Skip to main content
SpringerLink
Log in

Regulation of Plasmodesmal Transport and Modification of Plasmodesmata During Development and Following Infection by Viruses and Viral Proteins

  • Chapter
  • First Online:
Plant-Virus Interactions

Abstract

Plant cells are encased in cellulose precluding direct contact. To enable intercellular communication, plants evolved cell wall-spanning channels called plasmodesmata. Plasmodesmata are essential to facilitate transport of small molecules such as photosynthate, as well as critical signaling macromolecules such as transcription factors and RNAs. Plasmodesmata are indispensible for all stages of plant development, from embryogenesis, through vegetative and reproductive development. Plasmodesmata are not passive channels, but instead they are highly dynamic and change their apertures in response to intracellular signals such as reactive oxygen species, hormones, and chloroplast and mitochondrial homeostasis. To date the best-known mechanism for controlling the degree of plasmodesmata transport is the reversible deposition of callose polysaccharides in the cell wall immediately surrounding plasmodesmata channels. Plant viruses have evolved to counteract innate plasmodesmata regulatory mechanisms and are well-known pirates of plasmodesmata during infectious spread.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 109.99
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

  • Amari K, Boutant E, Hofmann C, Schmitt-Keichinger C, Fernandez-Calvino L, Didier P, Lerich A, Mutterer J, Thomas CL, Heinlein M, Mely Y, Maule AJ, Ritzenthaler C (2010) A family of plasmodesmal proteins with receptor-like properties for plant viral movement proteins. PLoS Pathog 6(9), e1001119

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Arisz WH (1969) Intercellular polar transport and the role of the plasmodesmata in coleoptiles and Vallisneria leaves. Acta Bot Neerl 10:14–38

    Article  Google Scholar 

  • Ayre BG (2011) Membrane-transport systems for sucrose in relation to whole-plant carbon partitioning. Mol Plant 4(3):377–394

    Article  CAS  PubMed  Google Scholar 

  • Balasubramanian V, Vashisht D, Cletus J, Sakthivel N (2012) Plant beta-1,3-glucanases: Their biological functions and transgenic expression against phytopathogenic fungi. Biotechnol Lett 34(11):1983–1990

    Article  CAS  PubMed  Google Scholar 

  • Baluska F, Cvrckova F, Kendrick-Jones J, Volkmann D (2001) Sink plasmodesmata as gateways for phloem unloading. Myosin VIII and calreticulin as molecular determinants of sink strength? Plant Physiol 126(1):39–46

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baluska F, Samaj J, Hlavacka A, Kendrick-Jones J, Volkmann D (2004) Actin-dependent fluid-phase endocytosis in inner cortex cells of maize root apices. J Exp Bot 55(396):463–473

    Article  CAS  PubMed  Google Scholar 

  • Band LR, Wells DM, Fozard JA, Ghetiu T, French AP, Pound MP, Wilson MH, Yu L, Li W, Hijazi HI, Oh J, Pearce SP, Perez-Amador MA, Yun J, Kramer E, Alonso JM, Godin C, Vernoux T, Hodgman TC, Pridmore TP, Swarup R, King JR, Bennett MJ (2014) Systems analysis of auxin transport in the Arabidopsis root apex. Plant Cell. doi:10.1105/tpc.113.119495

    PubMed  PubMed Central  Google Scholar 

  • Barratt DH, Kolling K, Graf A, Pike M, Calder G, Findlay K, Zeeman SC, Smith AM (2011) Callose synthase GSL7 is necessary for normal phloem transport and inflorescence growth in Arabidopsis. Plant Physiol 155(1):328–341

    Article  CAS  PubMed  Google Scholar 

  • Barton DA, Cole L, Collings DA, Liu DY, Smith PM, Day DA, Overall RL (2011) Cell-to-cell transport via the lumen of the endoplasmic reticulum. Plant J 66(5):806–817

    Article  CAS  PubMed  Google Scholar 

  • Bayer EM, Bottrill AR, Walshaw J, Vigouroux M, Naldrett MJ, Thomas CL, Maule AJ (2006) Arabidopsis cell wall proteome defined using multidimensional protein identification technology. Proteomics 6(1):301–311

    Article  CAS  PubMed  Google Scholar 

  • Bayer E, Thomas C, Maule A (2008) Symplastic domains in the Arabidopsis shoot apical meristem correlate with PDLP1 expression patterns. Plant Signal Behav 3(10):853–855

    Article  PubMed  PubMed Central  Google Scholar 

  • Beachy RN, Heinlein M (2000) Role of P30 in replication and spread of TMV. Traffic 1(7):540–544

    Article  CAS  PubMed  Google Scholar 

  • Beffa RS, Hofer RM, Thomas M, Meins F Jr (1996) Decreased susceptibility to viral disease of [beta]-1,3-glucanase-deficient plants generated by antisense transformation. Plant Cell 8(6):1001–1011

    CAS  PubMed  PubMed Central  Google Scholar 

  • Beleyur T, Abdul Kareem VK, Shaji A, Prasad K (2013) A mathematical basis for plant patterning derived from physico-chemical phenomena. Bioessays 35(4):366–376

    Article  PubMed  Google Scholar 

  • Benitez-Alfonso Y, Cilia M, San Roman A, Thomas C, Maule A, Hearn S, Jackson D (2009) Control of Arabidopsis meristem development by thioredoxin-dependent regulation of intercellular transport. Proc Natl Acad Sci U S A 106(9):3615–3620

