Skip to main content

Function of Plasmodesmata in the Interaction of Plants with Microbes and Viruses

  • Protocol
  • First Online:
Plasmodesmata

Part of the book series: Methods in Molecular Biology ((MIMB,volume 2457))

Abstract

Plasmodesmata (PD) are gated plant cell wall channels that allow the trafficking of molecules between cells and play important roles during plant development and in the orchestration of cellular and systemic signaling responses during interactions of plants with the biotic and abiotic environment. To allow gating, PD are equipped with signaling platforms and enzymes that regulate the size exclusion limit (SEL) of the pore. Plant-interacting microbes and viruses target PD with specific effectors to enhance their virulence and are useful probes to study PD functions.

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

Access this chapter

Protocol
USD 49.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 249.99
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

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

    Article  Google Scholar 

  2. Grison MS, Brocard L, Fouillen L et al (2015) Specific membrane lipid composition is important for plasmodesmata function in Arabidopsis. Plant Cell 27:1228–1250

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  4. Vaten A, Dettmer J, Wu S et al (2011) Callose biosynthesis regulates symplastic trafficking during root development. Dev Cell 21:1144–1155

    Article  CAS  PubMed  Google Scholar 

  5. De Storme N, Geelen D (2014) Callose homeostasis at plasmodesmata: molecular regulators and developmental relevance. Front Plant Sci 5:138

    Article  PubMed  PubMed Central  Google Scholar 

  6. Brault ML, Petit JD, Immel F et al (2019) Multiple C2 domains and transmembrane region proteins (MCTPs) tether membranes at plasmodesmata. EMBO Rep 20:e47182

    Article  PubMed  PubMed Central  Google Scholar 

  7. Tucker EB, Boss WF (1996) Mastoparan induced intracellular Ca2+ fluxes may regulate cell-to-cell communication in plants. Plant Physiol 111:459–467

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Leijon F, Melzer M, Zhou Q et al (2018) Proteomic analysis of plasmodesmata from populus cell suspension cultures in relation with callose biosynthesis. Front Plant Sci 9:1681

    Article  PubMed  PubMed Central  Google Scholar 

  9. Yamazaki T, Kawamura Y, Minami A et al (2008) Calcium-dependent freezing tolerance in Arabidopsis involves membrane resealing via synaptotagmin SYT1. Plant Cell 20:3389–3404

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Tilsner J, Nicolas W, Rosado A et al (2016) Staying tight: plasmodesmal membrane contact sites and the control of cell-to-cell connectivity in plants. Annu Rev Plant Biol 67:337–364

    Article  CAS  PubMed  Google Scholar 

  11. Zambryski P, Crawford K (2000) Plasmodesmata: gatekeepers for cell-to-cell transport of developmental signals in plants. Annu Rev Cell Dev Biol 16:393–421

    Article  CAS  PubMed  Google Scholar 

  12. Sevilem I, Yadav SR, Helariutta Y (2015) Plasmodesmata: channels for intercellular signaling during plant growth and development. Methods Mol Biol 1217:3–24

    Article  CAS  PubMed  Google Scholar 

  13. Lu KJ, Danila FR, Cho Y et al (2018) Peeking at a plant through the holes in the wall - exploring the roles of plasmodesmata. New Phytol 218:1310–1314

    Article  PubMed  Google Scholar 

  14. Heinlein M (2002) Plasmodesmata: dynamic regulation and role in macromolecular cell-to-cell signaling. Curr Opin Plant Biol 5:543–552

    Article  CAS  PubMed  Google Scholar 

  15. Sager R, Lee JY (2014) Plasmodesmata in integrated cell signalling: insights from development and environmental signals and stresses. J Exp Bot 65:6337–6358

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Crawford KM, Zambryski PC (2001) Non-targeted and targeted protein movement through plasmodesmata in leaves in different developmental and physiological states. Plant Physiol 125:1802–1812

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Rinne PL, van der Schoot C (1998) Symplasmic fields in the tunica of the shoot apical meristem coordinate morphological events. Development 125:1477–1485

    Article  CAS  PubMed  Google Scholar 

  18. Palevitz BA, Hepler PK (1985) Changes in dye coupling of stomatal cells of Allium and Commelina demonstrated by microinjection of lucifer yellow. Planta 164:473–479

    Article  CAS  PubMed  Google Scholar 

  19. Duckett CM, Oparka KJ, Prior DAM et al (1994) Dye-coupling in the root epidermis of Arabidopsis is progressively reduced during development. Development 120:3247–3255

    Article  CAS  Google Scholar 

  20. 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 expansin. Plant Cell 13:47–60

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Imlau A, Truernit E, Sauer N (1999) Cell-to-cell and long-distance trafficking of green fluorescent protein in the phloem and symplastic unloading of the protein into sink tissues. Plant Cell 11:309–322

    Article  CAS  PubMed  Google Scholar 

  22. Godel-Jedrychowska K, Kulinska-Lukaszek K, Horstman A et al (2020) Symplasmic isolation marks cell fate changes during somatic embryogenesis. J Exp Bot 71:2612–2628

    Article  CAS  PubMed  Google Scholar 

  23. Oparka KJ, Turgeon R (1999) Sieve elements and companion cells - traffic control centers of the phloem. Plant Cell 11:739–750

    CAS  PubMed  Google Scholar 

  24. Hepler PK (1982) Endoplasmic reticulum in the formation of the cell plate and plasmodesmata. Protoplasma 111:121–133

    Article  Google Scholar 

  25. Knox K, Wang P, Kriechbaumer V et al (2015) Putting the squeeze on plasmodesmata: a role for reticulons in primary plasmodesmata formation. Plant Physiol 168:1563–1572

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Ding B, Haudenshield JS, Willmitzer L et al (1993) Correlation between arrested secondary plasmodesmal development and onset of accelerated leaf senescence in yeast acid invertase transgenic tobacco plants. Plant J 4:179–189

    Article  CAS  PubMed  Google Scholar 

  27. Evert RF, Russin WA, Bosabalidis AM (1996) Anatomical and ultrastructural changes associated with sink-to-source transition in developing maize leaves. Int J Plant Sci 157:247–261

