Staying Tight: Plasmodesmal Membrane Contact Sites and the Control of Cell-to-Cell Connectivity in Plants

Annual Review of Plant Biology

Volumn 67, Issue , 2016, Pages 337-364

  Tilsner, Jens ^a,b   Nicolas, William ^c   Rosado, Abel ^d   Bayer, Emmanuelle M ^c  

^a UNIVERSITY OF ST ANDREWS   (United Kingdom)

^b SCOTTISH CROP RESEARCH INSTITUTE   (United Kingdom)

^c UNIVERSITÉ DE BORDEAUX   (France)

^d UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Calcium signaling; Callose; Intercellular trafficking; Lipid; Membrane contact site; Non cell autonomous; Plasmodesmata

Indexed keywords

ANIMAL; CELL MEMBRANE; CYTOSKELETON; ENDOPLASMIC RETICULUM; PHYSIOLOGY; PLANT; PLANT CELL; PLASMODESMA; SIGNAL TRANSDUCTION; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; BIOLOGICAL TRANSPORT; CELL MEMBRANE; CYTOSKELETON; ENDOPLASMIC RETICULUM; PLANT CELLS; PLANTS; PLASMODESMATA; SIGNAL TRANSDUCTION;

EID: 84968813481     PISSN: 15435008     EISSN: 15452123     Source Type: Book Series    
DOI: 10.1146/annurev-arplant-043015-111840     Document Type: Review

References (151)

1. Aimon S, Callan-Jones A, Berthaud A, Pinot M, Toombes GS, Bassereau P. 2014. Membrane shape modulates transmembrane protein distribution. Dev. Cell 28:212-18
2. Amari K, Boutant E,Hofmann C, Schmitt-Keichinger C, Fernandez-Calvino L, et al. 2010. A family of plasmodesmal proteins with receptor-like properties for plant viral movement proteins. PLOS Pathog. 6:e1001119
3. Amor Y, Haigler CH, Johnson S, Wainscott M, Delmer DP. 1995. A membrane-associated form of sucrose synthase and its potential role in synthesis of cellulose and callose in plants. PNAS 92:9353-57
4. Andrawis A, Solomon M, Delmer DP. 1993. Cotton fiber annexins: a potential role in the regulation of callose synthase. Plant J. 3:763-72
5. Aoki K, Kragler F, Xoconostle-Cazares B, Lucas WJ. 2002. A subclass of plant heat shock cognate 70 chaperones carries a motif that facilitates trafficking through plasmodesmata. PNAS 99:16342-47
6. Baluska F, Samaj J, Napier R, Volkmann D. 1999. Maize calreticulin localizes preferentially to plasmodesmata in root apex. Plant J. 19:481-88
7. Benitez-Alfonso Y, Faulkner C, Pendle A, Miyashima S, Helariutta Y, Maule A. 2013. Symplastic intercellular connectivity regulates lateral root patterning. Dev. Cell 26:136-47
8. Benitez-Alfonso Y, Faulkner C, Ritzenthaler C,Maule AJ. 2010. Plasmodesmata: gateways to local and systemic virus infection. Mol. Plant-Microbe Interact. 23:1403-12
9. Benkovics AH, Timmermans MCP. 2014. Developmental patterning by gradients of mobile small RNAs. Curr. Opin. Genet. Dev. 27:83-91
10. Bigay J, Antonny B. 2012. Curvature, lipid packing, and electrostatics of membrane organelles: defining cellular territories in determining specificity. Dev. Cell 23:886-95
11. Bilska A, Sowinski P. 2010. Closure of plasmodesmata in maize (Zea mays) at low temperature: a new mechanism for inhibition of photosynthesis. Ann. Bot. 106:675-86
12. Blackman L, Overall R. 1998. Immunolocalisation of the cytoskeleton to plasmodesmata of Chara corallina. Plant J. 14:733-41
13. Boutté Y, Moreau P. 2014. Modulation of endomembranes morphodynamics in the secretory/ retrograde pathways depends on lipid diversity. Curr. Opin. Plant Biol. 22:22-29
