Plasmodesmata: Channels for intercellular signaling during plant growth and development

Methods in Molecular Biology

Volumn 1217, Issue , 2015, Pages 3-24

  Sevilem, Iris ^a   Yadav, Shri Ram ^a   Helariutta, Ykaö ^a  

^a NONE

Author keywords

Callose; Non cell autonomous proteins (NCAP); Plant development; Plasmodesmata (PD); Rafts

Indexed keywords

ARABIDOPSIS; ARTICLE; ASYMMETRIC CELL DIVISION; CELL COMMUNICATION; CELL MEMBRANE; CELL STRUCTURE; EMBRYO DEVELOPMENT; ENDOPLASMIC RETICULUM; HOMEOSTASIS; HYPOPHYSIS; INTRACELLULAR SIGNALING; LIPID COMPOSITION; MERISTEM; NONHUMAN; PLANT DEVELOPMENT; PLANT GROWTH; PLANT LEAF; PLASMODESMA; PRIORITY JOURNAL; ROOT CELL; ROOT GROWTH; STEM CELL NICHE; TRICHOME; CELL DIFFERENTIATION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PLANT; PLANT CELL; SIGNAL TRANSDUCTION; TRANSPORT AT THE CELLULAR LEVEL; ULTRASTRUCTURE;

CALLOSE; GLUCAN; VEGETABLE PROTEIN;

BIOLOGICAL TRANSPORT; CELL COMMUNICATION; CELL DIFFERENTIATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; GLUCANS; PLANT CELLS; PLANT DEVELOPMENT; PLANT PROTEINS; PLANTS; PLASMODESMATA; SIGNAL TRANSDUCTION;

EID: 84921821300     PISSN: 10643745     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-1-4939-1523-1_1     Document Type: Article

References (120)

