Actin, Myosin VIII and ABP1 as Central Organizers of Auxin-Secreting Synapses

Chapter

Abstract

In the root apex transition zone, large portion of the polar auxin transport (PAT) is accomplished via endocytic vesicular recycling at F-actin and myosin VIII-enriched cell–cell adhesion domains which are characterized as plant synapses. In these cells, PINs act as vesicular transporters that enrich recycling vesicles and endosomes with auxin, which is then secreted out of cells in a neurotransmitter-like mode. Besides F-actin and myosin VIII, auxin receptor auxin binding protein 1 (ABP1) emerges as critical organizing molecule not only for the plant synapses but also for the whole transition zone. Synaptic auxin transport in root apices is directly linked for sensing environment, and also central for translating these perceptions, via sensory-motoric circuits, into adaptive root tropisms. Finally, PINs acting also as vesicular transportes are suggested to represent transceptors, and the synaptic activity is proposed act as flux sensor for the polar transport of auxin

Keywords

Auxin Transport Root Apex Polar Auxin Transport Polar Transport Electrical Synapse 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Baluška F (2010) Recent surprising similarities between plant cells and neurons. Plant Signal Behav 5:87–89PubMedCrossRefGoogle Scholar
  2. Baluška F, Hlavacka A (2005) Plant formins come to age: something special about cross-walls. New Phytol 168:499–503PubMedCrossRefGoogle Scholar
  3. Baluška F, Mancuso S (2009) Plants and animals: convergent evolution in action? In: Baluška F (ed) Plant-environment interactions from sensory plant biology to active plant behavior. Springer Verlag, Berlin, pp 285–301Google Scholar
  4. Baluška F, Volkmann D (2011) Mechanical aspects of gravity-controlled growth, development and morphogenesis. In: Wojtaszek P (ed) Mechanical integration of plant cells and plants. Springer Verlag, Berlin, pp 195–222CrossRefGoogle Scholar
  5. Baluška F, Vitha S, Barlow PW, Volkmann D (1997) Rearrangements of F-actin arrays in growing cells of intact maize root apex tissues: a major developmental switch occurs in the postmitotic transition region. Eur J Cell Biol 72:113–121PubMedGoogle Scholar
  6. Baluška F, Barlow PW, Volkmann D (2000) Actin and myosin VIII in developing root cells. In: Staiger CJ, Baluška F, Volkmann D, Barlow PW (eds) Actin–a dynamic framework for multiple plant cell functions. Kluwer Academic Publishers, Dordrecht, pp 457–476Google Scholar
  7. Baluška F, Cvrčková 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 Physiol 126:39–46PubMedCrossRefGoogle Scholar
  8. Baluška F, Hlavačka A, Šamaj J, Palme K, Robinson DG, Matoh T, McCurdy DW, Menzel D, Volkmann D (2002) F-actin-dependent endocytosis of cell wall pectins in meristematic root cells: insights from brefeldin a-induced compartments. Plant Physiol 130:422–431PubMedCrossRefGoogle Scholar
  9. Baluška F, Wojtaszek P, Volkmann D, Barlow PW (2003a) The architecture of polarized cell growth: the unique status of elongating plant cells. BioEssays 25:569–576PubMedCrossRefGoogle Scholar
  10. Baluška F, Šamaj J, Wojtaszek P, Volkmann D, Menzel D (2003b) Cytoskeleton–plasma membrane—cell wall continuum in plants: emerging links revisited. Plant Physiol 133:482–491PubMedCrossRefGoogle Scholar
  11. Baluška F, Šamaj J, Menzel D (2003c) Polar transport of auxin: carrier-mediated flux across the plasma membrane or neurotransmitter-like secretion? Trends Cell Biol 13:282–285PubMedCrossRefGoogle Scholar
  12. Baluška F, Šamaj J, Hlavačka A, Kendrick-Jones J, Volkmann D (2004) Myosin VIII and F-actin enriched plasmodesmata in maize root inner cortex cells accomplish fluid-phase endocytosis via an actomyosin-dependent process. J Exp Bot 55:463–473PubMedCrossRefGoogle Scholar
  13. Baluška F, Liners F, Hlavačka A, Schlicht M, Van Cutsem P, McCurdy D, Menzel D (2005a) Cell wall pectins and xyloglucans are internalized into dividing root cells and accumulate within cell plates during cytokinesis. Protoplasma 225:141–155PubMedCrossRefGoogle Scholar