14. Burch-Smith TM, Zambryski PC. 2010. Loss of increased size exclusion limit (ISE)1 or ISE2 increases the formation of secondary plasmodesmata. Curr. Biol. 20:989-93
15. Burgoyne T, Patel S, Eden ER. 2015. Calcium signaling at ERmembrane contact sites. Biochim. Biophys. Acta 1853:2012-17
16. CaillaudM-C,Wirthmueller L, Sklenar J, Findlay K, Piquerez SJM, et al. 2014. The plasmodesmal protein PDLP1 localises to haustoria-associated membranes during downy mildew infection and regulates callose deposition. PLOS Pathog. 10:e1004496
17. Carella P, Isaacs M, Cameron RK. 2015. Plasmodesmata-located protein overexpression negatively impacts the manifestation of systemic acquired resistance and the long-distance movement ofDefective in Induced Resistance1 in Arabidopsis. Plant Biol. 17:395-401
18. Carlsbecker A, Lee J-Y, Roberts CJ, Dettmer J, Lehesranta S, et al. 2010. Cell signalling by microRNA165/6 directs gene dose-dependent root cell fate. Nature 465:316-21
19. Chang CL, Hsieh TS, Yang TT, Rothberg KG, Azizoglu DB, et al. 2013. Feedback regulation of receptor-induced Ca2+ signalingmediated by E-Syt1 andNir2 at endoplasmic reticulum-plasma membrane junctions. Cell Rep. 5:813-25
20. Chitwood DH, Nogueira FTS, Howell MD, Montgomery TA, Carrington JC, Timmermans MCP. 2009. Pattern formation via small RNA mobility. Mol. Cell. Biol. 23:549-54
21. Christensen A, Svensson K, Persson S, Jung J, Michalak M, et al. 2008. Functional characterization of Arabidopsis calreticulin1a: a key alleviator of endoplasmic reticulum stress. Plant Cell Physiol. 49:912-24
22. Cosgrove DJ. 2005. Growth of the plant cell wall. Nat. Rev. Mol. Cell Biol. 6:850-61
23. Crawford KM, Zambryski PC. 2001. Non-targeted and targeted protein movement through plasmodesmata in leaves in different developmental and physiological states. Plant Physiol. 125:1802-12
24. De Saint-Jean M, Delfosse V, Douguet D, Chicanne G, Payrastre B, et al. 2011. Osh4p exchanges sterols for phosphatidylinositol 4-phosphate between lipid bilayers. J. Cell Biol. 195:965-78
25. De Storme N, Geelen D. 2014. Callose homeostasis at plasmodesmata: molecular regulators and developmental relevance. Front. Plant Sci. 5:138
26. DeeksMJ, Calcutt JR, Ingle EKS, Hawkins TJ, Chapman S, et al. 2012. A superfamily of actin-binding proteins at the actin-membrane nexus of higher plants. Curr. Biol. 22:1595-600
27. Ding B, Kwon M, Warnberg L. 1996. Evidence that actin filaments are involved in controlling the permeability of plasmodesmata in tobacco mesophyll. Plant J. 10:157-64
28. Ding B, Turgeon R, Parthasarathy MV. 1992. Substructure of freeze-substituted plasmodesmata. Protoplasma 169:28-41
29. Drin G, Casella J-F, Gautier R, Boehmer T, Schwartz TU, Antonny B. 2007. A general amphipathic -helical motif for sensing membrane curvature. Nat. Struct. Mol. Biol. 14:138-46
30. Dunoyer P, Schott G, Himber C, Meyer D, Takeda A, et al. 2010. Small RNA duplexes function as mobile silencing signals between plant cells. Science 328:912-16
31. Ellinger D, Voigt CA. 2014. Callose biosynthesis in Arabidopsis with a focus on pathogen response: what we have learned within the last decade. Ann. Bot. 114:1349-58
32. Faulkner C. 2013. Receptor-mediated signaling at plasmodesmata. Front. Plant Sci. 4:521
33. 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 20:1504-18
