Plasmodesmata in integrated cell signalling: Insights from development and environmental signals and stresses

Journal of Experimental Botany

Volumn 65, Issue 22, 2014, Pages 6337-6358

  Sager, Ross ^a   Lee, Jung Youn ^a  

^a UNIVERSITY OF DELAWARE   (United States)

Author keywords

biotic and abiotic stress; callose.; cell signalling; cell to cell communication; development; environmental stresses; hormones; Plasmodesmata

Indexed keywords

ENVIRONMENT; METABOLISM; PERMEABILITY; PHYSIOLOGICAL STRESS; PLANT DEVELOPMENT; PLASMODESMA; SIGNAL TRANSDUCTION;

ENVIRONMENT; PERMEABILITY; PLANT DEVELOPMENT; PLASMODESMATA; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL;

EID: 84919425727     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/eru365     Document Type: Review

References (180)

1. Agbeci M, Grangeon R, Nelson RS, Zheng H, Laliberte JF. 2013. Contribution of host intracellular transport machineries to intercellular movement of turnip mosaic virus. Plos Pathogens 9, e1003683.
2. Amari K, Lerich A, Schmitt-Keichinger C, Dolja VV, Ritzenthaler C. 2011. Tubule-guided cell-to-cell movement of a plant virus requires class XI myosin motors. Plos Pathogens 7, e1002327.
3. An Q, Ehlers K, Kogel KH, van Bel AJ, Huckelhoven R. 2006. Multivesicular compartments proliferate in susceptible and resistant MLA12-barley leaves in response to infection by the biotrophic powdery mildew fungus. New Phytologist 172, 563-576.
4. Avisar D, Prokhnevsky AI, Dolja VV. 2008. Class VIII myosins are required for plasmodesmatal localization of a closterovirus Hsp70 homolog. Journal of Virology 82, 2836-2843.
5. Baluska F, Cvrckova F, Kendrick-Jones J, Volkmann D. 2001 Sink plasmodesmata as gateways for phloem unloading. Myosin VIII and calreticulin as molecular determinants of sink strength? Plant Physiology 126, 39-46.
6. Baluska F, Samaj J, Hlavacka A, Kendrick-Jones J, Volkmann D. 2004. Actin-dependent fluid-phase endocytosis in inner cortex cells of maize root apices. Journal of Experimental Botany 55, 463-473.
7. Baluska F, Samaj J, Napier R, Volkmann D. 1999. Maize calreticulin localizes preferentially to plasmodesmata in root apex. The Plant Journal 19, 481-488.
8. Bar-Dror T, Dermastia M, Kladnik A et al. 2011. Programmed cell death occurs asymmetrically during abscission in tomato. Plant Cell 23, 4146-4163.
9. Barratt DH, Kolling K, Graf A, Pike M, Calder G, Findlay K, Zeeman SC, Smith AM. 2011. Callose synthase GSL7 is necessary for normal phloem transport and inflorescence growth in Arabidopsis. Plant Physiology 155, 328-341.
10. Beffa RS, Hofer RM, Thomas M, Meins F, Jr. 1996. Decreased susceptibility to viral disease of β-1, 3-glucanase-deficient plants generated by antisense transformation. Plant Cell 8, 1001-1011.
11. Benitez-Alfonso Y, Cilia M, San Roman A, Thomas C, Maule A, Hearn S, Jackson D. 2009. Control of Arabidopsis meristem development by thioredoxin-dependent regulation of intercellular transport. Proceedings of the National Academy of Sciences, USA 106, 3615-3620.
12. Benitez-Alfonso Y, Faulkner C, Pendle A, Miyashima S, Helariutta Y, Maule A. 2013. Symplastic intercellular connectivity regulates lateral root patterning. Developmental Cell 26, 136-147.
13. Benitez-Alfonso Y, Faulkner C, Ritzenthaler C, Maule AJ. 2010. Plasmodesmata: gateways to local and systemic virus infection. Molecular Plant-Microbe Interactions 23, 1403-1412.
14. Benitez-Alfonso Y, Jackson D. 2009. Redox homeostasis regulates plasmodesmal communication in Arabidopsis meristems. Plant Signaling and Behavior 4, 655-659.
15. Bergmans ACJ, de Boer AD, Derksen JWM, van der Schoot C. 1997. The symplasmic coupling of L2-cells diminishes in early floral development of Iris. Planta 203, 245-252.
16. Bilska A, Sowinski P. 2010. Closure of plasmodesmata in maize (Zea mays) at low temperature: a new mechanism for inhibition of photosynthesis. Annals of Botany 106, 675-686.
17. Blackman LM, Harper JD, Overall RL. 1999. Localization of a centrinlike protein to higher plant plasmodesmata. European Journal of Cell Biology 78, 297-304.
