Development in multicellular organisms requires the coordinated production of a large number of specialized cell types through sophisticated signaling mechanisms. Non-cell-autonomous signals are one of the key mechanisms by which organisms coordinate development. In plants, intercellular movement of transcription factors and other mobile signals, such as hormones and peptides, is essential for normal development. Through a combination of different approaches, a large number of non-cell-autonomous signals that control plant development have been identified. We review some of the transcriptional regulators that traffic between cells, as well as how changes in symplasmic continuity affect and are affected by development. We also review current models for how mobile signals move via plasmodesmata and how movement is inhibited. Finally, we consider challenges in and new tools for studying protein movement.


Article metrics loading...

Loading full text...

Full text loading...


Literature Cited

  1. Ahn JH, Miller D, Winter VJ, Banfield MJ, Lee JH. et al. 2006. A divergent external loop confers antagonistic activity on floral regulators FT and TFL1. EMBO J. 25:605–14 [Google Scholar]
  2. Balkunde R, Bouyer D, Hülskamp M. 2011. Nuclear trapping by GL3 controls intercellular transport and redistribution of TTG1 protein in Arabidopsis. Development 138:5039–48 [Google Scholar]
  3. Balkunde R, Pesch M, Hulskamp M. 2010. Trichome patterning in Arabidopsis thaliana from genetic to molecular models. Curr. Top. Dev. Biol. 91:299–321 [Google Scholar]
  4. Barratt DH, Kölling K, Graf A, Pike M, Calder G. et al. 2011. Callose synthase GSL7 is necessary for normal phloem transport and inflorescence growth in Arabidopsis. Plant Physiol. 155:328–41 [Google Scholar]
  5. Barton DA, Cole L, Collings DA, Liu DY, Smith PM. et al. 2011. Cell-to-cell transport via the lumen of the endoplasmic reticulum. Plant J. 66:806–17 [Google Scholar]
  6. Benitez-Alfonso Y, Cilia M, San Roman A, Thomas C, Maule A. et al. 2009. Control of Arabidopsis meristem development by thioredoxin-dependent regulation of intercellular transport. Proc. Natl. Acad. Sci. USA 106:3615–20 [Google Scholar]
  7. Benitez-Alfonso Y, Faulkner C, Pendle A, Miyashima S, Helariutta Y, Maule A. 2013. Symplastic intercellular connectivity regulates lateral root patterning. Dev. Cell 26:136–47 [Google Scholar]
  8. Bishopp A, Lehesranta S, Vaten A, Help H, El-Showk S. et al. 2011. Phloem-transported cytokinin regulates polar auxin transport and maintains vascular pattern in the root meristem. Curr. Biol. 21:927–32 [Google Scholar]
  9. Bolduc N, Hake S. 2009. The maize transcription factor KNOTTED1 directly regulates the gibberellin catabolism gene ga2ox1. Plant Cell 21:1647–58 [Google Scholar]
  10. Bouyer D, Geier F, Kragler F, Schnittger A, Pesch M. 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 [Google Scholar]
  11. Brand U, Fletcher JC, Hobe M, Meyerowitz EM, Simon R. 2000. Dependence of stem cell fate in Arabidopsis on a feedback loop regulated by CLV3 activity. Science 289:617–19 [Google Scholar]
  12. 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. Plant J. 28:361–69 [Google Scholar]
  13. Buhtz A, Springer F, Chappell L, Baulcombe DC, Kehr J. 2008. Identification and characterization of small RNAs from the phloem of Brassica napus. Plant J. 53:739–49 [Google Scholar]
  14. Burch-Smith TM, Brunkard JO, Choi YG, Zambryski PC. 2011a. Organelle-nucleus cross-talk regulates plant intercellular communication via plasmodesmata. Proc. Natl. Acad. Sci. USA 108:E1451–60 [Google Scholar]
  15. 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 [Google Scholar]
  16. Carlsbecker A, Lee JY, Roberts CJ, Dettmer J, Lehesranta S. et al. 2010. Cell signalling by microRNA165/6 directs gene dose-dependent root cell fate. Nature 465:316–21 [Google Scholar]
  17. Chen H, Ahmad M, Rim Y, Lucas WJ, Kim JY. 2013. Evolutionary and molecular analysis of Dof transcription factors identified a conserved motif for intercellular protein trafficking. New Phytol. 198:1250–60 [Google Scholar]
  18. Chen XY, Kim JY. 2009. Callose synthesis in higher plants. Plant Signal. Behav. 4:489–92 [Google Scholar]
