Abstract
A significant amount of work has been expended to identify the elusive components of plasmodesmata (PD) to help understand their structure, as well as how proteins are targeted to them. This review focuses on the role that lipid membranes may play in defining PD both structurally and as subcellular targeting addresses. Parallels are drawn to findings in other areas of research which focus on the lateral segregation of membrane domains and the generation of three-dimensional organellar shapes from flat lipid bilayers. We conclude that consideration of the protein–lipid interactions in cell biological studies of PD components and PD-targeted proteins may yield new insights into some of the many open questions regarding these unique structures.
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Abbreviations
- DRM:
-
Detergent resistant membrane
- DT:
-
Desmotubule
- EM:
-
Electron microscopy
- ER:
-
Endoplasmic reticulum
- GFP:
-
Green fluorescent protein
- GPI:
-
Glycosyl phosphatidyl inositol
- Ld :
-
Liquid-disordered
- Lo :
-
Liquid-ordered
- MP:
-
Movement protein
- PD:
-
Plasmodesma(ta)
- PDLP:
-
Plasmodesmata-located protein
- PDCB:
-
Pd callose binding protein
- PIP:
-
Phosphatidylinositol phosphate
- PMTV:
-
Potato mop-top virus
- PVX:
-
Potato virus X
- So :
-
Solid-ordered
- TMD:
-
Transmembrane domain
- TMV:
-
Tobacco mosaic virus
References
Amari K, Boutant E, Hofmann C, Schmitt-Keichinger C, Fernandez-Calvino L, Didier P, Lerich A, Mutterer J, Thomas CL, Heinlein M, Mély Y, Maule AJ, Ritzenthaler C (2010) A family of plasmodesmal proteins with receptor-like properties for plant viral movement proteins. PLoS Pathog. doi:10.1371/journal.ppat.1001119
Ambroggio E, Sorre B, Bassereau P, Goud B, Manneville JB, Antonny B (2010) ArfGAP1 generates an Arf1 gradient on continuous lipid membranes displaying flat and curved regions. EMBO J 29:292–303
Andersson MX, Goksör M, Sandelius AS (2007) Optical manipulation reveals strong attracting forces at membrane contact sites between endoplasmic reticulum and chloroplasts. J Biol Chem 282:1170–1174
Auth T, Gov NS (2009) Diffusion in a fluid membrane with a flexible cortical cytoskeleton. Biophys J 96:818–830
Avisar D, Prokhnevsky AI, Dolja VV (2008) Class VIII myosins are required for plasmodesmatal localization of a closterovirus Hsp70 homolog. J Virol 82:2836–2843
Avisar D, bu-Abied M, Belausov E, Sadot E, Hawes C, Sparkes IA (2009) A comparative study of the involvement of 17 Arabidopsis myosin family members on the motility of Golgi and other organelles. Plant Physiol 150:700–709
Backues SK, Konopka CA, McMichael CM, Bednarek SY (2007) Bridging the divide between cytokinesis and cell expansion. Curr Opin Plant Biol 10:607–615
Badelt K, White RG, Overall RL, Vesk M (1994) Ultrastructural specializations in the cell wall sleeve around plasmodesmata. Am J Bot 81:1422–1427
Bagatolli LA, Ipsen JH, Simonsen AC, Mouritsen OG (2010) An outlook on organization of lipids in membranes: searching for a realistic connection with the organization of biological membranes. J Lipid Res 49:378–389
Baluska F, Samaj J, Napier R, Volkmann D (1999) Maize calreticulin localizes preferentially to plasmodesmata in root apex. Plant J 19:481–488
Baluska F, Cvrcková 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 126:39–46
Bariola P, Retelska D, Stasiak A, Kammerer R, Fleming A, Hijri M, Frank S, Farmer E (2004) Remorins form a novel family of coiled coil-forming oligomeric and filamentous proteins associated with apical, vascular and embryonic tissues in plants. Plant Mol Biol 55:579–594
Bauer M, Pelkmans L (2006) A new paradigm for membrane-organizing and -shaping scaffolds. FEBS Lett 580:5559–5564
Bednarek SY, Falbel TG (2002) Membrane trafficking during plant cytokinesis. Traffic 3:621–629
Bhat R, Panstruga R (2005) Lipid rafts in plants. Planta 223:5–19
Blackman LM, Overall RL (1998) Immunolocalisation of the cytoskeleton to plasmodesmata of Chara corallina. Plant J 14:733–741
Blackman LM, Overall RL (2001) Structure and function of plasmodesmata. Aust J Plant Physiol 28:709–727
Blackman LM, Harper JDI, Overall RL (1999) Localization of a centrin-like protein to higher plant plasmodesmata. Eur J Cell Biol 78:297–304
Boevink P, Oparka KJ, Santa Cruz S, Martin B, Betteridge A, Hawes C (1998) Stacks on tracks: the plant Golgi apparatus traffics on an actin/ER network. Plant J 15:441–447
Borner GHH, Sherrier DJ, Weimar T, Michaelson LV, Hawkins ND, MacAskill A, Napier JA, Beale MH, Lilley KS, Dupree P (2005) Analysis of detergent-resistant membranes in Arabidopsis. Evidence for plasma membrane lipid rafts. Plant Physiol 137:104–116
Bortolotti C, Murillo I, Fontanet P, Coca M, San Segundo B (2005) Long-distance transport of the maize pathogenesis-related PRms protein through the phloem in transgenic tobacco plants. Plant Sci 168:813–821