34. Faulkner C, Blackman LM, Collings DA, Cordwell SJ, Overall RL. 2009. Anti-tropomyosin antibodies co-localise with actin microfilaments and label plasmodesmata. Eur. J. Cell Biol. 88:357-69
35. Faulkner C, Petutschnig E, Benitez-Alfonso Y, Beck M, Robatzek S, et al. 2013. Lym2-dependent chitin perception limits molecular flux via plasmodesmata. PNAS 110:9166-70
36. Fernández-Busnadiego R, Saheki Y, De Camilli P. 2015. Three-dimensional architecture of extended synaptotagmin-mediated endoplasmic reticulum-plasma membrane contact sites. PNAS 112:E2004-13
37. Fernandez-Calvino L, Faulkner C, Walshaw J, Saalbach G, Bayer E, et al. 2011. Arabidopsis plasmodesmal proteome. PLOS ONE 6:e18880
38. Foreman J, Demidchik V, Bothwell JHF, Mylona P, Miedema H, et al. 2003. Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422:442-46
39. Furch ACU, van Bel AJE, Fricker MD, Felle HH, Fuchs M, Hafke JB. 2009. Sieve element Ca2+ channels as relay stations between remote stimuli and sieve tube occlusion in Vicia faba. Plant Cell 21:2118-32
40. Gallagher KL, Sozzani R, Lee C-M. 2014. Intercellular protein movement: deciphering the language of development. Annu. Rev. Cell Dev. Biol. 30:207-33
41. Gaudioso-Pedraza R, Benitez-Alfonso Y. 2014. A phylogenetic approach to study the origin and evolution of plasmodesmata-localized glycosyl hydrolases family 17. Front. Plant Sci. 5:212
42. Giordano F, Saheki Y, Idevall-Hagren O, Colombo SF, Pirruccello M, et al. 2013. PI(4,5)P2-dependent and Ca2+-regulated ER-PM interactions mediated by the extended synaptotagmins. Cell 153:1494-509
43. Goswami D, Gowrishankar K, Bilgrami S, Ghosh S, Raghupathy R, et al. 2008. Nanoclusters of GPIanchored proteins are formed by cortical actin-driven activity. Cell 135:1085-97
44. Grison MS, Brocard L, Fouillen L, Nicolas W, Wewer V, et al. 2015. Specific membrane lipid composition is important for plasmodesmata function in Arabidopsis. Plant Cell 27:1228-50
45. 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. 21:335-45
46. Gui J, Liu C, Shen J, Li L. 2014. Grain setting defect1, encoding a remorin protein, affects the grain setting in rice through regulating plasmodesmatal conductance. Plant Physiol. 166:1463-78
47. Guseman JM, Lee JS, BogenschutzNL, Peterson KM, Virata RE, et al. 2010. Dysregulation of cell-tocell connectivity and stomatal patterning by loss-of-function mutation in Arabidopsis CHORUS (GLUCAN SYNTHASE-LIKE 8). Development 137:1731-41
48. Han X,HyunT, Zhang M, Kumar R,Koh EJ, et al. 2014. Auxin-callose-mediated plasmodesmal gating is essential for tropic auxin gradient formation and signaling. Dev. Cell 28:132-46
49. Haraguchi T, Tominaga M, Matsumoto R, Sato K, Nakano A, et al. 2014. Molecular characterization and subcellular localization of Arabidopsis class VIII myosin, ATM1. J. Biol. Chem. 289:12343-55
50. Harries P, Ding B. 2011. Cellular factors in plant virus movement: at the leading edge of macromolecular trafficking in plants. Virology 411:237-43
51. Heilmann M, Heilmann I. 2015. Plant phosphoinositides-complex networks controlling growth and adaptation. Biochim. Biophys. Acta 1851:759-69
52. Helle SCJ, Kanfer G, Kolar K, Lang A, Michel AH, Kornmann B. 2013. Organization and function of membrane contact sites. Biochim. Biophys. Acta 1833:2526-41