  19. Chen XY, Liu L, Lee E, Han X, Rim Y. et al. 2009. The Arabidopsis callose synthase gene GSL8 is required for cytokinesis and cell patterning. Plant Physiol. 150:105–13 [Google Scholar]
  20. Chitwood DH, Nogueira FT, Howell MD, Montgomery TA, Carrington JC, Timmermans MC. 2009. Pattern formation via small RNA mobility. Genes Dev. 23:549–54 [Google Scholar]
  21. Corbesier L, Vincent C, Jang S, Fornara F, Fan Q. et al. 2007. FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science 316:1030–33 [Google Scholar]
  22. Crawford KM, Zambryski PC. 2000. Subcellular localization determines the availability of non-targeted proteins to plasmodesmatal transport. Curr. Biol. 10:1032–40 [Google Scholar]
  23. Crawford KM, Zambryski PC. 2001. Non-targeted and targeted protein movement through plasmodesmata in leaves in different developmental and physiological states. Plant Physiol. 125:1802–12 [Google Scholar]
  24. Cruz-Ramírez A, Diaz-Triviño S, Blilou I, Grieneisen VA, Sozzani R. et al. 2012. A bistable circuit involving SCARECROW-RETINOBLASTOMA integrates cues to inform asymmetric stem cell division. Cell 150:1002–15 [Google Scholar]
  25. Cui H, Levesque MP, Vernoux T, Jung JW, Paquette AJ. et al. 2007. An evolutionarily conserved mechanism delimiting SHR movement defines a single layer of endodermis in plants. Science 316:421–25 [Google Scholar]
  26. Cuperus JT, Carbonell A, Fahlgren N, Garcia-Ruiz H, Burke RT. et al. 2010. Unique functionality of 22-nt miRNAs in triggering RDR6-dependent siRNA biogenesis from target transcripts in Arabidopsis. Nat. Struct. Mol. Biol. 17:997–1003 [Google Scholar]
  27. Di Cristina M, Sessa G, Dolan L, Linstead P, Baima S. et al. 1996. The Arabidopsis Athb-10 (GLABRA2) is an HD-Zip protein required for regulation of root hair development. Plant J. 10:393–402 [Google Scholar]
  28. Digiuni S, Schellmann S, Geier F, Greese B, Pesch M. et al. 2008. A competitive complex formation mechanism underlies trichome patterning on Arabidopsis leaves. Mol. Syst. Biol. 4:217 [Google Scholar]
  29. Digman MA, Gratton E. 2011. Lessons in fluctuation correlation spectroscopy. Annu. Rev. Phys. Chem. 62:645–68 [Google Scholar]
  30. Dunoyer P, Schott G, Himber C, Meyer D, Takeda A. et al. 2010. Small RNA duplexes function as mobile silencing signals between plant cells. Science 328:912–16 [Google Scholar]
  31. Dunoyer P, Voinnet O. 2009. Movement of RNA silencing between plant cells: Is the question now behind us?. Trends Plant Sci. 14:643–44 [Google Scholar]
  32. Ehlers K, Kollmann R. 2001. Primary and secondary plasmodesmata: structure, origin, and functioning. Protoplasma 216:1–30 [Google Scholar]
  33. Ehlers K, Maike W. 2013. Developmental control of plasmodesmata frequency, structure, and function. Symplastic Transport in Vascular Plants K Sokolowska, P Sowinski 41–82 New York: Springer [Google Scholar]
  34. Esau K. 1965. Plant Anatomy New York: Wiley767
  35. Faulkner C. 2013. Receptor-mediated signaling at plasmodesmata. Front. Plant Sci. 4:521 [Google Scholar]
  36. Fernandez A, Hilson P, Beeckman T. 2013. GOLVEN peptides as important regulatory signalling molecules of plant development. J. Exp. Bot. 64:5263–68 [Google Scholar]
  37. Fernandez-Calvino L, Faulkner C, Walshaw J, Saalbach G, Bayer E. et al. 2011. Arabidopsis plasmodesmal proteome. PLOS ONE 6:e18880 [Google Scholar]
  38. Fichtenbauer D, Xu XM, Jackson D, Kragler F. 2012. The chaperonin CCT8 facilitates spread of tobamovirus infection. Plant Signal. Behav. 7:318–21 [Google Scholar]
  39. 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 [Google Scholar]
  40. Fletcher JC, Brand U, Running MP, Simon R, Meyerowitz EM. 1999. Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems. Science 283:1911–14 [Google Scholar]
  41. Freeling M, Hake S. 1985. Developmental genetics of mutants that specify knotted leaves in maize. Genetics 111:617–34 [Google Scholar]
  42. Fujimoto S, Matsunaga S, Yonemura M, Uchiyama S, Azuma T, Fukui K. 2004. Identification of a novel plant MAR DNA binding protein localized on chromosomal surfaces. Plant Mol. Biol. 56:225–39 [Google Scholar]
  43. Gallagher KL, Benfey PN. 2009. Both the conserved GRAS domain and nuclear localization are required for SHORT-ROOT movement. Plant J. 57:785–97 [Google Scholar]