18. Boyko V, Ferralli J, Ashby J, Schellenbaum P, Heinlein M. 2000. Function of microtubules in intercellular transport of plant virus RNA. Nature Cell Biology 2, 826-832.
19. Boyko V, Hu Q, Seemanpillai M, Ashby J, Heinlein M. 2007. Validation of microtubule-associated Tobacco mosaic virus RNA movement and involvement of microtubule-aligned particle trafficking. The Plant Journal 51, 589-603.
20. Bucher GL, Tarina C, Heinlein M, Di Serio F, Meins F, Jr., Iglesias VA. 2001. Local expression of enzymatically active class I β-1, 3-glucanase enhances symptoms of TMV infection in tobacco. The Plant Journal 28, 361-369.
21. Burch-Smith TM, Brunkard JO, Choi YG, Zambryski PC. 2011a. Organelle-nucleus cross-talk regulates plant intercellular communication via plasmodesmata. Proceedings of the National Academy of Sciences, USA 108, E1451-1460.
22. Burch-Smith TM, Stonebloom S, Xu M, Zambryski PC. 2011b. Plasmodesmata during development: re-examination of the importance of primary, secondary, and branched plasmodesmata structure versus function. Protoplasma 248, 61-74.
23. Burch-Smith TM, Zambryski PC. 2010. Loss of INCREASED SIZE EXCLUSION LIMIT (ISE)1 or ISE2 increases the formation of secondary plasmodesmata. Current Biology 20, 989-993.
24. Burch-Smith TM, Zambryski PC. 2011. Plasmodesmata paradigm shift: Regulation from without versus within. Annual Review of Plant Biology
25. Chandler JW. 2012. Floral meristem initiation and emergence in plants. Cellular and Molecular Life Sciences 69, 3807-3818.
26. Chen XY, Liu L, Lee E, Han X, Rim Y, Chu H, Kim SW, Sack F, Kim JY. 2009. The Arabidopsis callose synthase gene GSL8 is required for cytokinesis and cell patterning. Plant Physiology 150, 105-113.
27. Christensen NM, Faulkner C, Oparka K. 2009. Evidence for unidirectional flow through plasmodesmata. Plant Physiology 150, 96-104.
28. Citovsky V, Ghoshroy S, Tsui F, Klessig D. 1998. Non-toxic concentrations of cadmium inhibit systemic movement of turnip vein clearing virus by a salicylic acid-independent mechanism. The Plant Journal 16, 13-20.
29. Clement C, Audran JC. 1995. Anther wall layers control pollen sugar nutrition in lilium. Protoplasma 187, 172-181.
30. Conti L, Bradley D. 2007. TERMINAL FLOWER1 is a mobile signal controlling Arabidopsis architecture. Plant Cell 19, 767-778.
31. Ding B. 2009. The biology of viroid-host interactions. Annual Review of Phytopathology 47, 105-131.
32. Ding B, Kwon M, Warnberg L. 1996. Evidence that actin filaments are involved in controlling the permeability of plasmodesmata in tobacco mesophyll. The Plant Journal 10, 157-164.
33. Dobnik D, Baebler S, Kogovsek P, Pompe-Novak M, Stebih D, Panter G, Janez N, Morisset D, Zel J, Gruden K. 2013. β-1, 3- glucanase class III promotes spread of PVY and improves protein production. Plant Biotechnology Report 7, 547-555.
34. Dong X, Hong Z, Chatterjee J, Kim S, Verma DP. 2008. Expression of callose synthase genes and its connection with Npr1 signaling pathway during pathogen infection. Planta 229, 87-98.
35. Dong X, Hong Z, Sivaramakrishnan M, Mahfouz M, Verma DP. 2005. Callose synthase (CalS5) is required for exine formation during microgametogenesis and for pollen viability in Arabidopsis. The Plant Journal 42, 315-328.
36. Doxey AC, Yaish MW, Moffatt BA, Griffith M, McConkey BJ. 2007. Functional divergence in the Arabidopsis β-1, 3-glucanase gene family inferred by phylogenetic reconstruction of expression states. Molecular Biology and Evolution 24, 1045-1055.
37. Dute RR, Peterson CM, Rushing AE. 1989. Utrastructural changes of the egg apparatus associated with fertilization and proembryo development of soybean, Glycine max (Fabaceae). Annals of Botany 64, 123-135.
38. Ehlers K, Kollmann R. 2001. Primary and secondary plasmodesmata: structure, origin, and functioning. Protoplasma 216, 1-30.
39. Ehlers K, van Bel AJ. 2010. Dynamics of plasmodesmal connectivity in successive interfaces of the cambial zone. Planta 231, 371-385.
40. Ehlers K, Westerloh MG. 2013. Developmental control of plasmodesmata frequency, structure, and function. In: Sokolowska K, Sowinski P, eds. Symplasmic transport in vascular plants . New York: Springer Science, 41-82.