Botha CEJ, Cross RHM (2000) Towards reconciliation of structure with function in plasmodesmata—who is the gatekeeper? Micron 31:713–721
Botha CEJ, Hartley BJ, Cross RHM (1993) The ultrastructure and computer-enhanced digital image analysis of plasmodesmata at the kranz mesophyll-bundle sheath interface of Themeda triandra var. imberbis (Retz) A. Camus in conventionally fixed blades. Ann Bot 72:255–261
Boutant E, Didier P, Niehl A, Mély Y, Ritzenthaler C, Heinlein M (2010) Fluorescent protein recruitment assay for demonstration and analysis of in vivo protein interactions in plant cells and its application to Tobacco mosaic virus movement protein. Plant J 62:171–177
Brandizzi F, Frangne N, Marc-Martin S, Hawes C, Neuhaus JM, Paris M (2002) The destination for single-pass membrane proteins is influenced markedly by the length of the hydrophobic domain. Plant Cell 14:1077–1092
Brill LM, Nunn RS, Kahn TW, Yeager M, Beachy RN (2000) Recombinant tobacco mosaic virus movement protein is an RNA-binding, α-helical membrane protein. Proc Natl Acad Sci USA 97:7112–7117
Cantrill LC, Overall RL, Goodwin PB (1999) Cell-to-cell communication via plant endomembranes. Cell Biol Int 23:653–661
Chen MH, Sheng J, Hind G, Handa AK, Citovsky V (2000) Interaction between the tobacco mosaic virus movement protein and host cell pectin methylesterases is required for viral cell-to-cell movement. EMBO J 19:913–920
Chen M-H, Tian G-W, Gafni Y, Citovsky V (2005) Effects of calreticulin on viral cell-to-cell movement. Plant Physiol 138:1866–1876
Chernomordik LV, Zimmerberg J, Kozlov MM (2006) Membranes of the world unite! J Cell Biol 175:201–207
Ciczora Y, Callens N, Penin F, Pecheur EI, Dubuisson J (2007) Transmembrane domains of hepatitis C virus envelope glycoproteins: residues involved in E1E2 heterodimerization and involvement of these domains in virus entry. J Virol 81:2372–2381
Cook ME, Graham LE, Botha CEJ, Lavin CA (1997) Comparative ultrastructure of plasmodesmata of Chara and selective bryophytes: toward an elucidation of the evolutionary origin of plant plasmodesmata. Am J Bot 84:1169–1178
Cory GOC, Cullen P (2007) Membrane curvature: the power of bananas, zeppelins and boomerangs. 17:R455–R457
Cowan GH, Lioliopoulou F, Ziegler A, Torrance L (2002) Subcellular localisation, protein interactions, and RNA binding of potato mop-top virus triple gene block proteins. Virology 298:106–115
Craig S, Staehelin LA (1988) High pressure freezing of intact plant tissues. Evaluation and characterization of novel features of the endoplasmic reticulum and associated membrane systems. Eur J Cell Biol 46:81–93
Crawford KM, Zambryski PC (2000) Subcellular localization determines the availability of non-targeted proteins to plasmodesmatal transport. Curr Biol 10:1032–1040
de Brito OM, Scorrano L (2008) Mitofusin 2 tethers endoplasmic reticulum to mitochondria. Nature 456:605–610
Delmer DP, Volokita M, Solomon M, Fritz U, Delphendahl W, Herth W (1993) A monoclonal antibody recognizs a 65 kDa higher plant membrane polypeptide which undergoes cation dependent association with callose synthase in vitro and colocalizes with sites of high callose deposition in vivo. Protoplasma 176:33–42
Diener AC, Li HX, Zhou WX, Whoriskey WJ, Nes WD, Fink GR (2000) STEROL METHYLTRANSFERASE 1 controls the level of cholesterol in plants. Plant Cell 12:853–870
Ding B, Turgeon R, Parthasarathy MV (1992) Substructure of freeze-substituted plasmodesmata. Protoplasma 169:28–41
Ding B, Kwon M-O, Warnberg L (1996) Evidence that actin filaments are involved in controlling the permeability of plasmodesmata in tobacco mesophyll. Plant J 10:157–164
Dorokhov YL, Mäkinen K, Frolova OY, Merits A, Saarinen J, Kalkkinen N, Atabekov JG, Saarma M (1999) A novel function for a ubiquitous plant enzyme pectin methylesterase: the host-cell receptor for the tobacco mosaic virus movement protein. FEBS Lett 461:223–228
Dowhan W, Bogdanov M (2009) Lipid-dependent membrane protein topogenesis. Ann Rev Biochem 78:515–540
Downes CP, Gray A, Lucocq JM (2005) Probing phosphoinositide functions in signaling and membrane trafficking. Trends Cell Biol 15:259–268
Drin G, Antonny B (2010) Amphipathic helices and membrane curvature. FEBS Lett 584:1840–1847
Drin G, Morello V, Casella JF, Gounon P, Antonny B (2008) Asymmetric tethering of flat and curved lipid membranes by a golgin. Science 320:670–673
Ehlers K, Kollmann R (1996) Formation of branched plasmodesmata in regenerating Solanum nigrum protoplasts. Planta 199:126–138
Ehlers K, Kollmann R (2001) Primary and secondary plasmodesmata: structure, origin and functioning. Protoplasma 216:1–30
Ehlers K, Schulz M, Kollmann R (1996) Subcellular localization of ubiquitin in plant protoplasts and the function of ubiquitin in selective degradation of outer-wall plasmodesmata in regenerating protoplasts. Planta 199:139–151