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  29. Ormenese S, Havelange A, Bernier G et al (2002) The shoot apical meristem of Sinapis alba L. expands its central symplasmic field during the floral transition. Planta 215:67–78

    Article  CAS  PubMed  Google Scholar 

  30. Oparka KJ, Roberts AG, Boevink P et al (1999) Simple, but not branched, plasmodesmata allow the nonspecific trafficking of proteins in developing tobacco leaves. Cell 97:743–754

    Article  CAS  PubMed  Google Scholar 

  31. Roberts AG, Oparka K (2003) Plasmodesmata and the control of symplastic transport. Plant Cell Environ 26:103–124

    Article  Google Scholar 

  32. Faulkner C, Akman OE, Bell K et al (2008) Peeking into pit fields: a multiple twinning model of secondary plasmodesmata formation in tobacco. Plant Cell 20:1504–1518

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Roberts IM, Boevink P, Roberts AG et al (2001) Dynamic changes in the frequency and architecture of plasmodesmata during the sink-source transition in tobacco leaves. Protoplasma 218:31–44

    Article  CAS  PubMed  Google Scholar 

  34. Fitzgibbon J, Beck M, Zhou J et al (2013) A developmental framework for complex plasmodesmata formation revealed by large-scale imaging of the Arabidopsis leaf epidermis. Plant Cell 25:57–70

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Zavaliev R, Dong X, Epel BL (2016) Glycosylphosphatidylinositol (GPI) modification serves as a primary plasmodesmal sorting signal. Plant Physiol 172:1061–1073

    CAS  PubMed  PubMed Central  Google Scholar 

  36. Cantrill LC, Overall RL, Goodwin PB (1999) Cell-to-cell communication via plant endomembranes. Cell Biol Int 23:653–661

    Article  CAS  PubMed  Google Scholar 

  37. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Nicolas WJ, Grison MS, Trepout S et al (2017) Architecture and permeability of post-cytokinesis plasmodesmata lacking cytoplasmic sleeves. Nat Plants 3:17082

    Article  CAS  PubMed  Google Scholar 

  39. Siao W, Wang PW, Voigt B et al (2016) Arabidopsis SYT1 maintains stability of cortical endoplasmic reticulum networks and VAP27-1-enriched endoplasmic reticulum-plasma membrane contact sites. J Exp Bot 67:6161–6171

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Schapire AL, Voigt B, Jasik J et al (2008) Arabidopsis synaptotagmin 1 is required for the maintenance of plasma membrane integrity and cell viability. Plant Cell 20:3374–3388

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Kriechbaumer V, Botchway SW, Slade SE et al (2015) Reticulomics: protein-protein interaction studies with two plasmodesmata-localized reticulon family proteins identify binding partners enriched at plasmodesmata, endoplasmic reticulum, and the plasma membrane. Plant Physiol 169:1933–1945

    CAS  PubMed  PubMed Central  Google Scholar 

  42. 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 25:2018–2025

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Ishikawa K, Tamura K, Fukao Y et al (2020) Structural and functional relationships between plasmodesmata and plant endoplasmic reticulum-plasma membrane contact sites consisting of three synaptotagmins. New Phytol 226:798–808

    Article  CAS  PubMed  Google Scholar 

  44. Fernandez-Busnadiego R, Saheki Y, De Camilli P (2015) Three-dimensional architecture of extended synaptotagmin-mediated endoplasmic reticulum-plasma membrane contact sites. Proc Natl Acad Sci U S A 112:E2004–E2013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Lin CC, Seikowski J, Perez-Lara A et al (2014) Control of membrane gaps by synaptotagmin-Ca2+ measured with a novel membrane distance ruler. Nat Commun 5:5859

    Article  CAS  PubMed  Google Scholar 

  46. Liu L, Li C, Liang Z et al (2018) Characterization of multiple C2 domain and transmembrane region proteins in Arabidopsis. Plant Physiol 176:2119–2132

    Article  CAS  PubMed  Google Scholar 

  47. Vaddepalli P, Herrmann A, Fulton L 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 141:4139–4148

    Article  CAS  PubMed  Google Scholar 

  48. 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

    Article  Google Scholar 

  49. Robinson-Beers K, Evert RF (1991) Fine structure of plasmodesmata in mature leaves of sugar cane. Planta 184:307–318

    CAS  PubMed  Google Scholar 

  50. Waigmann E, Turner A, Peart J et al (1997) Ultrastructural analysis of leaf trichome plasmodesmata reveals major differences from mesophyll plasmodesmata. Planta 203:75–84

    Article  CAS  PubMed  Google Scholar 

  51. Chen S, Novick P, Ferro-Novick S (2012) ER network formation requires a balance of the dynamin-like GTPase Sey1p and the Lunapark family member Lnp1p. Nat Cell Biol 14:707–716

    Article  CAS  PubMed  Google Scholar 

  52. Tolley N, Sparkes IA, Hunter PR et al (2008) Overexpression of a plant reticulon remodels the lumen of the cortical endoplasmic reticulum but does not perturb protein transport. Traffic 9:94–102

    Article  CAS  PubMed  Google Scholar 

  53. Tolley N, Sparkes I, Craddock CP et al (2010) Transmembrane domain length is responsible for the ability of a plant reticulon to shape endoplasmic reticulum tubules in vivo. Plant J 64:411–418

    Article  CAS  PubMed  Google Scholar 

  54. Fernandez-Calvino L, Faulkner C, Walshaw J et al (2011) Arabidopsis plasmodesmal proteome. PLoS One 6:e18880

    Article  CAS  PubMed  Google Scholar 

  55. Wu SW, Kumar R, Iswanto ABB et al (2018) Callose balancing at plasmodesmata. J Exp Bot 69:5325–5339

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  57. Hughes JE, Gunning BES (1980) Glutaraldehyde-induced deposition of callose. Can J Bot 58:250–258

    Article  CAS  Google Scholar 

  58. Wang X, Sager R, Cui W et al (2013) Salicylic acid regulates plasmodesmata closure during innate immune responses in Arabidopsis. Plant Cell 25:2315–2329

