Skip to main content

Developmental Control of Plasmodesmata Frequency, Structure, and Function

  • Chapter
  • First Online:
Symplasmic Transport in Vascular Plants

Abstract

The plant’s cell connections called plasmodesmata mediate symplasmic communication processes which play a crucial role in the control of plant development. Several developmental regulators, including a variety of transcription factor proteins and sRNA species, have been shown to move through plasmodesmata in order to regulate gene expression non-cell-autonomously on the transcriptional and posttranscriptional level. The symplasmic exchange of such regulatory molecules is a crucial element in the complex molecular networks controlling plant growth and morphogenesis. It is generally accepted that plasmodesmal communication is essential for the coordination of cell-division activity, cell-fate specification, tissue patterning, and organogenesis. Dynamics of the plasmodesmal networks in the developing tissues are supposed to facilitate modulations of the intercellular communication pathways which correlate with the developmental requirements. The symplasmic organization can be modulated to cause morphogenetic switches in response to environmental or endogenous signals. In the present review, we summarize the distinct modes by which structural and functional alterations of the plasmodesmal networks can be achieved, and we discuss possible molecular control mechanisms. Moreover, we will give an overview on the programmed developmental changes in the number, structure, and in the functional state of plasmodesmata which occur in growing plant tissues, including embryos, leaves, roots, and shoots during primary and secondary growth, as well as during the transition to flowering.

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 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
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

  • Agusti J, Lichtenberger R, Schwarz M, Nehlin L, Greb T. Characterization of transcriptome remodeling during cambium formation identifies MOL1 and RUL1 as opposing regulators of secondary growth. PLoS Genet. 2011;7:e1001312.

    PubMed  CAS  Google Scholar 

  • Amari K, Boutant E, Hofmann C, Schmitt-Keichinger C, Fernandez-Calvino L, Didier P, et al. A family of plasmodesmal proteins with receptor-like properties for plant viral movement proteins. PLoS Pathog. 2010;6:e1001119.

    PubMed  Google Scholar 

  • Anwar K, Klemm RW, Condon A, Severin KN, Zhang M, Ghirlando R, et al. The dynamin-like GTP-ase Sey1p mediates homotypic ER fusions in S. cerevisiae. J Cell Biol. 2012;197:209–17.

    PubMed  CAS  Google Scholar 

  • Badelt K, White RG, Overall RL, Vesk M. Ultrastructural specializations of the wall sleeve around plasmodesmata. Am J Bot. 1994;81:1422–77.

    Google Scholar 

  • Barnett JL. Changes in the distribution of plasmodesmata in developing fibre-tracheid pit membranes of Sorbus aucuparia L. Ann Bot. 1987;59:269–79.

    Google Scholar 

  • Barton DA, Cole L, Collings DA, Liu DYT, Smith PMC, Day DA, et al. Cell-to-cell transport via the lumen of the endoplasmic reticulum. Plant J. 2011;66:806–17.

    PubMed  CAS  Google Scholar 

  • Bayer E, Thomas C, Maule A. Symplasmic domains in the Arabidopsis shoot apical meristem correlate with PDLP1 expression patterns. Plant Signal Behav. 2008;3:853–5.

    PubMed  Google Scholar 

  • Beebe DU, Russin WA. Plasmodesmata in the phloem-loading pathway. In: van Bel AJE, van Kesteren WJP, editors. Plasmodesmata: structure, function, role in cell communication. Berlin: Springer; 1999. p. 261–93.

    Google Scholar 

  • Benitez-Alfonso Y, Cilia M, San Roman A, Thomas C, Maule A, Hearn S, et al. Control of Arabidopsis meristem development by thioredoxin-dependent regulation of intercellular transport. Proc Natl Acad Sci USA. 2009;106:3615–20.

    PubMed  CAS  Google Scholar 

  • Benitez-Alfonso Y, Jackson D, Maule A. Redox regulation of intercellular transport. Protoplasma. 2011;248:131–40.

    PubMed  CAS  Google Scholar 

  • Bergmans ACJ, de Boer AD, Derksen JWM, van der Schoot C. The symplasmic coupling of L2-cells diminishes in early floral development of Iris. Planta. 1997;203:245–52.

    CAS  Google Scholar 

  • Bilska A, Sowiński P. Closure of plasmodesmata in maize (Zea mays) at low temperature: a new mechanism for inhibition of photosynthesis. Ann Bot. 2010;106:675–86.

    PubMed  CAS  Google Scholar 

  • Bitonti MB, Chiappetta A. Root apical meristem pattern: Hormone circuitry and transcriptional networks. In: Lüttge U, Beyschlag W, Büdel B, Francis D, editors. Progress in Botany 72, genetics, physiology, systematics, ecology. Berlin: Springer; 2011. p. 37–71.

    Google Scholar 

  • Blachutzik J, Demir F, Kreuzer I, Hedrich R, Harms GS. Methods of staining and visualization of sphingolipid enriched and non-enriched plasma membrane regions of Arabidopsis thaliana with fluorescent dyes and lipid analogues. Plant Methods. 2012;8:28. doi:10.1186/ 1746-4811-8-28.

    PubMed  CAS  Google Scholar 

  • Boevink P, Oparka K, Santa Cruz S, Martin B, Betteridge A, Hawes C. Stacks on the tracks: the plant Golgi apparatus traffics on an actin/ER network. Plant J. 1998;3:441–7.

    Google Scholar 

  • Burch-Smith TM, Zambryski PC. Loss of INCREASED SIZE EXCLUSION LIMIT (ISE)1 or ISE2 increases the formation of secondary plasmodesmata. Curr Biol. 2010;20:989–93.

    PubMed  CAS  Google Scholar 

  • Burch-Smith TM, Zambryski PC. Plasmodesmata paradigm shift: Regulation from without versus within. Annu Rev Plant Biol. 2012;63:239–60.

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Burch-Smith TM, Brunkard JO, Choi YG, Zambryski PC. Organelle-nucleus cross-talk regulates plant intercellular communication via plasmodesmata. Proc Natl Acad Sci USA. 2011b;108:E1451–60.

    PubMed  CAS  Google Scholar 

  • Burch-Smith TM, Cui Y, Zambryski PC. Reduced levels of class 1 reversibly glycosylated polypeptide increase intercellular transport via plasmodesmata. Plant Signal Behav. 2012;7:62–7.

