Skip to main content

Plasmodesmata and Phloem-Based Trafficking of Macromolecules

  • Chapter
  • First Online:
Symplasmic Transport in Vascular Plants

Abstract

Plant cell fate specification, responses to stimuli, and developmental coordination at multicellular level are achieved by cell-to-cell communication. Plasmodesmata (PD), cytoplasmic nanochannels interconnecting neighboring cells, sophisticate such communication by regulating exchange of molecules. The composition, organization, and architecture of these interconnecting channels have emerged, and several models are available. PD play as major gatekeepers of signaling macromolecules such as proteins and/or RNAs and establish domains of symplasmically connected cells either to facilitate or restrict the transport of such signaling molecules. This chapter is dedicated for those who seek insightful review through supporting evidence on intercellular trafficking of a range of endogenous proteins and their updated non-cell-autonomous protein pathway (NCAPP) machinery/components taking care, together, of plant development.

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

Abbreviations

CC:

Companion cell

CmPP1 CmPP2, CmPP16, and CmPP36:

Cucurbita maxima phloem protein 1, 2, 16, and 36

CPC:

CAPRICE

FLO:

FLORICAULA

FT:

FLOWERING LOCUS T

GFP:

Green fluorescent protein

KN1:

KNOTTED1

LFY:

LEAFY

NCAP:

Non-cell-autonomous protein

NCAPP:

Non-cell-autonomous protein pathway

PD:

Plasmodesmata

RNA:

Ribonucleic acid

SE:

Sieve element

SHR:

SHORT-ROOT

STM:

SHOOT MERISTEMLESS

UPB1:

UPBEAT1

References

  • An HL, Roussot C, Suarez-Lopez P, Corbesier L, Vincent C, Pineiro M, et al. CONSTANS acts in the phloem to regulate a systemic signal that induces photoperiodic flowering of Arabidopsis. Development. 2004;131:3615–26.

    PubMed  CAS  Google Scholar 

  • Aoki K, Kragler F, Xoconostle-Cazares B, Lucas WJ. A subclass of plant heat shock cognate 70 chaperones carries a motif that facilitates trafficking through plasmodesmata. Proc Natl Acad Sci USA. 2002;99:16342–7.

    PubMed  CAS  Google Scholar 

  • Ayre K, Turgeon R. Graft transmission of a floral stimulant derived from CONSTANS. Plant Physiol. 2004;135:2271–8.

    PubMed  CAS  Google Scholar 

  • Balachandran S, Xiang Y, Schobert C, Thompson GA, Lucas WJ. Phloem sap proteins from Cucurbita maxima and Ricinus communis have the capacity to traffic cell to cell through plasmodesmata. Proc Natl Acad Sci USA. 1997;94:14150–5.

    PubMed  CAS  Google Scholar 

  • Balkunde R, Pesch M, Hulskamp M. Trichome patterning in Arabidopsis thaliana: from genetic to molecular models. Curr Top Dev Biol. 2010;91:299–321.

    PubMed  CAS  Google Scholar 

  • Banerjee AK, Chatterjee M, Yu Y, Suh SG, Miller WA, Hannapel DJ. Dynamics of a mobile RNA of potato involved in a long-distance signaling pathway. Plant Cell. 2006;18:3443–57.

    PubMed  CAS  Google Scholar 

  • Baumberger N, Tsai CH, Lie M, Havecker E, Baulcombe DC. The Polerovirus silencing suppressor P0 targets ARGONAUTE proteins for degradation. Curr Biol. 2007;17:1609–14.

    PubMed  CAS  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 

  • Bennett T, Scheres B. Root development-two meristems for the price of one? Curr Top Dev Biol. 2010;91:67–102.

    PubMed  CAS  Google Scholar 

  • Bernhardt C, Lee MM, Gonzalez A, Zhang F, Lloyd A, Schiefelbein J. The bHLH genes GLABRA3 (GL3) and ENHANCER OF GLABRA3 (EGL3) specify epidermal cell fate in the Arabidopsis root. Development. 2003;130:6431–9.

    PubMed  CAS  Google Scholar 

  • Bernhardt C, Zhao M, Gonzalez A, Lloyd A, Schiefelbein J. The bHLH genes GL3 and EGL3 participate in an intercellular regulatory circuit that controls cell patterning in the Arabidopsis root epidermis. Development. 2005;132:291–8.