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Benitez-Alfonso Y, Jackson D, Maule A (2011) Redox regulation of intercellular transport. Protoplasma 248(1):131–140

    Article  CAS  PubMed  Google Scholar 

  • Benitez-Alfonso Y, Faulkner C, Pendle A, Miyashima S, Helariutta Y, Maule A (2013) Symplastic intercellular connectivity regulates lateral root patterning. Dev Cell 26(2):136–147

    Article  CAS  PubMed  Google Scholar 

  • Bhat S, Folimonova SY, Cole AB, Ballard KD, Lei Z, Watson BS, Sumner LW, Nelson RS (2013) Influence of host chloroplast proteins on tobacco mosaic virus accumulation and intercellular movement. Plant Physiol 161(1):134–147

    Article  CAS  PubMed  Google Scholar 

  • Blackman LM, Overall RL (1998) Immunolocalisation of the cytoskeleton to plasmodesmata of Chara corallina. Plant J 14(6):733–741

    Article  CAS  Google Scholar 

  • Borner GH, Lilley KS, Stevens TJ, Dupree P (2003) Identification of glycosylphosphatidylinositol-anchored proteins in Arabidopsis. A proteomic and genomic analysis. Plant Physiol 132(2):568–577

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Botha CEJ, Cross RHM, van Bel AJE, Peter CI (2000) Phloem loading in the sucrose-export-defective (SXD-1) mutant maize is limited by callose deposition at plasmodesmata in bundle sheath-vascular parenchyma interface. Protoplasma 214(1–2):65–72

    Article  CAS  Google Scholar 

  • Bouyer D, Geier F, Kragler F, Schnittger A, Pesch M, Wester K, Balkunde R, Timmer J, Fleck C, Hulskamp M (2008) Two-dimensional patterning by a trapping/depletion mechanism: The role of TTG1 and GL3 in Arabidopsis trichome formation. PLoS Biol 6(6), e141

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Brizard JP, Carapito C, Delalande F, Van Dorsselaer A, Brugidou C (2006) Proteome analysis of plant-virus interactome: Comprehensive data for virus multiplication inside their hosts. Mol Cell Proteomics 5(12):2279–2297

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Bucher GL, Tarina C, Heinlein M, Di Serio F, Meins F Jr, Iglesias VA (2001) Local expression of enzymatically active class I beta-1, 3-glucanase enhances symptoms of TMV infection in tobacco. Plant J 28(3):361–369

    Article  CAS  PubMed  Google Scholar 

  • Burch-Smith TM, Zambryski PC (2010) Loss of INCREASED SIZE EXCLUSION LIMIT (ISE)1 or ISE2 increases the formation of secondary plasmodesmata. Curr Biol 20(11):989–993

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Burch-Smith TM, Brunkard JO, Choi YG, Zambryski PC (2011a) Organelle-nucleus cross-talk regulates plant intercellular communication via plasmodesmata. Proc Natl Acad Sci U S A 108(51):E1451–E1460

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burch-Smith TM, Stonebloom S, Xu M, Zambryski PC (2011b) Plasmodesmata during development: Re-examination of the importance of primary, secondary, and branched plasmodesmata structure versus function. Protoplasma 248(1):61–74

    Article  CAS  PubMed  Google Scholar 

  • Burch-Smith TM, Cui Y, Zambryski PC (2012) Reduced levels of class 1 reversibly glycosylated polypeptide increase intercellular transport via plasmodesmata. Plant Signal Behav 7(1):62–67

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carlsbecker A, Lee J-Y, Roberts CJ, Dettmer J, Lehesranta S, Zhou J, Lindgren O, Moreno-Risueno MA, Vaten A, Thitamadee S, Campilho A, Sebastian J, Bowman JL, Helariutta Y, Benfey PN (2010) Cell signaling by microRNA165/6 directs gene-dose dependent root cell fate. Nature 465:316–321

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carr DJ (1976) Historical perspectives on plasmodesmata. In: Gunning BES, Robards AW (eds) Intercellular communication in plants: Studies on plasmodesmata. Springer, Berlin/Heidelberg, pp 291–295

    Chapter  Google Scholar 

  • Chapman EJ, Carrington JC (2007) Specialization and evolution of endogenous small RNA pathways. Nat Rev Genet 8(11):884–896

    Article  CAS  PubMed  Google Scholar 

  • Chen LQ, Qu XQ, Hou BH, Sosso D, Osorio S, Fernie AR, Frommer WB (2012) Sucrose efflux mediated by SWEET proteins as a key step for phloem transport. Science 335(6065):207–211

    Article  CAS  PubMed  Google Scholar 

  • Chitwood DH, Nogueira FT, Howell MD, Montgomery TA, Carrington JC, Timmermans MC (2009) Pattern formation via small RNA mobility. Genes Dev 23(5):549–554

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cleland RE, Fujiwara T, Lucas WJ (1994) Plasmodesmal-mediated cell-to-cell transport in wheat roots is modulated by anaerobic stress. Protoplasma 178:81–85

    Article  CAS  PubMed  Google Scholar 

  • Conti G, Rodriguez MC, Manacorda CA, Asurmendi S (2012) Transgenic expression of tobacco mosaic virus capsid and movement proteins modulate plant basal defense and biotic stress responses in Nicotiana tabacum. Mol Plant Microbe Interact 25(10):1370–1384