53. Henne WM, Liou J, Emr SD. 2015. Molecular mechanisms of inter-organelle ER-PM contact sites. Curr. Opin. Cell Biol. 35:123-30
54. Holdaway-Clarke TL, Walker NA, Hepler PK, Overall RL. 2000. Physiological elevations in cytoplasmic free calcium by cold or ion injection result in transient closure of higher plant plasmodesmata. Planta 210:329-35
55. Hong Z, Zhang Z, Olson JM, Verma DP. 2001. A novel UDP-glucose transferase is part of the callose synthase complex and interacts with phragmoplastin at the forming cell plate. Plant Cell 13:769-79
56. Kagiwada S,Hashimoto M. 2007. The yeastVAPhomolog Scs2p has a phosphoinositide-binding ability that is correlated with its activity. Biochem. Biophys. Res. Commun. 364:870-76
57. Kankanala P, Czymmek K, Valent B. 2007. Roles for rice membrane dynamics and plasmodesmata during biotrophic invasion by the blast fungus. Plant Cell 19:706-24
58. Kawade K, Horiguchi G, Usami T, Hirai MY, Tsukaya H. 2013. ANGUSTIFOLIA3 signaling coordinates proliferation between clonally distinct cells in leaves. Curr. Biol. 23:788-92
59. Khang CH, Berruyer R, GiraldoMC, Kankanala P, Park S-Y, et al. 2010. Translocation of Magnaporthe oryzae effectors into rice cells and their subsequent cell-to-cell movement. Plant Cell 22:1388-403
60. Kim I, Cho E, Crawford K, Hempel FD, Zambryski PC. 2005. Cell-to-cell movement of GFP during embryogenesis and early seedling development in Arabidopsis. PNAS 102:2227-31
61. Kim I, Kobayashi K, Cho E, Zambryski PC. 2005. Subdomains for transport via plasmodesmata corresponding to the apical-basal axis are established during Arabidopsis embryogenesis. PNAS 102:11945-50
62. Kim J-Y, Rim Y, Wang J, Jackson D. 2005. A novel cell-to-cell trafficking assay indicates that the KNOX homeodomain is necessary and sufficient for intercellular protein and mRNA trafficking. Genes Dev. 19:788-93
63. Kim J-Y, Yuan Z, Jackson D. 2003. Developmental regulation and significance of KNOX protein trafficking in Arabidopsis. Development 130:4351-62
64. Knight A, Jones J. 1993. A myosin like protein for higher plants. J. Mol. Biol. 231:148-54
65. Knox JP, Benitez-Alfonso Y. 2014. Roles and regulation of plant cell walls surrounding plasmodesmata. Curr. Opin. Plant Biol. 22:93-100
66. Knox K, Wang P, Kriechbaumer V, Tilsner J, Frigerio L, et al. 2015. Putting the squeeze on plasmodesmata: a role for reticulons in primary plasmodesmata formation. Plant Physiol. 44:1563-72
67. Kobayashi K, Otegui MS, Krishnakumar S, Mindrinos M, Zambryski P. 2007. INCREASED SIZE EXCLUSION LIMIT2 encodes a putativeDEVHboxRNAhelicase involved in plasmodesmata function during Arabidopsis embryogenesis. Plant Cell 19:1885-97
68. Koizumi K, Wu S, MacRae-Crerar A, Gallagher KL. 2011. An essential protein that interacts with endosomes and promotes movement of the short-root transcription factor. Curr. Biol. 21:1559-64
69. Koldsø H, Shorthouse D, Helie J, Sansom MSP. 2014. Lipid clustering correlates with membrane curvature as revealed by molecular simulations of complex lipid bilayers. PLOS Comput. Biol. 10:e1003911
70. Lahiri S, Toulmay A, Prinz WA. 2015. Membrane contact sites, gateways for lipid homeostasis. Curr. Opin. Cell Biol. 33:82-87
71. Larsen JB, Jensen MB, Bhatia VK, Pedersen SL, Bjørnholm T, et al. 2015. Membrane curvature enables N-Ras lipid anchor sorting to liquid-ordered membrane phases. Nat. Chem. Biol. 11:192-94