    PubMed  CAS  Google Scholar 

  • Bernier G, Havelange A, Houssa C, Petitjean A, Lejeune P. Physiological signals that induce flowering. Plant Cell. 1993;5:1147–55.

    PubMed  CAS  Google Scholar 

  • Bharathan G, Janssen BJ, Kellogg EA, Sinha N. Phylogenetic relationships and evolution of the KNOTTED class of plant homeodomain proteins. Mol Biol Evol. 1999;16:553–63.

    PubMed  CAS  Google Scholar 

  • Bouhidel K, Irish VF. Cellular interactions mediated by the homeotic PISTILLATA gene determine cell fate in the Arabidopsis flower. Dev Biol. 1996;174:22–31.

    PubMed  CAS  Google Scholar 

  • Bouyer D, Geier F, Kragler F, Schnittger A, Pesch M, Wester K, et al. Two-dimensional patterning by a trapping/depletion mechanism: the role of TTG1 and GL3 in Arabidopsis trichome formation. PLoS Biol. 2008;6:e141.

    PubMed  Google Scholar 

  • Brosnan CA, Voinnet O. Cell-to-cell and long-distance siRNA movement in plants: mechanisms and biological implications. Curr Opin Plant Biol. 2011;14:580–7.

    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. 2011;108:1451–60.

    Google Scholar 

  • Carpenter R, Coen ES. Floral homeotic mutations produced by transposon-mutagenesis in Antirrhinum majus. Genes Dev. 1990;4:1483–93.

    PubMed  CAS  Google Scholar 

  • Carpenter R, Coen ES. Transposon induced chimeras show that floricaula, a meristem identity gene, acts non-autonomously between cell layers. Development. 1995;121:19–26.

    PubMed  CAS  Google Scholar 

  • Casson S, Lindsey K. Genes and signaling in root development. New Phytol. 2003;158:11–38.

    CAS  Google Scholar 

  • Chailakhyan MK. New facts in support of the hormonal theory of plant development. Compt Rend Acad Sci URSS. 1936;13:79–83.

    Google Scholar 

  • Chitwood DH, Timmermans MCP. Small RNAs are on the move. Nature. 2010;467:415–9.

    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 

  • Corbesier L, Vincent C, Jang S, Fornara F, Fan Q, Searle I, et al. FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science. 2007;316:1030–3.

    PubMed  CAS  Google Scholar 

  • Crawford KM, Zambryski PC. Phloem transport: are you chaperoned? Curr Biol. 1999;9:281–5.

    Google Scholar 

  • Crawford KM, Zambryski PC. Subcellular localization determines the availability of non-targeted proteins to plasmodesmatal transport. Curr Biol. 2000;10:1032–40.

    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 

  • Cui H, Levesque MP, Vernoux T, Jung JW, Paquette AJ, Gallagher KL, et al. An evolutionarily conserved mechanism delimiting SHR movement defines a single layer of endodermis in plants. Science. 2007;316:421–5.

    PubMed  CAS  Google Scholar 

  • Dennis ES, Finnegan EJ, Bilodeau P, Chaudhury A, Genger R, Helliwell CA, et al. Vernalization and the initiation of flowering. Semin Cell Dev Biol. 1996;7:441–8.

    CAS  Google Scholar 

  • Ding B, Itaya A, Qi YJ. Symplasmic protein and RNA traffic: regulatory points and regulatory factors. Curr Opin Plant Biol. 2003;6:596–602.

    PubMed  CAS  Google Scholar 

  • Doerner P. Plant meristems: a merry-go-round of signals. Curr Biol. 2003;13:368–74.

    Google Scholar 

  • Dolan L, Costa S. Evolution and genetics of root hair stripes in the root epidermis. J Exp Bot. 2001;52:413–7.

    PubMed  CAS  Google Scholar 

  • Dolan L, Janmaat K, Willemsen V, Linstead P, Poethig S, Roberts K, et al. Cellular organisation of the Arabidopsis thaliana root. Development. 1993;119:71–84.

    PubMed  CAS  Google Scholar 

  • Douglas SJ, Chuck G, Dengler RE, Pelecanda L, Riggs CD. KNAT1 and ERECTA regulate inflorescence architecture in Arabidopsis. Plant Cell. 2002;14:547–58.

    PubMed  CAS  Google Scholar 

  • Efremova N, Perbal MC, Yephremov A, Hofmann WA, Saedler H, Schwarz-Sommer Z. Epidermal control of floral organ identity by class B homeotic genes in Antirrhinum and Arabidopsis. Development. 2001;128:2661–71.