  44. Gallagher KL, Paquette AJ, Nakajima K, Benfey PN. 2004. Mechanisms regulating SHORT-ROOT intercellular movement. Curr. Biol. 14:1847–51 [Google Scholar]
  45. Gallavotti A, Malcomber S, Gaines C, Stanfield S, Whipple C. et al. 2011. BARREN STALK FASTIGIATE1 is an AT-hook protein required for the formation of maize ears. Plant Cell 23:1756–71 [Google Scholar]
  46. Geisler M, Nadeau J, Sack FD. 2000. Oriented asymmetric divisions that generate the stomatal spacing pattern in Arabidopsis are disrupted by the too many mouths mutation. Plant Cell 12:2075–86 [Google Scholar]
  47. Gisel A, Barella S, Hempel FD, Zambryski PC. 1999. Temporal and spatial regulation of symplastic trafficking during development in Arabidopsis thaliana apices. Development 126:1879–89 [Google Scholar]
  48. Gisel A, Hempel FD, Barella S, Zambryski P. 2002. Leaf-to-shoot apex movement of symplastic tracer is restricted coincident with flowering in Arabidopsis. Proc. Natl. Acad. Sci. USA 99:1713–17 [Google Scholar]
  49. Gordon SP, Chickarmane VS, Ohno C, Meyerowitz EM. 2009. Multiple feedback loops through cytokinin signaling control stem cell number within the Arabidopsis shoot meristem. Proc. Natl. Acad. Sci. USA 106:16529–34 [Google Scholar]
  50. Guseman JM, Lee JS, Bogenschutz NL, Peterson KM, Virata RE. 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 137:1731–41 [Google Scholar]
  51. Hay A, Tsiantis M. 2010. KNOX genes: versatile regulators of plant development and diversity. Development 137:3153–65 [Google Scholar]
  52. Helariutta Y, Fukaki H, Wysocka-Diller J, Nakajima K, Jung J. et al. 2000. The SHORT-ROOT gene controls radial patterning of the Arabidopsis root through radial signaling. Cell 101:555–67 [Google Scholar]
  53. Hong Z, Delauney AJ, Verma DP. 2001. A cell plate-specific callose synthase and its interaction with phragmoplastin. Plant Cell 13:755–68 [Google Scholar]
  54. Iglesias VA, Meins Jr 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. Plant J. 21:157–66 [Google Scholar]
  55. Imaichi R, Hiratsuka R. 2007. Evolution of shoot apical meristem structures in vascular plants with respect to plasmodesmatal network. Am. J. Bot. 94:1911–21 [Google Scholar]
  56. Ishida T, Hattori S, Sano R, Inoue K, Shirano Y. et al. 2007. Arabidopsis TRANSPARENT TESTA GLABRA2 is directly regulated by R2R3 MYB transcription factors and is involved in regulation of GLABRA2 transcription in epidermal differentiation. Plant Cell 19:2531–43 [Google Scholar]
  57. Ishikawa R, Aoki M, Kurotani K, Yokoi S, Shinomura T. et al. 2011. Phytochrome B regulates Heading date 1 (Hd1)-mediated expression of rice florigen Hd3a and critical day length in rice. Mol. Genet. Genomics 285:461–70 [Google Scholar]
  58. Jaeger KE, Wigge PA. 2007. FT protein acts as a long-range signal in Arabidopsis. Curr. Biol. 17:1050–54 [Google Scholar]
  59. Jasinski S, Piazza P, Craft J, Hay A, Woolley L. et al. 2005. KNOX action in Arabidopsis is mediated by coordinate regulation of cytokinin and gibberellin activities. Curr. Biol. 15:1560–65 [Google Scholar]
  60. Kang YH, Song SK, Schiefelbein J, Lee MM. 2013. Nuclear trapping controls the position-dependent localization of CAPRICE in the root epidermis of Arabidopsis. Plant Physiol. 163:193–204 [Google Scholar]
  61. Kardailsky I, Shukla VK, Ahn JH, Dagenais N, Christensen SK. et al. 1999. Activation tagging of the floral inducer FT. Science 286:1962–65 [Google Scholar]
  62. Kaya H, Shibahara KI, Taoka KI, Iwabuchi M, Stillman B, Araki T. 2001. FASCIATA genes for chromatin assembly factor-1 in Arabidopsis maintain the cellular organization of apical meristems. Cell 104:131–42 [Google Scholar]
  63. 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 129:1261–72 [Google Scholar]
  64. Kim I, Kobayashi K, Cho E, Zambryski PC. 2005a. Subdomains for transport via plasmodesmata corresponding to the apical-basal axis are established during Arabidopsis embryogenesis. Proc. Natl. Acad. Sci. USA 102:11945–50 [Google Scholar]
  65. Kim JY, Rim Y, Wang J, Jackson D. 2005b. A novel cell-to-cell trafficking assay indicates that the KNOX homeodomain is necessary and sufficient for intercellular protein and mRNA trafficking. Genes Dev. 19:788–93 [Google Scholar]