41. Esau K, Thorsch J. 1984. The sieve plate of Echium (Boraginaceae): Developmental aspects and response of P-protein to protein digestion. Journal of Ultrastructure Research 86, 31-45.
42. Estornell LH, Agusti J, Merelo P, Talon M, Tadeo FR. 2013. Elucidating mechanisms underlying organ abscission. Plant Science 199-200, 48-60.
43. Faulkner C, Akman OE, Bell K, Jeffree C, Oparka K. 2008. Peeking into pit fields: A multiple twinning model of secondary plasmodesmata formation in tobacco. Plant Cell 20, 1504-1518.
44. Fitzgibbon J, Beck M, Zhou J, Faulkner C, Robatzek S, Oparka K. 2013. A developmental framework for complex plasmodesmata formation revealed by large-scale imaging of the Arabidopsis leaf epidermis. Plant Cell 25, 57-70.
45. Geimer S, Melkonian M. 2005. Centrin scaffold in Chlamydomonas reinhardtii revealed by immunoelectron microscopy. Eukaryotic Cell 4, 1253-1263.
46. Gisel A, Barella S, Hempel FD, Zambryski PC. 1999. Temporal and spatial regulation of symplastic trafficking during development in Arabidopsis thaliana apices. Development 126, 1879-1889.
47. Gisel A, Hempel FD, Barella S, Zambryski P. 2002. Leaf-to-shoot apex movement of symplastic tracer is restricted coincident with flowering in Arabidopsis. Proceedings of the National Academy of Sciences, USA 99, 1713-1717.
48. Guseman JM, Lee JS, Bogenschutz NL, Peterson KM, Virata RE, Xie B, Kanaoka MM, Hong Z, Torii KU. 2010. Dysregulation of cellto- cell connectivity and stomatal patterning by loss-of-function mutation in Arabidopsis chorus (glucan synthase-like 8). Development 137, 1731-1741.
49. Han X, Hyun TK, Zhang M, Kumar R, Koh E, Kang BH, Lucas WJ, Kim JY. 2014. Auxin-callose-mediated plasmodesmal gating is essential for tropic auxin gradient formation and signaling. Developmental Cell 28, 132-146.
50. Han YZ, Huang BQ, Zee SY, Yuan M. 2000. Symplastic communication between the central cell and the egg apparatus cells in the embryo sac of Torenia fournieri Lind. before and during fertilization. Planta 211, 158-162.
51. Harries PA, Palanichelvam K, Yu W, Schoelz JE, Nelson RS. 2009a. The cauliflower mosaic virus protein P6 forms motile inclusions that traffic along actin microfilaments and stabilize microtubules. Plant Physiology 149, 1005-1016.
52. Harries PA, Park JW, Sasaki N, Ballard KD, Maule AJ, Nelson RS. 2009b. Differing requirements for actin and myosin by plant viruses for sustained intercellular movement. Proceedings of the National Academy of Sciences, USA 106, 17594-17599.
53. Heinlein M. 2002. Plasmodesmata: dynamic regulation and role in macromolecular cell-to-cell signaling. Current Opinion in Plant Biology 5, 543-552.
54. Henry EW. 1979. Peroxidases in tobacco abscission zone tissue. VI. Ultrastructural localization in plasmodesmata during ethylene-induced abscission. Cytologia 44, 135-152.
55. Henslop-Harrison J. 1966. Cytoplasmic connexions between angiosperm meiocytes. Annals of Botany 30, 221-222.
56. Hepler PK. 1982. Endoplasmic reticulum in the formation of the cell plate and plasmodesmata. Protoplasma 111, 121-133.
57. Hepler PK, Newcomb EH. 1967. Fine structure of cell plate formation in the apical meristem of Phaseolus roots. Journal of Ultrastructure Research 19, 498-513.
58. Hofius D, Hajirezaei MR, Geiger M, Tschiersch H, Melzer M, Sonnewald U. 2004. RNAi-mediated tocopherol deficiency impairs photoassimilate export in transgenic potato plants. Plant Physiology 135, 1256-1268.
59. 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, 329-335.
60. Holdaway-Clarke TL, Walker NA, Overall RL. 1996. Measurement of the electrical resistance of plasmodesmata and membranes of corn suspension-culture cells. Planta 199, 537-544.
61. Hong Z, Delauney AJ, Verma DP. 2001. A cell plate-specific callose synthase and its interaction with phragmoplastin. Plant Cell 13, 755-768.
62. Hu H, Sheehan JH, Chazin WJ. 2004. The mode of action of centrin. Binding of Ca2+ and a peptide fragment of Kar1p to the C-terminal domain. The Journal of Biological Chemistry 279, 50895-50903.