    PubMed  CAS  Google Scholar 

  • Fichtenbauer D, Xu XM, Jackson D, Kragler F. The chaperonin CCT8 facilitates spread of tobacovirus infection. Plant Signal Behav. 2012;7:318–21.

    PubMed  CAS  Google Scholar 

  • Fisher DB, Wu Y, Ku MSB. Turnover of soluble proteins in the wheat sieve tube. Plant Physiol. 1992;100:1433–41.

    PubMed  CAS  Google Scholar 

  • Gallagher KL, Benfey PN. Both the conserved GRAS domain and nuclear localization are required for SHORT-ROOT movement. Plant J. 2009;57:785–97.

    PubMed  CAS  Google Scholar 

  • Gallagher KL, Paquette AJ, Nakajima K, Benfey PN. Mechanisms regulating SHORT-ROOT intercellular movement. Curr Biol. 2004;14:1847–51.

    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-LIKE 8). Development. 2010;137:1731–41.

    PubMed  CAS  Google Scholar 

  • Hake S, Freeling M. Analysis of genetic mosaics shows that the extra epidermal cell divisions in Knotted1 mutant maize plants are induced by adjacent mesophyll cells. Nature. 1986;320:621–3.

    Google Scholar 

  • Ham BK, Brandom JL, Xoconostle-Cazares B, Ringgold V, Lough TJ, Lucas WJ. Polypyrimidine tract binding protein, CmRBP50, forms the basis of a pumpkin phloem ribonucleoprotein complex. Plant Cell. 2009;21:197–215.

    PubMed  CAS  Google Scholar 

  • Hantke SS, Carpenter R, Coen ES. Expression of floricaula in single cell layers of periclinal chimeras activates downstream homeotic genes in all layers of floral meristems. Development. 1995;121:27–35.

    PubMed  CAS  Google Scholar 

  • Hayashi H, Fukuda A, Suzui N, Fujimaki S. Proteins in the sieve element-companion cell complexes: their detection, localization and possible functions. Aust J Plant Physiol. 2000;27:489–96.

    CAS  Google Scholar 

  • Haywood V, Kragler F, Lucas WJ. Plasmodesmata: pathways for protein and ribonucleoprotein signaling. Plant Cell. 2002;14:303–25.

    Google Scholar 

  • Haywood V, Yu TS, Huang NC, Lucas WJ. Phloem long-distance trafficking of GIBBERELLIC ACID-INSENSITIVE RNA regulates leaf development. Plant J. 2005;42:49–68.

    PubMed  CAS  Google Scholar 

  • Helariutta Y, Fukaki H, Wysocka-Diller J, Nakajima K, Jung J, Sena G, et al. The SHORT-ROOT gene controls radial patterning of the Arabidopsis root through radial signaling. Cell. 2000;101:555–67.

    PubMed  CAS  Google Scholar 

  • Hoffmann-Benning S, Gage DA, McIntosh L, Kende H, Zeevaart JAD. Comparison of peptides in the phloem sap of flowering and non-flowering Perilla and lupine plants using microbore HPLC followed by matrix-assisted laser desorption/ionization time-off light mass spectrometry. Planta. 2002;216:140–7.

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Imlau A, Truernit E, Sauer N. 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. 1999;11:309–22.

    PubMed  CAS  Google Scholar 

  • Ishiwatari Y, Fujiwara T, McFarland KC, Nemoto K, Hayashi H, Chino M, et al. Rice phloem thioredoxin h has the capacity to mediate its own cell-to-cell transport through plasmodesmata. Planta. 1998;205:12–22.

    PubMed  CAS  Google Scholar 

  • Jackson D. Transcription factor movement through plasmodesmata. In: Oparka KJ, editor. Plasmodesmata: annual plant reviews. Oxford: Blackwell; 2005. p. 114.

    Google Scholar 

  • Jackson D, Veit B, Hake S. Expression of maize KNOTTED1 related homeobox genes in the shoot apical meristem predicts patterns of morphogenesis in the vegetative shoot. Development. 1994;120:405–13.

    CAS  Google Scholar 

  • Jaeger KE, Wigge PA. FT protein acts as a long-range signal in Arabidopsis. Curr Biol. 2007;17:1050–4.