  14. Baluška F, Volkmann D, Menzel D (2005b) Plant synapses: actin-based adhesion domains for cell-to-cell communication. Trends Plant Sci 10:106–111PubMedCrossRefGoogle Scholar
  15. Baluška F, Schlicht M, Volkmann D, Mancuso S (2008) Vesicular secretion of auxin: evidences and implications. Plant Signal Behav 3:254–256PubMedCrossRefGoogle Scholar
  16. Baluška F, Schlicht M, Wan Y-L, Burbach C, Volkmann D (2009a) Intracellular domains and polarity in root apices: from synaptic domains to plant neurobiology. Nova Acta Leopold 96:103–122Google Scholar
  17. Baluška F, Mancuso S, Volkmann D, Barlow PW (2009b) The ‘root-brain’ hypothesis of Charles and Francis Darwin: revival after more than 125 years. Plant Signal Behav 4(1121):1127Google Scholar
  18. Baluška F, Mancuso S, Volkmann D, Barlow PW (2010) Root apex transition zone: a signalling-response nexus in the root. Trends Plant Sci 15:402–408PubMedCrossRefGoogle Scholar
  19. Barbier-Brygoo H, Ephritikhine G, Klämbt D, Ghislain M, Guern J (1989) Functional evidence for an auxin receptor at the plasmalemma of tobacco mesophyll protoplasts. Proc Natl Acad Sci U S A 86:891–895PubMedCrossRefGoogle Scholar
  20. Barlow PW, Volkmann D, Baluška F (2004) Polarity in roots. In: Lindsey K (ed) Polarity in plants. Blackwell Publishing, pp 192–241Google Scholar
  21. Bezanilla M, Horton AC, Sevener HC, Quatrano RS (2003) Phylogenetic analysis of new plant myosin sequences. J Mol Evol 57:229–239PubMedCrossRefGoogle Scholar
  22. Blilou I, Xu J, Wildwater M, Willemsen V, Paponov I, Friml J, Heidstra R, Aida M, Palme K, Scheres B (2005) The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433:39–44PubMedCrossRefGoogle Scholar
  23. Boutté Y, Crosnier MT, Carraro N, Traas J, Satiat-Jeunemaitre B (2006) The plasma membrane recycling pathway and cell polarity in plants: studies on PIN proteins. J Cell Sci 119:1255–1265PubMedCrossRefGoogle Scholar
  24. Chen R, Masson PH (2005) Auxin transport and recycling of PIN proteins in plants. In: Samaj J, Baluska F, Menzel D (eds) Plant endocytosis. Springer Verlag, pp 139–157Google Scholar
  25. Chow CM, Neto H, Foucart C, Moore I (2008) Rab-A2 and Rab-A3 GTPases define a trans-golgi endosomal membrane domain in Arabidopsis that contributes substantially to the cell plate. Plant Cell 20:101–123PubMedCrossRefGoogle Scholar
  26. Collings DA, White RG, Overall RL (1992) Ionic current changes associated with the gravity-induced bending response in roots of Zea mays L. Plant Physiol 100:1417–1426PubMedCrossRefGoogle Scholar
  27. Dahlke RI, Luethen H, Steffens B (2010) ABP1: an auxin receptor for fast responses at the plasma membrane. Plant Signal Behav 5:1–3PubMedCrossRefGoogle Scholar
  28. deGuzman CC, dela Fuente RK (1984) Polar calcium flux in sunflower hypocotyl segments, I. The effect of auxin. Plant Physiol 76:347–352CrossRefGoogle Scholar
  29. Dela Fuente RK (1984) Role of calcium in the polar secretion of indoleacetic acid. Plant Physiol 76:334–342CrossRefGoogle Scholar
  30. Dello Ioio R, Linhares FS, Scacchi E, Casamitjana-Martinez E, Heidstra R, Costantino P, Sabatini S (2007) Cytokinins determine Arabidopsis root-meristem size by controlling cell differentiation. Curr Biol 17:678–682PubMedCrossRefGoogle Scholar
  31. Depuydt S, Hardtke CS (2011) Hormone signalling crosstalk in plant growth regulation. Curr Biol 21:R365–R373PubMedCrossRefGoogle Scholar
  32. Dettmer J, Hong-Hermesdorf A, Stierhof YD, Schumacher K (2006) Vacuolar H+-ATPase activity is required for endocytic and secretory trafficking in Arabidopsis. Plant Cell 18:715–730PubMedCrossRefGoogle Scholar
  33. Dhonukshe P, Baluška F, Schlicht M, Hlavačka A, Šamaj J, Friml J, Gadella TWJ Jr (2006) Endocytosis of cell surface material mediates cell plate formation during plant cytokinesis. Dev Cell 10:137–150PubMedCrossRefGoogle Scholar
  34. Drake GA, Carr DJ, Anderson WP (1978) Plasmolysis, plasmodesmata, and the electrical coupling of oat coleoptile cells. J Exp Bot 29:1205–1214CrossRefGoogle Scholar
  35. Effendi Y, Rietz S, Fischer U, Scherer GF (2011) The heterozygous abp1/ABP1 insertional mutant has defects in functions requiring polar auxin transport and in regulation of early auxin-regulated genes. Plant J 65:282–294PubMedCrossRefGoogle Scholar