63. Iglesias VA, Meins F. 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. The Plant Journal 21, 157-166.
64. Isono K, Shimizu M, Yoshimoto K, Niwa Y, Satoh K, Yokota A, Kobayashi H. 1997. Leaf-specifically expressed genes for polypeptides destined for chloroplasts with domains of σ70 factors of bacterial RNA polymerases in Arabidopsis thaliana. Proceedings of the National Academy of Sciences, USA 94, 14948-14953.
65. Jacobs AK, Lipka V, Burton RA, Panstruga R, Strizhov N, Schulze- Lefert P, Fincher GB. 2003. An Arabidopsis callose synthase, GSL5, is required for wound and papillary callose formation. Plant Cell 15, 2503-2513.
66. Jensen TE, Valdovinos JG. 1967. Fine structure of abscission zones: i. abscission zones of the pedicels of tobacco and tomato flowers at anthesis. Planta 77, 298-318.
67. Jia XY, He LH, Jing RL, Li RZ. 2009. Calreticulin: conserved protein and diverse functions in plants. Physiologia Plantarum 136, 127-138.
68. Karlson DT, Fujino T, Kimura S, Baba K, Itoh T, Ashworth EN. 2003. Novel plasmodesmata association of dehydrin-like proteins in coldacclimated Red-osier dogwood (Cornus sericea). Tree Physiology 23, 759-767.
69. Kawakami S, Watanabe Y, Beachy RN. 2004. Tobacco mosaic virus infection spreads cell to cell as intact replication complexes. Proceedings of the National Academy of Sciences, USA 101, 6291-6296.
70. Kim I, Cho E, Crawford K, Hempel FD, Zambryski PC. 2005a. Cell-to-cell movement of GFP during embryogenesis and early seedling development in Arabidopsis. Proceedings of the National Academy of Sciences, USA 102, 2227-2231.
71. Kim I, Hempel FD, Sha K, Pfluger J, Zambryski PC. 2002. Identification of a developmental transition in plasmodesmatal function during embryogenesis in Arabidopsis thaliana. Development 129, 1261-1272.
72. Kim I, Kobayashi K, Cho E, Zambryski PC. 2005b. Subdomains for transport via plasmodesmata corresponding to the apical-basal axis are established during Arabidopsis embryogenesis. Proceedings of the National Academy of Sciences, USA 102, 11945-11950.
73. Knight AE, Kendrick-Jones J. 1993. A myosin-like protein from a higher plant. Journal of Molecular Biology 231, 148-154.
74. Knoblauch M, van Bel AJ. 1998. Sieve tubes in action. Plant Cell 10, 35-50.
75. Kollmann R, Glockmann C. 1991. Studies on graft unions. Protoplasma 165, 71-85.
76. Kozieradzka-Kiszkurno M, Bohdanowicz J. 2010. Unusual electrondense dome associates with compound plasmodesmata in the embryosuspensor of genus Sedum (Crassulaceae). Protoplasma 247, 117-120.
77. Kozieradzka-Kiszkurno M, Plachno BJ. 2012. Are there symplastic connections between the endosperm and embryo in some angiosperms? A lesson from the Crassulaceae family. Protoplasma 249, 1081-1089.
78. Kurusu T, Kuchitsu K, Nakano M, Nakayama Y, Iida H. 2013. Plant mechanosensing and Ca2+ transport. Trends Plant Science 18, 227-233.
79. Lee J-Y, Cho S, Sager R. 2011a. Plasmodesmata and non-cell autonomous signling in plants. In: Murphy AS, ed. The Plant Plasma Membrane . Berlin: Springer-Verlag, 87-106.
80. Lee JJ, Woodward AW, Chen ZJ. 2007. Gene expression changes and early events in cotton fibre development. Annals of Botany 100, 1391-1401.
81. Lee JY. 2014. New and old roles of plasmodesmata in immunity and parallels to tunneling nanotubes. Plant Science 221-222, 13-20.
82. Lee JY, Cui WE. 2009. Non-cell autonomous RNA trafficking and longdistance signaling. Journal of Plant Biology 52, 10-18.
83. Lee JY, Taoka K, Yoo BC, Ben-Nissan G, Kim DJ, Lucas WJ. 2005. Plasmodesmal-associated protein kinase in tobacco and Arabidopsis recognizes a subset of non-cell-autonomous proteins. Plant Cell 17, 2817-2831.
84. Lee JY, Wang X, Cui W et al. 2011b. A plasmodesmata-localized protein mediates crosstalk between cell-to-cell communication and innate immunity in Arabidopsis. Plant Cell 23, 3353-3373.
85. Levy A, Erlanger M, Rosenthal M, Epel BL. 2007. A plasmodesmataassociated β-1, 3-glucanase in Arabidopsis. The Plant Journal 49, 669-682.