    Article  CAS  PubMed  Google Scholar 

  59. Benitez-Alfonso Y, Faulkner C, Pendle A et al (2013) Symplastic intercellular connectivity regulates lateral root patterning. Dev Cell 26:136–147

    Article  CAS  PubMed  Google Scholar 

  60. Guseman JM, Lee JS, Bogenschutz NL et al (2010) Dysregulation of cell-to-cell connectivity and stomatal patterning by loss-of-function mutation in Arabidopsis chorus (glucan synthase-like 8). Development 137:1731–1741

    Article  CAS  PubMed  Google Scholar 

  61. Han X, Hyun TK, Zhang M et al (2014) Auxin-callose-mediated plasmodesmal gating is essential for tropic auxin gradient formation and signaling. Dev Cell 28:132–146

    Article  CAS  PubMed  Google Scholar 

  62. Simpson C, Thomas C, Findlay K et al (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

    Article  CAS  PubMed  Google Scholar 

  63. Slewinski TL, Baker RF, Stubert A et al (2012) Tie-dyed2 encodes a callose synthase that functions in vein development and affects symplastic trafficking within the phloem of maize leaves. Plant Physiol 160:1540–1550

    Article  CAS  PubMed  Google Scholar 

  64. Zavaliev R, Sagi G, Gera A et al (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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  66. Gaudioso-Pedraza R, Beck M, Frances L et al (2018) Callose-regulated symplastic communication coordinates symbiotic root nodule development. Curr Biol 28:3562–3577.e6

    Article  CAS  PubMed  Google Scholar 

  67. Liu NJ, Zhang T, Liu ZH et al (2020) Phytosphinganine affects plasmodesmata permeability via facilitating PDLP5-stimulated callose accumulation in Arabidopsis. Mol Plant 13:128–143

    Article  CAS  PubMed  Google Scholar 

  68. Roberts AG, Santa Cruz S, Roberts IM et al (1997) Phloem unloading in sink leaves of Nicotiana benthamiana: comparison of a fluorescent solute with a fluorescent virus. Plant Cell 9:1381–1396

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  70. Lucas WJ, Bouche-Pillon S, Jackson DP et al (1995) Selective trafficking of KNOTTED1 homeodomain protein and its RNA through plasmodesmata. Science 270:1980–1983

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  72. Helariutta Y, Fukaki H, Wysocka-Diller J et al (2000) The SHORT-ROOT gene controls radial patterning of the Arabidopsis root through radial signaling. Cell 101:555–567

    Article  CAS  PubMed  Google Scholar 

  73. Mezitt LA, Lucas WJ (1996) Plasmodesmal cell-to-cell transport of proteins and nucleic acids. Plant Mol Biol 32:251–273

    Article  CAS  PubMed  Google Scholar 

  74. Kragler F, Monzer J, Shash K et al (1998) Cell-to-cell transport of proteins: requirement for unfolding and characterization of binding to a putative plasmodesmal receptor. Plant J 15:367–381

    Article  CAS  Google Scholar 

  75. Perbal M-C, Haughn G, Saedler H et al (1996) Non-autonomous function of Antirrhinum floral homeotic proteins DEFICIENS and GLOBOSA is exerted by their polar cell-to-cell trafficking. Development 122:3433–3441

    Article  CAS  PubMed  Google Scholar 

  76. Yoo SC, Chen C, Rojas M et al (2013) Phloem long-distance delivery of FLOWERING LOCUS T (FT) to the apex. Plant J 75:456–468

    Article  CAS  PubMed  Google Scholar 

  77. Crawford KM, Zambryski PC (2000) Subcellular localization determines the availability of non-targeted proteins to plasmodesmatal transport. Curr Biol 10:1032–1040

    Article  CAS  PubMed  Google Scholar 

  78. Cui H, Levesque MP, Vernoux T et al (2007) An evolutionarily conserved mechanism delimiting SHR movement defines a single layer of endodermis in plants. Science 316:421–425

    Article  CAS  PubMed  Google Scholar 

  79. Schiefelbein J, Huang L, Zheng X (2014) Regulation of epidermal cell fate in Arabidopsis roots: the importance of multiple feedback loops. Front Plant Sci 5:47

    Article  PubMed  Google Scholar 

  80. Bouyer D, Geier F, Kragler F et al (2008) Two-dimensional patterning by a trapping/depletion mechanism: the role of TTG1 and GL3 in Arabidopsis trichome formation. PLoS Biol 6:e141

    Article  PubMed  PubMed Central  Google Scholar 

  81. Balkunde R, Bouyer D, Hulskamp M (2011) Nuclear trapping by GL3 controls intercellular transport and redistribution of TTG1 protein in Arabidopsis. Development 138:5039–5048

    Article  CAS  PubMed  Google Scholar 

  82. Daum G, Medzihradszky A, Suzaki T et al (2014) A mechanistic framework for noncell autonomous stem cell induction in Arabidopsis. Proc Natl Acad Sci U S A 111:14619–14624

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Yadav RK, Perales M, Gruel J et al (2011) WUSCHEL protein movement mediates stem cell homeostasis in the Arabidopsis shoot apex. Genes Dev 25:2025–2030

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Kim I, Zambryski PC (2005) Cell-to-cell communication via plasmodesmata during Arabidopsis embryogenesis. Curr Opin Plant Biol 8:593–599

    Article  CAS  PubMed  Google Scholar 

  85. Kim I, Cho E, Crawford K et al (2005) Cell-to-cell movement of GFP during embryogenesis and early seedling development in Arabidopsis. Proc Natl Acad Sci U S A 102:2227–2231

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Xu XM, Wang J, Xuan Z et al (2011) Chaperonins facilitate KNOTTED1 cell-to-cell trafficking and stem cell function. Science 333:1141–1144

    Article  CAS  PubMed  Google Scholar 

  87. Kehr J, Kragler F (2018) Long distance RNA movement. New Phytol 218:29–40

    Article  CAS  PubMed  Google Scholar 

  88. Carlsbecker A, Lee JY, Roberts CJ et al (2010) Cell signalling by microRNA165/6 directs gene dose-dependent root cell fate. Nature 465:316–321

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Deom MC, Lapidot M, Beachy RN (1992) Plant virus movement proteins. Cell 69:221–224