  36. Epel BL, Erlanger MA (1991) Light regulates symplastic communication in etiolated corn seedlings. Physiol Plant 83:149–153CrossRefGoogle Scholar
  37. Evans EC III (1964) Polar transport of calcium in the primary root of Zea mays. Science 144:174–177PubMedCrossRefGoogle Scholar
  38. Felten J, Kohler A, Morin E, Bhalerao RP, Palme K, Martin F, Ditengou FA, Legué V (2009) The ectomycorrhizal fungus Laccaria bicolor stimulates lateral root formation in poplar and Arabidopsis through auxin transport and signaling. Plant Physiol 151:1991–2005PubMedCrossRefGoogle Scholar
  39. Felten J, Legué V, Ditengou FA (2010) Lateral root stimulation in the early interaction between Arabidopsis thaliana and the ectomycorrhizal fungus Laccaria bicolor: is fungal auxin the trigger? Plant Signal Behav 5:864–867PubMedCrossRefGoogle Scholar
  40. Feraru E, Feraru MI, Kleine-Vehn J, Martinière A, Mouille G, Vanneste S, Vernhettes S, Runions J, Friml J (2011) PIN polarity maintenance by the cell wall in Arabidopsis. Curr Biol 21:338–343PubMedCrossRefGoogle Scholar
  41. Friml J (2003) Auxin transport–shaping the plant. Curr Opin Plant Biol 6:7–12PubMedCrossRefGoogle Scholar
  42. Garnett P, Steinacher A, Stepney S, Clayton R, Leyser O (2010) Computer stimulation: the imaginary friend of auxin transport biology. BioEssays 32:828–835PubMedCrossRefGoogle Scholar
  43. Geldner N, Hyman DL, Wang X, Schumacher K, Chory J (2007) Endosomal signaling of plant steroid receptor kinase BRI1. Genes Dev 21:1598–1602PubMedCrossRefGoogle Scholar
  44. Gojon A, Krouk G, Perrine-Walker F, Laugier E (2011) Nitrate transceptor(s) in plants. J Exp Bot 62:2299–2308PubMedCrossRefGoogle Scholar
  45. Goldsmith MHM (1967a) Movement of pulses of labeled auxin in corn coleoptiles. Plant Physiol 42:258–263PubMedCrossRefGoogle Scholar
  46. Goldsmith MHM (1967b) Separation of transit of auxin from uptake: average velocity and reversible inhibition by anaerobic conditions. Science 156:661–663PubMedCrossRefGoogle Scholar
  47. Golomb L, Abu-Abied M, Belausov E, Sadot E (2008) Different subcellular localizations and functions of Arabidopsis myosin VIII. BMC Plant Biol 8:3PubMedCrossRefGoogle Scholar
  48. Goswami KKA, Audus LJ (1976) Distribution of calcium, potassium and phosphorous in Helianthus anuus hypocotyls and Zea mays coleoptiles in relation to tropic stimuli and curvatures. Ann Bot 40:49–64Google Scholar
  49. Hacham Y, Sela A, Friedlander L, Savaldi-Goldstein S (2011) BRI1 activity in the root meristem involves post-transcriptional regulation of PIN auxin efflux carriers. Plant Signal Behav 7:68–70 CrossRefGoogle Scholar
  50. Hause G, Šamaj J, Menzel D, Baluška F (2006) Fine structural analysis of brefeldin a-induced compartment formation after high-pressure freeze fixation of maize root epidermis: compound exocytosis resembling cell plate formation during cytokinesis. Plant Signal Behav 1:134–139PubMedCrossRefGoogle Scholar
  51. Hertel R, Lomax TL, Briggs WR (1983) Auxin transport in membrane vesicles from Cucurbita pepo L. Planta 157:193–201CrossRefGoogle Scholar
  52. Heyn A, Hoffmann S, Hertel R (1987) In vitro auxin transport in membrane vesicles from maize coleoptiles. Planta 172:285–287CrossRefGoogle Scholar
  53. Hochholdinger F, Zimmermann R (2008) Conserved and diverse mechanisms in root development. Curr Opin Plant Biol 11:70–74PubMedCrossRefGoogle Scholar
  54. Hodge A (2009) Root decisions. Plant Cell Environ 32:628–640PubMedCrossRefGoogle Scholar
  55. Hössel D, Schmeiser C, Hertel R (2005) Specificity patterns indicate that auxin exporters and receptors are the same proteins. Plant Biol 7:41–48PubMedCrossRefGoogle Scholar
  56. Hundal HS, Taylor PM (2009) Amino acid transceptors: gate keepers of nutrient exchange and regulators of nutrient signaling. Am J Physiol Endocrinol Metab 296:E603–E613PubMedCrossRefGoogle Scholar
  57. Jenkinson IS, Scott BIH (1961) Bioelectric oscillations of bean roots: further evidence for a feedback oscillator. I. Extracellular response to oscillations in osmotic pressure and auxin. Aust J Biol Sci 14:231–247Google Scholar