86. Liu JZ, Blancaflor EB, Nelson RS. 2005. The tobacco mosaic virus 126-kilodalton protein, a constituent of the virus replication complex, alone or within the complex aligns with and traffics along microfilaments. Plant Physiology 138, 1853-1865.
87. Liu N, Lin Z, Guan L, Gaughan G, Lin G. 2014. Antioxidant enzymes regulate reactive oxygen species during pod elongation in Pisum sativum and Brassica chinensis. PLoS ONE 9, e87588.
88. Lucas WJ. 2006. Plant viral movement proteins: agents for cell-to-cell trafficking of viral genomes. Virology 344, 169-184.
89. Lucas WJ, Lee JY. 2004. Plasmodesmata as a supracellular control network in plants. Nature Reviews Molecular Cell Biology 5, 712-726.
90. Malamy JE, Benfey PN. 1997. Organization and cell differentiation in lateral roots of Arabidopsis thaliana. Development 124, 33-44.
91. Mamun EA, Cantrill LC, Overall RL, Sutton BG. 2005a. Cellular organisation and differentiation of organelles in pre-meiotic rice anthers. Cell Biology International 29, 792-802.
92. Mamun EA, Cantrill LC, Overall RL, Sutton BG. 2005b. Cellular organisation in meiotic and early post-meiotic rice anthers. Cell Biology International 29, 903-913.
93. Mansfield SG, Briarty LG. 1991. Early embryogenesis in Arabidopsis thaliana. 2. The developing embryo. Canadian Journal of Botany-Revue Canadienne De Botanique 69, 461-476.
94. Meng L, Wong JH, Feldman LJ, Lemaux PG, Buchanan BB. 2010. A membrane-associated thioredoxin required for plant growth moves from cell to cell, suggestive of a role in intercellular communication. Proceedings of the National Academy of Sciences, USA 107, 3900-3905.
95. Milyaeva EL. 2007. Presumable role of plasmodesmata in floral signal transduction in shoot apical meristems of rudbeckia and perilla plants. Russian Journal of Plant Physiology 54, 498-506.
96. Mou Z, Fan W, Dong X. 2003. Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113, 935-944.
97. Mumm P, Wolf T, Fromm J, Roelfsema MR, Marten I. 2011. Cell type-specific regulation of ion channels within the maize stomatal complex. Plant and Cell Physiology 52, 1365-1375.
98. Mursalimov SR, Baiborodin SI, Sidorchuk YV, Shumny VK, Deineko EV. 2010. Characteristics of the cytomictic channel formation in Nicotiana tabacum L. pollen mother cells. Cytology and Genetics 44, 14-18.
99. Myouga F, Hosoda C, Umezawa T, Iizumi H, Kuromori T, Motohashi R, Shono Y, Nagata N, Ikeuchi M, Shinozaki K. 2008. A heterocomplex of iron superoxide dismutases defends chloroplast nucleoids against oxidative stress and is essential for chloroplast development in Arabidopsis. Plant Cell 20, 3148-3162.
100. Nanda AK, Andrio E, Marino D, Pauly N, Dunand C. 2010. Reactive oxygen species during plant-microorganism early interactions. Journal of Integrative Plant Biology 52, 195-204.
101. Niehl A, Heinlein M. 2011. Cellular pathways for viral transport through plasmodesmata. Protoplasma 248, 75-99.
102. Niehl A, Pena EJ, Amari K, Heinlein M. 2013. Microtubules in viral replication and transport. The Plant Journal 75, 290-308.
103. Niu N, Liang W, Yang X, Jin W, Wilson ZA, Hu J, Zhang D. 2013. EAT1 promotes tapetal cell death by regulating aspartic proteases during male reproductive development in rice. Nature Communications 4, 1445.
104. Northcote DH, Davey R, Lay J. 1989. Use of antisera to localize callose, xylan and arabinogalactan in the cell-plate, primary and secondary walls of plant-cells. Planta 178, 353-366.
105. Oparka KJ, Prior DAM, Wright KM. 1995. Symplastic communication between primary and developing lateral roots of Arabidopsis thaliana. Journal of Experimental Botany 46, 187-197.
106. Oparka KJ, Roberts AG, Boevink P, Santa Cruz S, Roberts I, Pradel KS, Imlau A, Kotlizky G, Sauer N, Epel B. 1999. Simple, but not branched, plasmodesmata allow the nonspecific trafficking of proteins in developing tobacco leaves. Cell 97, 743-754.
107. Ormenese S, Havelange A, Bernier G, van der Schoot C. 2002. The shoot apical meristem of Sinapis alba L. expands its central symplasmic field during the floral transition. Planta 215, 67-78.
108. Ormenese S, Havelange A, Deltour R, Bernier G. 2000. The frequency of plasmodesmata increases early in the whole shoot apical meristem of Sinapis alba L. during floral transition. Planta 211, 370-375.