    PubMed  CAS  Google Scholar 

  • Cantrill LC, Overall RL, Goodwin PB. Cell-to-cell communication via plant endomembranes. Cell Biol Int. 1999;23:653–61.

    PubMed  CAS  Google Scholar 

  • Carlsbecker A, Lee JY, Roberts CJ, Dettmer J, Lehesranta S, Zhou J, et al. Cell signalling by microRNA165/6 directs gene dose dependent root cell fate. Nature. 2010;465:316–21.

    PubMed  CAS  Google Scholar 

  • Carraro N, Peaucelle A, Laufs P, Traas J. Cell differentiation and organ initiation at the shoot apical meristem. Plant Mol Biol. 2006;60:811–26.

    PubMed  CAS  Google Scholar 

  • Cederholm HM, Iyer-Pascuzzi AS, Benfey PN. Patterning the primary root in Arabidopsis. WIREs Dev Biol. 2012;1:675–91.

    CAS  Google Scholar 

  • Chen X-Y, Kim J-Y. Transport of macromolecules through plasmodesmata and the phloem. Physiol Plant. 2006;126:560–71.

    CAS  Google Scholar 

  • Chen CN, Chen HR, Yeh SY, Vittore G, Ho TH. Autophagy is enhanced and floral development is impaired in AtHVA22d RNA interference Arabidopsis. Plant Physiol. 2009;149:1679–89.

    PubMed  CAS  Google Scholar 

  • Chen J, Stefano G, Brandizzi F, Zheng H. Arabidopsis RHD3 mediates the generation of the tubular ER network and is required for Golgi distribution and motility in plant cells. J Cell Sci. 2011;124:2241–52.

    PubMed  CAS  Google Scholar 

  • Chen J, Doyle C, Qi X, Zheng H. The endoplasmic reticulum: a social network in plant cells. J Integr Plant Biol. 2012;54:840–50.

    PubMed  CAS  Google Scholar 

  • Choob VV, Sinyushin AA. Flower and shoot fasciation: from phenomenology to the construction of models of apical meristem transformations. Russ J Plant Physiol. 2012;59:530–45.

    CAS  Google Scholar 

  • Chow C-M, Neto H, Foucart C, Moore I. Rab-A2 and Rab-A3 GTPases define a trans-Golgi endosomal membrane domain in Arabidopsis that contributes substantially to the cell plate. Plant Cell. 2008;20:101–23.

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Cleland RE, Fujiwara T, Lucas WJ. Plasmodesmal mediated cell-to-cell transport in wheat roots is modulated by anaerobic stress. Protoplasma. 1994;178:81–5.

    PubMed  CAS  Google Scholar 

  • Cook ME, Graham LE. Evolution of plasmodesmata. In: van Bel AJE, van Kesteren WJP, editors. Plasmodesmata: structure, function, role in cell communication. Berlin: Springer; 1999. p. 101–17.

    Google Scholar 

  • Cook ME, Graham LE, Botha CEJ, Lavin CA. Comparative ultrastructure of plasmodesmata of Chara and selected bryophytes: towards an elucidation of the evolutionary origin of plant plasmodesmata. Am J Bot. 1997;84:1169–78.

    PubMed  CAS  Google Scholar 

  • Cosgrove DJ. Growth of the plant cell wall. Nat Rev Mol Cell Biol. 2005;6:850–61.

    PubMed  CAS  Google Scholar 

  • Crawford KM, Zambryski PC. Non-targeted and targeted protein movement through plasmodesmata in leaves in different developmental and physiological states. Plant Physiol. 2001;125:1802–12.

    PubMed  CAS  Google Scholar 

  • Deeks MJ, Calcutt JR, Ingle EKS, Hawkins TJ, Chapman S, Richardson AC, et al. A superfamily of actin-binding proteins at the actin-membrane nexus of higher plants. Curr Biol. 2012;22:1595–600.

    PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Ding B, Haudenshield JS, Hull RJ, Wolf S, Beachy RN, Lucas WJ. Secondary plasmodesmata are specific sites of localization of the tobacco mosaic virus movement protein in transgenic tobacco plants. Plant Cell. 1992b;4:915–28.

    PubMed  CAS  Google Scholar 

  • Dodsworth S. A diverse and intricate signalling network regulates stem cell fate in the shoot apical meristem. Dev Biol. 2009;336:1–9.

    PubMed  CAS  Google Scholar 

  • Du J, Groover A. Transcriptional control of secondary growth and wood formation. J Integr Plant Biol. 2010;52:17–27.

    PubMed  CAS  Google Scholar 

  • Duckett CM, Oparka KJ, Prior DAM, Dolan L, Roberts K. Dye-coupling in the root epidermis of Arabidopsis is progressively reduced during development. Development. 1994;120:3247–55.

    CAS  Google Scholar 

  • Durbak A, Yao H, McSteen P. Hormone signaling in plant development. Curr Opin Plant Biol. 2012;15:92–6.

    PubMed  CAS  Google Scholar 

  • Ehlers K, Kollmann R. Formation of branched plasmodesmata in regenerating Solanum nigrum-protoplasts. Planta. 1996;199:126–38.

    CAS  Google Scholar 

  • Ehlers K, Kollmann R. Synchronization of mitotic activity in protoplast-derived Solanum nigrum L. microcallus is correlated with plasmodesmal connectivity. Planta. 2000;210:269–78.

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Ehlers K, van Bel AJE. The physiological and developmental consequences of plasmodesmal connectivity. In: van Bel AJE, van Kesteren WJP, editors. Plasmodesmata: structure, function, role in cell communication. Berlin: Springer; 1999. p. 243–60.

    Google Scholar 

  • Ehlers K, van Bel AJE. Dynamics of plasmodesmal connectivity in successive interfaces of the cambial zone. Planta. 2010;231:371–85.

    PubMed  CAS  Google Scholar 

  • Ehlers K, Schulz M, Kollmann R. Subcellular localization of ubiquitin in plant protoplasts and the function of ubiquitin in selective degradation of outer wall plasmodesmata in regenerating protoplasts. Planta. 1996;199:139–51.

    CAS  Google Scholar 

  • Ehlers K, Binding H, Kollmann R. The formation of symplasmic domains by plugging of plasmodesmata: a general event in plant morphogenesis? Protoplasma. 1999;209:181–92.