English AR, Zurek N, Voeltz GK (2009) Peripheral ER structure and function. Curr Opin Cell Biol 21:596–602
Epel BL (2009) Plant viruses spread by diffusion on ER-associated movement-protein-rafts through plasmodesmata gated by viral induced host β-1, 3-glucanases. Sem Cell Dev Biol 20:1074–1081
Escobar NM, Haupt S, Thow G, Boevink P, Chapman S, Oparka KJ (2003) High-throughput viral expression of cdna-green fluorescent protein fusions reveals novel subcellular addresses and identifies unique proteins that interact with plasmodesmata. Plant Cell 15:1507–1523
Fagone P, Jackowski S (2009) Membrane phospholipid synthesis and endoplasmic reticulum function. J Lipid Res 50:S311–S316
Farsad K, De Camilli PD (2003) Mechanisms of membrane deformation. Curr Opin Cell Biol 15:372–381
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 20:1504–1518
Faulkner CR, Blackman LM, Collings DA, Cordwell SJ, Overall RL (2009) Anti-tropomyosin antibodies co-localise with actin microfilaments and label plasmodesmata. Eur J Cell Biol 88:357–369
Fischer U, Men S, Grebe M (2004) Lipid function in plant cell polarity. Curr Opin Plant Biol 7:670–676
Fitzgibbon J, Bell K, King E, Oparka K (2010) Super-resolution imaging of plasmodesmata using 3D-structured illumination microscopy (3D-SIM). Plant Physiol. doi:10.1104/pp.110.157941
Fleurat-Lessard P, Bouché-Pillon S, Leloup C, Lucas WJ, Serrano R, Bonnemain J-L (1995) Absence of plasma membrane H+-ATPase in plasmodesmata located in pit-fields of the young reactive pulvinus of Mimosa pudica L. Protoplasma 188:180–185
Frost A, Unger VM, De Camilli P (2009) The BAR domain superfamily: membrane-molding macromolecules. Cell 137:191–196
Gechev TS, Gadjev IZ, Hille J (2004) An extensive microarray analysis of AAL-toxin-induced cell death in Arabidopsis thaliana brings new insights into the complexity of programmed cell death in plants. Cell Mol Life Sci 61:1185–1197
Gechev TS, Ferwerda MA, Mehterov N, Laloi C, Qureshi MK, Hille J (2008) Arabidopsis AAL-toxin-resistant mutant atr1 shows enhanced tolerance to programmed cell death induced by reactive oxygen species. Biochem Biophys Res Commun 375:639–644
Glockmann C, Kollmann R (1996) Structure and development of cell connections in the phloem of Metasequoia glyptostroboides needles I. Ultrastructural aspects of modified primary plasmodesmata in Strasburger cells. Protoplasma 193:191–203
Goetz JG, Genty H, St-Pierre P, Dang T, Joshi B, Sauve R, Vogl W, Nabi IR (2007) Reversible interactions between smooth domains of the endoplasmic reticulum and mitochondria are regulated by physiological cytosolic Ca2+ levels. J Cell Sci 120:3553–3564
Golomb L, bu-Abied M, Belausov E, Sadot E (2008) Different subcellular localizations and functions of Arabidopsis myosin VIII. BMC Plant Biol 8:3
Grabski S, de Feijter AW, Schindler M (1993) Endoplasmic reticulum forms a dynamic continuum for lipid diffusion between contiguous soybean root cells. Plant Cell 5:25–38
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 Microb Interact 21:335–345
Gupton SL, Collings DA, Allen NS (2002) Endoplasmic reticulum targeted GFP reveals ER organization in tobacco NT-1 cells during cell division. Plant Physiol Biochem 44:95–105
Hancock JF (2006) Lipid rafts: contentious only from simplistic standpoints. Nat Rev Mol Cell Biol 7:456–462
Hansen CG, Nichols BJ (2010) Exploring the caves: cavins, caveolins and caveolae. Trends Cell Biol 20:177–186
Hanzal-Bayer MF, Hancock JF (2007) Lipid rafts and membrane traffic. FEBS Lett 581:2098–2104
Haucke V, Di Paolo G (2007) Lipids and lipid modifications in the regulation of membrane traffic. Curr Opin Cell Biol 19:426–435
Haupt S, Cowan GH, Ziegler A, Roberts AG, Oparka KJ, Torrance L (2005) Two plant-viral movement proteins traffic in the endocytic recycling pathway. Plant Cell 17:164–181
Hawes CR, Juniper BE, Horne JC (1981) Low and high voltage electron microscopy of mitosis and cytokinesis in maize roots. Planta 152:397–407
Heinlein M, Padgett HS, Gens JS, Pickard BG, Casper SJ, Epel BL, Beachy RN (1998) Changing patterns of localization of the Tobacco mosaic virus movement protein and replicase to the endoplasmic reticulum and microtubules during infection. Plant Cell 10:1107–1120
Helms JB, Zurzolo C (2004) Lipids as targeting signals: lipid rafts and intracellular trafficking. Traffic 5:247–254
Hepler PK (1982) Endoplasmic reticulum in the formation of the cell plate and plasmodesmata. Protoplasma 111:121–133
Hepler PK, Palevitz BA, Lancelle SA, McCauley MM, Lichtscheidl L (1990) Cortical endoplasmic reticulum in plants. J Cell Sci 96:355–373
Herrmann C, Wary J, Travers F, Barman T (1992) Effect of 2, 3-butanedione monoxime on myosin and myofibrillar ATPases. An example of an uncompetitive inhibitor. Biochemistry 31:12227–12232