    PubMed  CAS  Google Scholar 

  • Jenik PD, Irish VF. The Arabidopsis floral homeotic gene APETALA3 differentially regulates intercellular signaling required for petal and stamen development. Development. 2001;128:13–23.

    PubMed  CAS  Google Scholar 

  • Joliot A, Maizel A, Rosenberg D, Trembleau A, Dupas S, Volovitch M, et al. Identification of a signal sequence necessary for the unconventional secretion of Engrailed homeoprotein. Curr Biol. 1998;8:856–63.

    PubMed  CAS  Google Scholar 

  • Jongebloed U, Szederkényi J, Hartig K, Schober C, Komor E. Sequence of morphological and physiological events during natural ageing and senescence of a castor bean leaf: sieve tube occlusion and carbohydrate back-up precede chlorophyll degradation. Physiol Plant. 2004;120:338–46.

    PubMed  CAS  Google Scholar 

  • Kardailsky I, Shukla VK, Ahn JH, Dagenais N, Christensen SK, Nguyen JT, et al. Activation tagging of the floral inducer FT. Science. 1999;286:1962–5.

    PubMed  CAS  Google Scholar 

  • Karol KG, McCourt RM, Cimino MT, Delwiche CF. The closest living relatives of land plants. Science. 2001;294:2351–3.

    PubMed  CAS  Google Scholar 

  • Kauss H. Callose biosynthesis as a Ca2+-regulated process and possible relations to the induction of other metabolic changes. J Cell Sci Suppl. 1985;2:89–103.

    PubMed  CAS  Google Scholar 

  • Kehr J, Buhtz A. Long-distance transport and movement of RNA through the phloem. J Exp Bot. 2008;59:85–92.

    PubMed  CAS  Google Scholar 

  • Kim M, Canio W, Kessler S, Sinha N. Developmental changes due to long-distance movement of a homeobox fusion transcript in tomato. Science. 2001;293:287–9.

    PubMed  CAS  Google Scholar 

  • Kim JY, Yuan Z, Cilia M, Khalfan-Jagani Z, Jackson D. Intercellular trafficking of a KNOTTED1 green fluorescent protein fusion in the leaf and shoot meristem of Arabidopsis. Proc Natl Acad Sci USA. 2002;99:4103–8.

    PubMed  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 JY, Rim Y, Wang J, Jackson D. A novel cell-to-cell trafficking assay indicates that the KNOX homeodomain is necessary and sufficient for intercellular protein and mRNA trafficking. Genes Dev. 2005;19:788–93.

    PubMed  CAS  Google Scholar 

  • King RW, Zeevaart JAD. Floral stimulus movement in Perilla and flower inhibition by noninduced leaves. Plant Physiol. 1973;51:727–38.

    PubMed  CAS  Google Scholar 

  • Knott JE. Effect of a localized photoperiod on spinach. Proc Soc Horticult Sci. 1934;31:152–4.

    Google Scholar 

  • Kobayashi Y, Kaya H, Goto K, Iwabuchi M, Araki T. A pair of related genes with antagonistic roles in mediating flowering signals. Science. 1999;286:1960–2.

    PubMed  CAS  Google Scholar 

  • Koizumi K, Wu S, MacRae-Crerar A, Gallagher KL. An essential protein that interacts with endosomes and promotes movement of the SHORT-ROOT transcription factor. Curr Biol. 2011;21:1559–64.

    PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Kragler F, Monzer J, Shash K, Xoconostle-Cazares B, Lucas WJ. Cell-to-cell transport of proteins: Requirement for unfolding and characterization of binding to a putative plasmodesmal receptor. Plant J. 1998b;15:367–81.

    CAS  Google Scholar 

  • Kragler F, Monzer J, Xoconostle-Cazares B, Lucas WJ. Peptide antagonists of the plasmodesmal macromolecular trafficking pathway. EMBO J. 2000;19:2856–68.

    PubMed  CAS  Google Scholar 

  • Kragler F, Curin M, Trutnyeva K, Gansch A, Waigmann E. MPB2C, a microtubule-associated plant protein binds to and interferes with cell-to-cell transport of tobacco mosaic virus movement protein. Plant Physiol. 2003;132:1870–83.

    PubMed  CAS  Google Scholar 

  • Kuhn C, Franceschi VR, Schulz A, Lemoine R, Frommer WB. Macromolecular trafficking indicated by localization and turnover of sucrose transporters in enucleate sieve elements. Science. 1997;275:1298–300.