  58. Jönsson H, Gruel J, Krupinski P, Troein C (2011) On evaluating models in computational morphodynamics. Curr Opin Plant Biol 15:103–110PubMedCrossRefGoogle Scholar
  59. Juniper BE, Barlow PW (1969) The distribution of plasmodesmata in the root tip of maize. Planta 89:352–360CrossRefGoogle Scholar
  60. Kang BH (2011) Shrinkage and fragmentation of the trans-Golgi network in non-meristematic plant cells. Plant Signal Behav 6:884–886PubMedCrossRefGoogle Scholar
  61. Kasprowicz A, Szuba A, Volkmann D, Baluška F, Wojtaszek F (2009) Nitric oxide modulates dynamic actin cytoskeleton and vesicle trafficking in a cell type-specific manner in root apices. J Exp Bot 60:1605–1617PubMedCrossRefGoogle Scholar
  62. Kleine-Vehn J, Friml J (2008) Polar targeting and endocytic recycling in auxin-dependent plant development. Annu Rev Cell Dev Biol 24:447–473PubMedCrossRefGoogle Scholar
  63. Kramer EM (2009) Auxin-regulated cell polarity: an inside job? Trends Plant Sci 14:242–247PubMedCrossRefGoogle Scholar
  64. Krecek P, Skupa P, Libus J, Naramoto S, Tejos R, Friml J, Zazímalová E (2009) The PIN-FORMED (PIN) protein family of auxin transporters. Genome Biol 10:249PubMedCrossRefGoogle Scholar
  65. Kriel J, Haesendonckx S, Rubio-Texeira M, Van Zeebroeck G, Thevelein JM (2011) From transporter to transceptor: signaling from transporters provokes re-evaluation of complex trafficking and regulatory controls: endocytic internalization and intracellular trafficking of nutrient transceptors may, at least in part, be governed by their signaling function. BioEssays 33:870–879PubMedCrossRefGoogle Scholar
  66. Krupinski P, Jönsson H (2010) Modeling auxin-regulated development. Cold Spring Harb Perspect Biol 2:a001560PubMedCrossRefGoogle Scholar
  67. Kwon C, Panstruga R, Schulze-Lefert P (2008) Les liaisons dangereuses: immunological synapse formation in animals and plants. Trends Immunol 29:159–166Google Scholar
  68. Lam SK, Cai Y, Hillmer S, Robinson DG, Jiang L (2008) SCAMPs highlight the developing cell plate during cytokinesis in tobacco BY-2 cells. Plant Physiol 147:1637–1645PubMedCrossRefGoogle Scholar
  69. Lee JS, Evans ML (1985) Polar transport of calcium across elongation zone of gravistimulated roots. Plant Cell Physiol 26:1587–1595PubMedGoogle Scholar
  70. Lee JS, Mulkey TJ, Evans ML (1983) Gravity-induced polar transport of calcium across root tips of maize. Plant Physiol 73:874–876PubMedCrossRefGoogle Scholar
  71. Lee JS, Mulkey TJ, Evans ML (1984) Inhibition of polar calcium movement and gravitropism in roots treated with auxin-transport inhibitors. Planta 160:536–543PubMedCrossRefGoogle Scholar
  72. Lew RR (1994) Regulation of electrical coupling between Arabidopsis root hairs. Planta 193:67–73CrossRefGoogle Scholar
  73. Lima PT, Faria VG, Patraquim P, Ramos AC, Feijó JA, Sucena E (2009) Plant-microbe symbioses: new insights into common roots. Bioessays 31:1233–1244Google Scholar
  74. Lomax TL, Mehlhorn RJ, Briggs WR (1985) Active auxin uptake by zucchini membrane vesicles: quantitation using ESR volume and ApH determinations. Proc Natl Acad Sci U S A 82:6541–6545PubMedCrossRefGoogle Scholar
  75. Mancuso S, Boselli M (2002) Characterisation of the oxygen fluxes in the division, elongation and mature zones of vitis roots: influence of oxygen availability. Planta 214:767–774Google Scholar
  76. Mancuso S, Marras AM, Magnus V, Baluska F (2005) Noninvasive and continuous recordings of auxin fluxes in intact root apex with a carbon nanotube-modified and self-referencing microelectrode. Anal Biochem 341:344–351PubMedCrossRefGoogle Scholar
  77. Mancuso S, Marras AM, Mugnai S, Schlicht M, Zarsky V, Li G, Song L, Hue HW, Baluška F (2007) Phospholipase Dζ2 drives vesicular secretion of auxin for its polar cell–cell transport in the transition zone of the root apex. Plant Signal Behav 2:240–244PubMedCrossRefGoogle Scholar
  78. Masi E, Ciszak M, Stefano G, Renna L, Azzarello E, Pandolfi C, Mugnai S, Baluska F, Arecchi FT, Mancuso S (2009) Spatiotemporal dynamics of the electrical network activity in the root apex. Proc Natl Acad Sci U S A 106:4048–4053PubMedCrossRefGoogle Scholar