Holmes KC, Popp D, Gebhard W, Kabsch W (1990) Atomic model of the actin filament. Nature 347:44–49
Holthuis JCM, Levine TP (2005) Lipid traffic: floppy drives and a superhighway. Nat Rev Mol Cell Biol 6:209–220
Hölttä-Vuori M, Uronen R-L, Repakova J, Salonen E, Vattulainen I, Panula P, Li Z, Bittman R, Ikonen E (2008) BODIPY-cholesterol: a new tool to visualize sterol trafficking in living cells and organisms. Traffic 9:1839–1849
Howard AR, Heppler ML, Ju HJ, Krishnamurthy K, Payton ME, Verchot-Lubicz J (2004) Potato virus X TGBp1 induces plasmodesmata gating and moves between cells in several host species whereas CP moves only in N. benthamiana leaves. Virology 328:185–197
Hu J, Shibata Y, Voss C, Shemesh T, Li Z, Coughlin M, Kozlov MM, Rapoport TA, Prinz WA (2008) Membrane proteins of the endoplasmic reticulum induce high-curvature tubules. Science 319:1247–1250
Hu J, Shibata Y, Zhu PP, Voss C, Rismanchi N, Prinz WA, Rapoport TA, Blackstone C (2009) A class of dynamin-like gtpases involved in the generation of the tubular er network. Cell 138:549–561
Huang B (2010) Super-resolution optical microscopy: multiple choices. Curr Opin Chem Biol 14:10–14
Hurley JH, Meyer T (2001) Subcellular targeting by membrane lipids. Curr Opin Cell Biol 13:146–152
Itoh T, Takenawa T (2009) Mechanisms of membrane deformation by lipid-binding domains. Prog Lipid Res 48:298–305
Jacobson K, Mouritsen OG, Anderson RGW (2007) Lipid rafts: at a crossroad between cell biology and physics. Nat Cell Biol 9:7–14
Janmey PA, Kinnunen PKJ (2006) Biophysical properties of lipids and dynamic membranes. Trends Cell Biol 16:538–546
Ju HJ, Samuels TD, Wang Y-S, Blancaflor E, Payton M, Mitra R, Krishnamurty K, Nelson RS, Verchot-Lubicz J (2005) The potato virus X TGBp2 movement protein associates with endoplasmic reticulum-derived vesicles during virus infection. Plant Physiol 138:1877–1895
Kierszniowska S, Seiwert B, Schulze WX (2009) Definition of Arabidopsis sterol-rich membrane microdomains by differential treatment with methyl-β-cyclodextrin and quantitative proteomics. Mol Cell Proteomics 8:612–623
Klopfenstein DR, Klumperman J, Lustig A, Kammerer RA, Oorschot V, Hauri H-P (2001) Subdomain-specific localization of CLIMP-63 (p63) in the endoplasmic reticulum is mediated by its luminal-helical segment. J Cell Biol 153:1287–1299
Knight A, Kendrick-Jones J (1993) A myosin-like protein from a higher plant. J Mol Biol 231:148–154
Kollmann R, Glockmann C (1991) Studies on graft unions III: on the mechanism of secondary formation of plasmodesmata at the graft interface. Protoplasma 165:71-85
Krishnamurty K, Mitra R, Payton ME, Verchot-Lubicz J (2002) Cell-to-cell movement of the PVX 12 k, 8 k, or coat proteins may depend on the host, leaf developmental stage, and the PVX 25 k protein. Virology 300:269–281
Krishnamurty K, Heppler M, Mitra R, Blancaflor E, Payton M, Nelson RS, Verchot-Lubicz J (2003) The Potato virus X TGBp3 protein associates with the ER network for virus cell-to-cell movement. Virology 309:269–281
Kühn C, Franceschi VR, Schulz A, Lemoine R, Frommer WB (1997) Macromolecular trafficking indicated by localization and turnover of sucrose transporters in enucleate sieve elements. Science 275:1298–1300
Kusumi A, Suzuki K (2005) Toward understanding the dynamics of membrane-raft-based molecular interactions. Biochim Biophys Acta Mol Cell Res 1746:234–251
Kusumi A, Nakada C, Ritchie K, Murase K, Suzuki H, Murakoshi H, Kasai RS, Kondo J, Fujiwara T (2005) Paradigm shift of the plasma membrane concept from the two-dimensional continuum fluid to the partitioned fluid: high-speed single-molecule tracking of membrane molecules. Annu Rev Biophys Biomol Struct 34:351–378
Laloi M, Perret AM, Chatre L, Melser S, Cantrel C, Vaultier MN, Zachowski A, Bathany K, Schmitter JM, Vallet M, Lessire R, Hartmann MA, Moreau P (2007) Insights into the role of specific lipids in the formation and delivery of lipid microdomains to the plasma membrane of plant cells. Plant Physiol 143:461–472
Lalonde S, Weise A, Walsh RP, Ward JM, Frommer WB (2003) Fusion to GFP blocks intercellular trafficking of the sucrose transporter SUT1 leading to accumulation in companion cells. BMC Plant Biol 3:8
Lee J-Y, Taoka K-I, Yoo B-C, Ben-Nissan G, Kim D-J, Lucas WJ (2005) Plasmodesmal-associated protein kinase in tobacco and Arabidopsis recognizes a subset of non-cell autonomous proteins. Plant Cell 17:2817–2831
Lee KP, Yuan JP, Hong JH, So I, Worley PF, Muallem S (2010a) An endoplasmic reticulum/plasma membrane junction: STIM1/Orai1/TRPCs. FEBS Lett 584:2022–2027
Lee S-C, Wu C-H, Wang C-W (2010b) Traffic of a viral movement protein complex to the highly curved tubules of the cortical endoplasmic reticulum. Traffic 11:912–930