109. Osborne DJ, Sargent JA. 1976. The positional differentiation of ethyleneresponsive cells in rachis abscission zones in leaves of Sambucus nigra and their growth and ultrastructural changes at senescence and separation. Planta 130, 203-210.
110. 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.
111. Perdue TD, Loukides CA, Bedinger PA. 1992. The formation of cytoplasmic channels between tapetal cells in Zea mays. Protoplasma 171, 75-79.
112. Pirselova B, Mistrikova V, Libantova J, Moravcikova J, Matusikova I. 2012. Study on metal-triggered callose deposition in roots of maize and soybean. Biologia 67, 698-705.
113. Radford JE, Vesk M, Overall RL. 1998. Callose deposition at plasmodesmata. Protoplasma 201, 30-37.
114. Radford JE, White RG. 1998. Localization of a myosin-like protein to plasmodesmata. The Plant Journal 14, 743-750.
115. Radford JE, White RG. 2011. Inhibitors of myosin, but not actin, alter transport through Tradescantia plasmodesmata. Protoplasma 248, 205-216.
116. Radice S, Ontivero M, Giordani E, Bellini E. 2008. Anatomical differences on development of fertile and sterile pollen grains of Prunus salicina Lindl. Plant Systemics and Evolution 273, 63-69.
117. Ranty B, Aldon D, Galaud JP. 2006. Plant calmodulins and calmodulinrelated proteins: multifaceted relays to decode calcium signals. Plant Signaling and Behavior 1, 96-104.
118. Reichelt S, Knight AE, Hodge TP, Baluska F, Samaj J, Volkmann D, Kendrick-Jones J. 1999. Characterization of the unconventional myosin VIII in plant cells and its localization at the post-cytokinetic cell wall. The Plant Journal 19, 555-567.
119. Rinne PL, Kaikuranta PM, van der Schoot C. 2001. The shoot apical meristem restores its symplasmic organization during chilling-induced release from dormancy. The Plant Journal 26, 249-264.
120. Rinne PL, van der Schoot C. 1998. Symplasmic fields in the tunica of the shoot apical meristem coordinate morphogenetic events. Development 125, 1477-1485.
121. Rinne PL, Welling A, Vahala J, Ripel L, Ruonala R, Kangasjarvi J, van der Schoot C. 2011. Chilling of dormant buds hyperinduces FLOWERING LOCUS T and recruits GA-inducible 1, 3-β-glucanases to reopen signal conduits and release dormancy in Populus. Plant Cell 23, 130-146.
122. Roberts AG, Oparka KJ. 2003. Plasmodesmata and the control of symplastic transport. Plant Cell and Environment 26, 103-124.
123. Roschzttardtz H, Seguela-Arnaud M, Briat JF, Vert G, Curie C. 2011. The FRD3 citrate effluxer promotes iron nutrition between symplastically disconnected tissues throughout Arabidopsis development. Plant Cell 23, 2725-2737.
124. Ruan YL, Llewellyn DJ, Furbank RT. 2001. The control of singlecelled cotton fiber elongation by developmentally reversible gating of plasmodesmata and coordinated expression of sucrose and K+ transporters and expansin. Plant Cell 13, 47-60.
125. Ruan YL, Llewellyn DJ, Furbank RT, Chourey PS. 2005. The delayed initiation and slow elongation of fuzz-like short fibre cells in relation to altered patterns of sucrose synthase expression and plasmodesmata gating in a lintless mutant of cotton. Journal of Experimental Botany 56, 977-984.
126. Ruan YL, Xu SM, White R, Furbank RT. 2004. Genotypic and developmental evidence for the role of plasmodesmatal regulation in cotton fiber elongation mediated by callose turnover. Plant Physiology 136, 4104-4113.
127. Russell SD. 1979. Fine structure of megagametophyte development in Zea mays. Canadian Journal of Botany 57.
128. Sager R, Lee JY. 2012. To close or not to close: plasmodesmata in defense. Plant Signaling and Behavior 7, 431-436.
129. Samardakiewicz S, Krzeslowska M, Bilski H, Bartosiewicz R, Wozny A. 2012. Is callose a barrier for lead ions entering Lemna minor L. root cells? Protoplasma 249, 347-351.
130. Sanders MA, Salisbury JL. 1989. Centrin-mediated microtubule severing during flagellar excision in Chlamydomonas reinhardtii. The Journal of Cell Biology 108, 1751-1760.
131. Saure MC. 1985. Dormancy release in deciduous fruit trees. Horticultural Reviews 7, 239-300.
132. Saxena IM, Brown RM, Jr. 2000. Cellulose synthases and related enzymes. Current Opinion in Plant Biology 3, 523-531.