  79. Maule AJ, Benitez-Alfonso Y, Faulkner C (2011) Plasmodesmata—membrane tunnels with attitude. Curr Opin Plant Biol 14:1–8CrossRefGoogle Scholar
  80. Maurel C, Leblanc N, Barbier-Brygoo H, Perrot-Rechenmann C, Bouvier-Durand M, Guern J (1994) Alterations of auxin perception in rolB-transformed tobacco protoplasts. Time course of rolB mRNA expression and increase in auxin sensitivity reveal multiple control by auxin. Plant Physiol 105:1209–1215PubMedCrossRefGoogle Scholar
  81. McLamore ES, Diggs A, Calvo Marzal P, Shi J, Blakeslee JJ, Peer WA, Murphy AS, Porterfield DM (2010a) Non-invasive quantification of endogenous root auxin transport using an integrated flux microsensor technique. Plant J 63:1004–1016PubMedCrossRefGoogle Scholar
  82. McLamore ES, Jaroch D, Rameez Chatni M, Porterfield DM (2010b) Self-referencing optrodes for measuring spatially resolved, real-time metabolic oxygen flux in plant systems. Planta 232:1087–1099PubMedCrossRefGoogle Scholar
  83. Merks RMH, de Peer YV, Inze D, Beemster GTS (2007) Canalization without flux sensors: a traveling-wave hypothesis. Trends Plant Sci 12:384–390PubMedCrossRefGoogle Scholar
  84. Michniewicz M, Zago MK, Abas L, Weijers D, Schweighofer A, Meskiene I, Heisler MG, Ohno C, Zhang J, Huang F, Schwab R, Weigel D, Meyerowitz EM, Luschnig C, Offringa R, Friml J (2007) Antagonistic regulation of PIN phosphorylation by PP2A and PINOID directs auxin flux. Cell 130:1044–1056PubMedCrossRefGoogle Scholar
  85. Mongrand S, Stanislas T, Bayer EMF, Lherminier J, Simon-Plas F (2010) Membrane rafts in plant cells. Trends Plant Sci 15:656–663PubMedCrossRefGoogle Scholar
  86. Moreno-Risueno MA, Benfey PN (2011) Time-based patterning in development: the role of oscillating gene expression. Transcription 2:124–129PubMedCrossRefGoogle Scholar
  87. Moreno-Risueno MA, Van Norman JM, Moreno A, Zhang J, Ahnert SE, Benfey PN (2010) Oscillating gene expression determines competence for periodic Arabidopsis root branching. Science 329:1306–1311PubMedCrossRefGoogle Scholar
  88. Mravec J, Skůpa P, Bailly A, Hoyerová K, Krecek P, Bielach A, Petrásek J, Zhang J, Gaykova V, Stierhof YD, Dobrev PI, Schwarzerová K, Rolcík J, Seifertová D, Luschnig C, Benková E, Zazímalová E, Geisler M, Friml J (2009) Subcellular homeostasis of phytohormone auxin is mediated by the ER-localized PIN5 transporter. Nature 459:1136–1140PubMedCrossRefGoogle Scholar
  89. Mugnai S, Azzarello E, Baluška F, Mancuso S (2012) Local root apex hypoxia at the transition zone induces NO-mediated hypoxic acclimation of the whole root. Plant Cell Physiology [Accepted]Google Scholar
  90. Napier RM, David KM, Perrot-Rechenmann C (2002) A short history of auxin-binding proteins. Plant Mol Biol 49:339–348PubMedCrossRefGoogle Scholar
  91. Panigrahi KC, Panigrahy M, Vervliet-Scheebaum M, Lang D, Reski R, Johri MM (2009) Auxin-binding proteins without KDEL sequence in the moss Funaria hygrometrica. Plant Cell Rep 28:1747–1758PubMedCrossRefGoogle Scholar
  92. Paponov IA, Teale WD, Trebar M, Blilou I, Palme K (2005) The PIN auxin efflux facilitators: evolutionary and functional perspectives. Trends Plant Sci 10:170–177PubMedCrossRefGoogle Scholar
  93. Peremyslov VV, Mockler TC, Filichkin SA, Fox SE, Jaiswal P, Makarova KS, Koonin EV, Dolja VV (2011) Expression, splicing, and evolution of the myosin gene family in plants. Plant Physiol 155:1191–1204PubMedCrossRefGoogle Scholar
  94. Pinosa F (2010) Analysis of PIN2 polarity regulation and Mob1 function in Arabidopsis root development. PhD Thesis, Albert-Ludwig-Universität Freiburg im Breisgau, GermanyGoogle Scholar
  95. Rahman A, Takahashi M, Shibasaki K, Wu S, Inaba T, Tsurumi S, Baskin TI (2010) Gravitropism of Arabidopsis thaliana roots requires the polarization of PIN2 toward the root tip in meristematic cortical cells. Plant Cell 22:1762–1776PubMedCrossRefGoogle Scholar
  96. Reddy ASN, Day IS (2001) Analysis of the myosins encoded in the recently completed Arabidopsis thaliana genome sequence. Genome Biol 2:0024.1–0024.17CrossRefGoogle Scholar