Lefebvre B, Timmers T, Mbengue M, Moreau S, Hervé C, Tóth K, Bittencourt-Silvestre J, Klaus D, Deslandes L, Godiard L, Murray JD, Udvardi MK, Raffaele S, Mongrand S, Cullimore J, Gamas P, Niebel A, Ott T (2010) A remorin protein interacts with symbiotic receptors and regulates bacterial infection. Proc Natl Acad Sci USA 107:2343–2348
Lemmon MA, Flanagan JM, Hunt JF, Adair BD, Bormann BJ, Dempsey CE, Engelman DM (1992) Glycophorin a dimerization is driven by specific interactions between transmembrane alpha-helices. J Biol Chem 267:7683-7689
Levine T, Rabouille C (2005) Endoplasmic reticulum: one continuous network compartmentalized by extrinsic cues. Curr Opin Cell Biol 17:362–368
Levy A, Erlanger M, Rosenthal M, Epel B (2007) A plasmodesmata-associated β-1, 3-glucanase in Arabidopsis. Plant J 49:669–682
Li JF, Nebenführ A (2007) Organelle targeting of myosin XI is mediated by two globular tail subdomains with separate cargo binding sites. J Biol Chem 282:20593–20602
Li J-F, Nebenführ A (2008) The tail that wags the dog: the globular tail domain defines the function of myosin V/XI. Traffic 9:290–298
Li X-D, Jung HS, Mabuchi K, Craig R, Ikebe M (2006) The globular tail domain of myosin Va functions as an inhibitor of the myosin Va motor. J Biol Chem 281:21789–21798
Lichtenberg D, Goñi FM, Heerklotz H (2005) Detergent-resistant membranes should not be identified with membrane rafts. Trends Biochem Sci 30:430–436
Lichtscheidl IK, Lancelle SA, Hepler PK (1990) Actin-endoplasmic reticulum complexes in Drosera. Their structural relationship with plasmalemma, nucleus, and organelles in cells prepared by high pressure freezing. Protoplasma 155:116–126
Lingwood D, Simons K (2010) Lipid rafts as a membrane-organizing principle. Science 327:46–50
Liu J, Taylor DW, Krementsova EB, Trybus KM, Taylor KA (2006) Three-dimensional structure of the myosin V inhibited state by cryoelectron tomography. Nature 442:208–211
Lucas WJ (2006) Plant viral movement proteins: agents for cell-to-cell trafficking of viral geneomes. Virology 344:169–184
Lucas WJ, Ham BK, Kim JY (2009) Plasmodesmata—bridging the gap between neighboring plant cells. Trends Cell Biol 19:495–503
Luedeke C, Frei SB, Sbalzarini I, Schwarz H, Spang A, Barral Y (2005) Septin-dependent compartmentalization of the endoplasmic reticulum during yeast polarized growth. J Cell Biol 169:897–908
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 142:471–480
Martínez-Gil L, Sanchez-Navarro JA, Cruz A, Pallas V, Perez-Gil J, Mingarro I (2009) Plant virus cell-to-cell movement is not dependent on the transmembrane disposition of its movement protein. J Virol 83:5535–5543
Maule AJ (2008) Plasmodesmata: structure, function and biogenesis. Curr Opin Plant Biol 11:680–686
Melcher U (2000) The ‘30 K’ superfamily of viral movement proteins. J Gen Virol 81:257–266
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 USA 107:3900–3905
Miernyk JA, Thelen JJ (2008) Biochemical approaches for discovering protein–protein interactions. Plant J 53:597–609
Mitra K, Ubarretxena-Belandia I, Taguchi T, Warren G, Engelman DM (2004) Modulation of the bilayer thickness of exocytic pathway membranes by membrane proteins rather than cholesterol. Proc Natl Acad Sci USA 101:4083–4088
Mongrand S, Morel J, Laroche J, Claverol S, Carde J, Hartmann MA, Bonneu M, Simon-Plas F, Lessire R, Bessoule JJ (2004) Lipid rafts in higher plant cells—purification and characterization of triton X-100-insoluble microdomains from tobacco plasma membrane. J Biol Chem 279:36277–36286
Moore PJ, Fenczik CA, Deom CM, Beachy RN (1992) Developmental changes in plasmodesmata in transgenic tobacco expressing the movement protein of tobacco mosaic virus. Protoplasma 170:115–127
Morozov SY, Solovyev AG (2003) Triple gene block: modular design of a multifunctional machine for plant virus movement. J Gen Virol 84:1351–1366
Mouritsen OG (2010) The liquid-ordered state comes of age. Biochim Biophys Acta 1798:1286–1288
Munnik T, Testerink C (2009) Plant phospholipid signaling: “in a nutshell”. J Lipid Res 50:S260–S265
Murillo I, Cavallarin L, San Segundo B (1997) The maize pathogenesis-related PRms protein localizes to plasmodesmata in maize radicles. Plant Cell 9:145–156
Nziengui H, Bouhidel K, Pillon D, Der C, Marty F, Schoefs B (2007) Reticulon-like proteins in Arabidopsis thaliana: structural organization and ER localization. FEBS Lett 581:3356–3362
Oparka K (2004) Getting the message across: how do plant cells exchange macromolecular complexes? Trends Plant Sci 9:33–41
Oparka KJ, Turgeon R (1999) Sieve elements and companion cells-traffic control centers of the phloem. Plant Cell 11:739–750
Oparka KJ, Prior DAM, Crawford JW (1994) Behavior of plasma-membrane, cortical ER and plasmodesmata during plasmolysis of onion epidermal-cells. Plant Cell Environ 17:163–171