1. Cilia ML, Jackson D (2004) Plasmodesmata form and function. Curr Opin Cell Biol 16:500–506
2. Lucas WJ, Lee JY (2004) Plasmodesmata as a supracellular control network in plants. Nat Rev Mol Cell Biol 5:712–726
3. Lucas WJ, Ham BK, Kim JY (2009) Plasmodesmata - bridging the gap between neighboring plant cells. Trends Cell Biol 19:495–503
4. 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
5. Barton DA, Cole L, Collings DA et al (2011) Cell-to-cell transport via the lumen of the endoplasmic reticulum. Plant J 66:806–817
6. Bayer EM, Bottrill AR, Walshaw J et al (2006) Arabidopsis cell wall proteome defi ned using multidimensional protein identifi cation technology. Proteomics 6:301–311
7. Levy A, Erlanger M, Rosenthal M et al (2007) A plasmodesmata-associated beta-1,3- glucanase in Arabidopsis. Plant J 49:669–682
8. Thomas CL, Bayer EM, Ritzenthaler C et al (2008) Specific targeting of a plasmodesmal protein affecting cell-to-cell communication. PLoS Biol 6:7
9. 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 traffi cking. Plant Cell 21:581–594
10. Fernandez-Calvino L, Faulkner C, Walshaw J et al (2011) Arabidopsis plasmodesmal proteome. PLoS One 6:e18880
11. Ham BK, Li G, Kang BH et al (2012) Overexpression of Arabidopsis plasmodesmata germin-like proteins disrupts root growth and development. Plant Cell 24:3630–3648
12. Salmon MS, Bayer EM (2013) Dissecting plasmodesmata molecular composition by mass spectrometry-based proteomics. Front Plant Sci 3:307
13. Zalepa-King L, Citovsky V (2013) A plasmodesmal glycosyltransferase-like protein. PLoS One 8:580-825
14. 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
15. Raffaele S, Bayer E, Mongrand S (2009) Upregulation of the plant protein remorin correlates with dehiscence and cell maturation: A link with the maturation of plasmodesmata? Plant Signal Behav 4:915–919
16. Mongrand S, Stanislas T, Bayer EM et al (2010) Membrane rafts in plant cells. Trends Plant Sci 15:656–663
17. Keinath NF, Kierszniowska S, Lorek J et al (2010) PAMP (pathogen-associated molecular pattern)-induced changes in plasma membrane compartmentalization reveal novel components of plant immunity. J Biol Chem 285:39140–39149
18. Simon-Plas F, Perraki A, Bayer E et al (2011) An update on plant membrane rafts. Curr Opin Plant Biol 14:642–649
19. Tilsner J, Amari K, Torrance L (2011) Plasmodesmata viewed as specialised membrane adhesion sites. Protoplasma 248:39–60
20. White RG, Barton DA (2011) The cytoskeleton in plasmodesmata: A role in intercellular transport? J Exp Bot 62:5249–5266
21. Burch-Smith TM, Stonebloom S, Xu M et al (2011) Plasmodesmata during development: re-examination of the importance of primary, secondary, and branched plasmodesmata structure versus function. Protoplasma 248:61–74
22. Crawford KM, Zambryski PC (2000) Subcellular localization determines the availability of non-targeted proteins to plasmodesmatal transport. Curr Biol 10:1032–1040
23. Kim I, Cho E, Crawford K et al (2005) Cell-tocell movement of GFP during embryogenesis and early seedling development in Arabidopsis. Proc Natl Acad Sci U S A 102:2227–2231
24. Rim Y, Huang L, Chu H et al (2011) Analysis of Arabidopsis transcription factor families revealed extensive capacity for cell-to-cell movement as well as discrete traffi cking patterns. Mol Cells 32:519–526
25. Terry Terry BR, Robards AW (1987) Hydrodynamic radius alone governs the mobility of molecules through plasmodesmata. Planta 171:145–157
26. Dashevskaya S, Kopito RB, Friedman R et al (2008) Diffusion of anionic and neutral GFP derivatives through plasmodesmata in epidermal cells of Nicotiana benthamiana. Protoplasma 234:13–23
27. 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
28. Kim I, Zambryski PC (2005) Cell-to-cell communication via plasmodesmata during Arabidopsis embryogenesis. Curr Opin Plant Biol 8:593–599
29. Zhu T, Lucas WJ, Rost TL (1998) Directional cell-to-cell communication in the Arabidopsis root apical meristem I. An ultrastructural and functional analysis. Protoplasma 203:35–47
30. Zhu T, O’Quinn RL, Lucas WJ et al (1998) Directional cell-to-cell communication in the Arabidopsis root apical meristem II. Dynamics of plasmodesmatal formation. Protoplasma 204:84–93
31. Stadler R, Lauterbach C, Sauer N (2005) Cell-to-cell movement of green fl uorescent protein reveals post-phloem transport in the outer integument and identifi es symplastic domains in Arabidopsis seeds and embryos. Plant Physiol 139:701–712