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  91. Kragler F, Monzer J, Xoconostle-Cazares B et al (2000) Peptide antagonists of the plasmodesmal macromolecular trafficking pathway. EMBO J 19:2856–2868

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Zhang W, Thieme CJ, Kollwig G et al (2016) tRNA-related sequences trigger systemic mRNA transport in plants. Plant Cell 28:1237–1249

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Ham BK, Brandom JL, Xoconostle-Cazares B et al (2009) A polypyrimidine tract binding protein, pumpkin RBP50, forms the basis of a phloem-mobile ribonucleoprotein complex. Plant Cell 21:197–215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Huang NC, Yu TS (2009) The sequences of Arabidopsis GA-INSENSITIVE RNA constitute the motifs that are necessary and sufficient for RNA long-distance trafficking. Plant J 59:921–929

    Article  CAS  PubMed  Google Scholar 

  95. Cho SK, Sharma P, Butler NM et al (2015) Polypyrimidine tract-binding proteins of potato mediate tuberization through an interaction with StBEL5 RNA. J Exp Bot 66:6835–6847

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Yang L, Perrera V, Saplaoura E et al (2019) m(5)C methylation guides systemic transport of messenger rna over graft junctions in plants. Curr Biol 29:2465–2476.e5

    Article  CAS  PubMed  Google Scholar 

  97. Zipfel C, Oldroyd GE (2017) Plant signalling in symbiosis and immunity. Nature 543:328–336

    Article  CAS  PubMed  Google Scholar 

  98. Chinchilla D, Zipfel C, Robatzek S et al (2007) A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448:497–500

    Article  CAS  PubMed  Google Scholar 

  99. Heese A, Hann DR, Gimenez-Ibanez S et al (2007) The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants. Proc Natl Acad Sci U S A 104:12217–12222

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Schulze B, Mentzel T, Jehle AK et al (2010) Rapid heteromerization and phosphorylation of ligand-activated plant transmembrane receptors and their associated kinase BAK1. J Biol Chem 285:9444–9451

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Roux M, Schwessinger B, Albrecht C et al (2011) The Arabidopsis leucine-rich repeat receptor-like kinases BAK1/SERK3 and BKK1/SERK4 are required for innate immunity to hemibiotrophic and biotrophic pathogens. Plant Cell 23:2440–2455

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Schwessinger B, Roux M, Kadota Y et al (2011) Phosphorylation-dependent differential regulation of plant growth, cell death, and innate immunity by the regulatory receptor-like kinase BAK1. PLoS Genet 7:e1002046

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Sun Y, Li L, Macho AP et al (2013) Structural basis for flg22-induced activation of the Arabidopsis FLS2-BAK1 immune complex. Science 342:624–628

    Article  CAS  PubMed  Google Scholar 

  104. Xu B, Cheval C, Laohavisit A et al (2017) A calmodulin-like protein regulates plasmodesmal closure during bacterial immune responses. New Phytol 215:77–84

    Article  CAS  PubMed  Google Scholar 

  105. Faulkner C, Petutschnig E, Benitez-Alfonso Y et al (2013) LYM2-dependent chitin perception limits molecular flux via plasmodesmata. Proc Natl Acad Sci U S A 110:9166–9170

    Article  CAS  PubMed  Google Scholar 

  106. Kadota Y, Sklenar J, Derbyshire P et al (2014) Direct regulation of the NADPH oxidase RBOHD by the PRR-associated kinase BIK1 during plant immunity. Mol Cell 54:43–55

    Article  CAS  PubMed  Google Scholar 

  107. Castro B, Citterico M, Kimura S et al (2021) Stress-induced reactive oxygen species compartmentalization, perception and signalling. Nat Plants 7:403–412

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Thor K, Jiang S, Michard E et al (2020) The calcium-permeable channel OSCA1.3 regulates plant stomatal immunity. Nature 585:569–573

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Lee JY, Wang X, Cui W et al (2011) A plasmodesmata-localized protein mediates crosstalk between cell-to-cell communication and innate immunity in Arabidopsis. Plant Cell 23:3353–3373

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Cheval C, Samwald S, Johnston MG et al (2020) Chitin perception in plasmodesmata characterizes submembrane immune-signaling specificity in plants. Proc Natl Acad Sci U S A 117:9621–9629

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Mou Z, Fan W, Dong X (2003) Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113:935–944

    Article  CAS  PubMed  Google Scholar 

  112. Carella P, Isaacs M, Cameron RK (2015) Plasmodesmata-located protein overexpression negatively impacts the manifestation of systemic acquired resistance and the long-distance movement of defective in induced Resistance1 in Arabidopsis. Plant Biol (Stuttg) 17:395–401

    Article  CAS  Google Scholar 

  113. Lim GH, Shine MB, de Lorenzo L et al (2016) Plasmodesmata localizing proteins regulate transport and signaling during systemic acquired immunity in plants. Cell Host Microbe 19:541–549

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  115. Stonebloom S, Brunkard JO, Cheung AC et al (2012) Redox states of plastids and mitochondria differentially regulate intercellular transport via plasmodesmata. Plant Physiol 158:190–199

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  117. Stahl Y, Faulkner C (2016) Receptor complex mediated regulation of symplastic traffic. Trends Plant Sci 21:450–459

    Article  CAS  PubMed  Google Scholar 

  118. Liu T, Liu Z, Song C et al (2012) Chitin-induced dimerization activates a plant immune receptor. Science 336:1160–1164

    Article  CAS  PubMed  Google Scholar 

  119. Grison MS, Kirk P, Brault ML et al (2019) Plasma membrane-associated receptor-like kinases relocalize to plasmodesmata in response to osmotic stress. Plant Physiol 181:142–160

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Hunter K, Kimura S, Rokka A et al (2019) CRK2 enhances salt tolerance by regulating callose deposition in connection with PLDalpha1. Plant Physiol 180:2004–2021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Aung K, Kim P, Li Z et al (2020) Pathogenic bacteria target plant plasmodesmata to colonize and invade surrounding tissues. Plant Cell 32:595–611