72. Lee J-Y. 2014. New and old roles of plasmodesmata in immunity and parallels to tunneling nanotubes. Plant Sci. 221-222:13-20
73. Lee J-Y,Wang X, Cui W, Sager R, Modla S, et al. 2011. A plasmodesmata-localized protein mediates crosstalk between cell-to-cell communication and innate immunity in Arabidopsis. Plant Cell 23:3353-73
74. LemmonMA, Ferguson KM. 2001. Molecular determinants in pleckstrin homology domains that allow specific recognition of phosphoinositides. Biochem. Soc. Trans. 29:377-84
75. Lev S. 2010. Non-vesicular lipid transport by lipid-transfer proteins and beyond. Nat. Rev. Mol. Cell Biol. 11:739-50
76. Levy A, Erlanger M, Rosenthal M, Epel BL. 2007. A plasmodesmata-associated -1,3-glucanase in Arabidopsis. Plant J. 49:669-82
77. Levy A, Zheng JY, Lazarowitz SG. 2015. Synaptotagmin SYTA forms ER-plasma membrane junctions that are recruited to plasmodesmata for plant virus movement. Curr. Biol. 25:1-8
78. Lingwood D, Simons K. 2010. Lipid rafts as a membrane-organizing principle. Science 327:46-50
79. Loewen CJR, Roy A, Levine TP. 2003. A conserved ER targetingmotif in three families of lipid binding proteins and in Opi1p binds VAP. EMBO J. 22:2025-35
80. Ma P, Morvan O, Quentin M, Jauneau A, Mareck A, Morvan C. 1998. Immunogold localization of pectin methylesterases in the cortical tissues of flax hypocotyl. Protoplasma 202:175-84
81. Manford AG, Stefan CJ, Yuan HL, Macgurn JA, Emr SD. 2012. ER-to-plasma membrane tethering proteins regulate cell signaling and ER morphology. Dev. Cell 23:1129-40
82. Martens S,Kozlov MM, McMahonHT. 2007. How synaptotagmin promotesmembrane fusion. Science 316:1205-8
83. McMahon HT, Boucrot E. 2015. Membrane curvature at a glance. J. Cell Sci. 128:1065-70
84. Meng L, Wong JH, Feldman LJ, Lemaux PG, Buchanan BB. 2010. Amembrane-associated thioredoxin required for plant growth moves from cell to cell, suggestive of a role in intercellular communication. PNAS 107:3900-5
85. Mesmin B, Bigay J, Moser von Filseck J, Lacas-Gervais S, Drin G, Antonny B. 2013. A four-step cycle driven by PI(4)P hydrolysis directs sterol/PI(4)P exchange by the ER-Golgi tether OSBP. Cell 155:830-43
86. MilovanovicD,Honigmann A, Koike S,Göttfert F, PahlerG, et al. 2015. Hydrophobicmismatch sorts SNARE proteins into distinct membrane domains. Nat. Commun. 6:5984
87. Molnar A, Melnyk CW, Bassett A, Hardcastle TJ, Dunn R, Baulcombe DC. 2010. Small silencing RNAs in plants are mobile and direct epigenetic modification in recipient cells. Science 328:872-75
88. Moser von Filseck J, Alenka C , Delfosse V, Vanni S, Jackson CL, et al. 2015. Phosphatidylserine transport by ORP/OSH proteins is driven by phosphatidylinositol 4-phosphate. Science 349:4322015
89. Moser von Filseck J, Vanni S, Mesmin B, Antonny B, Drin G. 2015. A phosphatidylinositol-4-phosphate powered exchange mechanism to create a lipid gradient between membranes. Nat. Commun. 6:6671
90. Musetti R, Buxa SV, De Marco F, Loschi A, Polizzotto R, et al. 2013. Phytoplasma-triggered Ca2+ influx is involved in sieve-tube blockage. Mol. Plant-Microbe Interact. 26:379-86
91. Nakajima K, Sena G, Nawy T, Benfey PN. 2001. Intercellular movement of the putative transcription factor SHR in root patterning. Nature 413:307-11