    Google Scholar 

  • Corbesier L, Vincent C, Jang S, Fornara F, Fan Q, Searle I, Giakountis A, Farrona S, Gissot L, Turnbull C, Coupland G (2007) FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science 316(5827):1030–1033

    Article  CAS  PubMed  Google Scholar 

  • Cotton S, Grangeon R, Thivierge K, Mathieu I, Ide C, Wei T, Wang A, Laliberte JF (2009) Turnip mosaic virus RNA replication complex vesicles are mobile, align with microfilaments, and are each derived from a single viral genome. J Virol 83(20):10460–10471

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Deeks MJ, Calcutt JR, Ingle EK, Hawkins TJ, Chapman S, Richardson AC, Mentlak DA, Dixon MR, Cartwright F, Smertenko AP, Oparka K, Hussey PJ (2012) A superfamily of actin-binding proteins at the actin-membrane nexus of higher plants. Curr Biol 22(17):1595–1600

    Article  CAS  PubMed  Google Scholar 

  • Ding B, Turgeon R, Parthasarathy MV (1992) Substructure of freeze-substituted plasmodesmata. Protoplasma 169(1–2):28–41

    Article  Google Scholar 

  • Doxey AC, Yaish MW, Moffatt BA, Griffith M, McConkey BJ (2007) Functional divergence in the Arabidopsis beta-1,3-glucanase gene family inferred by phylogenetic reconstruction of expression states. Mol Biol Evol 24(4):1045–1055

    Article  CAS  PubMed  Google Scholar 

  • Dunoyer P, Schott G, Himber C, Meyer D, Takeda A, Carrington JC, Voinnet O (2010) Small RNA duplexes function as mobile silencing signals between plant cells. Science 328(5980):912–916

    Article  CAS  PubMed  Google Scholar 

  • Ehlers K, Grobe Westerloh M (2013) Developmental control of plasmodesmata frequency, structure and function. In: Sokolowska K, Sowinski P (eds) Symplasmic transport in vascular plants. Springer Science + Business Media, New York, pp 41–82

    Chapter  Google Scholar 

  • Ehlers K, Kollmann R (2001) Primary and secondary plasmodesmata: Structure, origin, and functioning. Protoplasma 216(1–2):1–30

    Article  CAS  PubMed  Google Scholar 

  • Ehlers K, van Bel AJ (2010) Dynamics of plasmodesmal connectivity in successive interfaces of the cambial zone. Planta 231(2):371–385

    Article  CAS  PubMed  Google Scholar 

  • Elortza F, Nuhse TS, Foster LJ, Stensballe A, Peck SC, Jensen ON (2003) Proteomic analysis of glycosylphosphatidylinositol-anchored membrane proteins. Mol Cell Proteomics 2(12):1261–1270

    Article  CAS  PubMed  Google Scholar 

  • Epel BL (2009) Plant viruses spread by diffusion on ER-associated movement-protein-rafts through plasmodesmata gated by viral induced host beta-1,3-glucanases. Semin Cell Dev Biol 20(9):1074–1081

    Article  CAS  PubMed  Google Scholar 

  • Epel B, van Lent JWM, Cohen L, Kotlizky G, Katz A, Yahalom A (1996) A 41 kDa protein isolated from maize mesocotyl cell walls immunolocalizes to plasmodesmata. Protoplasma 191:70–78

    Article  CAS  Google Scholar 

  • Faulkner C (2013) Receptor-mediated signaling at plasmodesmata. Front Plant Sci 4:521

    Article  PubMed  PubMed Central  Google Scholar 

  • Faulkner C, Akman OE, Bell K, Jeffree C, Oparka K (2008) Peeking into pit fields: A multiple twinning model of secondary plasmodesmata formation in tobacco. Plant Cell 20(6):1504–1518

    Article  CAS  PubMed  PubMed Central  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 U S A 110(22):9166–9170

    Article  CAS  PubMed  PubMed Central  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(4), e18880

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fisher DB (2000) Long-distance transport. In: Buchanan BB, Gruissem W, Jones RL (eds) Biochemistry and molecular biology of plants. ASPB, Rockville, pp 730–785

    Google Scholar 

  • Fitzgibbon J, Beck M, Zhou J, Faulkner C, Robatzek S, Oparka K (2013) A developmental framework for complex plasmodesmata formation revealed by large-scale imaging of the Arabidopsis leaf epidermis. Plant Cell 25(1):57–70

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Foyer CH, Noctor G (2003) Redox sensing and signalling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. Physiol Plant 119:355–364

    Article  CAS  Google Scholar 

  • Fridborg I, Grainger J, Page A, Coleman M, Findlay K, Angell S (2003) TIP, a novel host factor linking callose degradation with the cell-to-cell movement of potato virus X. Mol Plant Microbe Interact 16(2):132–140

    Article  CAS  PubMed  Google Scholar 

  • Gamalei Y (1989) Structure and function of leaf minor veins in trees and herbs. Trees 3(2):96–110

    Article  Google Scholar 

  • Gisel A, Barella S, Hempel FD, Zambryski PC (1999) Temporal and spatial regulation of symplastic trafficking during development in Arabidopsis thaliana apices. Development 126(9):1879–1889