32. Reddy GV, Heisler MG, Ehrhardt DW et al (2004) Real-time lineage analysis reveals oriented cell divisions associated with morphogenesis at the shoot apex of Arabidopsis thaliana. Development 131:4225–4237
33. Williams L, Fletcher JC (2005) Stem cell regulation in the Arabidopsis shoot apical meristem. Curr Opin Plant Biol 8:582–586
34. Marcotrigiano M (2001) Genetic mosaics and the analysis of leaf development. Int J Plant Sci 162:513–525
35. Jackson D, Veit B, Hake S (1994) Expression of maize KNOTTED1 related homeobox genes in the shoot apical meristem predicts patterns of morphogenesis in the vegetative shoot. Development 120:405–413
36. Lucas WJ, Bouché-Pillon S, Jackson DP et al (1995) Selective traffi cking of KNOTTED1 homeodomain protein and its mRNA through plasmodesmata. Science 270:1980–1983
37. Kim JY, Yuan Z, Jackson D (2003) Developmental regulation and signifi cance of KNOX protein traffi cking in Arabidopsis. Development 130:4351–4362
38. Laux T, Mayer KF, Berger J et al (1996) The WUSCHEL gene is required for shoot and fl oral meristem integrity in Arabidopsis. Development 122:87–96
39. Mayer KF, Schoof H, Haecker A et al (1998) Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 95:805–815
40. Tucker MR, Laux T (2007) Connecting the paths in plant stem cell regulation. Trends Cell Biol 17:403–410
41. Schoof H, Lenhard M, Haecker A et al (2000) The stem cell population of Arabidopsis shoot meristems is maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell 100:635–644
42. 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
43. Ishida T, Kurata T, Okada K et al (2008) A genetic regulatory network in the development of trichomes and root hairs. Annu Rev Plant Biol 59:365–386
44. Schiefelbein J, Kwak SH, Wieckowski Y et al (2009) The gene regulatory network for root epidermal cell-type pattern formation in Arabidopsis. J Exp Bot 60:1515–1521
45. Pesch M, Hülskamp M (2009) One, two, three models for trichome patterning in Arabidopsis ? Curr Opin Plant Biol 12: 587–592
46. Balkunde R, Pesch M, Hülskamp M (2010) Trichome patterning in Arabidopsis thaliana: from genetic to molecular models. Curr Top Dev Biol 91:299–321
47. 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
48. Balkunde R, Bouyer D, Hülskamp M (2011) Nuclear trapping by GL3 controls intercellular transport and redistribution of TTG1 protein in Arabidopsis. Development 138:5039–5048
49. Wester K, Digiuni S, Geier F et al (2009) Functional diversity of R3 single-repeat genes in trichome development. Development 136:1487–1496
50. Wada T, Tachibana T (1997) Epidermal cell differentiation in Arabidopsis determined by a Myb homolog, CPC. Science 277:1113–1116
51. Wada T, Kurata T, Tominaga R et al (2002) Role of a positive regulator of root hair development, CAPRICE, in Arabidopsis root epidermal cell differentiation. Development 129:5409–5419
52. Schellmann S, Schnittger A, Kirik V et al (2002) TRIPTYCHON and CAPRICE mediate lateral inhibition during trichome and root hair patterning in Arabidopsis. EMBO J 21:5036–5046
53. Kurata T, Ishida T, Kawabata-Awai C et al (2005) Cell-to-cell movement of the CAPRICE proteinin Arabidopsis root epidermal cell differentiation. Development 132:5387–5398
54. Bernhardt C, Lee MM, Gonzalez A et al (2003) The bHLH genes GLABRA3 (GL3) and ENHANCER OF GLABRA3 (EGL3) specify epidermal cell fate in the Arabidopsis root. Development 130:6431–6439
55. Bernhardt C, Zhao M, Gonzalez A et al (2005) The bHLH genes GL3 and EGL3 participate in an intercellular regulatory circuit that controls cell patterning in the Arabidopsis root epidermis. Development 132:291–298
56. Putterill J, Laurie R, Macknight R (2004) It’s time to fl ower: The genetic control of fl owering time. Bioessays 26:363–373
57. Imaizumi T, Kay S (2006) Photoperiodic control of flowering: not only by coincidence. Trends Plant Sci 11:550–558
58. Corbesier L, Vincent C, Jang S et al (2007) FT protein movement contributes to longdistance signaling in fl oral induction of Arabidopsis. Science 316:1030–1033
59. Jaeger K, Wigge P (2007) FT protein acts as a long-range signal in Arabidopsis. Curr Biol 17:1050–1054
60. Mathieu J, Warthmann N, Kuttner F et al (2007) Export of FT protein from phloem companion cells is suffi cient for fl oral induction in Arabidopsis. Curr Biol 17:1055–1060
61. Abe M, Kobayashi Y, Yamamoto S et al (2005) FD, a bZIP protein mediating signals from the fl oral pathway integrator FT at the shoot apex. Science 309:1052–1056
62. Wigge P, Kim M, Jaeger K et al (2005) Integration of spatial and temporal information during fl oral induction in Arabidopsis. Science 309:1056–1059