133. Schlereth A, Moller B, Liu W, Kientz M, Flipse J, Rademacher EH, Schmid M, Jurgens G, Weijers D. 2010. MONOPTEROS controls embryonic root initiation by regulating a mobile transcription factor. Nature 464, 913-916.
134. Schubert AM, Benedict CR, Berlin JD, Kohel RJ. 1973. Cotton fiber development-kinetics of cell elongation and secondary wall thickening. Crop Science 13, 704-709.
135. Schulz A. 1994. Phloem transport and differential unloading in pea seedlings after source and sink manipulations. Planta 192, 239-248.
136. Schulz A. 1995. Plasmodesmal widening accompanies the short-term increase in symplasmic phloem unloading in pea root tips under osmotic stress. Protoplasma 188, 22-37.
137. Scott PC, Miller LW, Webster BD, Leopold AC. 1967. Structural changes during bean leaf abscission. American Journal of Botany 54, 730-734.
138. Serrano M, Wang B, Aryal B, Garcion C, Abou-Mansour E, Heck S, Geisler M, Mauch F, Nawrath C, Metraux JP. 2013. Export of salicylic acid from the chloroplast requires the multidrug and toxin extrusion-like transporter EDS5. Plant Physiology 162, 1815-1821.
139. Sexton R, Roberts JA. 1982. Cell biology of abscission. Annual Review of Plant Physiology 33, 133-162.
140. Shemyakina EA, Solovyev AG, Leonova OG, Popenko VI, Schiemann J, Morozov SY. 2011. The role of microtubule association in plasmodesmal targeting of potato mop-top virus movement protein TGBp1. The Open Virology Journal 5, 1-11.
141. Sivaguru M, Fujiwara T, Samaj J, Baluska F, Yang Z, Osawa H, Maeda T, Mori T, Volkmann D, Matsumoto H. 2000. Aluminuminduced 1→3-β-d-glucan inhibits cell-to-cell trafficking of molecules through plasmodesmata. A new mechanism of aluminum toxicity in plants. Plant Physiology 124, 991-1006.
142. Sowinski P, Bilska A, Baranska K, Fronk J, Kobus P. 2007. Plasmodesmata density in vascular bundles in leaves of C4 grasses grown at different light conditions in respect to photosynthesis and photosynthate export efficiency. Environmental and Experimental Botany 61, 74-84.
143. Sowinski P, Rudzinska-Langwald A, Kobus P. 2003. Changes in plasmodesmata frequency in vascular bundles of maize seedling leaf induced by growth at sub-optimal temperatures in relation to photosynthesis and assimilate export. Environmental and Experimental Botany 50, 183-196.
144. Stadler R, Lauterbach C, Sauer N. 2005. Cell-to-cell movement of green fluorescent protein reveals post-phloem transport in the outer integument and identifies symplastic domains in Arabidopsis seeds and embryos. Plant Physiology 139, 701-712.
145. Steer MW. 1977. Differentiation of the tapetum in Avena. I. The cell surface. Journal of Cell Science 25, 125-138.
146. Stonebloom S, Brunkard JO, Cheung AC, Jiang KN, Feldman L, Zambryski P. 2012. Redox states of plastids and mitochondria differentially regulate intercellular transport via plasmodesmata. Plant Physiology 158, 190-199.
147. 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. Proceedings of the National Academy of Sciences, USA 106, 17229-17234.
148. Su S, Liu Z, Chen C, Zhang Y, Wang X, Zhu L, Miao L, Wang XC, Yuan M. 2010. Cucumber mosaic virus movement protein severs actin filaments to increase the plasmodesmal size exclusion limit in tobacco. Plant Cell 22, 1373-1387.
149. Thijssen MH. 2003. Ovules, megagametophytes and embryos: Ultrastructural studies after cryofixation . PhD Thesis, Wageningen University.
150. Thomas CL, Bayer EM, Ritzenthaler C, Fernandez-Calvino L, Maule AJ. 2008. Specific targeting of a plasmodesmal protein affecting cell-tocell communication. PLoS Biology 6, e7.
151. Tian S, Qin G, Li B. 2013. Reactive oxygen species involved in regulating fruit senescence and fungal pathogenicity. Plant Molecular Biology 82, 593-602.
152. Tilsner J, Linnik O, Wright KM, Bell K, Roberts AG, Lacomme C, Santa Cruz S, Oparka KJ. 2012. The TGB1 movement protein of Potato virus X reorganizes actin and endomembranes into the X-body, a viral replication factory. Plant Physiology 158, 1359-1370.
153. Tucker EB. 1990. Calcium-loaded 1, 2-bis(2-aminophenoxy)ethane- N, N, N, N-tetraacetic acid blocks cell-to-cell diffusion of carboxyfluorescein in staminal hairs of Setcreasea purpurea. Planta 182, 34-38.