    Article  CAS  PubMed  Google Scholar 

  122. Tomczynska I, Stumpe M, Doan TG et al (2020) A Phytophthora effector protein promotes symplastic cell-to-cell trafficking by physical interaction with plasmodesmata-localised callose synthases. New Phytol 227:1467–1478

    Article  CAS  PubMed  Google Scholar 

  123. Li Z, Variz H, Chen Y et al (2021) Plasmodesmata-dependent intercellular movement of bacterial effectors. Front Plant Sci 12:640277

    Article  PubMed  PubMed Central  Google Scholar 

  124. Sakulkoo W, Oses-Ruiz M, Oliveira Garcia E et al (2018) A single fungal MAP kinase controls plant cell-to-cell invasion by the rice blast fungus. Science 359:1399–1403

    Article  CAS  PubMed  Google Scholar 

  125. Cao L, Blekemolen MC, Tintor N et al (2018) The Fusarium oxysporum Avr2-Six5 effector pair alters plasmodesmatal exclusion selectivity to facilitate cell-to-cell movement of Avr2. Mol Plant 11:691–705

    Article  CAS  PubMed  Google Scholar 

  126. Di X, Gomila J, Ma L et al (2016) Uptake of the fusarium effector Avr2 by tomato is not a cell autonomous event. Front Plant Sci 7:1915

    Article  PubMed  PubMed Central  Google Scholar 

  127. Di X, Cao L, Hughes RK et al (2017) Structure-function analysis of the Fusarium oxysporum Avr2 effector allows uncoupling of its immune-suppressing activity from recognition. New Phytol 216:897–914

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Wu JH, Dimitman JE (1970) Leaf structure and callose formation as determinants of TMV movement in bean leaves as revealed by UV irradiation studies. Virology 40:820–827

    Article  CAS  PubMed  Google Scholar 

  129. Moore AE, Stone BA (1972) Effect of infection with TMV and other viruses on the level of a −1,3-glucan hydrolase in leaves of Nicotiana glutinosa. Virology 50:791–798

    Article  CAS  PubMed  Google Scholar 

  130. Leisner SM, Turgeon R (1993) Movement of virus and photoassimilate in the phloem: a comparative analysis. BioEssays 15:741–748

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  132. Allison AV, Shalla TA (1973) The ultrastructure of local lesions induced by Potato virus X: a sequence of cytological events in the course of infection. Phytopathology 64:784–793

    Article  Google Scholar 

  133. Pennazio S, D’Agostino G, Appiano A et al (1978) Ultrastructure and histochemistry of the resistant tissue surrounding lesions of Tomato bushy stunt virus in Gomphrena globosa leaves. Physiol Plant Pathol 13:165–168

    Article  Google Scholar 

  134. Dong X, Hong Z, Chatterjee J et al (2008) Expression of callose synthase genes and its connection with Npr1 signaling pathway during pathogen infection. Planta 229:87–98

    Article  CAS  PubMed  Google Scholar 

  135. Huang D, Sun Y, Ma Z et al (2019) Salicylic acid-mediated plasmodesmal closure via Remorin-dependent lipid organization. Proc Natl Acad Sci U S A 116:21274–21284

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. Jarsch IK, Konrad SS, Stratil TF et al (2014) Plasma membranes are subcompartmentalized into a plethora of coexisting and diverse microdomains in Arabidopsis and Nicotiana benthamiana. Plant Cell 26:1698–1711

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  137. Konrad SS, Popp C, Stratil TF et al (2014) S-acylation anchors remorin proteins to the plasma membrane but does not primarily determine their localization in membrane microdomains. New Phytol 203:758–769

    Article  CAS  PubMed  Google Scholar 

  138. Martinez D, Legrand A, Gronnier J et al (2019) Coiled-coil oligomerization controls localization of the plasma membrane REMORINs. J Struct Biol 206:12–19

    Article  CAS  PubMed  Google Scholar 

  139. Zhou T, Murphy AM, Lewsey MG et al (2014) Domains of the Cucumber mosaic virus 2b silencing suppressor protein affecting inhibition of salicylic acid-induced resistance and priming of salicylic acid accumulation during infection. J Gen Virol 95:1408–1413

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Raffaele S, Bayer E, Lafarge D et al (2009) Remorin, a solanaceae protein resident in membrane rafts and plasmodesmata, impairs Potato virus X movement. Plant Cell 21:1541–1555

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  141. Perraki A, Gronnier J, Gouguet P et al (2018) REM1.3’s phospho-status defines its plasma membrane nanodomain organization and activity in restricting PVX cell-to-cell movement. PLoS Pathog 14:e1007378

    Article  PubMed  PubMed Central  Google Scholar 

  142. Fu S, Xu Y, Li C et al (2018) Rice stripe virus interferes with S-acylation of remorin and induces its autophagic degradation to facilitate virus infection. Mol Plant 11:269–287

    Article  CAS  PubMed  Google Scholar 

  143. Cheng G, Yang Z, Zhang H et al (2020) Remorin interacting with PCaP1 impairs Turnip mosaic virus intercellular movement but is antagonised by VPg. New Phytol 225:2122–2139

    Article  CAS  PubMed  Google Scholar 

  144. Sasaki N, Takashima E, Nyunoya H (2018) Altered subcellular localization of a tobacco membrane raft-associated remorin protein by tobamovirus infection and transient expression of viral replication and movement proteins. Front Plant Sci 9:619

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  146. Heinlein M (2015) Plasmodesmata: channels for viruses on the move. Methods Mol Biol 1217:25–52

    Article  CAS  PubMed  Google Scholar 

  147. Amari K, Boutant E, Hofmann C et al (2010) A family of plasmodesmal proteins with receptor-like properties for plant viral movement proteins. PLoS Pathog 6:e1001119

    Article  PubMed  PubMed Central  Google Scholar 

  148. Lekkerkerker A, Wellink J, Yuan P et al (1996) Distinct functional domains in the Cowpea mosaic virus movement protein. J Virol 70:5658–5661

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  149. Belin C, Schmitt C, Gaire F et al (1999) The nine C-terminal residues of the grapevine fanleaf nepovirus movement protein are critical for systemic virus spread. J Gen Virol 80(Pt 6):1347–1356