63. Gisel A, Barella S, Hempel FD et al (1999) Temporal and spatial regulation of symplastic trafficking during development in Arabidopsis thaliana apices. Development 126:1879–1889
64. Rinne PL, van der Schoot C (1998) Symplasmic fields in the tunica of the shoot apical meristem coordinate morphogenetic events. Development 125:1477–1485
65. Rinne PL, Welling A, Vahala J et al (2011) Chilling of dormant buds hyperinduces FLOWERING LOCUS T and recruits GA-inducible 1,3-beta glucanases to reopen signal conduits and release dormancy in Populus. Plant Cell 23:130–146
66. Sessions A, Yanofsky MF, Weigel D (2000) Cell-cell signaling and movement by the fl oral transcription factors LEAFY and APETALA1. Science 289:779–782
67. Wu X, Dinneny JR, Crawford KM et al (2003) Modes of intercellular transcription factor movement in the Arabidopsis apex. Development 130:3735–3745
68. Tröbner W, Ramirez L, Motte P et al (1992) GLOBOSA: A homeotic gene which interacts with DEFICIENS in the control of Antirrhinum fl oral organogenesis. EMBO J 11:4693–4704
69. Perbal MC, Haughn G, Saedler H et al (1996) Non-cell-autonomous function of the Antirrhinum fl oral homeotic proteins DEFICIENS and GLOBOSA is exerted by their polar cell-to-cell traffi cking. Development 122:3433–3441
70. Bowman JL, Smyth DR, Meyerowitz EM (1989) Genes directing flower development in Arabidopsis. Plant Cell 1:37–52
71. Lenhard M, Bohnert A, Jürgens G et al (2001) Termination of stem cell maintenance in Arabidopsis fl oral meristems by interactions between WUSCHEL and AGAMOUS. Cell 105:805–814
72. Urbanus SL, Martinelli AP, Dinh QD et al (2010) Intercellular transport of epidermisexpressed MADS domain transcription factors and their effect on plant morphology and fl oral transition. Plant J 63:60–72
73. Dolan L, Janmaat K, Willemsen V et al (1993) Cellular organisation of the Arabidopsis thaliana root. Development 119:71–84
74. Weijers D, Schlereth A, Ehrismann JS et al (2006) Auxin triggers transient local signaling for cell specifi cation in Arabidopsis embryogenesis. Dev Cell 10:265–270
75. Schlereth A, Möller B, Liu W et al (2010) MONOPTEROS controls embryonic root initiation by regulating a mobile transcription factor. Nature 464:913–916
76. 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
77. Nakajima K, Sena G, Nawy T et al (2001) Intercellular movement of the putative transcription factor SHR in root patterning. Nature 413:307–311
78. Sabatini S, Heidstra R, Wildwater M et al (2003) SCARECROW is involved in positioning the stem cell niche in the Arabidopsis root meristem. Genes Dev 17:354–358
79. Sarkar AK, Luijten M, Miyashima S et al (2007) Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers. Nature 446:811–814
80. Stahl Y, Wink RH, Ingram GC et al (2009) A signaling module controlling the stem cell niche in Arabidopsis root meristems. Curr Biol 19:909–914
81. Stahl Y, Grabowski S, Bleckmann A et al (2013) Moderation of Arabidopsis root stemness by CLAVATA1 and ARABIDOPSISCRINKLY4 receptor kinase Complexes. Curr Biol 23:362–371
82. Sozzani R, Cui H, Moreno-Risueno MA et al (2010) Spatiotemporal regulation of cellcycle genes by SHORTROOT links patterning and growth. Nature 466:128–132
83. 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
84. Miyashima S, Koi S, Hashimoto T et al (2011) Non-cell-autonomous microRNA165 acts in a dose-dependent manner to regulate multiple differentiation status in the Arabidopsis root. Development 138:2303–2313
85. Samuels AL, Giddings TH Jr, Staehelin LA (1995) Cytokinesis in tobacco BY-2 and root tip cells: a new model of cell plate formation in higher plants. J Cell Biol 130:1345–1357
86. Parre E, Geitmann A (2005) More than a leak sealant. The mechanical properties of callose in pollen tubes. Plant Physiol 137:274–286
87. Chen XY, Kim JY (2009) Callose synthesis in higher plants. Plant Signal Behav 4:489–492
88. Zavaliev R, Ueki S, Epel BL et al (2011) Biology of callose (beta-1,3-glucan) turnover at plasmodesmata. Protoplasma 248:117–130
89. Bucher GL, Tarina C, Heinlein M et al (2001) Local expression of enzymatically active class I beta-1, 3-glucanase enhances symptoms of TMV infection in tobacco. Plant J 28:361–369
90. Rinne PL, Kaikuranta PM, van der Schoot C (2001) The shoot apical meristem restores its symplasmic organization during chillinginduced release from dormancy. Plant J 26:249–264
91. Levy A, Guenoune-Gelbart D, Epel BL (2007) beta-1,3-Glucanases: Plasmodesmal gate keepers for intercellular communication. Plant Signal Behav 2:404–407
92. Benitez-Alfonso Y, Faulkner C, Pendle A et al (2013) Symplastic intercellular connectivity regulates lateral root patterning. Dev Cell 26:136–147