    PubMed  CAS  Google Scholar 

  • Kurata T, Ishida T, Kawabata-Awai C, Noguchi M, Hattori S, Sano R, et al. Cell-to-cell movement of the CAPRICE protein in Arabidopsis root epidermal cell differentiation. Development. 2005;132:5387–98.

    PubMed  CAS  Google Scholar 

  • Larkin JC, Brown ML, Schiefelbein J. How do cells know what they want to be when they grow up? Lessons from epidermal patterning in Arabidopsis. Annu Rev Plant Biol. 2003;54:403–30.

    PubMed  CAS  Google Scholar 

  • Lee MM, Schiefelbein J. Cell pattern in the Arabidopsis root epidermis determined by lateral inhibition with feedback. Plant Cell. 2002;14:611–8.

    PubMed  CAS  Google Scholar 

  • Lee JY, Yoo B, Rojas MR, Gomez-Ospina N, Staehelin LA, Lucas WJ. Selective trafficking of non-cell-autonomous proteins mediated by NtNCAPP1. Science. 2003;299:392–6.

    PubMed  CAS  Google Scholar 

  • Lee JY, Colinas J, Wang JY, Mace D, Ohler U, Benfey PN. Transcriptional and posttranscriptional regulation of transcription factor expression in Arabidopsis roots. Proc Natl Acad Sci USA. 2006;103:6055–60.

    PubMed  CAS  Google Scholar 

  • Levesque MP, Vernoux T, Busch W, Cui H, Wang JY, Blilou I, et al. Whole-genome analysis of the SHORT-ROOT developmental pathway in Arabidopsis. PLoS Biol. 2006;4:e143.

    PubMed  Google Scholar 

  • Lewis JD, Lazarowitz SG. Arabidopsis synaptotagmin SYTA regulates endocytosis and virus movement protein cell-to-cell transport. Proc Natl Acad Sci USA. 2010;107:2491–6.

    PubMed  CAS  Google Scholar 

  • Li P, Ham BK, Lucas WJ. CmRBP50 protein phosphorylation is essential for assembly of a stable phloem-mobile high-affinity ribonucleoprotein complex. J Biol Chem. 2011;286:23142–9.

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Lifschitz E, Eviatar T, Rozman A, Goldshmidt A, Amsellem Z, Alvarez JP, et al. The tomato FT ortholog triggers systemic signals that regulate growth and flowering and substitute for diverse environmental stimuli. Proc Natl Acad Sci USA. 2006;103:6398–403.

    PubMed  CAS  Google Scholar 

  • Lin MK, Lee YJ, Lough TJ, Phinney B, Lucas WJ. Analysis of the pumpkin phloem proteome provides functional insights into angiosperm sieve tube function. Mol Cell Proteomics. 2009;8:343–56.

    PubMed  CAS  Google Scholar 

  • Liu L, Liu C, Hou X, Xi W, Shen L, Tao Z, et al. FTIP1 is an essential regulator required for florigen transport. PLoS Biol. 2012;10:e1001313.

    PubMed  CAS  Google Scholar 

  • Long JA, Moan EI, Medford JI, Barton MK. A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis. Nature. 1996;379:66–9.

    PubMed  CAS  Google Scholar 

  • Lough TJ, Lucas WJ. Integrative plant biology: role of phloem long-distance macromolecular trafficking. Annu Rev Plant Biol. 2006;57:203–32.

    PubMed  CAS  Google Scholar 

  • Lucas WJ. Plasmodesmata: intercellular channels for macrocellular transport in plants. Curr Opin Cell Biol. 1995;7:673–80.

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Lucas WJ, Bouche-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 

  • Masucci JD, Rerie WG, Foreman DR, Zhang M, Galway ME, Marks MD, et al. The homeobox gene GLABRA2 is required for position-dependent cell differentiation in the root epidermis of Arabidopsis thaliana. Development. 1996;122:1253–60.

    PubMed  CAS  Google Scholar 

  • Mathieu J, Warthmann N, Kuttner F, Schmid M. Export of FT protein from phloem companion cells is sufficient for floral induction in Arabidopsis. Curr Biol. 2007;17:1055–60.

    PubMed  CAS  Google Scholar 

  • Maule AJ. Plasmodesmata: structure, function and biogenesis. Curr Opin Plant Biol. 2008;11:680–6.