    CAS  PubMed  Google Scholar 

  • Gisel A, Hempel FD, Barella S, Zambryski P (2002) Leaf-to-shoot apex movement of symplastic tracer is restricted coincident with flowering in Arabidopsis. Proc Natl Acad Sci U S A 99(3):1713–1717

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grabski S, De Feijter AW, Schindler M (1993) Endoplasmic reticulum forms a dynamic continuum for lipid diffusion between contiguous soybean root cells. Plant Cell 5(1):25–38

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grangeon R, Agbeci M, Chen J, Grondin G, Zheng H, Laliberte JF (2012) Impact on the endoplasmic reticulum and Golgi apparatus of turnip mosaic virus infection. J Virol 86(17):9255–9265

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grangeon R, Jiang J, Wan J, Agbeci M, Zheng H, Laliberte JF (2013) 6K2-induced vesicles can move cell to cell during turnip mosaic virus infection. Front Microbio 4:351

    Article  Google Scholar 

  • Guenoune-Gelbart D, Elbaum M, Sagi G, Levy A, Epel BL (2008) 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 21(3):335–345

    Article  CAS  PubMed  Google Scholar 

  • Gupta R, Luan S (2003) Redox control of protein tyrosine phosphatases and mitogen-activated protein kinases in plants. Plant Physiol 132(3):1149–1152

    Article  CAS  PubMed  PubMed Central  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(10):1731–1741

    Article  CAS  PubMed  Google Scholar 

  • Han X, Hyun TK, Zhang M, Kumar R, Koh EJ, Kang BH, Lucas WJ, Kim JY (2014a) Auxin-callose-mediated plasmodesmal gating is essential for tropic auxin gradient formation and signaling. Dev Cell 28(2):132–146

    Article  CAS  PubMed  Google Scholar 

  • Han X, Kumar D, Chen H, Wu S, Kim JY (2014b) Transcription factor-mediated cell-to-cell signalling in plants. J Exp Bot 65(7):1737–1749

    Article  CAS  PubMed  Google Scholar 

  • Hanson MR, Sattarzadeh A (2011) Stromules: Recent insights into a long neglected feature of plastid morphology and function. Plant Physiol 155(4):1486–1492

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Helariutta Y, Fukaki H, Wysocka-Diller J, Nakajima K, Jung J, Sena G, Hauser MT, Benfey PN (2000) The SHORT-ROOT gene controls radial patterning of the Arabidopsis root through radial signaling. Cell 101(5):555–567

    Article  CAS  PubMed  Google Scholar 

  • Hofmann J, Youssef-Banora M, de Almeida-Engler J, Grundler FM (2010) The role of callose deposition along plasmodesmata in nematode feeding sites. Mol Plant Microbe Interact 23(5):549–557

    Article  CAS  PubMed  Google Scholar 

  • Iglesias VA, Meins F Jr (2000) Movement of plant viruses is delayed in a beta-1,3-glucanase-deficient mutant showing a reduced plasmodesmatal size exclusion limit and enhanced callose deposition. Plant J 21(2):157–166

    Article  CAS  PubMed  Google Scholar 

  • Jackson D, Veit B, Hake S (1994) Expression of maize KNOTTED1 related homeobox genes in the shoot apical meristem predicts patterns of morphogenesis in the vegetative shoot. Development 120:405–413

    CAS  Google Scholar 

  • Jaeger KE, Wigge PA (2007) FT protein acts as a long-range signal in Arabidopsis. Curr Biol 17(12):1050–1054

    Article  CAS  PubMed  Google Scholar 

  • Jarsch IK, Ott T (2011) Perspectives on remorin proteins, membrane rafts, and their role during plant-microbe interactions. Mol Plant Microbe Interact 24(1):7–12

    Article  CAS  PubMed  Google Scholar 

  • Joo JH, Wang S, Chen JG, Jones AM, Fedoroff NV (2005) Different signaling and cell death roles of heterotrimeric G protein alpha and beta subunits in the Arabidopsis oxidative stress response to ozone. Plant Cell 17(3):957–970

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kawade K, Horiguchi G, Tsukaya H (2010) Non-cell-autonomously coordinated organ size regulation in leaf development. Development 137(24):4221–4227

    Article  CAS  PubMed  Google Scholar 

  • Kawade K, Horiguchi G, Usami T, Hirai MY, Tsukaya H (2013) ANGUSTIFOLIA3 signaling coordinates proliferation between clonally distinct cells in leaves. Curr Biol 23(9):788–792

    Article  CAS  PubMed  Google Scholar 

  • Kawakami S, Watanabe Y, Beachy RN (2004) Tobacco mosaic virus infection spreads cell to cell as intact replication complexes. Proc Natl Acad Sci U S A 101(16):6291–6296

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim JY, Yuan Z, Jackson D (2003) Developmental regulation and significance of KNOX protein trafficking in Arabidopsis. Development 130(18):4351–4362

    Article  CAS  PubMed  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(6):2227–2231

    Article  CAS  PubMed  PubMed Central  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 U S A 102(33):11945–11950

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kobayashi K, Otegui MS, Krishnakumar S, Mindrinos M, Zambryski P (2007) INCREASED SIZE EXCLUSION LIMIT 2 encodes a putative DEVH box RNA helicase involved in plasmodesmata function during Arabidopsis embryogenesis. Plant Cell 19(6):1885–1897

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kohler RH, Hanson MR (2000) Plastid tubules of higher plants are tissue-specific and developmentally regulated. J Cell Sci 113(Pt 1):81–89