  97. Richter S, Geldner N, Schrader J, Wolters H, Stierhof YD, Rios G, Koncz C, Robinson DG, Jürgens G (2007) Functional diversification of closely related ARF–GEFs in protein secretion and recycling. Nature 448:488–492PubMedCrossRefGoogle Scholar
  98. Richter S, Anders N, Wolters H, Beckmann H, Thomann A, Heinrich R, Schrader J, Singh MK, Geldner N, Mayer U, Jürgens G (2010) Role of the GNOM gene in Arabidopsis apical-basal patterning–from mutant phenotype to cellular mechanism of protein action. Eur J Cell Biol 89:138–144PubMedCrossRefGoogle Scholar
  99. Robert S, Kleine-Vehn J, Barbez E, Sauer M, Paciorek T, Baster P, Vanneste S, Zhang J, Simon S, Čovanová M, Hayashi K, Dhonukshe P, Yang Z, Bednarek SY, Jones AM, Luschnig C, Aniento F, Zažímalová E, Friml J (2010) ABP1 mediates auxin inhibition of clathrin-dependent endocytosis in Arabidopsis. Cell 143:111–121PubMedCrossRefGoogle Scholar
  100. Rück A, Palme K, Venis MA, Napier RM, Felle H (1993) Patch-clamp analysis establishes a role for an auxin binding protein in the auxin stimulation of plasma membrane current in Zea mays protoplasts. Plant J 4:41–46CrossRefGoogle Scholar
  101. Sachs T (1969) Polarity and the induction of organized vascular tissues. Ann Bot 33:263–275Google Scholar
  102. Sachs T (1991) Cell polarity and tissue patterning in plants. Development 91(Suppl 1):83–93Google Scholar
  103. Santuari L, Scacchi E, Rodriguez-Villalon A, Salinas P, Dohmann EM, Brunoud G, Vernoux T, Smith RS, Hardtke CS (2011) Positional information by differential endocytosis splits auxin response to drive Arabidopsis root meristem growth. Curr Biol 21:1918–1923PubMedCrossRefGoogle Scholar
  104. Šamaj J, Baluška F, Voigt B, Schlicht M, Volkmann D, Menzel D (2004) Endocytosis, actin cytoskeleton and signalling. Plant Physiol 135:1150–1161PubMedCrossRefGoogle Scholar
  105. Šamaj J, Read ND, Volkmann D, Menzel D, Baluška F (2005) The endocytic network in plants. Trends Cell Biol 15:425–433PubMedCrossRefGoogle Scholar
  106. Samaj J, Chaffey NJ, Tirlapur U, Jasik J, Volkmann D, Menzel D, Baluška F (2006) Actin and myosin VIII in plasmodesmata cell–cell channels. In: Baluška F et al (eds) Cell–cell channels. Landes bioscience, pp 119–134Google Scholar
  107. Sattarzadeh A, Franzen R, Schmelzer E (2008) The Arabidopsis class VIII myosin ATM2 is involved in endocytosis. Cell Motil Cytoskel 65:457–468CrossRefGoogle Scholar
  108. Scacchi E, Osmont KS, Beuchat J, Salinas P, Navarrete-Gómez M, Trigueros M, Ferrándiz C, Hardtke CS (2009) Dynamic, auxin-responsive plasma membrane-to-nucleus movement of Arabidopsis BRX. Development 136:2059–2067PubMedCrossRefGoogle Scholar
  109. Scacchi E, Salinas P, Gujas B, Santuari L, Krogan N, Ragni L, Berleth T, Hardtke CS (2010) Spatio-temporal sequence of cross-regulatory events in root meristem growth. Proc Natl Acad Sci U S A 107:22734–22739PubMedCrossRefGoogle Scholar
  110. Scherer GF (2011) AUXIN-BINDING-PROTEIN1, the second auxin receptor: what is the significance of a two-receptor concept in plant signal transduction? J Exp Bot 62:3339–3357PubMedCrossRefGoogle Scholar
  111. Schlicht M, Strnad M, Scanlon MJ, Mancuso S, Hochholdinger F, Palme K, Volkmann D, Menzel D, Baluška F (2006) Auxin immunolocalization implicates vesicular neurotransmitter-like mode of polar auxin transport in root apices. Plant Signal Behav 1:122–133PubMedCrossRefGoogle Scholar
  112. Schlicht M, Samajová O, Schachtschabel D, Mancuso S, Menzel D, Boland W, Baluska F (2008) D’orenone blocks polarized tip growth of root hairs by interfering with the PIN2-mediated auxin transport network in the root apex. Plant J 55:709–717PubMedCrossRefGoogle Scholar
  113. Scott BIH (1957) Electric oscillations generated by plant roots and a possible feedback mechanism responsible for them. Aust J Biol Sci 10:164–179Google Scholar
  114. Seagull RW (1983) Differences in the frequency and disposition of plasmodesmata resulting from root cell elongation. Planta 159:497–504CrossRefGoogle Scholar
