a model system for cell-to-cell movement. Adv Bot Res 31:261–283

    Article  Google Scholar 

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

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Wu S, Gallagher KL (2011) Mobile protein signals in plant development. Curr Opin Plant Biol 14:563–570

    CAS  PubMed  Article  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

  • Wu XL, Dinneny JR, Crawford KM, Rhee Y, Citovsky V, Zambryski PC, Weigel D (2003) Modes of intercellular transcription factor movement in the Arabidopsis apex. Development 130:3735–3745

    CAS  PubMed  Article  Google Scholar 

  • Wu S, Koizumi K, MacRae-Crerar A, Gallagher KL (2011) Assessing the utility of photoswitchable fluorescent proteins for tracking intercellular protein movement in the Arabidopsis root. PLoS One 6:e27536

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Yadav SR, Yan D, Sevilem I, Helariutta Y (2014) Plasmodesmata-mediated intercellular signaling during plant growth and development. Front Plant Sci 5:44

    PubMed Central  PubMed  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

    CAS  PubMed  Article  Google Scholar 

  • Zimmer AD, Lang D, Buchta K, Rombauts S, Nishiyama T, Hasebe M, Van de Peer Y, Rensing SA, Reski R (2013) Reannotation and extended community resources for the genome of the non-seed plant Physcomitrella patens provide insights into the evolution of plant gene structures and functions. BMC Gen 14:498

    CAS  Article  Google Scholar 

Download references

Acknowledgments

We thank Drs. Yoshikatsu Sato, Kotaro Yamamoto, Masaaki Watahiki and Mr. Bao Liang for valuable discussions through this research. We also thank Drs. Konstantin Lukyanov, Minoru Kubo and Mitsuyasu Hasebe for kindly providing vectors, pDendra2-C and pT1OG, respectively. We apologize to any authors whose papers have not been cited due to the space limitations in the article. This work was supported, in part, by grants-in-aid from the Ministry of Education, Culture, Sports, Science and Technology of Japan and the Japan Society for the Promotion of Science to T.F. M.K. was the recipient of a Research Fellowship for Young Scientists from the Japan Society for the Promotion of Science, and a Grants-in-Aid for Scientific Research for Plant Graduate Students from Nara Institute of Science and Technology, the Ministry of Education, Culture, Sports, Science, and Technology.

Conflict of interest

The authors have declared that no competing interests exist.

Author information

Authors and Affiliations

  1. Center for Sustainable Resource Science, RIKEN, 1-7-22, Suehiro, Tsurumi, Yokohama, 230-0045, Japan

    Munenori Kitagawa

  2. Department of Biological Sciences, Faculty of Science, Hokkaido University, Kita 10 Nishi 8, Kita-ku, Sapporo, 060-0810, Japan

    Tomomichi Fujita

Authors
  1. Munenori Kitagawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tomomichi Fujita
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Tomomichi Fujita.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Kitagawa, M., Fujita, T. A model system for analyzing intercellular communication through plasmodesmata using moss protonemata and leaves. J Plant Res 128, 63–72 (2015). https://doi.org/10.1007/s10265-014-0690-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10265-014-0690-7

Keywords

  • Plasmodesmata
  • Physcomitrella patens
  • Photoconvertible fluorescent protein