    Google Scholar 

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

    Google Scholar 

  • Elo A, Immanen J, Nieminen K, Helariutta Y. Stem cell function during plant vascular development. Sem Cell Dev Biol. 2009;20:1097–106.

    CAS  Google Scholar 

  • Esau K, Thorsch J. Sieve plate pores and plasmodesmata, the communication channels of the symplast: Ultrastructural aspects and developmental relations. Am J Bot. 1985;72:1641–53.

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Faulkner C, Akman OE, Bell K, Jeffree C, Oparka K. Peeking into pit fields: a multiple twinning model of secondary plasmodesmata formation in tobacco. Plant Cell. 2008;20:1504–18.

    PubMed  CAS  Google Scholar 

  • Fernandez-Calvino L, Faulkner C, Walshaw J, Saalbach G, Bayer E, Benitez-Alfonso Y, et al. Arabidopsis plasmodesmal proteome. PLoS One. 2011;6:e18880.

    PubMed  CAS  Google Scholar 

  • Fuchs M, van Bel AJE, Ehlers K. Season-associated modifications in symplasmic organization of the cambium in Populus nigra. Ann Bot. 2010a;105:375–87.

    PubMed  Google Scholar 

  • Fuchs M, Ehlers K, Will T, van Bel AJE. Immunolocalization indicates plasmodesmal trafficking of storage proteins during cambial reactivation in Populus nigra. Ann Bot. 2010b;106:385–94.

    PubMed  CAS  Google Scholar 

  • Fuchs M, van Bel AJE, Ehlers K. Do symplasmic networks in cambial zones correspond with secondary growth patterns. Protoplasma. 2011;248:141–51.

    PubMed  Google Scholar 

  • Furuta K, Lichtenberger R, Helariutta Y. The role of mobile small RNA species during root growth and development. Curr Opin Cell Biol. 2012;24:211–6.

    PubMed  CAS  Google Scholar 

  • Gisel A, Barella S, Hempel FD, Zambryski PC. Temporal and spatial regulation of symplastic trafficking during development in Arabidopsis thaliana apices. Development. 1999; 126:1879–89.

    PubMed  CAS  Google Scholar 

  • Gisel A, Hempel FD, Barella S, Zambryski P. Leaf-to-shoot apex movement of symplastic tracer is restricted coincident with flowering in Arabidopsis. Proc Natl Acad Sci USA. 2002; 99:1713–7.

    PubMed  CAS  Google Scholar 

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

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Guenoune-Gelbart D, Elbaum M, Sagi G, Levy A, Epel BL. Tobacco mosaic virus (TMV) replicase and movement protein function synergistically in facilitating TMV spread by lateral diffusion in the plasmodesmal desmotubule of Nicotiana benthamiana. Mol Plant Microbe Interact. 2008;21:335–45.

    PubMed  CAS  Google Scholar 

  • Gunning BES. Age-related and origin-related control of the numbers of plasmodesmata in cell walls of developing Azolla roots. Planta. 1978;143:181–90.

    Google Scholar 

  • Guo Y, Han L, Hymes M, Denver R, Clark SE. CLAVATA2 forms a distinct CLE-binding receptor complex regulating Arabidopsis stem cell specification. Plant J. 2010;63:889–900.

    PubMed  CAS  Google Scholar 

  • Guseman JM, Lee JS, Bogenschutz NL, Peterson KM, Virata RE, Xie B, et al. Dysregulation of cell-to-cell connectivity and stomatal patterning by loss-of function mutation in Arabidopsis CHORUS (GLUCAN SYNTHASE-LIKE8). Development. 2010;137:1731–41.

    PubMed  CAS  Google Scholar 

  • Hafke J, van Amerongen J-K, Kelling F, Furch AJU, Gaupels F, van Bel AJE. Thermodynamic battle for photosynthate acquisition between sieve tubes and adjoining parenchyma in transport phloem. Plant Physiol. 2005;138:1527–37.

    PubMed  CAS  Google Scholar 

  • Hepler PK. Endoplasmic reticulum in the formation of the cell plate and plasmodesmata. Protoplasma. 1982;111:121–33.

    Google Scholar 

  • Holdaway-Clarke TL. Regulation of plasmodesmal conductance. In: Oparka KJ, editor. Plasmodesmata, Annual Plant Reviews 18. Oxford, UK: Blackwell Publishing Ltd; 2005. p. 279–97.

    Google Scholar 

  • Holdaway-Clarke TL, Walker NA, Hepler PK, Overall RL. Physiological elevations in cytosolic free calcium by cold or ion injection results in transient closure of higher plant plasmodesmata. Planta. 2000;210:329–35.

    PubMed  CAS  Google Scholar 

  • Hou H-W, Zhou Y-T, Mwange K-N, Li W-F, He X-Q, Cui K-M. ABP1 expression regulated by IAA and ABA is associated with the cambium periodicity in Eucommia ulmoides Oliv. J Exp Bot. 2006;57:3857–67.

    PubMed  CAS  Google Scholar 

  • Hu J, Shibata Y, Voss C, Shemesh T, Li Z, Coughlin M, et al. Membrane proteins of the endoplasmic reticulum induce high-curvature tubules. Science. 2008;319:1247–50.

    PubMed  CAS  Google Scholar 

  • Hu J, Shibata Y, Zhu PP, Voss C, Rismanchi N, Prinz WA, et al. A class of dynamin-like GTPases involved in the generation of the tubular ER network. Cell. 2009;138:549–61.

    PubMed  CAS  Google Scholar 

  • Hu J, Prinz WA, Rapoport TA. Weaving the web of ER tubules. Cell. 2011;147:1226–31.

    PubMed  CAS  Google Scholar 

  • Hyun TK, Uddin MN, Rim Y, Kim J-Y. Cell-to-cell trafficking of RNA and RNA silencing through plasmodesmata. Protoplasma. 2011;248:101–16.

    PubMed  CAS  Google Scholar 

  • Imaichi R, Hiratsuka R. Evolution of the shoot apical meristem structures in vascular plants with respect to plasmodesmatal network. Am J Bot. 2007;94:1911–21.

    PubMed  Google Scholar 

  • Ispolatov I, Ackermann M, Doebeli M. Division of labour and the evolution of multicellularity. Proc R Soc B. 2012;279:1768–76.