    CAS  PubMed  Google Scholar 

  • Kotlizky G, Shurtz S, Yahalom A, Malik Z, Traub O, Epel BL (1992) An improved procedure for the isolation of plasmodesmata embedded in clean maize cell walls. Plant J 2(4):623–630

    Article  Google Scholar 

  • Kovtun Y, Chiu WL, Tena G, Sheen J (2000) Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants. Proc Natl Acad Sci U S A 97(6):2940–2945

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krenz B, Windeisen V, Wege C, Jeske H, Kleinow T (2010) A plastid-targeted heat shock cognate 70kDa protein interacts with the Abutilon mosaic virus movement protein. Virology 401(1):6–17

    Article  CAS  PubMed  Google Scholar 

  • Krenz B, Jeske H, Kleinow T (2012) The induction of stromule formation by a plant DNA-virus in epidermal leaf tissues suggests a novel intra- and intercellular macromolecular trafficking route. Front Plant Sci 3:291

    Article  PubMed  PubMed Central  Google Scholar 

  • Kurata T, Ishida T, Kawabata-Awai C, Noguchi M, Hattori S, Sano R, Nagasaka R, Tominaga R, Koshino-Kimura Y, Kato T, Sato S, Tabata S, Okada K, Wada T (2005) Cell-to-cell movement of the CAPRICE protein in Arabidopsis root epidermal cell differentiation. Development 132(24):5387–5398

    Article  CAS  PubMed  Google Scholar 

  • Kwiatkowska M (1991) Autoradiographic studies on the role of plasmodesmata in the transport of gibberellin. Planta 183(2):294–299

    Article  CAS  PubMed  Google Scholar 

  • Lee J-Y, Lucas WJ (2001) Phosphorylation of viral movement proteins--regulation of cell-to-cell trafficking. Trends Microbiol 9(1):5–8

    Article  CAS  PubMed  Google Scholar 

  • Lee JY, Wang X, Cui W, Sager R, Modla S, Czymmek K, Zybaliov B, van Wijk K, Zhang C, Lu H, Lakshmanan V (2011) A plasmodesmata-localized protein mediates crosstalk between cell-to-cell communication and innate immunity in Arabidopsis. Plant Cell 23(9):3353–3373

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Levy A, Erlanger M, Rosenthal M, Epel BL (2007) A plasmodesmata-associated beta-1,3-glucanase in Arabidopsis. Plant J 49(4):669–682

    Article  CAS  PubMed  Google Scholar 

  • Lewis JD, Lazarowitz SG (2010) Arabidopsis synaptotagmin SYTA regulates endocytosis and virus movement protein cell-to-cell transport. Proc Natl Acad Sci U S A 107(6):2491–2496

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liang D, White RG, Waterhouse PM (2012) Gene silencing in Arabidopsis spreads from the root to the shoot, through a gating barrier, by template-dependent, nonvascular, cell-to-cell movement. Plant Physiol 159(3):984–1000

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liszkay A, Kenk B, Schopfer P (2003) Evidence for the involvement of cell wall peroxidase in the generation of hydroxyl radicals mediating extension growth. Planta 217(4):658–667

    Article  CAS  PubMed  Google Scholar 

  • Lucas WJ (2006) Plant viral movement proteins: Agents for cell-to-cell trafficking of viral genomes. Virology 344(1):169–184

    Article  CAS  PubMed  Google Scholar 

  • Lucas WJ, Bouche-Pillon S, Jackson DP, Nguyen L, Baker L, Ding B, Hake S (1995) Selective trafficking of KNOTTED1 homeodomain protein and its mRNA through plasmodesmata. Science 270(5244):1980–1983

    Article  CAS  PubMed  Google Scholar 

  • Lucas WJ, Balachandran S, Park J, Wolf S (1996) Plasmodesmal companion cell-mesophyll communication in the control over carbon metabolism and phloem transport: insights gained from viral movement proteins. J Exp Bot 47 Spec No:1119–1128

    Google Scholar 

  • Martens HJ, Roberts AG, Oparka KJ, Schulz A (2006) Quantification of plasmodesmatal endoplasmic reticulum coupling between sieve elements and companion cells using fluorescence redistribution after photobleaching. Plant Physiol 142(2):471–480

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meng L, Wong JH, Feldman LJ, Lemaux PG, Buchanan BB (2010) A membrane-associated thioredoxin required for plant growth moves from cell to cell, suggestive of a role in intercellular communication. Proc Natl Acad Sci U S A 107(8):3900–3905

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meng Y, Shao C, Wang H, Chen M (2011) The regulatory activities of plant microRNAs: A more dynamic perspective. Plant Physiol 157(4):1583–1595

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Munch E (1930) Material flow in plants (trans: Milburn JA, Kreeb KH). Gustav Fischer Verlag, University of Bremen, Jena

    Google Scholar 

  • Nakajima K, Sena G, Nawy T, Benfey PN (2001) Intercellular movement of the putative transcription factor SHR in root patterning. Nature 413(6853):307–311

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Oparka KJ, Roberts AG, Boevink P, Santa Cruz S, Roberts I, 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(6):743–754

    Article  CAS  PubMed  Google Scholar 

  • Ormenese S, Havelange A, Deltour R, Bernier G (2000) The frequency of plasmodesmata increases early in the whole shoot apical meristem of Sinapis alba L. during floral transition. Planta 211(3):370–375