154. Tucker EB, Boss WF. 1996. Mastoparan-induced intracellular Ca2+ fluxes may regulate cell-to-cell communication in plants. Plant Physiology 111, 459-467.
155. van Bel AJ, Ehlers K, Knoblauch M. 2002. Sieve elements caught in the act. Trends Plant Science 7, 126-132.
156. Vaten A, Dettmer J, Wu S et al. 2011. Callose biosynthesis regulates symplastic trafficking during root development. Developmental Cell 21, 1144-1155.
157. Vaughn KC. 2003. Dodder hyphae invade the host: a structural and immunocytochemical characterization. Protoplasma 220, 189-200.
158. Verma DP, Hong Z. 2001. Plant callose synthase complexes. Plant Molecular Biology 47, 693-701.
159. Vinckier S, Smets E. 2005. A histological study of microsporogenesis in Tarenna gracilipes. Grana 44, 30-44.
160. Voinnet O, Vain P, Angell S, Baulcombe DC. 1998. Systemic spread of sequence-specific transgene RNA degradation in plants is initiated by localized introduction of ectopic promoterless DNA. Cell 95, 177-187.
161. Wang G, Fiers M. 2010. CLE peptide signaling during plant development. Protoplasma 240, 33-43.
162. Wang N, Fisher DB. 1994. The Use of fluorescent tracers to characterize the post-phloem transport pathway in maternal tissues of developing wheat grains. Plant Physiology 104, 17-27.
163. Wang X, Sager R, Cui W, Zhang C, Lu H, Lee JY. 2013. Salicylic acid regulates plasmodesmata closure during innate immune responses in Arabidopsis. Plant Cell 25, 2315-2329.
164. Wang XY, Guo GQ, Nie XW, Zheng GC. 1998. Cytochemical localization of cellulase activity in pollen mother cells of david lily during meiotic prophase i and its relation to secondary formation of plasmodesmata. Protoplasma 204, 128-138.
165. Wang XY, Yu CH, Li X, Wang CY, Zheng GC. 2004. Ultrastructural aspects and possible origin of cytoplasmic channels providing intercellular connection in vegetative tissues of anthers. Russian Journal of Plant Physiology 51, 97-106.
166. Webster BD. 1973. Ultrastructural studies of abscission in Phaseolus: Ethylene effects on cell walls. American Journal of Botany 60, 436-447.
167. Werner D, Gerlitz N, Satdler R. 2011. A dual switch in phloem unloading during ovule development in Arabidopsis. Protoplasma 248, 225-235.
168. White RG, Badelt K, Overall RL, Vesk M. 1994. Actin associated with plasmodesmata. Protoplasma 180, 169-184.
169. Wille AC, Lucas WJ. 1984. Ultrastructural and histochemical-studies on guard-cells. Planta . 160, 129-142.
170. Willemse MTM, van Went JL. 1984. The female gametophyte . Berlin: Springer-Verlag.
171. Willmer CM, Sexton R. 1979. Stomata and plasmodesmata. Protoplasma 100, 113-124.
172. Wright KM, Cowan GH, Lukhovitskaya NI, Tilsner J, Roberts AG, Savenkov EI, Torrance L. 2010. The N-terminal domain of PMTV TGB1 movement protein is required for nucleolar localization, microtubule association, and long-distance movement. Molecular Plant-Microbe Interactions 23, 1486-1497.
173. Wright KM, Wood NT, Roberts AG, Chapman S, Boevink P, Mackenzie KM, Oparka KJ. 2007. Targeting of TMV movement protein to plasmodesmata requires the actin/ER network: evidence from FRAP. Traffic 8, 21-31.
174. Wu HM, Cheun AY. 2000. Programmed cell death in plant reproduction. Plant Molecular Biology 44, 267-281.
175. Wu S, Gallagher KL. 2012. Transcription factors on the move. Current Opinion in Plant Biology 15, 645-651.
176. Wu S, Gallagher KL. 2013. Intact microtubules are required for the intercellular movement of the SHORT-ROOT transcription factor. The Plant Journal 74, 148-159.
177. Xie B, Wang X, Zhu M, Zhang Z, Hong Z. 2011. CalS7 encodes a callose synthase responsible for callose deposition in the phloem. The Plant Journal 65, 1-14.
178. Xiong L, Zhu JK. 2002. Molecular and genetic aspects of plant responses to osmotic stress. Plant, Cell and Environment 25, 131-139.
179. Zanewich KP, Rood SB. 1995. Vernalization and gibberellin physiology of winter canola (endogenous gibberellin (GA) content and metabolism of [3H] GA1 and [3H]GA20. Plant Physiology 108, 615-621.
180. Zavaliev R, Ueki S, Epel BL, Citovsky V. 2011. Biology of callose (β-1, 3-glucan) turnover at plasmodesmata. Protoplasma 248, 117-130.