  66. Kim JY, Yuan Z, Jackson D. 2003. Developmental regulation and significance of KNOX protein trafficking in Arabidopsis. Development 130:4351–62 [Google Scholar]
  67. Kinoshita A, Betsuyaku S, Osakabe Y, Mizuno S, Nagawa S. et al. 2010. RPK2 is an essential receptor-like kinase that transmits the CLV3 signal in Arabidopsis. Development 137:3911–20 [Google Scholar]
  68. Kirik V, Simon M, Huelskamp M, Schiefelbein J. 2004. The ENHANCER OF TRY AND CPC1 gene acts redundantly with TRIPTYCHON and CAPRICE in trichome and root hair cell patterning in Arabidopsis. Dev. Biol. 268:506–13 [Google Scholar]
  69. Kobayashi Y, Kaya H, Goto K, Iwabuchi M, Araki T. 1999. A pair of related genes with antagonistic roles in mediating flowering signals. Science 286:1960–62 [Google Scholar]
  70. Koizumi K, Wu S, MacRae-Crerar A, Gallagher KL. 2011. An essential protein that interacts with endosomes and promotes movement of the SHORT-ROOT transcription factor. Curr. Biol. 21:1559–64 [Google Scholar]
  71. Kojima S, Takahashi Y, Kobayashi Y, Monna L, Sasaki T. et al. 2002. Hd3a, a rice ortholog of the Arabidopsis FT gene, promotes transition to flowering downstream of Hd1 under short-day conditions. Plant Cell Physiol. 43:1096–105 [Google Scholar]
  72. Kragler F. 2013. Plasmodesmata: intercellular tunnels facilitating transport of macromolecules in plants. Cell Tissue Res. 352:49–58 [Google Scholar]
  73. Kragler F, Monzer J, Shash K, Xoconostle-Cázares B, Lucas WJ. 1998. Cell-to-cell transport of proteins: requirement for unfolding and characterization of binding to a putative plasmodesmal receptor. Plant J. 15:367–81 [Google Scholar]
  74. Kuijt SJH, Lamers GEM, Rueb S, Scarpella E, Ouwerkerk PBF. et al. 2004. Different subcellular localization and trafficking properties of KNOX class 1 homeodomain proteins from rice. Plant Mol. Biol. 55:781–96 [Google Scholar]
  75. Kurata T, Ishida T, Kawabata-Awai C, Noguchi M, Hattori S. et al. 2005. Cell-to-cell movement of the CAPRICE protein in Arabidopsis root epidermal cell differentiation. Development 132:5387–98 [Google Scholar]
  76. Lee JY, Colinas J, Wang JY, Mace D, Ohler U, Benfey PN. 2006. Transcriptional and posttranscriptional regulation of transcription factor expression in Arabidopsis roots. Proc. Natl. Acad. Sci. USA 103:6055–60 [Google Scholar]
  77. Lee JY, Wang X, Cui W, Sager R, Modla S. et al. 2011. A plasmodesmata-localized protein mediates crosstalk between cell-to-cell communication and innate immunity in Arabidopsis. Plant Cell 23:3353–73 [Google Scholar]
  78. Levesque MP, Vernoux T, Busch W, Cui H, Wang JY. et al. 2006. Whole-genome analysis of the SHORT-ROOT developmental pathway in Arabidopsis. PLOS Biol. 4:e143 [Google Scholar]
  79. Levy A, Erlanger M, Rosenthal M, Epel BL. 2007. A plasmodesmata-associated β-1,3-glucanase in Arabidopsis. Plant J. 49:669–82 [Google Scholar]
  80. Lewis JD, Lazarowitz SG. 2010. Arabidopsis synaptotagmin SYTA regulates endocytosis and virus movement protein cell-to-cell transport. Proc. Natl. Acad. Sci. USA 107:2491–96 [Google Scholar]
  81. Li C, Gu M, Shi N, Zhang H, Yang X. et al. 2011. Mobile FT mRNA contributes to the systemic florigen signalling in floral induction. Sci. Rep. 1:73 [Google Scholar]
  82. Lifschitz E, Eviatar T, Rozman A, Shalit A, Goldshmidt A. et al. 2006. The tomato FT ortholog triggers systemic signals that regulate growth and flowering and substitute for diverse environmental stimuli. Proc. Natl. Acad. Sci. USA 103:6398–403 [Google Scholar]
  83. Lim PO, Kim Y, Breeze E, Koo JC, Woo HR. et al. 2007. Overexpression of a chromatin architecture-controlling AT-hook protein extends leaf longevity and increases the post-harvest storage life of plants. Plant J. 52:1140–53 [Google Scholar]
  84. Lin Q, Aoyama T. 2012. Pathways for epidermal cell differentiation via the homeobox gene GLABRA2: update on the roles of the classic regulator. J. Integr. Plant Biol. 54:729–37 [Google Scholar]
  85. Liu L, Liu C, Hou X, Xi W, Shen L. et al. 2012. FTIP1 is an essential regulator required for florigen transport. PLOS Biol. 10:e1001313 [Google Scholar]
  86. Long JA, Moan EI, Medford JI, Barton MK. 1996. A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis. Nature 379:66–69 [Google Scholar]