    PubMed  CAS  Google Scholar 

  • Meng L, Wong JH, Feldman LJ, Lemaux PG, Buchanan BB. A membrane-associated thioredoxin required for plant growth moves from cell to cell, suggestive of a role in intercellular communication. Proc Natl Acad Sci USA. 2010;107:3900–5.

    PubMed  CAS  Google Scholar 

  • Nakajima K, Sena G, Nawy T, Benfey PN. Intercellular movement of the putative transcription factor SHR in root patterning. Nature. 2001;413:307–11.

    PubMed  CAS  Google Scholar 

  • Narvaez-Vasquez J, Pearce G, Orozco-Cardenas ML, Franceschi VR, Ryan CA. Autoradiographic and biochemical evidence for the systemic translocation of systemin in tomato plants. Planta. 1995;195:593–600.

    CAS  Google Scholar 

  • Omid A, Keilin T, Glass A, Leshkowitz D, Wolf S. Characterization of phloem-sap transcription profile in melon plants. J Exp Bot. 2007;58:3645–56.

    PubMed  CAS  Google Scholar 

  • Oparka KJ, Cruz SS. The great escape: phloem transport and unloading of macromolecules. Annu Rev Plant Physiol Plant Mol Biol. 2000;51:323–47.

    PubMed  CAS  Google Scholar 

  • Oparka KJ, Roberts AG, Boevink P, Santa Cruz S, Roberts I, Prade 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 

  • Paquette AJ, Benfey PN. Maturation of the ground tissue of the root is regulated by gibberellin and SCARECROW and requires SHORT-ROOT. Plant Physiol. 2005;138:636–40.

    PubMed  CAS  Google Scholar 

  • Parcy F, Nilsson O, Busch MA, Lee I, Weigel D. A genetic framework for floral patterning. Nature. 1998;395:561–6.

    PubMed  CAS  Google Scholar 

  • Perbal MC, Haughn G, Saedler H, Schwarz-Sommer Z. Non-cell-autonomous function of the Antirrhinum floral homeotic proteins DEFICIENS and GLOBOSA is exerted by their polar cell-to-cell trafficking. Development. 1996;122:3433–41.

    PubMed  CAS  Google Scholar 

  • Pesch M, Hulskamp M. One, two, three…models for trichome patterning in Arabidopsis? Curr Opin Plant Biol. 2009;12:587–92.

    PubMed  CAS  Google Scholar 

  • Schulz A. Phloem. Structure related to function. Prog Bot. 1998;59:431–75.

    Google Scholar 

  • Putterill J, Robson F, Lee K, Simon R, Coupland G. The CONSTANS gene of Arabidopsis promotes flowering and encodes a protein showing similarities to zinc finger transcription factors. Cell. 1995;80:847–57.

    PubMed  CAS  Google Scholar 

  • Reiser L, Sanchez-Baracaldo P, Hake S. Knots in the family tree: evolutionary relationships and functions of knox homeobox genes. Plant Mol Biol. 2000;42:151–66.

    PubMed  CAS  Google Scholar 

  • Riechmann JL, Meyerowitz EM. MADS domain proteins in plant development. Biol Chem. 1997;378:1079–101.

    PubMed  CAS  Google Scholar 

  • Rim Y, Huang L, Chu H, Han X, Cho WK, Kim JY. Analysis of Arabidopsis transcription factor families revealed extensive capacity for cell-to-cell movement as well as discrete trafficking patterns. Mol Cells. 2011;32:519–26.

    PubMed  CAS  Google Scholar 

  • Robards AW, Lucas WJ. Plasmodesmata. Annu Rev Plant Physiol. 1990;41:369–419.

    Google Scholar 

  • Roberts AG, Oparka KJ. Plasmodesmata and the control of symplastic transport. Plant Cell Environ. 2003;26:103–24.

    Google Scholar 

  • Rojas MR, Jiang H, Salati R, Xoconostle-Cazares B, Sudarshana MR, Lucas WJ, et al. Functional analysis of proteins involved in movement of the monopartite begomovirus, tomato yellow leaf curl virus. Virology. 2001;291:110–25.

    PubMed  CAS  Google Scholar 

  • Ruiz-Medrano R, Xoconostle‑Cazares B, Lucas WJ. The phloem as a conduit for inter-organ communication. Curr Opin Plant Biol. 2001;4:202–9.