92. Oide S, Bejai S, Staal J, Guan N, KaliffM, Dixelius C. 2013. A novel role of PR2 in abscisic acid (ABA) mediated, pathogen-induced callose deposition in Arabidopsis thaliana. New Phytol. 200:1187-99
93. Oparka KJ, Roberts AG, Boevink P, Santa Cruz S, Roberts I, et al. 1999. Simple, but not branched, plasmodesmata allow the nonspecific trafficking of proteins in developing tobacco leaves. Cell 97:743-54
94. Orfila C, Knox JP. 2000. Spatial regulation of pectic polysaccharides in relation to pit fields in cell walls of tomato fruit pericarp. Plant Physiol. 122:775-81
95. Overall RL, Blackman LM. 1996. A model of the macromolecular structure of plasmodesmata. Trends Plant Sci. 1:307-11
96. Pérez-Sancho J, Vanneste S, Lee E, McFarlane H, Esteban del Valle A, et al. 2015. The Arabidopsis SYT1 is enriched in ER-PM contact sites and confers cellular resistance to mechanical stresses. Plant Physiol. 168:132-43
97. Perraki A, Binaghi M, Mecchia MA, Gronnier J, German-Retana S, et al. 2014. StRemorin1.3 hampers Potato virus X TGBp1 ability to increase plasmodesmata permeability, but does not interfere with its silencing suppressor activity. FEBS Lett. 588:1699-705
98. Prinz WA. 2014. Bridging the gap: membrane contact sites in signaling, metabolism, and organelle dynamics. J. Cell Biol. 205:759-69
99. Radford JE, White RG. 1998. Localization of a myosin-like protein to plasmodesmata. Plant J. 14:743-50
100. Radford JE, White RG. 2011. Inhibitors of myosin, but not actin, alter transport through Tradescantia plasmodesmata. Protoplasma 248:205-16
101. Raffaele S, Bayer E, Lafarge D, Cluzet S, German Retana S, et al. 2009. Remorin, a solanaceae protein resident in membrane rafts and plasmodesmata, impairs Potato virus X movement. Plant Cell 21:1541-55
102. RodriguezA,Angel CA,LutzL,Leisner SM,NelsonRS, Schoelz JE. 2014. Association of the P6 protein of Cauliflower mosaic virus with plasmodesmata and plasmodesmal proteins. Plant Physiol. 166:1345-58
103. Roy S, Watada AE, Wergin WP. 1997. Characterization of the cell wall microdomain surrounding plasmodesmata in apple fruit. Plant Physiol. 114:539-47
104. Rubinstein E. 2011. The complexity of tetraspanins. Biochem. Soc. Trans. 39:501-5
105. Ryu Y-S, Lee I-H, Suh J-H, Park SC, Oh S, et al. 2014. Reconstituting ring-rafts in bud-mimicking topography of model membranes. Nat. Commun. 5:4507
106. Sager R, Lee J-Y. 2014. Plasmodesmata in integrated cell signalling: insights from development and environmental signals and stresses. J. Exp. Bot. 65:6337-58
107. Schapire AL, Valpuesta V, Botella MA. 2009. Plasma membrane repair in plants. Trends Plant Sci. 14:645-52
108. Schapire AL, Voigt B, Jasik J, Rosado A, Lopez-Cobollo R, et al. 2008. Arabidopsis synaptotagmin 1 is required for the maintenance of plasma membrane integrity and cell viability. Plant Cell 20:3374-88
109. Schauder CM, Wu X, Saheki Y, Narayanaswamy P, Torta F, et al. 2014. Structure of a lipid-bound extended synaptotagmin indicates a role in lipid transfer. Nature 510:552-55
110. Schulz TA, Creutz CE. 2004. The tricalbin C2 domains: lipid-binding properties of a novel, synaptotagmin-like yeast protein family. Biochemistry 43:3987-95
111. Simon MLA, Platre MP, Assil S, van Wijk R, Chen WY, et al. 2014. A multi-colour/multi-affinity marker set to visualize phosphoinositide dynamics in Arabidopsis. Plant J. 77:322-37