93. Verma DP, Hong Z (2001) Plant callose synthase complexes. Plant Mol Biol 47:693–701
94. Chen XY, Liu L, Lee E et al (2009) The Arabidopsis callose synthase gene GSL8 is required for cytokinesis and cell patterning. Plant Physiol 150:105–113
95. Guseman JM, Lee JS, Bogenschutz NL et al (2010) Dysregulation of cell-to-cell connectivity and stomatal patterning by loss-offunction mutation in Arabidopsis chorus (glucan synthase-like 8). Development 137:1731–1741
96. Barratt DH, Kölling K, Graf A et al (2011) Callose synthase GSL7 is necessary for normal phloem transport and infl orescence growth in Arabidopsis. Plant Physiol 155:328–341
97. Xie B, Wang X, Zhu M et al (2011) CalS7 encodes a callose synthase responsible for callose deposition in the phloem. Plant J 65:1–14
98. Vatén A, Dettmer J, Wu S et al (2011) Callose biosynthesis regulates symplastic traffi cking during root development. Dev Cell 21:1144–1155
99. Slewinski TL, Baker RF, Stubert A et al (2012) Tie-dyed2 encodes a callose synthase that functions in vein development and affects symplastic traffi cking within the phloem of maize leaves. Plant Physiol 160:1540–1550
100. Sagi G, Katz A, Guenoune-Gelbart D et al (2005) Class 1 reversibly glycosylated polypeptides are plasmodesmal-associated proteins delivered to plasmodesmata via the Golgi apparatus. Plant Cell 17:1788–1800
101. 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
102. 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 6:1001-1119
103. 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
104. Benitez-Alfonso Y, Cilia M, San Roman A et al (2009) Control of Arabidopsis meristem development by thioredoxin-dependent regulation of intercellular transport. Proc Natl Acad Sci U S A 106:3615–3620
105. Stonebloom S, Burch-Smith T, Kim I et al (2009) Loss of the plant DEAD-box protein ISE1 leads to defective mitochondria and increased cell-to-cell transport via plasmodesmata. Proc Natl Acad Sci U S A 106: 17229–17234
106. Kobayashi K, Otegui MS, Krishnakumar S et al (2007) INCREASED SIZE EXCLUSION LIMIT 2 encodes a putative DEVH box RNA helicase involved in plasmodesmata function during Arabidopsis embryogenesis. Plant Cell 19:1885–1897
107. 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
108. Kong D, Karve R, Willet A et al (2012) Regulation of plasmodesmatal permeability and stomatal patterning by the glycosyltransferase- like protein KOBITO1. Plant Physiol 159:156–168
109. Pagant S, Bichet A, Sugimoto K et al (2002) KOBITO1 encodes a novel plasma membrane protein necessary for normal synthesis of cellulose during cell expansion in Arabidopsis. Plant Cell 14:2001–2013
110. Brocard-Gifford I, Lynch TJ, Garcia ME et al (2004) The Arabidopsis thaliana ABSCISIC ACID-INSENSITIVE8 encodes a novel protein mediating abscisic acid and sugar responses essential for growth. Plant Cell 16:406–421
111. 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
112. Xu M, Cho E, Burch-Smith TM et al (2012) Plasmodesmata formation and cell-to-cell transport are reduced in decreased size exclusion limit 1 during embryogenesis in Arabidopsis. Proc Natl Acad Sci U S A 109:5098–5103
113. Yamagishi K, Nagata N, Yee KM et al (2005) TANMEI/EMB2757 encodes a WD repeat protein required for embryo development in Arabidopsis. Plant Physiol 139:163–173
114. Benitez-Alfonso Y, Faulkner C, Ritzenthaler C et al (2010) Plasmodesmata: Gateways to local and systemic virus infection. Mol. Plant Microbe Interact 23:1403–1412
115. Crawford KM, Zambryski PC (2001) Nontargeted and targeted protein movement through plasmodesmata in leaves in different developmental and physiological states. Plant Physiol 125:1802–1812
116. Kim JY, Rim Y, Wang J et al (2005) A novel cell-to-cell traffi cking assay indicates that the KNOX homeodomain is necessary and sufficient for intercellular protein and mRNA traffi cking. Genes Dev 19:788–793
117. Gallagher KL, Benfey PN (2009) Both the conserved GRAS domain and nuclear localization are required for SHORT-ROOT movement. Plant J 57:785–797
118. Koizumi K, Wu S, MacRae-Crerar A et al (2011) An essential protein that interacts with endosomes and promotes movement of the SHORT-ROOT transcription factor. Curr Biol 21:1559–1564
119. Wu S, Gallagher KL (2013) Intact microtubules are required for the intercellular movement of the SHORT-ROOT transcription factor. Plant J 74:148–159
120. Xu XM, Wang J, Xuan Z et al (2011) Chaperonins facilitate KNOTTED1 cell-tocell traffi cking and stem cell function. Science 333:1141–1144