    Article  CAS  PubMed  Google Scholar 

  • Ormenese S, Bernier G, Perilleux C (2006) Cytokinin application to the shoot apical meristem of Sinapis alba enhances secondary plasmodesmata formation. Planta 224(6):1481–1484

    Article  CAS  PubMed  Google Scholar 

  • Overall RL, Blackman LM (1996) A model of the macromolecular structure of plasmodesmata. Trends Plant Sci 1(9):307–311

    Article  Google Scholar 

  • Patrick JW (2013) Does Don Fisher’s high-pressure manifold model account for phloem transport and resource partitioning? Front Plant Sci 4:184

    Article  PubMed  PubMed Central  Google Scholar 

  • Pekker I, Alvarez JP, Eshed Y (2005) Auxin response factors mediate Arabidopsis organ asymmetry via modulation of KANADI activity. Plant Cell 17(11):2899–2910

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peragine A, Yoshikawa M, Wu G, Albrecht HL, Poethig RS (2004) SGS3 and SGS2/SDE1/RDR6 are required for juvenile development and the production of trans-acting siRNAs in Arabidopsis. Genes Dev 18(19):2368–2379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Perbal MC, Haughn G, Saedler H, Schwarz-Sommer Z (1996) Non-cell-autonomous function of the Antirrhinum floral homeotic proteins DEFICIENS and GLOBOSA is exerted by their polar cell-to-cell trafficking. Development 122(11):3433–3441

    CAS  PubMed  Google Scholar 

  • Petutschnig EK, Jones AM, Serazetdinova L, Lipka U, Lipka V (2010) The lysin motif receptor-like kinase (LysM-RLK) CERK1 is a major chitin-binding protein in Arabidopsis thaliana and subject to chitin-induced phosphorylation. J Biol Chem 285(37):28902–28911

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Porfirova S, Bergmuller E, Tropf S, Lemke R, Dormann P (2002) Isolation of an Arabidopsis mutant lacking vitamin E and identification of a cyclase essential for all tocopherol biosynthesis. Proc Natl Acad Sci U S A 99(19):12495–12500

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Provencher LM, Miao L, Sinha N, Lucas WJ (2001) Sucrose export defective1 encodes a novel protein implicated in chloroplast-to-nucleus signaling. Plant Cell 13(5):1127–1141

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raffaele S, Bayer E, Lafarge D, Cluzet S, German Retana S, Boubekeur T, Leborgne-Castel N, Carde JP, Lherminier J, Noirot E, Satiat-Jeunemaitre B, Laroche-Traineau J, Moreau P, Ott T, Maule AJ, Reymond P, Simon-Plas F, Farmer EE, Bessoule JJ, Mongrand S (2009) Remorin, a Solanaceae protein resident in membrane rafts and plasmodesmata, impairs potato virus X movement. Plant Cell 21(5):1541–1555

    Google Scholar 

  • Rennie EA, Turgeon R (2009) A comprehensive picture of phloem loading strategies. Proc Natl Acad Sci U S A 106(33):14162–14167

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rentel MC, Lecourieux D, Ouaked F, Usher SL, Petersen L, Okamoto H, Knight H, Peck SC, Grierson CS, Hirt H, Knight MR (2004) OXI1 kinase is necessary for oxidative burst-mediated signalling in Arabidopsis. Nature 427(6977):858–861

    Article  CAS  PubMed  Google Scholar 

  • Rinne PL, Kaikuranta PM, van der Schoot C (2001) The shoot apical meristem restores its symplasmic organization during chilling-induced release from dormancy. Plant J 26(3):249–264

    Article  CAS  PubMed  Google Scholar 

  • Rinne PL, Welling A, Vahala J, Ripel L, Ruonala R, Kangasjarvi J, van der Schoot C (2011) Chilling of dormant buds hyperinduces FLOWERING LOCUS T and recruits GA-inducible 1,3-beta-glucanases to reopen signal conduits and release dormancy in Populus. Plant Cell 23(1):130–146

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rivas-San Vicente M, Plasencia J (2011) Salicylic acid beyond defence: Its role in plant growth and development. J Exp Bot 62(10):3321–3338

    Article  CAS  PubMed  Google Scholar 

  • Robert HS, Friml J (2009) Auxin and other signals on the move in plants. Nat Chem Biol 5(5):325–332

    Article  CAS  PubMed  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 expansion. Plant Cell 13(1):47–60

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ruan YL, Xu SM, White R, Furbank RT (2004) Genotypic and developmental evidence for the role of plasmodesmatal regulation in cotton fiber elongation mediated by callose turnover. Plant Physiol 136(4):4104–4113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Russin WA, Evert RF, Vanderveer PJ, Sharkey TD, Briggs SP (1996) Modification of a specific class of plasmodesmata and loss of sucrose export ability in the sucrose export defective1 maize mutant. Plant Cell 8(4):645–658

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rutschow HL, Baskin TI, Kramer EM (2011) Regulation of solute flux through plasmodesmata in the root meristem. Plant Physiol 155(4):1817–1826

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sagi G, Katz A, Guenoune-Gelbart D, Epel BL (2005) Class 1 reversibly glycosylated polypeptides are plasmodesmal-associated proteins delivered to plasmodesmata via the golgi apparatus. Plant Cell 17(6):1788–1800