112. 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 21:581-94
113. Smith RS, Bayer EM. 2009. Auxin transport-feedback models of patterning in plants. Plant Cell Environ. 32:1258-71
114. Soboloff J, Spassova MA, Dziadek MA, Gill DL. 2006. Calcium signals mediated by STIM and Orai proteins-a new paradigm in inter-organelle communication. Biochim. Biophys. Acta 1763:1161-68
115. Stahl Y, Grabowski S, Bleckmann A, Kuhnemuth R, Weidtkamp-Peters S, et al. 2013. Moderation of Arabidopsis root stemness by CLAVATA1 and ARABIDOPSIS CRINKLY4 receptor kinase complexes. Curr. Biol. 23:362-71
116. Stefan CJ, Manford AG, Baird D, Yamada-Hanff J, Mao Y, Emr SD. 2011. Osh proteins regulate phosphoinositide metabolism at ER-plasma membrane contact sites. Cell 144:389-401
117. Stonebloom S, Brunkard JO, Cheung AC, Jiang K, Feldman L, Zambryski P. 2012. Redox states of plastids andmitochondria differentially regulate intercellular transport via plasmodesmata. Plant Physiol. 158:190-99
118. 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. PNAS 106:17229-34
119. Su S, Liu Z, Chen C, Zhang Y, Wang X, et al. 2010. Cucumber mosaic virus movement protein severs actin filaments to increase the plasmodesmal size exclusion limit in tobacco. Plant Cell 22:1373-87
120. Szittya G, Burgyan J. 2013. RNA interference-mediated intrinsic antiviral immunity in plants. Curr. Top. Microbiol. Immunol. 371:123-51
121. Takeshima H, Hoshijima M, Song L-S. 2015. Ca2+ microdomains organized by junctophilins. Cell Calcium 58:349-56
122. 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:e7
123. Tian Q, Olsen L, Sun B, Lid SE, Brown RC, et al. 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 19:3127-45
124. Tilsner J, Amari K, Torrance L. 2011. Plasmodesmata viewed as specialised membrane adhesion sites. Protoplasma 248:39-60
125. Tilsner J, Taliansky M, Torrance L. 2014. Plant virus movement. eLS. doi: 10.1002/9780470015902. a0020711.pub2
126. Toulmay A, Prinz WA. 2012. A conserved membrane-binding domain targets proteins to organelle contact sites. J. Cell Sci. 125:49-58
127. Tucker EB. 1988. Inositol bisphosphate and inositol trisphosphate inhibit cell-to-cell passage of carboxyfluorescein in staminal hairs of Setcreasea purpurea. Planta 174:358-63
128. Tucker EB, Boss WF. 1996. Mastoparan-induced intracellular Ca2+ fluxes may regulate cell-to-cell communication in plants. Plant Physiol. 111:459-67
129. 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:e1001201
130. Vaddepalli P, Herrmann A, Fulton L, Oelschner M, Hillmer S, et al. 2014. The C2-domain protein QUIRKY and the receptor-like kinase STRUBBELIG localize to plasmodesmata and mediate tissue morphogenesis in Arabidopsis thaliana. Development 141:4139-48
131. Van Gestel K, Slegers H, Von Witsch M, Samaj J, Baluska F, Verbelen J-P. 2003. Immunological evidence for the presence of plant homologues of the actin-related protein Arp3 in tobacco and maize: subcellular localization to actin-enriched pit fields and emerging root hairs. Protoplasma 222:45-52
132. Vanni S, Hirose H, Barelli H, Antonny B, Gautier R. 2014. A sub-nanometre view of how membrane curvature and composition modulate lipid packing and protein recruitment. Nat. Commun. 5:4916