    PubMed  Google Scholar 

  • Itaya A, Woo YM, Masuta C, Bao Y, Nelson RS, Ding B. Developmental regulation of intercellular protein trafficking through the plasmodesmata in tobacco leaf epidermis. Plant Physiol. 1998;118:373–85.

    PubMed  CAS  Google Scholar 

  • Jackson D. Transcription factor movement through plasmodesmata. In: Oparka KJ, editor. Plasmodesmata, Annual Plant Reviews 18. Oxford, UK: Blackwell Publishing Ltd; 2005. p. 113–34.

    Google Scholar 

  • Jo Y, Cho WK, Rim Y, Moon J, Chen XY, Chu H, et al. Plasmodesmal receptor-like kinases identified through analysis of rice cell wall extracted proteins. Protoplasma. 2011;248:191–203.

    PubMed  CAS  Google Scholar 

  • Katsaros C, Motomura T, Nagasato C, Galatis B. Diaphragm development in cytokinetic vegetative cells of brown algae. Bot. Mar. 2009;52:150–61.

    Google Scholar 

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

    CAS  Google Scholar 

  • Kempers R, Ammerlaan A, van Bel AJE. Symplasmic constriction and ultrastructural features of the sieve element/companion cell complex in the transport phloem of apoplasmically and symplasmically phloem-loading species. Plant Physiol. 1998;116:271–8.

    CAS  Google Scholar 

  • Kim JY, Yuan Z, Jackson D. Developmental regulation and significance of KNOX protein trafficking in Arabidopsis. Development. 2003;130:4351–62.

    PubMed  CAS  Google Scholar 

  • Kim I, Cho E, Crawford K, Hempel FB, Zambryski PC. Cell-to-cell movement of GFP during embryogenesis and early seedling development in Arabidopsis. Proc Natl Acad Sci USA. 2005a;102:2227–31.

    PubMed  CAS  Google Scholar 

  • Kim I, Kobayashi K, Cho E, Zambryski PC. Subdomains for transport via plasmodesmata corresponding to the apical-basal axis are established during Arabidopsis embryogenesis. Proc Natl Acad Sci USA. 2005b;102:11945–50.

    PubMed  CAS  Google Scholar 

  • Kinoshita A, Betsuyaku S, Osakabe Y, Mizuno S, Nagawa S, Stahl Y, et al. RPK2 is an essential receptor-like kinase that transmits the CLV3 signal in Arabidopsis. Development. 2010; 137:3911–20.

    PubMed  CAS  Google Scholar 

  • Kobayashi K, Kim I, Cho E, Zambryski P. Plasmodesmata and plant morphogenesis. In: Oparka KJ, editor. Plasmodesmata, Annual Plant Reviews 18. Oxford, UK: Blackwell Publishing Ltd; 2005. p. 90–112.

    Google Scholar 

  • Kobayashi K, Otegui MS, Krishnakumar S, Mindrinos M, Zambryski P. INCREASED SIZE EXCLUSION LIMIT 2 encodes a putative DEVH box RNA helicase involved in plasmodesmata function during Arabidopsis embryogenesis. Plant Cell. 2007;19:1885–97.

    PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Kollmann R, Glockmann C. Multimorphology and nomenclature of plasmodesmata in higher plants. In: van Bel AJE, van Kesteren WJP, editors. Plasmodesmata: structure, function, role in cell communication. Berlin: Springer; 1999. p. 149–72.

    Google Scholar 

  • Kong D, Karve R, Willet A, Chen M-K, Oden J, Shpak ED. Regulation of plasmodesmatal permeability and stomatal patterning by the glycosyltransferase-like protein KOBITO1. Plant Physiol. 2012;159:156–68.

    PubMed  CAS  Google Scholar 

  • Krizek BA, Fletcher JC. Molecular mechanisms of flower development: an armchair guide. Nature Rev Gen. 2005;6:688–98.

    CAS  Google Scholar 

  • Kwiatkowska M. Plasmodesmal coupling and cell differentiation in algae. In: van Bel AJE, van Kesteren WJP, editors. Plasmodesmata: structure, function, role in cell communication. Berlin: Springer; 1999. p. 205–24.

    Google Scholar 

  • Lachaud S, Catesson A-M, Bonnemain J-L. Structure and function of the vascular cambium. CR Acad Sci Paris. 1999;322:633–50.

    CAS  Google Scholar 

  • Lazzaro MD, Thomson WW. The vacuolar-tubular continuum in living trichomes of chickpea (Cicer arietinum) provides a rapid means of solute delivery from base to tip. Protoplasma. 1996;193:181–90.

    Google Scholar 

  • Lee JY, Taoka K, Yoo BC, Ben-Nissan G, Kim DJ, Lucas WJ. Plasmodesmal-associated protein kinase in tobacco and Arabidopsis recognizes a subset of non-cell-autonomous proteins. Plant Cell. 2005;17:2817–31.

    PubMed  CAS  Google Scholar 

  • Levy A, Erlanger M, Rosenthal M, Epel BL. A plasmodesmata associated β-1,3-glucanase in Arabidopsis. Plant J. 2007;49:669–82.

    PubMed  CAS  Google Scholar 

  • Li S, He Y, Zhao J, Zhang L, Sun M-X. Polar protein transport between apical and basal cells during tobacco early embryogenesis. Plant Cell Rep. 2013;32:285–91.

    PubMed  CAS  Google Scholar 

  • Lin S, Sun S, Hu J. Molecular basis for sculpting the endoplasmic reticulum membrane. Int J Biochem Cell Biol. 2012;44:1436–43.

    PubMed  CAS  Google Scholar 

  • Liszkay A, Kenk B, Schopfer P. Evidence for the involvement of cell wall peroxidase in the generation of hydroxyl radicals mediating extension growth. Planta. 2003;217:658–67.

    PubMed  CAS  Google Scholar 

  • Lucas WJ, Lee J-Y. Plasmodesmata as a supracellular control network in plants. Nature Rev Mol Cell Biol. 2004;5:712–26.

    CAS  Google Scholar 

  • Lucas WJ, Bouché-Pillon S, Jackson DP, Nguyen L, Baker L, Ding B, et al. Selective trafficking of KNOTTED1 homeodomain protein and its mRNA through plasmodesmata. Science. 1995;270:1980–3.

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Martens HJ, Roberts AG, Oparka KJ, Schulz A. Quantification of plasmodesmatal endoplasmic reticulum coupling between sieve elements and companion cells using fluorescence redistribution after photobleaching. Plant Physiol. 2006;142:471–80.