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sandhu AP, Randhawa GS, Dhugga KS (2009) Plant cell wall matrix polysaccharide biosynthesis. Mol Plant 2(5):840–850

    Article  CAS  PubMed  Google Scholar 

  • Schapire AL, Voigt B, Jasik J, Rosado A, Lopez-Cobollo R, Menzel D, Salinas J, Mancuso S, Valpuesta V, Baluska F, Botella MA (2008) Arabidopsis synaptotagmin 1 is required for the maintenance of plasma membrane integrity and cell viability. Plant Cell 20(12):3374–3388

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schlereth A, Moller B, Liu W, Kientz M, Flipse J, Rademacher EH, Schmid M, Jurgens G, Weijers D (2010) MONOPTEROS controls embryonic root initiation by regulating a mobile transcription factor. Nature 464(7290):913–916

    Article  CAS  PubMed  Google Scholar 

  • Schubert M, Koteyeva NK, Wabnitz PW, Santos P, Buttner M, Sauer N, Demchenko K, Pawlowski K (2011) Plasmodesmata distribution and sugar partitioning in nitrogen-fixing root nodules of Datisca glomerata. Planta 233(1):139–152

    Article  CAS  PubMed  Google Scholar 

  • Sessions A, Yanofsky MF, Weigel D (2000) Cell-cell signaling and movement by the floral transcription factors LEAFY and APETALA1. Science 289(5480):779–782

    Article  CAS  PubMed  Google Scholar 

  • Simon-Plas F, Perraki A, Bayer E, Gerbeau-Pissot P, Mongrand S (2011) An update on plant membrane rafts. Curr Opin Plant Biol 14(6):642–649

    Article  CAS  PubMed  Google Scholar 

  • Simpson C, Thomas C, Findlay K, Bayer E, Maule AJ (2009) An Arabidopsis GPI-anchor plasmodesmal neck protein with callose binding activity and potential to regulate cell-to-cell trafficking. Plant Cell 21(2):581–594

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sobczak MaG W (2008) Structure of cyst nematode feeding sites. In: Berg RH, Taylor CG (eds) Cell biology of plant nematode parasitism, vol 15, 1st edn, Plant cell monographs. Springer, Heidelberg, pp 153–187

    Google Scholar 

  • Stadler R, Lauterbach C, Sauer N (2005) Cell-to-cell movement of green fluorescent protein reveals post-phloem transport in the outer integument and identifies symplastic domains in Arabidopsis seeds and embryos. Plant Physiol 139(2):701–712

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stonebloom S, Burch-Smith T, Kim I, Meinke D, Mindrinos M, Zambryski P (2009) Loss of the plant DEAD-box protein ISE1 leads to defective mitochondria and increased cell-to-cell transport via plasmodesmata. Proc Natl Acad Sci U S A 106(40):17229–17234

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stonebloom S, Brunkard JO, Cheung AC, Jiang K, Feldman L, Zambryski P (2012) Redox states of plastids and mitochondria differentially regulate intercellular transport via plasmodesmata. Plant Physiol 158(1):190–199

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Szittya G, Burgyan J (2013) RNA interference-mediated intrinsic antiviral immunity in plants. Curr Top Microbiol Immunol 371:153–181

    CAS  PubMed  Google Scholar 

  • Thomas CL, Bayer EM, Ritzenthaler C, Fernandez-Calvino L, Maule AJ (2008) Specific targeting of a plasmodesmal protein affecting cell-to-cell communication. PLoS Biol 6(1), e7

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tilney LG, Cooke TJ, Connelly PS, Tilney MS (1991) The structure of plasmodesmata as revealed by plasmolysis, detergent extraction, and protease digestion. J Cell Biol 112(4):739–747

    Article  CAS  PubMed  Google Scholar 

  • Tilsner J, Amari K, Torrance L (2011) Plasmodesmata viewed as specialised membrane adhesion sites. Protoplasma 248(1):39–60

    Article  CAS  PubMed  Google Scholar 

  • Tilsner J, Linnik O, Louveaux M, Roberts IM, Chapman SN, Oparka KJ (2013) Replication and trafficking of a plant virus are coupled at the entrances of plasmodesmata. J Cell Biol 201(7):981–995

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsukagoshi H, Busch W, Benfey PN (2010) Transcriptional regulation of ROS controls transition from proliferation to differentiation in the root. Cell 143(4):606–616

    Article  CAS  PubMed  Google Scholar 

  • Turgeon R, Medville R (2004) Phloem loading. A reevaluation of the relationship between plasmodesmatal frequencies and loading strategies. Plant Physiol 136(3):3795–3803

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ueki S, Spektor R, Natale DM, Citovsky V (2010) ANK, a host cytoplasmic receptor for the tobacco mosaic virus cell-to-cell movement protein, facilitates intercellular transport through plasmodesmata. PLoS Pathog 6(11), e1001201

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Urbanus SL, Martinelli AP, Peter Dinh QD, Aizza LC, Dornelas MC, Angenent GC, Immink RG (2010) Intercellular transport of epidermis-expressed MADS domain transcription factors and their effect on plant morphology and floral transition. Plant J 63:60–72

    CAS  PubMed  Google Scholar 

  • van den Berg C, Willemsen V, Hage W, Weisbeek P, Scheres B (1995) Cell fate in the Arabidopsis root meristem determined by directional signalling. Nature 378(6552):62–65