133. Vatén A, Dettmer J, Wu S, Stierhof Y-D, Miyashima S, et al. 2011. Callose biosynthesis regulates symplastic trafficking during root development. Dev. Cell 21:1144-55
134. Verma DPS, Hong Z. 2001. Plant callose synthase complexes. Plant Mol. Biol. 47:693-701
135. Vogler H, Kwon M-O, Dang V, Sambade A, Fasler M, et al. 2008. Tobacco mosaic virus movement protein enhances the spread of RNA silencing. PLOS Pathog. 4:e1000038
136. Voss C, Lahiri S, Young BP, Loewen CJ, Prinz WA. 2012. ER-shaping proteins facilitate lipid exchange between the ER and mitochondria in S. cerevisiae. J. Cell Sci. 125:4791-99
137. Wang P, Hawkins TJ, Richardson C, Cummins I, Deeks MJ, et al. 2014. The plant cytoskeleton, NET3C, and VAP27 mediate the link between the plasma membrane and endoplasmic reticulum. Curr. Biol. 24:1397-405
138. Wang P, Richardson C, Hawkins TJ, Sparkes I, Hawes C, Hussey PJ. 2016. Plant VAP27 proteins: domain characterization, intercellular localization and role in plant development. New Phytol. In press. doi: 10.1111/nph.13857
139. Wang X, Sager R, Cui W, Zhang C, Lu H, Lee J-Y. 2013. Salicylic acid regulates plasmodesmata closure during innate immune responses in Arabidopsis. Plant Cell 25:2315-29
140. Weinl C, Marquardt S, Kuijt SJH, Nowack MK, Jakoby MJ. 2005. Novel functions of plant cyclindependent kinase inhibitors, ICK1/KRP1, can act non-cell-autonomously and inhibit entry into mitosis. Plant Cell 17:1704-22
141. West M, Zurek N, Hoenger A, Voeltz GK. 2011. A 3D analysis of yeast ER structure reveals how ER domains are organized by membrane curvature. J. Cell Biol. 193:333-46
142. White R, Barton D. 2011. The cytoskeleton in plasmodesmata: a role in intercellular transport J. Exp. Bot. 62:5249-66
143. Winter CM, Austin RS, Blanvillain-Baufumé S, Reback MA, Monniaux M, et al. 2011. LEAFY target genes reveal floral regulatory logic, cis motifs, and a link to biotic stimulus response. Dev. Cell 20:430-43
144. WuS, Gallagher KL. 2014. Themovement of the non-cell-autonomous transcription factor, SHORTROOT relies on endomembrane system. Plant J. 80:396-409
145. 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. 65:1-14
146. Xu XM,Wang J,XuanZ,Goldshmidt A, Borrill PGM, et al. 2011. Chaperonins facilitateKNOTTED1 cell-to-cell trafficking and stem cell function. Science 333:1141-44
147. Yamazaki T, Kawamura Y, Minami A, Uemura M. 2008. Calcium-dependent freezing tolerance in Arabidopsis involves membrane resealing via synaptotagmin SYT1. Plant Cell 20:3389-404
148. Yamazaki T, Takata N, Uemura M, Kawamura Y. 2010. Arabidopsis synaptotagmin SYT1, a type I signal-anchor protein, requires tandem C2 domains for delivery to the plasma membrane. J. Biol. Chem. 285:23165-76
149. Yao X,Wang H, Li H, Yuan Z, Li F, et al. 2009. Two types of cis-acting elements control the abaxial epidermis-specific transcription of the MIR165a and MIR166a genes. FEBS Lett. 583:3711-17
150. Yu CH, Guo GQ, Nie XW, Zheng GC. 2004. Cytochemical localization of pectinase activity in pollen mother cells of tobacco during meiotic prophase and its relation to the formation of secondary plasmodesmata and cytoplasmic channels. Acta Bot. Sin. 46:1443-53
151. Zavaliev R, Levy A, Gera A, Epel BL. 2013. Subcellular dynamics and role of Arabidopsis -1,3-glucanases in cell-to-cell movement of tobamoviruses. Mol. Plant-Microbe Interact. 26:1016-30