    Article  CAS  PubMed  Google Scholar 

  150. Schoelz JE, Angel CA, Nelson RS et al (2016) A model for intracellular movement of Cauliflower mosaic virus: the concept of the mobile virion factory. J Exp Bot 67:2039–2048

    Article  CAS  PubMed  Google Scholar 

  151. Wolf S, Deom CM, Beachy RN et al (1989) Movement protein of Tobacco mosaic virus modifies plasmodesmatal size exclusion limit. Science 246:377–379

    Article  CAS  PubMed  Google Scholar 

  152. Waigmann E, Lucas W, Citovsky V et al (1994) Direct functional assay for Tobacco mosaic virus cell-to-cell movement protein and identification of a domain involved in increasing plasmodesmal permeability. Proc Natl Acad Sci U S A 91:1433–1437

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  153. Vogler H, Kwon MO, Dang V et al (2008) Tobacco mosaic virus movement protein enhances the spread of RNA silencing. PLoS Pathog 4:e1000038

    Article  PubMed  PubMed Central  Google Scholar 

  154. Oparka KJ, Prior DAM, Santa Cruz S et al (1997) Gating of epidermal plasmodesmata is restricted to the leading edge of expanding infection sites of Tobacco mosaic virus. Plant J 12:781–789

    Article  CAS  PubMed  Google Scholar 

  155. Kim I, Kobayashi K, Cho E et al (2005) Subdomains for transport via plasmodesmata corresponding to the apical-basal axis are established during Arabidopsis embryogenesis. Proc Natl Acad Sci U S A 102:11945–11950

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  156. Haley A, Hunter T, Kiberstis P et al (1995) Multiple serine phosphorylation sites on the 30 kDa TMV cell-to-cell movement protein synthesized in tobacco protoplasts. Plant J 8:715–724

    Article  CAS  PubMed  Google Scholar 

  157. Tyulkina LG, Karger EM, Sheveleva AA et al (2010) Binding of monoclonal antibodies to the movement protein (MP) of Tobacco mosaic virus: influence of subcellular MP localization and phosphorylation. J Gen Virol 91:1621–1628

    Article  CAS  PubMed  Google Scholar 

  158. Kawakami S, Padgett HS, Hosokawa D et al (1999) Phosphorylation and/or presence of serine 37 in the movement protein of tomato mosaic tobamovirus is essential for intracellular localization and stability in vivo. J Virol 73:6831–6840

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  159. Watanabe Y, Meshi T, Okada Y (1992) In vivo phosphorylation of the 30-kDa protein of Tobacco mosaic virus. FEBS Lett 313:181–184

    Article  CAS  PubMed  Google Scholar 

  160. Citovsky V, McLean BG, Zupan JR et al (1993) Phosphorylation of Tobacco mosaic virus cell-to-cell movement protein by a developmentally regulated plant cell wall-associated protein kinase. Genes Dev 7:904–910

    Article  CAS  PubMed  Google Scholar 

  161. Ding B, Haudenshield JS, Hull RJ et al (1992) Secondary plasmodesmata are specific sites of localization of the tobacco mosaic virus movement protein in transgenic tobacco plants. Plant Cell 4:915–928

    Google Scholar 

  162. Moore PJ, Fenczik CA, Deom CM et al (1992) Developmental changes in plasmodesmata in transgenic tobacco expressing the movement protein of Tobacco mosaic virus. Protoplasma 170:115–127

    Article  Google Scholar 

  163. Heinlein M, Wood MR, Thiel T et al (1998) Targeting and modification of prokaryotic cell-cell junctions by Tobacco mosaic virus cell-to-cell movement protein. Plant J 14:345–351

    Article  CAS  PubMed  Google Scholar 

  164. Bucher GL, Tarina C, Heinlein M et al (2001) Local expression of enzymatically active class 1 beta-1,3-glucanase enhances symptoms of TMV infection in tobacco. Plant J 28:361–369

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  166. Guenoune-Gelbart D, Elbaum M, Sagi G et al (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 21:335–345

    Article  CAS  PubMed  Google Scholar 

  167. Levy A, Erlanger M, Rosenthal M et al (2007) A plasmodesmata-associated beta-1,3-glucanase in Arabidopsis. Plant J 49:669–682

    Article  CAS  PubMed  Google Scholar 

  168. Ueki S, Spektor R, Natale DM et al (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

    Article  PubMed  PubMed Central  Google Scholar 

  169. Fridborg I, Grainger J, Page A et al (2003) TIP, a novel host factor linking callose degradation with the cell-to-cell movement of Potato virus X. Mol Plant-Microbe Interact 16:132–140

    Article  CAS  PubMed  Google Scholar 

  170. 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 107:2491–2496

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  171. Uchiyama A, Shimada-Beltran H, Levy A et al (2014) The Arabidopsis synaptotagmin SYTA regulates the cell-to-cell movement of diverse plant viruses. Front Plant Sci 5:584

    Article  PubMed  PubMed Central  Google Scholar 

  172. Thomas CL, Bayer EM, Ritzenthaler C et al (2008) Specific targeting of a plasmodesmal protein affecting cell-to-cell communication. PLoS Biol 6:e7

    Article  PubMed  PubMed Central  Google Scholar 

  173. Tilsner J, Linnik O, Louveaux M et al (2013) Replication and trafficking of a plant virus are coupled at the entrances of plasmodesmata. J Cell Biol 201:981–995

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  174. Padgett HS, Epel BL, Kahn TW et al (1996) Distribution of tobamovirus movement protein in infected cells and implications for cell-to-cell spread of infection. Plant J 10:1079–1088

    Article  CAS  PubMed  Google Scholar 

  175. Heinlein M (2015) Plant virus replication and movement. Virology 479-480:657–671

    Article  CAS  PubMed  Google Scholar 

  176. Heinlein M, Padgett HS, Gens JS et al (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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  177. Heinlein M (2002) The spread of Tobacco mosaic virus infection: insights into the cellular mechanism of RNA transport. Cell Mol Life Sci 59:58–82

    Article  CAS  PubMed  Google Scholar 

  178. Niehl A, Pasquier A, Ferriol I et al (2014) Comparison of the Oilseed rape mosaic virus and Tobacco mosaic virus movement proteins (MP) reveals common and dissimilar MP functions for tobamovirus spread. Virology 456-457:43–54