    PubMed  CAS  Google Scholar 

  • Martinière A, Lavagi I, Nageswaran G, Rolfe DJ, Maneta-Peyret L, Luu DT, et al. Cell wall constrains lateral diffusion of plant plasma-membrane proteins. Proc Natl Acad Sci USA. 2012;109:12805–10.

    PubMed  Google Scholar 

  • Maule A, Faulkner C, Benitez-Alfonso Y. Plasmodesmata “in communicado”. Frontiers in Plant Sci Plant Physiol. 2012;3:30.

    CAS  Google Scholar 

  • Milyaeva EL. Presumable role of plasmodesmata in floral signal transduction in shoot apical meristems of Rudbeckia and Perilla plants. Russ J Plant Physiol. 2007;54:498–506.

    CAS  Google Scholar 

  • Mongrand S, Stanislas T, Bayer EMF, Lherminier JJ, Simon-Plas F. Membrane rafts in plant cells. Trends Plant Sci. 2010;15:656–63.

    PubMed  CAS  Google Scholar 

  • Monzer J. Ultrastructure of secondary plasmodesmata formation in regenerating Solanum nigrum-protoplast cultures. Protoplasma. 1991;165:86–95.

    Google Scholar 

  • Moore-Gordon CS, Cowan AK, Bertling I, Botha CEJ, Cross RHM. 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. 1998;39:1027–38.

    CAS  Google Scholar 

  • Moubayidin L, Perilli S, Dello Ioio R, Di Mambro R, Costantino P, Sabatini S. The rate of cell differentiation controls the Arabidopsis root meristem growth phase. Curr Biol. 2010;20:1138–43.

    PubMed  CAS  Google Scholar 

  • Nagasato C, Inoue A, Mizuno M, Kanazawa K, Ojima T, Okuda K, et al. Membrane fusion process and assembly of cell wall during cytokinesis in the brown alga, Silvetia babingtonii (Fucales, Phaeophyceae). Planta. 2010;232:287–98.

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Nieminen K, Robischon M, Immanen J, Helariutta Y. Towards optimizing wood development in bioenergy trees. New Phytol. 2012;194:46–53.

    PubMed  CAS  Google Scholar 

  • Nilsson J, Karlberg A, Antti H, Lopez-Vernaza M, Mellerowicz E, Perrot-Rechenmann C, et al. Dissecting the molecular basis of the regulation of wood formation by auxin in hybrid aspen. Plant Cell. 2008;20:843–55.

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Oparka KJ, Prior DAM. Direct evidence for pressure-generated closure of plasmodesmata. Plant J. 1992;2:741–50.

    Google Scholar 

  • Oparka KJ, Duckett CM, Prior DAM, Fisher DB. Real-time imaging of phloem unloading in the root tip of Arabidopsis. Plant J. 1994;6:759–66.

    Google Scholar 

  • Oparka KJ, Robards AG, Boevink P, Santa Cruz S, Roberts I, Pradel KS, et al. Simple, but not branched, plasmodesmata allow the nonspecific trafficking of proteins in developing tobacco leaves. Cell. 1999;97:743–54.

    PubMed  CAS  Google Scholar 

  • Orfila C, Knox JP. Spatial regulation of pectic polysaccharides in relation to pit fields in cell walls of tomato fruit pericarp. Plant Physiol. 2000;122:775–82.

    PubMed  CAS  Google Scholar 

  • Ormenese S, Havelange A, Deltour R, Bernier G. The frequency of plasmodesmata increases early in the whole shoot apical meristem of Sinapis alba L. during floral transition. Planta. 2000;211:370–5.

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Ormenese S, Bernier G, Périlleux C. Cytokinin application to the shoot apical meristem of Sinapis alba enhances secondary plasmodesmata formation. Planta. 2006;224:1481–4.

    PubMed  CAS  Google Scholar 

  • Orso G, Pendin D, Liu S, Tosetto J, Moss TJ, Faust JE, et al. Homotypic fusion of ER membranes requires the dynamin-like GTPase atlastin. Nature. 2009;460:978–83.

    PubMed  CAS  Google Scholar 

  • Overall RL. Substructure of plasmodesmata. In: van Bel AJE, van Kesteren WJP, editors. Plasmodesmata: structure, function, role in cell communication. Berlin: Springer; 1999. p. 129–48.

    Google Scholar 

  • Palevitz BA, Hepler PK. Changes in dye coupling of stomatal cells of Allium and Commelina demonstrated by microinjection of Lucifer Yellow. Planta. 1985;164:473–9.

    Google Scholar 

  • Pendin D, McNew JA, Daga A. Balancing ER dynamics: shaping, bending, severing, and mending membranes. Curr Opin Cell Biol. 2011;23:435–42.

    PubMed  CAS  Google Scholar 

  • Perilli S, Di Mambro R, Sabatini S. Growth and development of the root apical meristem. Curr Opin Plant Biol. 2012;15:17–23.

    PubMed  CAS  Google Scholar 

  • Perraki A, Cacas J-L, Crowet J-M, Lins L, Castroviejo M, German-Retana S, et al. Plasma membrane localization of Solanum tuberosum remorin from group 1, homolog 3 is mediated by conformational changes in a novel C-terminal anchor and required for the restriction of Potato Virus X movement. Plant Physiol. 2012;160:624–37.

    PubMed  CAS  Google Scholar 

  • Petricka JJ, Winter CM, Benfey PN. Control of Arabidopsis root development. Annu Rev Plant Biol. 2012;63:563–90.

    PubMed  CAS  Google Scholar 

  • Pfluger J, Zambryski PC. Cell growth: the power of symplastic isolation. Curr Biol. 2001;11:436–9.

    Google Scholar 

  • Prinz WA, Grzyb L, Veenhuis M, Kahana JA, Silver PA, Rapoport TA. Mutants affecting the structure of the cortical endoplasmic reticulum in Saccharomyces cerevisiae. J Cell Biol. 2000;150:461–74.

    PubMed  CAS  Google Scholar 

  • Puhka M, Joensuu M, Vihinen H, Belevich I, Jokitalo E. Progressive sheet-to-tubule transformation is a general mechanism for endoplasmic reticulum partitioning in dividing mammalian cells. Mol Biol Cell. 2012;23:2424–32.