  87. Lucas WJ, Bouché-Pillon S, Jackson DP, Nguyen L, Baker L. et al. 1995. Selective trafficking of KNOTTED1 homeodomain protein and its mRNA through plasmodesmata. Science 270:1980–83 [Google Scholar]
  88. Manavella PA, Koenig D, Weigel D. 2012. Plant secondary siRNA production determined by microRNA-duplex structure. Proc. Natl. Acad. Sci. USA 109:2461–66 [Google Scholar]
  89. Matsushita A, Furumoto T, Ishida S, Takahashi Y. 2007. AGF1, an AT-hook protein, is necessary for the negative feedback of AtGA3ox1 encoding GA 3-oxidase. Plant Physiol. 143:1152–62 [Google Scholar]
  90. Maule AJ, Benitez-Alfonso Y, Faulkner C. 2011. Plasmodesmata—membrane tunnels with attitude. Curr. Opin. Plant Biol. 14:683–90 [Google Scholar]
  91. Mayer KF, Schoof H, Haecker A, Lenhard M, Jürgens G, Laux T. 1998. Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 95:805–15 [Google Scholar]
  92. Mi S, Cai T, Hu Y, Chen Y, Hodges E. et al. 2008. Sorting of small RNAs into Arabidopsis argonaute complexes is directed by the 5′ terminal nucleotide. Cell 133:116–27 [Google Scholar]
  93. Miyashima S, Honda M, Hashimoto K, Tatematsu K, Hashimoto T. et al. 2013. A comprehensive expression analysis of the Arabidopsis MICRORNA165/6 gene family during embryogenesis reveals a conserved role in meristem specification and a non-cell-autonomous function. Plant Cell Physiol. 54:375–84 [Google Scholar]
  94. Miyashima S, Koi S, Hashimoto T, Nakajima K. 2011. Non-cell-autonomous microRNA165 acts in a dose-dependent manner to regulate multiple differentiation status in the Arabidopsis root. Development 138:2303–13 [Google Scholar]
  95. Molnar A, Melnyk CW, Bassett A, Hardcastle TJ, Dunn R, Baulcombe DC. 2010. Small silencing RNAs in plants are mobile and direct epigenetic modification in recipient cells. Science 328:872–75 [Google Scholar]
  96. Morohashi K, Grotewold E. 2009. A systems approach reveals regulatory circuitry for Arabidopsis trichome initiation by the GL3 and GL1 selectors. PLOS Genet. 5:e1000396 [Google Scholar]
  97. Müller R, Bleckmann A, Simon R. 2008. The receptor kinase CORYNE of Arabidopsis transmits the stem cell-limiting signal CLAVATA3 independently of CLAVATA1. Plant Cell 20:934–46 [Google Scholar]
  98. Murphy JE, Padilla BE, Hasdemir B, Cottrell GS, Bunnett NW. 2009. Endosomes: a legitimate platform for the signaling train. Proc. Natl. Acad. Sci. USA 106:17615–22 [Google Scholar]
  99. Nakajima K, Sena G, Nawy T, Benfey PN. 2001. Intercellular movement of the putative transcription factor SHR in root patterning. Nature 413:307–11 [Google Scholar]
  100. Napoli C, Lemieux C, Jorgensen R. 1990. Introduction of a chimeric chalcone synthase gene into petunia results in reversible co-suppression of homologous genes in trans. Plant Cell 2:279–89 [Google Scholar]
  101. Navarro C, Abelenda JA, Cruz-Oró E, Cuéllar CA, Tamaki S. et al. 2011. Control of flowering and storage organ formation in potato by FLOWERING LOCUS T. Nature 478:119–22 [Google Scholar]
  102. Nimchuk ZL, Tarr PT, Ohno C, Qu X, Meyerowitz EM. 2011. Plant stem cell signaling involves ligand-dependent trafficking of the CLAVATA1 receptor kinase. Curr. Biol. 21:345–52 [Google Scholar]
  103. Notaguchi M, Abe M, Kimura T, Daimon Y, Kobayashi T. et al. 2008. Long-distance, graft-transmissible action of Arabidopsis FLOWERING LOCUS T protein to promote flowering. Plant Cell Physiol. 49:1645–58 [Google Scholar]
  104. Ogawa M, Shinohara H, Sakagami Y, Matsubayashi Y. 2008. Arabidopsis CLV3 peptide directly binds CLV1 ectodomain. Science 319:294 [Google Scholar]
  105. Oparka KJ. 2004. Getting the message across: How do plant cells exchange macromolecular complexes?. Trends Plant Sci. 9:33–41 [Google Scholar]
  106. Pálfy M, Reményi A, Korcsmáros T. 2012. Endosomal crosstalk: meeting points for signaling pathways. Trends Cell Biol. 22:447–56 [Google Scholar]
  107. Perbal MC, Haughn G, Saedler H, Schwarz-Sommer Z. 1996. Non-cell-autonomous function of the Antirrhinum floral homeotic proteins DEFICIENS and GLOBOSA is exerted by their polar cell-to-cell trafficking. Development 122:3433–41 [Google Scholar]
  108. Perrimon N, Pitsouli C, Shilo BZ. 2012. Signaling mechanisms controlling cell fate and embryonic patterning. Cold Spring Harb. Perspect. Biol. 4:a005975 [Google Scholar]