    Article  CAS  PubMed  Google Scholar 

  179. Niehl A, Pena EJ, Amari K et al (2013) Microtubules in viral replication and transport. Plant J 75:290–308

    Article  CAS  PubMed  Google Scholar 

  180. Pont-Lezica RF, McNally JG, Pickard BG (1993) Wall-to-membrane linkers in onion epidermis: some hypotheses. Plant Cell Environ 16:111–123

    Article  CAS  Google Scholar 

  181. Oparka KJ (1994) Plasmolysis: new insights into an old process. New Phytol 126:571–591

    Article  CAS  Google Scholar 

  182. Ishikawa K, Tamura K, Ueda H et al (2018) Synaptotagmin-associated endoplasmic reticulum-plasma membrane contact sites are localized to immobile er tubules. Plant Physiol 178:641–653

    Article  PubMed  PubMed Central  Google Scholar 

  183. Brandner K, Sambade A, Boutant E et al (2008) Tobacco mosaic virus movement protein interacts with green fluorescent protein-tagged microtubule end-binding protein 1. Plant Physiol 147:611–623

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  184. Sambade A, Brandner K, Hofmann C et al (2008) Transport of TMV movement protein particles associated with the targeting of RNA to plasmodesmata. Traffic 9:2073–2088

    Article  CAS  PubMed  Google Scholar 

  185. Wang P, Hawkins TJ, Richardson C et al (2014) The plant cytoskeleton, NET3C, and VAP27 mediate the link between the plasma membrane and endoplasmic reticulum. Curr Biol 24:1397–1405

    Article  CAS  PubMed  Google Scholar 

  186. Heinlein M, Epel BL, Padgett HS et al (1995) Interaction of tobamovirus movement proteins with the plant cytoskeleton. Science 270:1983–1985

    Article  CAS  PubMed  Google Scholar 

  187. Ashby J, Boutant E, Seemanpillai M et al (2006) Tobacco mosaic virus movement protein functions as a structural microtubule-associated protein. J Virol 80:8329–8344

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  188. Boyko V, Ashby JA, Suslova E et al (2002) Intramolecular complementing mutations in tobacco mosaic virus movement protein confirm a role for microtubule association in viral RNA transport. J Virol 76:3974–3980

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  189. Boyko V, Ferralli J, Heinlein M (2000) Cell-to-cell movement of TMV RNA is temperature-dependent and corresponds to the association of movement protein with microtubules. Plant J 22:315–325

    Article  CAS  PubMed  Google Scholar 

  190. Boyko V, Hu Q, Seemanpillai M et al (2007) Validation of microtubule-associated Tobacco mosaic virus RNA movement and involvement of microtubule-aligned particle trafficking. Plant J 51:589–603

    Article  CAS  PubMed  Google Scholar 

  191. Boyko V, van der Laak J, Ferralli J et al (2000) Cellular targets of functional and dysfunctional mutants of Tobacco mosaic virus movement protein fused to green fluorescent protein. J Virol 74:11339–11346

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  192. Ouko MO, Sambade A, Brandner K et al (2010) Tobacco mutants with reduced microtubule dynamics are less susceptible to TMV. Plant J 62:829–839

    Article  CAS  PubMed  Google Scholar 

  193. Peña EJ, Ferriol I, Sambade A et al (2014) Experimental virus evolution reveals a role of plant microtubule dynamics and TORTIFOLIA1/SPIRAL2 in RNA trafficking. PLoS One 9:e105364

    Article  PubMed  PubMed Central  Google Scholar 

  194. Boyko V, Ferralli J, Ashby J et al (2000) Function of microtubules in intercellular transport of plant virus RNA. Nat Cell Biol 2:826–832

    Article  CAS  PubMed  Google Scholar 

  195. Wang P, Richardson C, Hawkins TJ et al (2016) Plant VAP27 proteins: domain characterization, intracellular localization and role in plant development. New Phytol 210:1311–1326

    Article  CAS  PubMed  Google Scholar 

  196. Pena EJ, Robles Luna G, Heinlein M (2020) In vivo imaging of tagged mRNA in plant tissues using the bacterial transcriptional antiterminator BglG. Plant J 105:271–282

    Article  PubMed  Google Scholar 

  197. Amari K, Di Donato M, Dolja VV et al (2014) Myosins VIII and XI play distinct roles in reproduction and transport of Tobacco mosaic virus. PLoS Pathog 10:e1004448

    Article  PubMed  PubMed Central  Google Scholar 

  198. Harries PA, Park JW, Sasaki N et al (2009) Differing requirements for actin and myosin by plant viruses for sustained intercellular movement. Proc Natl Acad Sci U S A 106:17594–17599

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  199. Hofmann C, Niehl A, Sambade A et al (2009) Inhibition of Tobacco mosaic virus movement by expression of an actin-binding protein. Plant Physiol 149:1810–1823

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  200. Golomb L, Abu-Abied M, Belausov E et al (2008) Different subcellular localizations and functions of Arabidopsis myosin VIII. BMC Plant Biol 8:3

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  202. Reichelt S, Knight AE, Hodge TP et al (1999) Characterization of the unconventional myosin VIII in plant cells and its localization at the post-cytokinetic cell wall. Plant J 19:555–567

    Article  CAS  PubMed  Google Scholar 

  203. Wu SZ, Bezanilla M (2014) Myosin VIII associates with microtubule ends and together with actin plays a role in guiding plant cell division. elife 3:e03498

    Article  PubMed Central  Google Scholar 

  204. Radford JE, White RG (2011) Inhibitors of myosin, but not actin, alter transport through Tradescantia plasmodesmata. Protoplasma 248:205–216

    Article  CAS  PubMed  Google Scholar 

  205. Su S, Liu Z, Chen C et al (2010) Cucumber mosaic virus movement protein severs actin filaments to increase the plasmodesmal size exclusion limit in tobacco. Plant Cell 22:1373–1387

    Article  CAS  PubMed  Google Scholar 

  206. Pitzalis N, Heinlein M (2017) The roles of membranes and associated cytoskeleton in plant virus replication and cell-to-cell movement. J Exp Bot 69:117–132