    PubMed  CAS  Google Scholar 

  • Qi X, Zheng H. Rab-A1c GTPase defines a population of the trans-Golgi network that is sensitive to endosidin 1 during cytokinesis in Arabidopsis. Mol Plant. 2012; doi:10.1093mp/sss116.

    Google Scholar 

  • Radford JE, White RG. Inhibitors of myosin, but not actin, alter transport through Tradescantia plasmodesmata. Protoplasma. 2011;248:205–16.

    PubMed  CAS  Google Scholar 

  • Raffaele S, Bayer E, Lafarge D, Cluzet S, German Retana S, Boubekeur T, et al. Remorin, a solanaceae protein resident in membrane rafts and plasmodesmata, impairs potato virus X movement. Plant Cell. 2009;21:1541–55.

    PubMed  CAS  Google Scholar 

  • Raven JA. Minireview: multiple origins of plasmodesmata. Eur J Phycol. 1997;32:95–101.

    Google Scholar 

  • Raven JA. Evolution of plasmodesmata. In: Oparka KJ, editor. Plasmodesmata, Annual Plant Reviews 18. Oxford, UK: Blackwell Publishing Ltd; 2005. p. 33–52.

    Google Scholar 

  • Ridge RW, Uozumi Y, Plazinski J, Hurley UA, Williamson RE. Developmental transitions and dynamics of the cortical ER of Arabidopsis cells seen with green fluorescent protein. Plant Cell Physiol. 1999;40:1253–61.

    PubMed  CAS  Google Scholar 

  • Rinne PLH, van der Schoot C. Symplasmic fields in the tunica of the shoot apical meristem coordinate morphogenetic events. Development. 1998;125:1477–85.

    PubMed  CAS  Google Scholar 

  • Rinne PL, Kaikuranta PM, van der Schoot C. The shoot apical meristem restores its symplasmic organization during chilling-induced release from dormancy. Plant J. 2001;26:249–64.

    PubMed  CAS  Google Scholar 

  • Rinne PLH, Welling A, Vahala J, Ripel L, Ruonala R, Kangasjärvi J, et al. Chilling of dormant buds hyperinduces FLOWERING LOCUS T and recruits GA-inducible 1,3-β-glucanases to reopen signal conduits and release dormancy in Populus. Plant Cell. 2011;23:130–46.

    PubMed  CAS  Google Scholar 

  • Risopatron JPM, Sun Y, Jones BJ. The vascular cambium: molecular control of cellular structure. Protoplasma. 2010;247:145–61.

    Google Scholar 

  • Roberts AG. Plasmodesmal structure and development. In: Oparka KJ, editor. Plasmodesmata, Annual Plant Reviews 18. Oxford, UK: Blackwell Publishing Ltd; 2005. p. 1–32.

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Robischon M, Du J, Miura E, Groover A. The Populus class III HD ZIP, popREVOLUTA, influences cambium initiation and patterning of woody stems. Plant Physiol. 2011;155:1214–25.

    PubMed  CAS  Google Scholar 

  • Rost TL. The organization of roots of dicotyledonous plants and the positions of control points. Ann Bot. 2011;107:1213–22.

    PubMed  Google Scholar 

  • Roy S, Watada AE, Wergin WP. Characterization of the cell wall microdomain surrounding plasmodesmata in apple fruit. Plant Physiol. 1997;114:539–47.

    PubMed  CAS  Google Scholar 

  • Ruan YL, Xu SM, White R, Furbank RT. Genotypic and developmental evidence for the role of plasmodesmatal regulation in cotton fiber elongation mediated by callose turnover. Plant Physiol. 2004;136:4104–13.

    PubMed  CAS  Google Scholar 

  • Rueffler C, Hermisson J, Wagner GP. Evolution of functional specialization and division of labor. Proc Natl Acad Sci USA. 2012;109:E326–35.

    PubMed  CAS  Google Scholar 

  • Ruiz-Medrano R, Xonocostle-Cazares B, Kragler F. The plasmodesmatal transport pathway for homeotic proteins, silencing signals and viruses. Curr Opin Plant Biol. 2004;7:641–50.

    PubMed  CAS  Google Scholar 

  • Ruonala R, Rinne PLH, Kangasjärvi J, van der Schoot C. CENL1 expression in the rib meristem affects stem elongation and the transition to dormancy in Populus. Plant Cell. 2008;20:59–74.

    PubMed  CAS  Google Scholar 

  • Rutschow HL, Baskin TI, Kramer EM. Regulation of solute flux through plasmodesmata in the root meristem. Plant Physiol. 2011;155:1817–26.

    PubMed  CAS  Google Scholar 

  • Schiefelbein JW, Somerville C. The genetic control of root hair development in Arabidopsis thaliana. Plant Cell. 1990;2:235–43.

    PubMed  CAS  Google Scholar 

  • Schnepf E, Sych A. Distribution of plasmodesmata in developing Sphagnum leaflets. Protoplasma. 1983;116:51–6.

    Google Scholar 

  • Schoelz JE, Harries PA, Nelson RS. Intracellular transport of plant viruses: finding the door out of the cell. Mol Plant. 2011;4:813–31.

    PubMed  CAS  Google Scholar 

  • Schopfer P. Biomechanics of plant growth. Am J Bot. 2006;93:1415–25.

    PubMed  Google Scholar 

  • Schopfer P, Liszkay A, Bechtold M, Frahry G, Wagner A. Evidence that hydroxyl radicals mediate auxin-induced extension growth. Planta. 2002;214:821–8.

    PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Schulz A. Physiological control of plasmodesmal gating. In: van Bel AJE, van Kesteren WJP, editors. Plasmodesmata: structure, function, role in cell communication. Berlin: Springer; 1999. p. 173–204.

    Google Scholar 

  • Schweikert C, Liszkay A, Schopfer P. Scission of polysaccharides by peroxidase-generated hydroxyl-radicals. Phytochemistry. 2000;53:565–70.

    PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Shibata Y, Shemesh T, Prinz WA, Palazzo AF, Kozlov MM, Rapoport TA. Mechanisms determining the morphology of the peripheral ER. Cell. 2010;143:774–88.

    PubMed  CAS  Google Scholar 

  • Simpson C, Thomas C, Findlay K, Bayer E, Maule AJ. An Arabidopsis GPI-anchor plasmodesmal neck protein with callose binding activity and potential to regulate cell-to-cell trafficking. Plant Cell. 2009;21:581–94.