    Article  PubMed  Google Scholar 

  • van den Berg C, Willemsen V, Hendriks G, Weisbeek P, Scheres B (1997) Short-range control of cell differentiation in the Arabidopsis root meristem. Nature 390(6657):287–289

    Article  PubMed  CAS  Google Scholar 

  • Vaten A, Dettmer J, Wu S, Stierhof YD, Miyashima S, Yadav SR, Roberts CJ, Campilho A, Bulone V, Lichtenberger R, Lehesranta S, Mahonen AP, Kim JY, Jokitalo E, Sauer N, Scheres B, Nakajima K, Carlsbecker A, Gallagher KL, Helariutta Y (2011) Callose biosynthesis regulates symplastic trafficking during root development. Dev Cell 21(6):1144–1155

    Article  CAS  PubMed  Google Scholar 

  • Vaucheret H (2006) Post-transcriptional small RNA pathways in plants: Mechanisms and regulations. Genes Dev 20(7):759–771

    Article  CAS  PubMed  Google Scholar 

  • Verchot-Lubicz J, Torrance L, Solovyev AG, Morozov SY, Jackson AO, Gilmer D (2010) Varied movement strategies employed by triple gene block-encoding viruses. Mol Plant Microbe Interact 23(10):1231–1247

    Article  CAS  PubMed  Google Scholar 

  • Verma DP, Hong Z (2001) Plant callose synthase complexes. Plant Mol Biol 47(6):693–701

    Article  CAS  PubMed  Google Scholar 

  • Waigmann E, Ueki S, Trutnyeva K, Citovsky V (2004) The ins and outs of nondestructive cell-to-cell and systemic movement of plant viruses. Crit Rev Plant Sci 23(3):195–250

    Article  CAS  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(6):2315–2329

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • White RG, Barton DA (2011) The cytoskeleton in plasmodesmata: A role in intercellular transport? J Exp Bot 62(15):5249–5266

    Article  CAS  PubMed  Google Scholar 

  • White RG, Badelt K, Overall RL, Vesk M (1994) Actin associated with plasmodesmata. Protoplasma 180(3–4):169–184

    Article  CAS  Google Scholar 

  • Wildermuth MC, Dewdney J, Wu G, Ausubel FM (2001) Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414(6863):562–565

    Article  CAS  PubMed  Google Scholar 

  • Xie B, Wang X, Zhu M, Zhang Z, Hong Z (2011) CalS7 encodes a callose synthase responsible for callose deposition in the phloem. Plant J 65(1):1–14

    Article  CAS  PubMed  Google Scholar 

  • Yadav RK, Perales M, Gruel J, Girke T, Jonsson H, Reddy GV (2011) WUSCHEL protein movement mediates stem cell homeostasis in the Arabidopsis shoot apex. Genes Dev 25(19):2025–2030

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zavaliev R, Sagi G, Gera A, Epel BL (2010) The constitutive expression of Arabidopsis plasmodesmal-associated class 1 reversibly glycosylated polypeptide impairs plant development and virus spread. J Exp Bot 61(1):131–142

    Article  CAS  PubMed  Google Scholar 

  • Zavaliev R, Ueki S, Citovsky V, Epel BL (2011) Biology of callose (beta-1,3-glucan) turnover at plasmodesmata. Protoplasma 248(1):117–130

    Article  CAS  PubMed  Google Scholar 

  • Zavaliev R, Levy A, Gera A, Epel BL (2013) Subcellular dynamics and role of Arabidopsis beta-1,3-glucanases in cell-to-cell movement of tobamoviruses. Mol Plant Microbe Interact 26(9):1016–1030

    Article  CAS  PubMed  Google Scholar 

  • Zhao J, Liu Q, Zhang H, Jia Q, Hong Y, Liu Y (2013) The rubisco small subunit is involved in tobamovirus movement and Tm-2(2)-mediated extreme resistance. Plant Physiol 161(1):374–383

    Article  CAS  PubMed  Google Scholar 

  • Zhou J, Wang X, Lee JY, Lee JY (2013) Cell-to-cell movement of two interacting AT-hook factors in Arabidopsis root vascular tissue patterning. Plant Cell 25(1):187–201

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

We thank Krzysztof Bobik, Jacob Brunkard, and John Zupan for superb help with the illustrations. TBS thanks the University of Tennessee at Knoxville for start-up funds.

Author information

Authors and Affiliations

  1. Department of Biochemistry, Cellular and Molecular Biology, University of Tennessee, Knoxville, TN, 37996, USA

    Tessa M. Burch-Smith

  2. Department of Plant and Microbial Biology, University of California, Berkeley, CA, 94720, USA

    Patricia C. Zambryski

Authors
  1. Tessa M. Burch-Smith
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Patricia C. Zambryski
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Patricia C. Zambryski .

Editor information

Editors and Affiliations

  1. Molecular Biology and Plant Virology, Universität Stuttgart Institute of Biology, Stuttgart, Germany

    Tatjana Kleinow

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Burch-Smith, T.M., Zambryski, P.C. (2016). Regulation of Plasmodesmal Transport and Modification of Plasmodesmata During Development and Following Infection by Viruses and Viral Proteins. In: Kleinow, T. (eds) Plant-Virus Interactions. Springer, Cham. https://doi.org/10.1007/978-3-319-25489-0_4

Download citation

Publish with us

Policies and ethics

Search

Navigation