  115. Shabala S, Shabala L, Gradmann D, Chen Z, Newman I, Mancuso S (2006) Oscillations in plant membrane transport: model predictions, experimental validation, and physiological implications. J Exp Bot 57:171–184PubMedCrossRefGoogle Scholar
  116. Shen WH, Davioud E, David C, Barbier-Brygoo H, Tempé J, Guern J (1990) High sensitivity to auxin is a common feature of hairy root. Plant Physiol 94:554–560PubMedCrossRefGoogle Scholar
  117. Shen H, Hou NY, Schlicht M, Wan Y, Mancuso S, Baluška F (2008) Aluminium toxicity targets PIN2 in Arabidopsis root apices: effects on PIN2 endocytosis, vesicular recycling, and polar auxin transport. Chin Sci Bull 53:2480–2487CrossRefGoogle Scholar
  118. Shen C, Bai Y, Wang S, Zhang S, Wu Y, Chen M, Jiang D, Qi Y (2010) Expression profile of PIN, AUX/LAX and PGP auxin transporter gene families in Sorghum bicolor under phytohormone and abiotic stress. FEBS J 277:2954–2969PubMedCrossRefGoogle Scholar
  119. Spanswick RM (1972) Electrical coupling between cells of higher plants: A direct demonstration of intercellular communication. Planta 102:215–227CrossRefGoogle Scholar
  120. Splivallo R, Fischer U, Göbel C, Feussner I, Karlovsky P (2009) Truffles regulate plant root morphogenesis via the production of auxin and ethylene. Plant Physiol 150:2018–2029PubMedCrossRefGoogle Scholar
  121. Stoma S, Lucas M, Chopard J, Schaedel M, Traas J, Godin C (2008) Flux-based transport enhancement as a plausible unifying mechanism for auxin transport in meristem development. PLoS Comput Biol 4:e1000207PubMedCrossRefGoogle Scholar
  122. Tarr PT, Tarling EJ, Bojanic DD, Edwards PA, Baldán Á (2009) Emerging new paradigms for ABCG transporters. Biochim Biophys Acta 1791:584–593PubMedGoogle Scholar
  123. Teale WD, Paponov IA, Palme K (2006) Auxin in action: signalling, transport and the control of plant growth and development. Nat Rev Mol Cell Biol 7:847–859PubMedCrossRefGoogle Scholar
  124. Teh OK, Moore I (2007) An ARF–GEF acting at the Golgi and in selective endocytosis in polarized plant cells. Nature 448:493–496PubMedCrossRefGoogle Scholar
  125. Thevelein JM, Voordeckers K (2009) Functioning and evolutionary significance of nutrient transceptors. Mol Biol Evol 26:2407–2414PubMedCrossRefGoogle Scholar
  126. Thompson RF, Langford GM (2002) Myosin superfamily evolutionary history. Anat Rec 268:276–289PubMedCrossRefGoogle Scholar
  127. Tilsner J, Amari K, Torrance L (2011) Plasmodesmata viewed as specialised membrane adhesion sites. Protoplasma 248:39–60PubMedCrossRefGoogle Scholar
  128. Traas J, Vernoux T (2010) Oscillating roots. Science 329:1290–1291PubMedCrossRefGoogle Scholar
  129. Trewavas A (2009) What is plant behaviour? Plant Cell Environ 32:606–616PubMedCrossRefGoogle Scholar
  130. Tromas A, Braun N, Muller P, Khodus T, Paponov IA, Palme K, Ljung K, Lee JY, Benfey P, Murray JA, Scheres B, Perrot-Rechenmann C (2009) The AUXIN BINDING PROTEIN 1 is required for differential auxin responses mediating root growth. PLoS ONE 4:e6648PubMedCrossRefGoogle Scholar
  131. Tromas A, Paponov I, Perrot-Rechenmann C (2010) AUXIN BINDING PROTEIN 1: functional and evolutionary aspects. Trends Plant Sci 15:436–446PubMedCrossRefGoogle Scholar
  132. Van Norman JM, Breakfield NW, Benfey PN (2011) Intercellular communication during plant development. Plant Cell 23:855–864PubMedCrossRefGoogle Scholar
  133. Vatsa P, Chiltz A, Bourque S, Wendehenne D, Garcia-Brugger A, Pugin A (2011) Involvement of putative glutamate receptors in plant defence signaling and NO production. Biochimie 93:2095–2101PubMedCrossRefGoogle Scholar
  134. Viotti C, Bubeck J, Stierhof YD, Krebs M, Langhans M, van den Berg W, van Dongen W, Richter S, Geldner N, Takano J, Jürgens G, de Vries SC, Robinson DG, Schumacher K (2010) Endocytic and secretory traffic in Arabidopsis merge in the trans-Golgi network/early endosome, an independent and highly dynamic organelle. Plant Cell 22:1344–1357PubMedCrossRefGoogle Scholar
  135. Volkmann D, Baluška F (1999) The actin cytoskeleton in plants: from transport networks to signaling networks. Microsc Res Tech 47:135–154PubMedCrossRefGoogle Scholar
  136. Volkmann D, Baluška F (2006) Gravity: one of the driving forces of evolution. Protoplasma 229:143–148PubMedCrossRefGoogle Scholar