Oparka KJ, Prior DA, Santa Cruz S, Padgett HS, Beachy RN (1997) Gating of epidermal plasmodesmata is restricted to the leading edge of expanding infection sites of tobacco mosaic virus (TMV). Plant J 12:781–789
Oparka KJ, Roberts AG, Boevink P, Santa Cruz S, Roberts IM, Pradel KS, Imlau A, Kotlizky G, Sauer N, Epel BL (1999) Simple, but not branched, plasmodesmata allow the nonspecific trafficking of proteins in developing tobacco leaves. Cell 97:743–754
Overall RL, Blackman LM (1996) A model of the macro-molecular structure of plasmodesmata. Trends Plant Sci 1:307–311
Overall RL, Wolfe J, Gunning BES (1982) Intercellular communication in Azolla roots: I. Ultrastructure of plasmodesmata. Protoplasma 111:134–150
Park SH, Blackstone C (2010) Further assembly required: construction and dynamics of the endoplasmic reticulum network. EMBO Rep 11:515–521
Parton RG, Richards AA (2003) Lipid rafts and caveolae as portals for endocytosis: new insights and common mechanisms. Traffic 4:724-738
Perinetti G, Müller T, Spaar A, Polishchuk R, Luini A, Egner A (2009) Correlation of 4Pi and electron microscopy to study transport through single Golgi stacks in living cells with super resolution. Traffic 10:379–391
Pike LJ (2006) Rafts defined: a report on the keystone symposium on lipid rafts and cell function. J Lipid Res 47:1597–1598
Pike LJ (2009) The challenge of lipid rafts. J Lipid Res 50:S323–S328
Pleskot R, Potocký M, Pejchar P, Linek J, Bezvoda R, Martinec J, Valentova O, Novotna Z, Zárský V (2010) Mutual regulation of plant phospholipase D and the actin cytoskeleton. Plant J 62:494–507
Praefcke GJK, McMahon HT (2004) The dynamin superfamily: universal membrane tubulation and fission molecules? Nat Rev Mol Cell Biol 5:133–147
Prekeris R, Gould GW (2008) Breaking up is hard to do—membrane traffic in cytokinesis. J Cell Sci 121:1569–1576
Radford JE, White RG (1998) Localization of a myosin-like protein to plasmodesmata. Plant J 14:743–750
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 21:1541–1555
Rayment I, Rypniewski WR, Schmidt-Bäse K, Smith R, Tomchick DR, Benning MM, Winkelmann DA, Wesenberg G, Holden HM (1993) Three-dimensional structure of myosin subfragment-1: a molecular motor. Science 261:50–58
Reichel C, Beachy RN (1998) Tobacco mosaic virus infection induces severe morphological changes of the endoplasmic reticulum. Proc Natl Acad Sci USA 95113:11169–11174
Reichelt S, Knight AE, Hodge TP, Baluska F, Samaj J, Volkmann D, Kendrick-Jones J (1999) Characterization of the unconventional myosin VIII in plant cells and its localization at the post-cytokinetic cell wall. Plant J 19:555–567
Rinne PLH, Kaikuranta PM, van der Schoot C (2001) The shoot apical meristem restores its symplastic organisation during chilling-induced release from dormancy. Plant J 26:249–264
Robards AW (1968a) A new interpretation of plasmodesmatal ultrastructure. Planta 82:200–210
Robards AW (1968b) Desmotubule—a plasmodesmatal substructure. Nature 218:784
Roberts AG, Oparka KJ (2003) Plasmodesmata and the control of symplastic transport. Plant Cell Environ 26:103–124
Robinson-Beers K, Evert RF (1991) Fine structure of plasmodesmata in mature leaves of sugarcane. Planta 184:307–318
Ronchi P, Colombo S, Francolini M, Borgese N (2008) Transmembrane domain-dependent partitioning of membrane proteins within the endoplasmic reticulum. J Cell Biol 181:105–118
Roux A, Cuvelier D, Nassoy P, Prost J, Bassereau P, Goud B (2005) Role of curvature and phase transition in lipid sorting and fission of membrane tubules. EMBO J 24:1537–1545
Rutherford S, Moore I (2002) The arabidopsis rab GTPase family: another enigma variation. Curr Opin Plant Biol 5:518–528
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 17:1788–1800
Sakamoto T, Wang F, Schmitz S, Xu Y, Xu Q, Molloy JE, Veigel C, Sellers JR (2003) Neck length and processivity of myosin V. J Biol Chem 278:29201–29207
Samuels TD, Ju H-J, Ye C-M, Motes CM, Blancaflor EB, Verchot-Lubicz J (2007) Subcellular targeting and interactions among the Potato virus X TGB proteins. Virology 367:375–389
Schepetilnikov MV, Manske U, Solovyev AG, Zamyatnin AA Jr, Schiemann J, Morozov SYu (2005) The hydrophobic segment of Potato virus X TGBp3 is a major determinant of the protein intracellular trafficking. J Gen Virol 86:2379–2391
Schepetilnikov MV, Solovyev AG, Gorshkova EN, Schiemann J, Prokhnevsky AI, Dolja VV, Morozov SY (2008) Intracellular targeting of a hordeiviral membrane-spanning movement protein: sequence requirements and involvement of an unconventional mechanism. J Virol 82:1284–1293
Schönknecht G, Brown JE, Verchot-Lubicz J (2008) Plasmodesmata transport of GFP alone or fused to potato virus X TGBp1 is diffusion driven. Protoplasma 232:143–152
Schulz A (1995) Plasmodesmal widening accompanies the short-term increase in symplasmic phloem unloading in pea root tips under osmotic stress. Protoplasma 188:22–37