    PubMed  CAS  Google Scholar 

  • Smaczniak C, Immink RG, Muiño JM, Blanvillain R, Busscher M, Busscher-Lange J, et al. Characterization of MADS-domain transcription factor complexes in Arabidopsis flower development. Proc Natl Acad Sci USA. 2012;31(109):1560–65.

    Google Scholar 

  • Sokołowska K, Zagórska-Marek B. Seasonal changes in the degree of symplasmic continuity between the cells of cambial region of Acer pseudoplatanus and Ulmus minor. Acta Soc Bot Pol. 2007;76:277–86.

    Google Scholar 

  • Sowiński P, Rudzińska-Langwald A, Kobus P. Changes in plasmodesmata frequency in vascular bundles of maize seedling leaf induced by growth at suboptimal temperatures in relation to photosynthesis and assimilate export. Environ Exp Bot. 2003;50:183–96.

    Google Scholar 

  • Sowiński P, Bilska A, Barańska K, Fronk J, Kobus P. 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. 2007;61:74–84.

    Google Scholar 

  • Sparkes IA, Tolley N, Aller I, Svozil J, Osterrieder A, Botchway S, et al. Five Arabidopsis reticulon isoforms share endoplasmic reticulon location, topology, and membrane-shaping properties. Plant Cell. 2010;22:1333–43.

    PubMed  CAS  Google Scholar 

  • Stadler R, Wright KM, Lauterbach C, Amon G, Gahrtz M, Feuerstein A, et al. 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. 2005;41:319–31.

    PubMed  CAS  Google Scholar 

  • Staehelin LA. The plant ER: a dynamic organelle composed of a large number of discrete functional domains. Plant J. 1997;11:1151–65.

    PubMed  CAS  Google Scholar 

  • Staehelin LA, Hepler PK. Cytokinesis in higher plants. Cell. 1996;84:821–4.

    PubMed  CAS  Google Scholar 

  • Stefano G, Renna L, Moss T, McNew JA, Brandizzi F. In Arabidopsis, the spatial and dynamic organization of the endoplasmic reticulum and Golgi apparatus is influenced by the integrity of the C-terminal domain of RHD3, a non-essential GTPase. Plant J. 2012;69:957–66.

    PubMed  CAS  Google Scholar 

  • Steinberg G, Kollmann R. A quantitative analysis of the interspecific plasmodesmata in the non-division walls of the plant chimera Laburnocytisus adamii (Poit.) Schneid. Planta. 1994;192:75–83.

    Google Scholar 

  • Stonebloom S, Burch-Smith T, Kim I, Meinke D, Mindrinos M, Zambryski P. Loss of the plant DEAD-box protein ISE1 leads to defective mitochondria and increased cell-to-cell transport via plasmodesmata. Proc Natl Acad Sci USA. 2009;106:17229–34.

    PubMed  CAS  Google Scholar 

  • Stonebloom S, Brunkard JO, Cheung AC, Jiang K, Feldman L, Zambryski P. Redox state of plastids and mitochondria differentially regulate intercellular transport via plasmodesmata. Plant Physiol. 2012;158:190–9.

    PubMed  CAS  Google Scholar 

  • Suer S, Agusti J, Sanchez P, Schwarz M, Greb T. WOX4 imparts auxin responsiveness to cambium cells in Arabidopsis. Plant Cell. 2011;23:3247–59.

    PubMed  CAS  Google Scholar 

  • Tanner W, Malinsky J, Opekarová M. In plant and animal cells, detergent-resistant membranes do not define functional membrane rafts. Plant Cell. 2011;23:1191–3.

    PubMed  CAS  Google Scholar 

  • Terauchi M, Nagasato C, Kajimura N, Mineyuki Y, Okuda K, Katsaros C, et al. Ultrastructural study of plasmodesmata in the brown alga Dictyota dichotoma (Dictyotales, Phaeophyceae). Planta. 2012;236:1013–26.

    PubMed  CAS  Google Scholar 

  • Tilney LG, Cooke TJ, Conelly PS, Tilney MS. The distribution of plasmodesmata and its relationship to morphogenesis in fern gametophytes. Development. 1990;110:1209–21.

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Tilsner J, Linnik O, Wright KM, Bell K, Roberts AG, Lacomme C, et al. The TGB1 movement protein of Potato virus X reorganizes actin and endomembranes into the X-body, a viral replication factory. Plant Physiol. 2012;158:1359–70.

    PubMed  CAS  Google Scholar 

  • Tolley N, Sparkes I, Craddock CP, Eastmond PJ, Runions J, Hawes C, et al. Transmembrane domain length is responsible for the ability of a plant reticulon to shape endoplasmic reticulum tubules in vivo. Plant J. 2010;64:411–8.

    PubMed  CAS  Google Scholar 

  • Torti S, Fornara F, Vincent C, Andrés F, Nordström K, Göbel U, et al. Analysis of the Arabidopsis shoot meristem transcriptome during floral transition identifies distinct regulatory patterns and a leucin-rich repeat protein that promotes flowering. Plant Cell. 2012;24:444–62.

    PubMed  CAS  Google Scholar 

  • Tucker EB. Inositol bisphosphate and inositol trisphosphate inhibit cell-to-cell passage of carboxyfluorescein in staminal hairs of Setcreasea purpurea. Planta. 1988;174:358–63.

    CAS  Google Scholar 

  • Tucker EB. Azide treatment enhances cell-to-cell diffusion in staminal hairs of Setcreasea purpurea. Protoplasma. 1993;174:45–9.

    CAS  Google Scholar 

  • Ueda H, Yokota E, Kutsuna N, Shimada T, Tamura K, Shimmen T, et al. Myosin-dependent endoplasmic reticulum motility and F-actin organization in plant cells. Proc Natl Acad Sci USA. 2010;107:6894–9.

    PubMed  CAS  Google Scholar 

  • Ursache R, Nieminen K, Helariutta Y. Genetic and hormonal regulation of cambial development. Physiol Plant. 2013;147:36–45.

    PubMed  CAS  Google Scholar 

  • van Bel AJE, Ehlers K. Symplasmic organization of the transport phloem controls assimilate supply of the cambium. In: Savidge R, Barnett JR, Napier R, editors. Cambium: the biology of wood formation. Oxford, UK: Bios; 2000. p. 85–99.