  109. Pesch M, Hülskamp M. 2009. One, two, three…models for trichome patterning in Arabidopsis?. Curr. Opin. Plant Biol. 12:587–92 [Google Scholar]
  110. Pickett-Heaps JD, Gunning BE, Brown RC, Lemmon BE, Cleary AL. 1999. The cytoplast concept in dividing plant cells: cytoplasmic domains and the evolution of spatially organized cell. Am. J. Bot. 86:153–72 [Google Scholar]
  111. Platta HW, Stenmark H. 2011. Endocytosis and signaling. Curr. Opin. Cell Biol. 23:393–403 [Google Scholar]
  112. Prochiantz A, Joliot A. 2003. Can transcription factors function as cell-cell signalling molecules?. Nat. Rev. Mol. Cell Biol. 4:814–19 [Google Scholar]
  113. Radford JE, White RG. 1998. Localization of a myosin-like protein to plasmodesmata. Plant J. 14:743–50 [Google Scholar]
  114. Rim Y, Huang L, Chu H, Han X, Cho WK. et al. 2011. Analysis of Arabidopsis transcription factor families revealed extensive capacity for cell-to-cell movement as well as discrete trafficking patterns. Mol. Cells 32:519–26 [Google Scholar]
  115. Rim Y, Jung J, Chu H, Cho WK, Kim S. et al. 2009. A non-cell-autonomous mechanism for the control of plant architecture and epidermal differentiation involves intercellular trafficking of BREVIPEDICELLUS protein. Funct. Plant Biol. 36:280–89 [Google Scholar]
  116. Rinne PL, Kaikuranta PM, van der Schoot C. 2001. The shoot apical meristem restores its symplasmic organization during chilling-induced release from dormancy. Plant J. 26:249–64 [Google Scholar]
  117. Rinne PL, van den Boogaard R, Mensink MG, Kopperud C, Kormelink R. et al. 2005. Tobacco plants respond to the constitutive expression of the tospovirus movement protein NSM with a heat-reversible sealing of plasmodesmata that impairs development. Plant J. 43:688–707 [Google Scholar]
  118. Rinne PL, van der Schoot C. 1998. Symplasmic fields in the tunica of the shoot apical meristem coordinate morphogenetic events. Development 125:1477–85 [Google Scholar]
  119. Rinne PL, Welling A, Vahala J, Ripel L, Ruonala R. et al. 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 23:130–46 [Google Scholar]
  120. Roberts IM, Boevink P, Roberts AG, Sauer N, Reichel C, Oparka KJ. 2001. Dynamic changes in the frequency and architecture of plasmodesmata during the sink-source transition in tobacco leaves. Protoplasma 218:31–44 [Google Scholar]
  121. Rubio-Somoza I, Cuperus JT, Weigel D, Carrington JC. 2009. Regulation and functional specialization of small RNA-target nodes during plant development. Curr. Opin. Plant Biol. 12:622–27 [Google Scholar]
  122. Ryu KH, Kang YH, Park YH, Hwang I, Schiefelbein J, Lee MM. 2005. The WEREWOLF MYB protein directly regulates CAPRICE transcription during cell fate specification in the Arabidopsis root epidermis. Development 132:4765–75 [Google Scholar]
  123. Sager R, Lee JY. 2012. To close or not to close: plasmodesmata in defense. Plant Signal. Behav. 7:431–36 [Google Scholar]
  124. Schuster C, Gaillochet C, Medzihradszky A, Busch W, Daum G. et al. 2014. A regulatory framework for shoot stem cell control integrating metabolic, transcriptional, and phytohormone signals. Dev. Cell 28:438–49 [Google Scholar]
  125. Sena G, Jung JW, Benfey PN. 2004. A broad competence to respond to SHORT ROOT revealed by tissue-specific ectopic expression. Development 131:2817–26 [Google Scholar]
  126. Sessions A, Yanofsky MF, Weigel D. 2000. Cell-cell signaling and movement by the floral transcription factors LEAFY and APETALA1. Science 289:779–82 [Google Scholar]
  127. Simpson C, Thomas C, Findlay K, Bayer E, Maule AJ. 2009. An Arabidopsis GPI-anchor plasmodesmal neck protein with callose binding activity and potential to regulate cell-to-cell trafficking. Plant Cell 21:581–94 [Google Scholar]
  128. Singh A, Singh S, Panigrahi KC, Reski R, Sarkar AK. 2014. Balanced activity of microRNA166/165 and its target transcripts from the class III homeodomain-leucine zipper family regulates root growth in Arabidopsis thaliana. Plant Cell Rep. 33:945–53 [Google Scholar]
  129. Sivaguru M, Fujiwara T, Samaj J, Baluska F, Yang Z. et al. 2000. Aluminum-induced 1→3-β-d-glucan inhibits cell-to-cell trafficking of molecules through plasmodesmata. A new mechanism of aluminum toxicity in plants. Plant Physiol. 124:991–1006 [Google Scholar]