Segui-Simarro JM, Austin JR II, White EA, Staehelin LA (2004) Electron tomographic analysis of somatic cell plate formation in meristematic cells of Arabidopsis preserved by high-pressure freezing. Plant Cell 16:836–856
Senes A, Engel DE, De Grado WF (2004) Folding of helical membrane proteins: the role of polar, GxxxG-like and proline motifs. Curr Opin Struct Biol 14:465–479
Shahollari B, Peskan-Berghofer T, Oelmuller R (2004) Receptor kinases with leucine-rich repeats are enriched in Triton X-100 insoluble plasma membrane microdomains from plants. Physiol Plant 122:397–403
Shibata Y, Voss C, Rist JM, Hu J, Rapoport TA, Prinz WA, Voeltz GK (2008) The reticulon and Dp1/Yop1p proteins form immobile oligomers in the tubular endoplasmic reticulum. J Biol Chem 283:18892–18904
Shibata Y, Hu J, Kozlov MM, Rapoport TA (2009) Mechanisms shaping the membranes of cellular organelles. Ann Rev Cell Dev Biol 25:329–354
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 21:581–594
Simpson-Holley M, Ellis D, Fisher D, Elton D, McCauley J, Digard PA (2002) Functional link between the actin cytoskeleton and lipid rafts during budding of filamentous influenza virions. Virology 301:212–225
Solovyev AG, Stroganova TA, Zamyatnin AA, Fedorkin ON, Schiemann J, Morozov SY (2000) Subcellular sorting of small membrane-associated triple gene block proteins: TGBp3-assisted targeting of TGBp2. Virology 269:113–127
Sorre B, Callan-Jones A, Manneville JB, Nassoy P, Joanny JF, Prost J, Goud B, Bassereau P (2009) Curvature-driven lipid sorting needs proximity to a demixing point and is aided by proteins. Proc Natl Acad Sci USA 106:5622–5626
Sparkes IA (2010) Motoring around the plant cell: insights from plant myosins. Biochem Soc Trans 38:833–838
Sparkes IA, Frigerio L, Tolley N, Hawes C (2009a) The plant endoplasmic reticulum: a cell-wide web. Biochem J 423:145–155
Sparkes IA, Ketelaar T, de Ruijter NCA, Hawes C (2009b) Grab a Golgi: laser trapping of Golgi bodies reveals in vivo interactions with the endoplasmic reticulum. Traffic 10:567–571
Sparkes IA, Runions J, Hawes C, Griffing L (2009c) Movement and remodeling of the endoplasmic reticulum in nondividing cells of tobacco leaves. Plant Cell 21:3937–3949
Sparkes IA, Tolley N, Aller I, Svozil J, Osterrieder A, Botchway S, Mueller C, Frigerio L, Hawes C (2010) Five arabidopsis reticulon isoforms share endoplasmic reticulum location, topology, and membrane-shaping properties. Plant Cell 22:1333–1343
Sprong H, van der Sluijs P, van Meer G (2001) How proteins move lipids and lipids move proteins. Nat Rev Mol Cell Biol 2:504–513
Staehelin LA (1997) The plant ER: a dynamic organelle composed of a large number of discrete functional domains. Plant J 11:1151–1165
Stahelin RV (2009) Lipid binding domains: more than simple lipid effectors. J Lipid Res 50:S299–S304
Stöckl MT, Herrmann A (2010) Detection of lipid domains in model and cell membranes by fluorescence lifetime imaging microscopy. Biochim Biophys Acta 1798:1444–1456
Su S, Liu Z, Chen C, Zhang Y, Wang X, Zhu L, Miao L, Wang XC, Yuan M (2010) Cucumber mosaic virus movement protein severs actin filaments to increase the plasmodesmal size exclusion limit in tobacco. Plant Cell 22:1373–1387
Takano K, Toyooka K, Suetsugu S (2008) EFC/F-BAR proteins and the N-WASP-WIP complex induce membrane curvature-dependent actin polymerization. EMBO J 27:2817–2828
Testerink C, Munnik T (2005) Phosphatidic acid: a multifunctional stress signaling lipid in plants. Trends Plant Sci 10:368–375
Thole JM, Nielsen E (2008) Phosphoinositides in plants: novel functions in membrane trafficking. Curr Opin Plant Biol 11:620–631
Thomas CL, Bayer E, Ritzenthaler C, Fernandez-Calvino L, Maule AJ (2008) Specific targeting of a plasmodesmal protein affecting cell-to-cell communication. PLoS Biol 6:e7
Tian Q, Olsen L, Sun B, Lid SE, Brown RC, Lemmon BE, Fosnes K, Gruis D, Opsahl-Sorteberg HG, Otegui MS, Olsen OA (2007) Subcellular localization and functional domain studies of DEFECTIVE KERNEL1 in maize and Arabidopsis suggest a model for aleurone cell fate specification involving CRINKLY4 and SUPERNUMERARY ALEURONE LAYER1. Plant Cell 19:3127–3145
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 112:739–747
Tilsner J, Cowan GH, Roberts AG, Chapman SN, Ziegler A, Savenkov E, Torrance L (2010) Plasmodesmal targeting and intercellular movement of potato mop-top pomovirus is mediated by a membrane anchored tyrosine-based motif on the lumenal side of the endoplasmic reticulum and the C-terminal transmembrane domain in the TGB3 movement protein. Virology 402:41–51
Tolley N, Sparkes IA, Hunter PR, Craddock CP, Nuttall J, Roberts LM, Hawes C, Pedrazzini E, Frigerio L (2010) Overexpression of a plant reticulon remodels the lumen of the cortical endoplasmic reticulum but does not perturb protein transport. Traffic 8:94–102