    Article  CAS  PubMed  Google Scholar 

  207. Schoelz JE, Harries PA, Nelson RS (2011) Intracellular transport of plant viruses: finding the door out of the cell. Mol Plant 4:813–831

    Article  CAS  PubMed  Google Scholar 

  208. Wang A (2015) Dissecting the molecular network of virus-plant interactions: the complex roles of host factors. Annu Rev Phytopathol 53:45–66

    Article  CAS  PubMed  Google Scholar 

  209. Martin-Hernandez AM, Baulcombe DC (2008) Tobacco rattle virus 16-kilodalton protein encodes a suppressor of RNA silencing that allows transient viral entry in meristems. J Virol 82:4064–4071

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  210. Pitzalis N, Amari K, Graindorge S et al (2020) Turnip mosaic virus in oilseed rape activates networks of sRNA-mediated interactions between viral and host genomes. Commun Biol 3:702

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  211. Shimura H, Pantaleo V, Ishihara T et al (2011) A viral satellite RNA induces yellow symptoms on tobacco by targeting a gene involved in chlorophyll biosynthesis using the RNA silencing machinery. PLoS Pathog 7:e1002021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  212. Smith NA, Eamens AL, Wang MB (2011) Viral small interfering RNAs target host genes to mediate disease symptoms in plants. PLoS Pathog 7:e1002022

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  213. Navarro B, Gisel A, Rodio ME et al (2012) Small RNAs containing the pathogenic determinant of a chloroplast-replicating viroid guide the degradation of a host mRNA as predicted by RNA silencing. Plant J 70:991–1003

    Article  CAS  PubMed  Google Scholar 

  214. Miozzi L, Gambino G, Burgyan J et al (2012) Genome-wide identification of viral and host transcripts targeted by viral siRNAs in Vitis vinifera. Mol Plant Pathol 14:30–43

    Article  PubMed  PubMed Central  Google Scholar 

  215. Schwach F, Vaistij FE, Jones L et al (2005) An RNA-dependent RNA polymerase prevents meristem invasion by Potato virus X and is required for the activity but not the production of a systemic silencing signal. Plant Physiol 138:1842–1852

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  216. Kørner CJ, Pitzalis N, Peña EJ et al (2018) Crosstalk between PTGS and TGS pathways in natural antiviral immunity and disease recovery. Nat Plants 4:157–164

    Article  PubMed  Google Scholar 

  217. Ghoshal B, Sanfacon H (2015) Symptom recovery in virus-infected plants: revisiting the role of RNA silencing mechanisms. Virology 479-480:167–179

    Article  CAS  PubMed  Google Scholar 

  218. Paudel DB, Sanfacon H (2018) Exploring the diversity of mechanisms associated with plant tolerance to virus infection. Front Plant Sci 9:1575

    Article  PubMed  PubMed Central  Google Scholar 

  219. Rosas-Diaz T, Zhang D, Fan P et al (2018) A virus-targeted plant receptor-like kinase promotes cell-to-cell spread of RNAi. Proc Natl Acad Sci U S A 115:1388–1393

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  220. Carluccio AV, Prigigallo MI, Rosas-Diaz T et al (2018) S-acylation mediates Mungbean yellow mosaic virus AC4 localization to the plasma membrane and in turns gene silencing suppression. PLoS Pathog 14:e1007207

    Article  PubMed  PubMed Central  Google Scholar 

  221. Garnelo Gomez B, Rosas-Diaz T, Shi C et al (2021) The viral silencing suppressor P19 interacts with the receptor-like kinases BAM1 and BAM2 and suppresses the cell-to-cell movement of RNA silencing independently of its ability to bind sRNA. New Phytol 229:1840–1843

    Article  CAS  PubMed  Google Scholar 

  222. Vu MH, Iswanto ABB, Lee J et al (2020) The role of plasmodesmata-associated receptor in plant development and environmental response. Plants (Basel) 9:216

    Article  CAS  Google Scholar 

  223. Niehl A, Wyrsch I, Boller T et al (2016) Double-stranded RNAs induce a pattern-triggered immune signaling pathway in plants. New Phytol 211:1008–1019

    Article  CAS  PubMed  Google Scholar 

  224. Kørner CJ, Klauser D, Niehl A et al (2013) The immunity regulator BAK1 contributes to resistance against diverse RNA viruses. Mol Plant-Microbe Interact 26:1271–1280

    Article  PubMed  Google Scholar 

  225. Yu H, Liu Y, Gulbranson DR et al (2016) Extended synaptotagmins are Ca2+-dependent lipid transfer proteins at membrane contact sites. Proc Natl Acad Sci U S A 113:4362–4367

    Article  CAS  PubMed  Google Scholar 

  226. Yuan C, Lazarowitz SG, Citovsky V (2018) The plasmodesmal localization signal of tmv mp is recognized by plant synaptotagmin SYTA. mBio 9:e01314–e01318

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  227. Diaz A, Wang X, Ahlquist P (2010) Membrane-shaping host reticulon proteins play crucial roles in viral RNA replication compartment formation and function. Proc Natl Acad Sci U S A 107:16291–16296

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

C.H. was supported by a PhD fellowship from the Chinese Scholarship Council (CSC).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Manfred Heinlein .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2022 The Author(s), under exclusive license to Springer Science+Business Media, LLC, part of Springer Nature

About this protocol

Check for updates. Verify currency and authenticity via CrossMark

Cite this protocol

Huang, C., Heinlein, M. (2022). Function of Plasmodesmata in the Interaction of Plants with Microbes and Viruses. In: Benitez-Alfonso, Y., Heinlein, M. (eds) Plasmodesmata. Methods in Molecular Biology, vol 2457. Humana, New York, NY. https://doi.org/10.1007/978-1-0716-2132-5_2

Download citation

  • DOI: https://doi.org/10.1007/978-1-0716-2132-5_2

  • Published:

  • Publisher Name: Humana, New York, NY

  • Print ISBN: 978-1-0716-2131-8

  • Online ISBN: 978-1-0716-2132-5

  • eBook Packages: Springer Protocols

Publish with us

Policies and ethics