    PubMed  CAS  Google Scholar 

  • Samach A, Onouchi H, Gold SE, Ditta GS, Schwarz-Sommer Z, Yanofsky MF, et al. Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science. 2000;288:1613–6.

    PubMed  CAS  Google Scholar 

  • Sauer N. Molecular physiology of higher plant sucrose transporters. FEBS Lett. 2007;581:2309–17.

    PubMed  CAS  Google Scholar 

  • Savage NS, Walker T, Wieckowski Y, Schiefelbein J, Dolan L, Monk NAM. Mutual support mechanism through intercellular movement of CAPRICE and GLABRA3 can pattern the Arabidopsis root epidermis. PLoS Biol. 2008;6:e235.

    PubMed  Google Scholar 

  • Schlereth A, Moller B, Liu W, Kientz M, Flipse J, Rademacher EH, et al. MONOPTEROS controls embryonic root initiation by regulating a mobile transcription factor. Nature. 2010;464:913–6.

    PubMed  CAS  Google Scholar 

  • Schobert C, Baker L, Szederkenyi J, Grossmann P, Komor E, Hayashi H, et al. Identification of immunologically related proteins in sieve-tube exudate collected from monocotyledonous and dicotyledonous plants. Planta. 1998;206:245–52.

    CAS  Google Scholar 

  • Schwarz-Sommer Z, Hue I, Huijser P, Flor PJ, Hansen R, Tetens F, et al. Characterization of the Antirrhinum floral homeotic MADS-box gene deficiens: evidence for DNA binding and autoregulation of its persistent expression throughout flower development. EMBO J. 1992;11:251–63.

    PubMed  CAS  Google Scholar 

  • Sena G, Jung JW, Benfey PN. A broad competence to respond to SHORT ROOT revealed by tissue-specific ectopic expression. Development. 2004;131:2817–26.

    PubMed  CAS  Google Scholar 

  • Sessions A, Yanofsky MF, Weigel D. Cell-cell signaling and movement by the floral transcription factors LEAFY and APETALA1. Science. 2000;289:779–82.

    PubMed  CAS  Google Scholar 

  • Sinha N, Hake S. Mutant characters of knotted maize leaves are determined in the inner most tissue layers. Dev Biol. 1990;141:203–10.

    PubMed  CAS  Google Scholar 

  • Sinha N, Williams R, Hake S. Overexpression of the maize homeobox gene, Knotted1, causes a switch from determinate to indeterminate cell fates. Genes Dev. 1993;7:787–95.

    PubMed  CAS  Google Scholar 

  • Sivaguru M, Fijiwara T, Samaj J, Baluska F, Yang Z, Osawa H, et al. Aluminium induced 1→3-β-D-glucan inhibits cell-to-cell trafficking of molecules through plasmodesmata: a new mechanism of aluminium toxicity in plants. Plant Physiol. 2000;124:991–1005.

    PubMed  CAS  Google Scholar 

  • Smith LG, Greene B, Veit B, Hake S. A dominant mutation in the maize homeobox gene, Knotted-1, causes its ectopic expression in leaf cells with altered fates. Development. 1992;116:21–30.

    PubMed  CAS  Google Scholar 

  • Sommer H, Beltran JP, Huijser P, Pape H, Lonnig WE, Saedler H, et al. Deficiens, a homeotic gene involved in the control of flower morphogenesis in Antirrhinum majus: the protein shows homology to transcription factors. EMBO J. 1990;9:605–13.

    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 

  • 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 states of plastids and mitochondria differentially regulate intercellular transport via plasmodesmata. Plant Physiol. 2012;158:190–9.

    PubMed  CAS  Google Scholar 

  • Tamaki S, Matsuo S, Wong HL, Yokoi S, Shimamoto K. Hd3a protein is a mobile flowering signal in rice. Science. 2007;316:1033–6.

    PubMed  CAS  Google Scholar 

  • Tsukagoshi H, Busch W, Benfey PN. Transcriptional regulation of ROS controls transition from proliferation to differentiation in the root. Cell. 2010;143:606–16.

    PubMed  CAS  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 

  • Venglat SP, Dumonceaux T, Rozwadowski K, Parnell L, Babic V, Keller W, et al. The homeobox gene BREVIPEDICELLUS is a key regulator of inflorescence architecture in Arabidopsis. Proc Natl Acad Sci USA. 2002;99:4730–5.