  130. Song SK, Ryu KH, Kang YH, Song JH, Cho YH. et al. 2011. Cell fate in the Arabidopsis root epidermis is determined by competition between WEREWOLF and CAPRICE. Plant Physiol. 157:1196–208 [Google Scholar]
  131. Souček P, Klíma P, Reková A, Brzobohatý B. 2007. Involvement of hormones and KNOXI genes in early Arabidopsis seedling development. J. Exp. Bot. 58:3797–810 [Google Scholar]
  132. Sozzani R, Cui H, Moreno-Risueno MA, Busch W, Van Norman JM. et al. 2010. Spatiotemporal regulation of cell-cycle genes by SHORTROOT links patterning and growth. Nature 466:128–32 [Google Scholar]
  133. Spielman M, Preuss D, Li FL, Browne WE, Scott RJ, Dickinson HG. 1997. TETRASPORE is required for male meiotic cytokinesis in Arabidopsis thaliana. Development 124:2645–57 [Google Scholar]
  134. Spinelli SV, Martin AP, Viola IL, Gonzalez DH, Palatnik JF. 2011. A mechanistic link between STM and CUC1 during Arabidopsis development. Plant Physiol. 156:1894–904 [Google Scholar]
  135. Stahl Y, Grabowski S, Bleckmann A, Kühnemuth R, Weidtkamp-Peters S. et al. 2013. Moderation of Arabidopsis root stemness by CLAVATA1 and ARABIDOPSIS CRINKLY4 receptor kinase complexes. Curr. Biol. 23:362–71 [Google Scholar]
  136. Stonebloom S, Brunkard JO, Cheung AC, Jiang K, Feldman L, Zambryski P. 2012. Redox states of plastids and mitochondria differentially regulate intercellular transport via plasmodesmata. Plant Physiol. 158:190–99 [Google Scholar]
  137. 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. Proc. Natl. Acad. Sci. USA 106:17229–34 [Google Scholar]
  138. Street IH, Shah PK, Smith AM, Avery N, Neff MM. 2008. The AT-hook-containing proteins SOB3/AHL29 and ESC/AHL27 are negative modulators of hypocotyl growth in Arabidopsis. Plant J. 54:1–14 [Google Scholar]
  139. Taelman VF, Dobrowolski R, Plouhinec JL, Fuentealba LC, Vorwald PP. et al. 2010. Wnt signaling requires sequestration of glycogen synthase kinase 3 inside multivesicular endosomes. Cell 143:1136–48 [Google Scholar]
  140. Tamaki S, Matsuo S, Wong HL, Yokoi S, Shimamoto K. 2007. Hd3a protein is a mobile flowering signal in rice. Science 316:1033–36 [Google Scholar]
  141. Thomas CL, Bayer EM, Ritzenthaler C, Fernandez-Calvino L, Maule AJ. 2008. Specific targeting of a plasmodesmal protein affecting cell-to-cell communication. PLOS Biol. 6:e7 [Google Scholar]
  142. Tsukagoshi H, Busch W, Benfey PN. 2010. Transcriptional regulation of ROS controls transition from proliferation to differentiation in the root. Cell 143:606–16 [Google Scholar]
  143. Turck F, Fornara F, Coupland G. 2008. Regulation and identity of florigen: FLOWERING LOCUS T moves center stage. Annu. Rev. Plant Biol. 59:573–94 [Google Scholar]
  144. Urbanus SL, Dinh QD, Angenent GC, Immink RG. 2010. Investigation of MADS domain transcription factor dynamics in the floral meristem. Plant Signal. Behav. 5:1260–62 [Google Scholar]
  145. Varkonyi-Gasic E, Gould N, Sandanayaka M, Sutherland P, MacDiarmid RM. 2010. Characterisation of microRNAs from apple (Malus domestica ‘Royal Gala’) vascular tissue and phloem sap. BMC Plant Biol. 10:159 [Google Scholar]
  146. Vaten A, Dettmer J, Wu S, Stierhof YD, Miyashima S. et al. 2011. Callose biosynthesis regulates symplastic trafficking during root development. Dev. Cell 21:1144–55 [Google Scholar]
  147. Vermeer JE, von Wangenheim D, Barberon M, Lee Y, Stelzer EH. et al. 2014. A spatial accommodation by neighboring cells is required for organ initiation in Arabidopsis. Science 343:178–83 [Google Scholar]
  148. Vom Endt D, Soares e Silva M, Kijne JW, Pasquali G, Memelink J. 2007. Identification of a bipartite jasmonate-responsive promoter element in the Catharanthus roseus ORCA3 transcription factor gene that interacts specifically with AT-Hook DNA-binding proteins. Plant Physiol. 144:1680–89 [Google Scholar]
  149. Wada T, Kurata T, Tominaga R, Koshino-Kimura Y, Tachibana T. et al. 2002. Role of a positive regulator of root hair development, CAPRICE, in Arabidopsis root epidermal cell differentiation. Development 129:5409–19 [Google Scholar]