    Google Scholar 

  • van Bel AJE, Ehlers K. Electrical signalling via plasmodesmata. In: Oparka KJ, editor. Plasmodesmata, Annual Plant Reviews 18. Oxford, UK: Blackwell Publishing Ltd; 2005. p. 263–78.

    Google Scholar 

  • van Bel AJE, van Rijen HVM. Microelectrode-recorded development of the symplasmic autonomy of the sieve element/companion cell complex in the stem phloem of Lupinus luteus L. Planta. 1994;192:165–75.

    Google Scholar 

  • van den Berg C, Willemsen V, Hage W, Weisbeek P, Scheres B. Cell fate in the Arabidopsis root meristem determined by directional signalling. Nature. 1995;378:62–5.

    PubMed  Google Scholar 

  • van der Schoot C, Rinne P. The symplasmic organization of the shoot apical meristem. In: van Bel AJE, van Kesteren WJP, editors. Plasmodesmata: structure, function, role in cell communication. Berlin: Springer; 1999a. p. 225–42.

    Google Scholar 

  • van der Schoot C, Rinne P. Networks for shoot design. Trends Plant Sci. 1999b;4:31–7.

    PubMed  Google Scholar 

  • van der Schoot C, Dietrich MA, Storms M, Verbeke JA, Lucas WJ. Establishment of a cell-to-cell communication pathway between separate carpels during gynoecium development. Planta. 1995;195:450–5.

    Google Scholar 

  • Vatén A, Dettmer J, Wu S, Stierhof YD, Miyashima S, Yadav SR, et al. Callose biosynthesis regulates symplastic trafficking during root development. Dev Cell. 2011;21:1144–55.

    PubMed  Google Scholar 

  • Vernoux T, Besnard F, Traas J. Auxin at the shoot apical meristem. Cold Spring Harb Perspect Biol. 2010;2:a001487.

    PubMed  Google Scholar 

  • Voeltz GK, Prinz WA, Shibata Y, Rist JM, Rapoport TA. A class of membrane proteins shaping the tubular endoplasmic reticulum. Cell. 2006;124:573–86.

    PubMed  CAS  Google Scholar 

  • Volk GM, Turgeon R, Beebe DU. Secondary plasmodesmata formation in the minor-vein phloem of Cucumis melo L. and Cucurbita pepo L. Planta. 1996;199:425–32.

    Google Scholar 

  • Wille AC, Lucas WJ. Ultrastructural and histochemical studies on guard cells. Planta. 1984;160:129–42.

    Google Scholar 

  • Willmer CM, Sexton R. Stomata and plasmodesmata. Protoplasma. 1979;100:113–24.

    Google Scholar 

  • Wu S, Gallagher KL. Mobile protein signals in plant development. Curr Opin Plant Biol. 2011;14:563–70.

    PubMed  CAS  Google Scholar 

  • Wu S, Gallagher KL. Transcription factors on the move. Curr Opin Plant Biol. 2012;15:645–51.

    PubMed  CAS  Google Scholar 

  • Xu XM, Jackson D. Lights at the end of the tunnel: new views of plasmodesmal structure and function. Curr Opin Plant Biol. 2010;13:684–92.

    PubMed  CAS  Google Scholar 

  • Xu M, Cho E, Burch-Smith TM, Zambryski PC. Plasmodesmata formation and cell-to-cell transport are reduced in decreased size exclusion limit 1 during embryogenesis in Arabidopsis. Proc Natl Acad Sci USA. 2012;109:5098–103.

    PubMed  CAS  Google Scholar 

  • Yadav RK, Perales M, Gruel J, Girke T, Jönsson H, Reddy GV. WUSCHEL protein movement mediates stem cell homeostasis in the Arabidopsis shoot apex. Genes Dev. 2011;25:2025–30.

    PubMed  CAS  Google Scholar 

  • Yokota E, Ueda H, Hashimoto K, Orii H, Shimada T, Hara-Nishimura I, et al. Myosin XI-dependent formation of tubular structures from endoplasmic reticulum isolated from tobacco cultured BY-2 cells. Plant Physiol. 2011;156:129–43.

    PubMed  CAS  Google Scholar 

  • Yordanov YS, Regan S, Busov V. Members of LATERAL ORGAN BOUNDARIES DOMAIN transcription factor family are involved in the regulation of secondary growth in Populus. Plant Cell. 2010;22:3662–77.

    PubMed  CAS  Google Scholar 

  • Zambryski PC, Xu M, Stonebloom S, Burch-Smith T. Embryogenesis as a model system to dissect the genetic and developmental regulation of cell-to-cell transport via plasmodesmata. In: Kragler F, Hülskamp M, editors. Short and long distance signaling, Advances in Plant Biology 3. New York: Springer; 2012. p. 45–60.

    Google Scholar 

  • Zavaliev R, Sagi G, Gera A, Epel BL. The constitutive expression of Arabidopsis plasmodesmal-associated class 1 reversibly glycosylated polypeptide impairs plant development and virus spread. J Exp Bot. 2010;61:131–42.

    PubMed  CAS  Google Scholar 

  • Zavaliev R, Ueki S, Epel BL, Citovsky V. Biology of callose (β-1,3-glucan) turnover at plasmodesmata. Protoplasma. 2011;248:117–30.

    PubMed  CAS  Google Scholar 

  • Zhu T, Rost TL. Directional cell-to-cell communication in the Arabidopsis root apical meristem. III. Plasmodesmata turnover and apoptosis in meristem and root cap cells during four weeks post-germination. Protoplasma. 2000;213:108–17.

    Google Scholar 

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

    Google Scholar 

Download references

Acknowledgements

K. E. was supported by grants of the Deutsche Forschungsgemeinschaft (BE 1925/4-1, 4–2); M. G. W. was supported by a “Graduiertenstipendium der Justus Liebig Universitaet (JLU)” Giessen. For transmission electron microscopy, we used the equipment of the Zentrale Biotechnische Betriebeinheit (ZBB) of the JLU Giessen.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Katrin Ehlers Ph.D. .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2013 Springer Science+Business Media New York

About this chapter

Cite this chapter

Ehlers, K., Westerloh, M.G. (2013). Developmental Control of Plasmodesmata Frequency, Structure, and Function. In: Sokołowska, K., Sowiński, P. (eds) Symplasmic Transport in Vascular Plants. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-7765-5_2

Download citation

Publish with us

Policies and ethics