    PubMed  CAS  Google Scholar 

  • Wada T, Tachibana T, Shimura Y, Okada K. Epidermal cell differentiation in Arabidopsis determined by a Myb homolog, CPC. Science. 1997;277:1113–6.

    PubMed  CAS  Google Scholar 

  • Wada T, Kurata T, Tominaga R, Koshino-Kimura Y, Tachibana T, Goto K, et al. Role of a positive regulator of root hair development, CAPRICE, in Arabidopsis root epidermal cell differentiation. Development. 2002;129:5409–19.

    PubMed  CAS  Google Scholar 

  • Weigel D, Alvarez J, Smyth DR, Yanofsky MF, Meyerowitz EM. LEAFY controls floral meristem identity in Arabidopsis. Cell. 1992;69:843–59.

    PubMed  CAS  Google Scholar 

  • Welch D, Hassan H, Blilou I, Immink R, Heidstra R, Scheres B. Arabidopsis JACKDAW and MAGPIE zinc finger proteins delimit asymmetric cell division and stabilize tissue boundaries by restricting SHORT-ROOT action. Genes Dev. 2007;21:2196–204.

    PubMed  CAS  Google Scholar 

  • Willemsen V, Bauch M, Bennett T, Campilho A, Wolkenfelt H, Xu J, et al. The NAC domain transcription factors FEZ and SMB control the orientation of cell division plane in Arabidopsis root stem cells. Dev Cell. 2008;15:913–22.

    PubMed  CAS  Google Scholar 

  • Winter N, Kollwig G, Zhang S, Kragler F. MPB2C, a microtubule-associated protein, regulates non-cell-autonomy of the homeodomain protein KNOTTED1. Plant Cell. 2007;19:3001–18.

    PubMed  CAS  Google Scholar 

  • Winter CM, Austin RS, Blanvillain-Baufume S, Reback MA, Monniaux M, Wu MF, et al. LEAFY target genes reveal floral regulatory logic, cis motifs, and a link to biotic stimulus response. Dev Cell. 2011;20:430–43.

    PubMed  CAS  Google Scholar 

  • Wolf S, Deom CM, Beachy RN, Lucas WJ. Movement protein of tobacco mosaic virus modifies plasmodesmatal size exclusion limit. Science. 1989;246:377–9.

    PubMed  CAS  Google Scholar 

  • Wu X, Dinneny JR, Crawford KM, Rhee Y, Citovsky V, Zambryski PC, et al. Modes of intercellular transcription factor movement in the Arabidopsis apex. Development. 2003;130:3735–45.

    PubMed  CAS  Google Scholar 

  • Xoconostle-Cazares B, Xiang Y, Ruiz-Medrano R, Wang HL, Monzer J, Yoo BC, et al. Plant paralog to viral movement protein that potentiates transport of mRNA into the phloem. Science. 1999;283:94–8.

    PubMed  CAS  Google Scholar 

  • Xoconostle-Cazares B, Ruiz-Medrano R, Lucas WJ. Proteolytic processing of CmPP36, a protein from the cytochrome b5 reductase family, is required for entry into the phloem translocation pathway. Plant J. 2000;24:735–47.

    PubMed  CAS  Google Scholar 

  • Xu XM, Wang J, Xuan ZY, Goldshmidt A, Borrill PGM, Hariharan N, et al. Chaperonins facilitate KNOTTED1 cell-to-cell trafficking and stem cell function. Science. 2011;333:1141–4.

    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 

  • Yoo BC, Kragler F, Varkonyi-Gasic E, Haywood V, Archer-Evans S, Lee YM, et al. A systemic small RNA signaling system in plants. Plant Cell. 2004;16:1979–2000.

    PubMed  CAS  Google Scholar 

  • Zambryski P. Cell-to-cell transport of proteins and fluorescent tracers via plasmodesmata during plant development. J Cell Biol. 2004;162:165–8.

    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 

  • Zeevaart JAD. Florigen coming of age after 70 years. Plant Cell. 2006;18:1783–9.

    PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by World Class University program grant R33-10002 through the National Research Foundation of Korea, funded by the Ministry of Education, Science and Technology and the Next-Generation BioGreen 21 Program (SSAC, grant PJ008109), Rural Development Administration, Republic of Korea.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jae-Yean Kim 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

Kumar, D., Kumar, R., Hyun, T.K., Kim, JY. (2013). Plasmodesmata and Phloem-Based Trafficking of Macromolecules. 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_7

Download citation

Publish with us

Policies and ethics