  137. Volkmann D, Mori T, Tirlapur UK, König K, Fujiwara T, Kendrick-Jones J, Baluška F (2003) Unconventional myosins of the plant-specific class VIII: endocytosis, cytokinesis, plasmodesmata–pit-fields, and cell-to-cell coupling. Cell Biol Int 27:289–291PubMedCrossRefGoogle Scholar
  138. Wabnik K, Govaerts W, Friml J, Kleine-Vehn J (2011) Feedback models for polarized auxin transport: an emerging trend. Mol BioSyst 7:2352–2359PubMedCrossRefGoogle Scholar
  139. Wabnik K, Kleine-Vehn J, Balla J, Sauer M, Naramoto S, Reinöhl V, Merks RM, Govaerts W, Friml J (2010) Emergence of tissue polarization from synergy of intracellular and extracellular auxin signaling. Mol Syst Biol 6:447PubMedCrossRefGoogle Scholar
  140. Wan Y-L, Jasik J, Wang L, Hao H, Volkmann D, Menzel D, Mancuso S, Baluška F, Lin J-X (2012) The signal transducer NPH3 integrates the phototropin1 photosensor with PIN2-based polar auxin transport in arabidopsis root phototropism. Plant Cell [In press]Google Scholar
  141. Wang JR, Hu H, Wang GH, Li J, Chen JY, Wu P (2009) Expression of PIN genes in rice (Oryza sativa L.): tissue specificity and regulation by hormones. FEBS J 277:2954–2969Google Scholar
  142. White RG, Barton DA (2011) The cytoskeleton in plasmodesmata: a role in intercellular transport? J Exp Bot 62:5249–5266 Google Scholar
  143. Wisniewska J, Xu J, Seifertová D, Brewer PB, Ruzicka K, Blilou I, Rouquié D, Benková E, Scheres B, Friml J (2006) Polar PIN localization directs auxin flow in plants. Science 312:883PubMedCrossRefGoogle Scholar
  144. Wojtaszek P, Volkmann D, Baluška F (2004) Polarity and cell walls. In: Lindsey K (ed) Polarity in Plants. Blackwell Publishing, pp 72–121Google Scholar
  145. Wojtaszek P, Baluska F, Kasprowicz A, Luczak M, Volkmann D (2007) Domain-specific mechanosensory transmission of osmotic and enzymatic cell wall disturbances to the actin cytoskeleton. Protoplasma 230:217–230PubMedCrossRefGoogle Scholar
  146. Wolters H, Jürgens G (2009) Survival of the flexible: hormonal growth control and adaptation in plant development. Nat Rev Genet 10:305–317PubMedCrossRefGoogle Scholar
  147. Xu J, Scheres B (2005) Dissection of Arabidopsis ADP-RIBOSYLATION FACTOR 1 function in epidermal cell polarity. Plant Cell 17:525–536PubMedCrossRefGoogle Scholar
  148. Xu T, Wen M, Nagawa S, Fu Y, Chen JG, Wu MJ, Perrot-Rechenmann C, Friml J, Jones AM, Yang Z (2010) Cell surface- and rho GTPase-based auxin signaling controls cellular interdigitation in Arabidopsis. Cell 143:99–110PubMedCrossRefGoogle Scholar
  149. Zhang J, Vanneste S, Brewer PB, Michniewicz M, Grones P, Kleine-Vehn J, Löfke C, Teichmann T, Bielach A, Cannoot B, Hoyerová K, Chen X, Xue HW, Benková E, Zažímalová E, Friml J (2011a) Inositol trisphosphate-induced Ca2+ signaling modulates auxin transport and PIN polarity. Dev Cell 20:855–866PubMedCrossRefGoogle Scholar
  150. Zhang L, Zhang H, Liu P, Hao H, Jin JB, Lin J (2011b) Arabidopsis R-SNARE proteins VAMP721 and VAMP722 are required for cell plate formation. PLoS ONE 6:e26129PubMedCrossRefGoogle Scholar
  151. Zhao H, Hertel R, Ishikawa H, Evans ML (2002) Species differences in ligand specificity of auxin-controlled elongation and auxin transport: comparing Zea and Vigna. Planta 216:293–301PubMedCrossRefGoogle Scholar
  152. Zhu T, Lucas WJ, Rost TL (1998a) Directional cell-to-cell communication, in the Arabidopsis root apical meristem. I. An ultrastructural, and functional analysis. Protoplasma 203:35–47CrossRefGoogle Scholar
  153. Zhu T, O’Quinn RL, Lucas WJ, Rost TL (1998b) Directional cell-to-cell communication in Arabidopsis root apical meristem. II. Dynamics of plasmodesmatal formation. Protoplasma 204:84–93CrossRefGoogle Scholar
  154. Zhu T, Rost TL (2000) Directional cell-to-cell communication, in the Arabidopsis root apical meristem. III. Plasmodesmata turnover and apoptosis in meristem and root cap cells during four weeks after germination. Protoplasma 213:99–107CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  1. 1.IZMBUniversity of BonnBonnGermany

Personalised recommendations