  150. Walker AR, Davison PA, Bolognesi-Winfield AC, James CM, Srinivasan N. et al. 1999. The TRANSPARENT TESTA GLABRA1 locus, which regulates trichome differentiation and anthocyanin biosynthesis in Arabidopsis, encodes a WD40 repeat protein. Plant Cell 11:1337–50 [Google Scholar]
  151. Wang F, Vandepoele K, Van Lijsebettens M. 2012. Tetraspanin genes in plants. Plant Sci. 190:9–15 [Google Scholar]
  152. Welch D, Hassan H, Blilou I, Immink R, Heidstra R, Scheres B. 2007. Arabidopsis JACKDAW and MAGPIE zinc finger proteins delimit asymmetric cell division and stabilize tissue boundaries by restricting SHORT-ROOT action. Genes Dev. 21:2196–204 [Google Scholar]
  153. Wester K, Digiuni S, Geier F, Timmer J, Fleck C, Hülskamp M. 2009. Functional diversity of R3 single-repeat genes in trichome development. Development 136:1487–96 [Google Scholar]
  154. Wigge PA, Kim MC, Jaeger KE, Busch W, Schmid M. et al. 2005. Integration of spatial and temporal information during floral induction in Arabidopsis. Science 309:1056–59 [Google Scholar]
  155. Wildermuth MC, Dewdney J, Wu G, Ausubel FM. 2001. Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414:562–65 [Google Scholar]
  156. Winter CM, Austin RS, Blanvillain-Baufumé S, Reback MA, Monniaux M. et al. 2011. LEAFY target genes reveal floral regulatory logic, cis motifs, and a link to biotic stimulus response. Dev. Cell 20:430–43 [Google Scholar]
  157. Winter N, Kollwig G, Zhang S, Kragler F. 2007. MPB2C, a microtubule-associated protein, regulates non-cell-autonomy of the homeodomain protein KNOTTED1. Plant Cell 19:3001–18 [Google Scholar]
  158. Wu S, Gallagher KL. 2013. Intact microtubules are required for the intercellular movement of the SHORT-ROOT transcription factor. Plant J. 74:148–59 [Google Scholar]
  159. Wu S, Koizumi K, MacRae-Crerar A, Gallagher KL. 2011. Assessing the utility of photoswitchable fluorescent proteins for tracking intercellular protein movement in the Arabidopsis root. PLOS ONE 6:e27536 [Google Scholar]
  160. Wu X, Dinneny JR, Crawford KM, Rhee Y, Citovsky V. et al. 2003. Modes of intercellular transcription factor movement in the Arabidopsis apex. Development 130:3735–45 [Google Scholar]
  161. Xie B, Wang X, Zhu M, Zhang Z, Hong Z. 2011. CalS7 encodes a callose synthase responsible for callose deposition in the phloem. Plant J. 65:1–14 [Google Scholar]
  162. Xu F, Rong X, Huang X, Cheng S. 2012. Recent advances of Flowering Locus T gene in higher plants. Int. J. Mol. Sci. 13:3773–81 [Google Scholar]
  163. Xu XM, Wang J, Xuan Z, Goldshmidt A, Borrill PGM. et al. 2011. Chaperonins facilitate KNOTTED1 cell-to-cell trafficking and stem cell function. Science 333:1141–44 [Google Scholar]
  164. Yadav RK, Perales M, Gruel J, Girke T, Jönsson H, Reddy GV. 2011. WUSCHEL protein movement mediates stem cell homeostasis in the Arabidopsis shoot apex. Genes Dev. 25:2025–30 [Google Scholar]
  165. Yun H, Hyun Y, Kang MJ, Noh YS, Noh B, Choi Y. 2011. Identification of regulators required for the reactivation of FLOWERING LOCUS C during Arabidopsis reproduction. Planta 234:1237–50 [Google Scholar]
  166. Yun J, Kim YS, Jung JH, Seo PJ, Park CM. 2012. The AT-hook motif-containing protein AHL22 regulates flowering initiation by modifying FLOWERING LOCUS T chromatin in Arabidopsis. J. Biol. Chem. 287:15307–16 [Google Scholar]
  167. Zeevaart JA. 2006. Florigen coming of age after 70 years. Plant Cell 18:1783–89 [Google Scholar]
  168. Zhao M, Morohashi K, Hatlestad G, Grotewold E, Lloyd A. 2008. The TTG1-bHLH-MYB complex controls trichome cell fate and patterning through direct targeting of regulatory loci. Development 135:1991–99 [Google Scholar]
  169. Zhou J, Wang X, Lee JY, Lee JY. 2013. Cell-to-cell movement of two interacting AT-hook factors in Arabidopsis root vascular tissue patterning. Plant Cell 25:187–201 [Google Scholar]
  170. Zhu H, Hu F, Wang R, Zhou X, Sze SH. et al. 2011. Arabidopsis Argonaute10 specifically sequesters miR166/165 to regulate shoot apical meristem development. Cell 145:242–56 [Google Scholar]
  171. Zuo J, Niu QW, Chua NH. 2000. Technical advance: An estrogen receptor-based transactivator XVE mediates highly inducible gene expression in transgenic plants. Plant J. 24:265–73 [Google Scholar]

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error