Tomenius K, Clapham D, Meshi T (1987) Localization by immunogold cytochemistry of the virus-coded 30 K protein in plasmodesmata of leaves infected with tobacco mosaic virus. Virology 160:363–371
Turner A, Wells B, Roberts K (1994) Plasmodesmata of maize root tips: structure and composition. J Cell Sci 107:3351–3361
Vale RD (2003) Myosin V motor proteins. J Cell Biol 163:445–450
Van Damme D, Bouget F-Y, Van Poucke K, Inzé D, Geelen D (2004) Molecular dissection of plant cytokinesis and phragmoplast structure: a survey of GFP-tagged proteins. Plant J 40:386–398
van Leeuwen W, Vermeer JEM, Gadella TWJ Jr, Munnik T (2007) Visualization of phosphatidylinositol 4, 5-bisphosphate in the plasma membrane of suspension-cultured tobacco BY-2 cells and whole Arabidopsis seedlings. Plant J 52:1014–1026
van Meer G, Sprong H (2004) Membrane lipids and vesicular traffic. Curr Opin Cell Biol 16:373–378
van Meer G, Voelker DR, Feigenson GW (2008) Membrane lipids: where they are and how they behave. Nat Rev Mol Cell Biol 9:112–124
Vedrenne C, Hauri HP (2006) Morphogenesis of the endoplasmic reticulum: beyond active membrane expansion. Traffic 7:639–646
Vermeer JEM, van Leeuwen W, Tobeña-Santamaria R, Laxalt AM, Jones DR, Divecha N, Gadella TWJ Jr, Munnik T (2006) Visualization of PtdIns3P dynamics in living plant cells. Plant J 47:687–700
Vermeer JEM, Thole JM, Goedhart J, Nielsen E, Munnik T, Gadella TWJ Jr (2009) Imaging phosphatidylinositol 4-phosphate dynamics in living plant cells. Plant J 57:356–372
Voeltz GK, Prinz WA (2007) Sheets, ribbons and tubules—how organelles get their shape. Nat Rev Mol Cell Biol 8:258–264
Voeltz GK, Prinz WA, Shibata Y, Rist JM, Rapoport TA (2006) A class of membrane proteins shaping the tubular endoplasmic reticulum. Cell 124:573–586
Volkmann D, Mori T, Tirlapur UK, Konig K, Fujiwara T, Kendrick-Jones J, Baluska F (2003) Unconventional myosins of the plant-specific class VIII: endocytosis, cytokinesis, plasmodesmata/pit-fields, and cell-to-cell coupling. Cell Biol Int 27:289–291
von Heijne G (2006) Membrane–protein topology. Nat Rev Mol Cell Biol 7:909–918
Waigmann E, Turner A, Peart J, Roberts K, Zambryski P (1997) Ultrastructural analysis of leaf trichome plasmodesmata reveals major differences from mesophyll plasmodesmata. Planta 203:75–84
Wang W, Yang X, Tangchaiburana S, Ndeh R, Markham JE, Tsegaye Y, Dunn TM, Wang GL, Bellizzi M, Parsons JF, Morrissey D, Bravo JE, Lynch DV, Xiao S (2008) An inositolphosphorylceramide synthase is involved in regulation of plant programmed cell death associated with defense in Arabidopsis. Plant Cell 20:3163–3179
White RG, Badelt K, Overall RL, Vesk M (1994) Actin associated with plasmodesmata. Protoplasma 180:169–184
Wolf S, Deom CM, Beachy RN, Lucas WJ (1989) Movement protein of tobacco mosaic virus modifies plasmodesmatal size exclusion limit. Science 246:377–379
Wright KM, Oparka KJ (2006) The ER within plasmodesmata. In: Robinson DG (ed) The plant endoplasmic reticulum. Springer, Berlin, pp 279–308
Xue H, Chen X, Mei Y (2009) Function and regulation of phospholipid signalling in plants. Biochem J 421:145–156
Yahalom A, Warmbrodt RD, Laird DW, Traub O, Revel J-P, Willecke K, Epel BL (1991) Maize mesocotyl plasmodesmata proteins cross-react with connexin gap junction protein antibodies. Plant Cell 3:407–417
Yahalom A, Lando R, Katz A, Epel BL (1998) A calcium-dependent protein kinase is associated with maize mesocotyl plasmodesmata. J Plant Physiol 153:354–362
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 61:131–142
Zhang Y, McCormick S (2010) The regulation of vesicle trafficking by small GTPases and phospholipids during pollen tube growth. Sex Plant Reprod 23:87–93
Zhao L, Naber N, Cooke R (1995) Muscle cross-bridges bound to actin are disordered in the presence of 2, 3-butanedione monoxime. Biophys J 68:1980–1990
Acknowledgements
We are grateful to Chris Hawes (Oxford, UK) for supplying Fig. 2a and to Christophe Ritzenthaler (Strasbourg, France), Christine Faulkner and Andy J. Maule (Norwich, UK) and Jesús A. Sánchez-Navarro (Valencia, Spain) for sharing unpublished results. We apologise to all colleagues whose work we were unable to cite due to space limitations. Funding by the Fundación Séneca, Spain (postdoctoral fellowship to K. Amari) and Scottish Government’s Rural and Environmental Research and Analysis Directorate (to SCRI) is gratefully acknowledged.
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Tilsner, J., Amari, K. & Torrance, L. Plasmodesmata viewed as specialised membrane adhesion sites. Protoplasma 248, 39–60 (2011). https://doi.org/10.1007/s00709-010-0217-6
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DOI: https://doi.org/10.1007/s00709-010-0217-6