Cortical Actin Interacts with the Plasma Membrane and Microtubules

  • David A. Collings
  • Nina S. Allen
Part of the Developments in Plant and Soil Sciences book series (DPSS, volume 89)


Cortical actin comprises a dynamic array of single actin microfilaments that interacts with the plasma membrane of most plant cells. These interactions, mediated by as yet unknown actin-binding proteins, may function to anchor the entire actin cytoskeleton, and contribute to cell signaling. In cells elongating by diffuse growth, cortical actin is typically transversely oriented, parallel to microtubules. Drug studies demonstrate that in some cases, cortical actin is necessary for the precise re-arrangements of cortical microtubules that control cell expansion and plant morphogenesis. However, in other cases, cortical actin depends on the cortical microtubules for its organization. This suggests that the cortical cytoskeleton is a closely controlled system involving feedback between actin and microtubules.

Key words

actin endoplasmic reticulum membrane interactions microtubules plant morphogenesis 


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  1. Allen NS and Brown DT (1988) Dynamics of the endoplasmic reticulum in living onion epidermal cells in relation to microtubules, microfilaments and intracellular particle movement. Cell Motil Cytoskel 10: 153–163CrossRefGoogle Scholar
  2. Barthou H, Petitprez M, Brière C, Souvré A and Alibert G (1999) RGD-mediated membrane-matrix adhesion triggers agarose-induced embryoid formation in sunflower protoplasts. Protoplasma 206: 143–151CrossRefGoogle Scholar
  3. Baskin TI and Bivens NJ (1995) Stimulation of radial expansion in Arabidopsis roots by inhibitors of actomyosin and vesicle secretion but not by various inhibitors of metabolism. Planta 197: 514–521PubMedCrossRefGoogle Scholar
  4. Boevink P, Oparka K, Santa Cruz S, Martin B, Betteridge A and Hawes C (1998) Stacks on tracks: the plant Golgi apparatus traffics on an actin/ER network. Plant J 15:441–447PubMedCrossRefGoogle Scholar
  5. Butler JH, Hu S, Brady S, Dixon MW and Muday GK (1998) In vitro and in vivo evidence for actin association of the naphthylphthalamic acid-binding protein from zucchini hypocotyls. Plant J 13: 291–301PubMedCrossRefGoogle Scholar
  6. Calvert CM, Gant SJ and Bowles DJ (1996) Tomato annexins p34 and p35 bind to F-actin and display nucleotide phosphodiesterase activity inhibited by phospholipid binding. Plant Cell 8: 333–342PubMedGoogle Scholar
  7. Canut H, Carrasco A, Galaud J, Cassan C, Bouyssou H, Vita N, Ferrara P and Pont-Lezica R (1998) High affinity RGD-binding sites at the plasma membrane of Arabidopsis thaliana links the cell wall. Plant J 16: 63–71PubMedCrossRefGoogle Scholar
  8. Carroll AD, Moyen C, van Kesteren P, Tooke F, Battey NH and Brownlee C (1998) Ca2+, annexins, and GTP modulate exocytosis from maize root cap protoplasts. Plant Cell 10: 1267–1276PubMedGoogle Scholar
  9. Chu B, Kerr P and Carter JV (1993) Stabilizing microtubules with taxol increases microfilament stability during freezing of rye root tips. Plant Cell Environ 16: 883–889CrossRefGoogle Scholar
  10. Clark EA and Brugge JS (1995) Integrins and signal transduction pathways: the road taken. Science 268: 233–239PubMedCrossRefGoogle Scholar
  11. Clark GB and Roux SJ (1995) Annexins of plant cells. Plant Physiol 109: 1133–1139PubMedCrossRefGoogle Scholar
  12. Geary AL (1995) F-actin redistributions at the dividing site in living Tradescantia stomatal complexes as revealed by microinjection of rhodamine-phalloidin. Protoplasma 185: 152–165CrossRefGoogle Scholar
  13. Collings DA, Asada T, Allen NS and Shibaoka H (1998) Plasma membrane-associated actin in Bright Yellow 2 tobacco cells: Evidence for interaction with microtubules. Plant Physiol 118:917–928PubMedCrossRefGoogle Scholar
  14. Collings DA, Asada T and Shibaoka H (1999) Plasma membrane ghosts form differently when produced from microtubule-free tobacco BY-2 cells. Plant Cell Physiol 40: 36–46CrossRefGoogle Scholar
  15. Collings DA, Wasteneys GO and Williamson RE (1995) Cytochalasin rearranges cortical actin of the alga Nitella into short stable rods. Plant Cell Physiol 36: 765–772Google Scholar
  16. Collings DA, Wasteneys GO and Williamson RE (1996) Actin-microtubule interactions in the alga Nitella: analysis of the mechanism by which microtubule depolymerization potentiates cytochalasin’s effects on streaming. Protoplasma 191: 178–190CrossRefGoogle Scholar
  17. Cox DN and Muday GK (1994) NPA binding activity is peripheral to the plasma membrane and is associated with the cytoskeleton. Plant Cell 6: 1941–1953PubMedGoogle Scholar
  18. Cyr RJ (1991) Calcium/calmodulin affects microtubule stability in lysed protoplasts. J Cell Sci 100: 311–317Google Scholar
  19. de Ruijter NCA, Rook MB, Bisseling T and Emons AMC (1998) Lipochito-oligosaccharides re-initiate root hair tip growth in Vicia sativa with high calcium and spectrin-like antigen at the tip. Plant J 13: 341–350CrossRefGoogle Scholar
  20. Ding B, Turgeon R and Parthasarathy MV (1991) Microfilament organization and distribution in freeze substituted tobacco plant tissues. Protoplasma 165: 96–105CrossRefGoogle Scholar
  21. Doohan ME and Palevitz BA (1980) Microtubules and coated vesicles in guard-cell protoplasts of Allium cepa L. Planta 149: 389–401CrossRefGoogle Scholar
  22. Eleftheriou EP and Palevitz BA (1992) The effect of cytochalasin D on preprophase band organisation in root tip cells of Allium. J Cell Sci 103: 989–998Google Scholar
  23. Faraday CD and Spanswick RM (1993) Evidence for a membrane skeleton in higher plants. FEBS Lett 318: 313–316PubMedCrossRefGoogle Scholar
  24. Gavin RH (1997) Microtubule-microfilament synergy in the cytoskeleton. Int Rev Cytol 173: 207–242PubMedCrossRefGoogle Scholar
  25. Gälweiler L, Guan C, Müller A, Wisman E, Mendgen K, Yephremov A and Palme K (1998) Regulation of polar auxin transport by AtPINl in Arabidopsis vascular tissue. Science 282: 2226–2230PubMedCrossRefGoogle Scholar
  26. Gens JS, Reuzeau C, Doolittle KW, McNally JG and Pickard BG (1996) Covisualization by computational optical-sectioning microscopy of integrin and associated proteins at the cell membrane of living onion protoplasts. Protoplasma 194: 215–230PubMedCrossRefGoogle Scholar
  27. Giddings Jr TH and Staehelin LA (1991) Microtubule-mediated control of microfibril deposition: a re-examination of the hypothesis. In: Lloyd CW (ed) The Cytoskeletal Basis of Plant Growth and Form. London: Academic Press, pp 85–99Google Scholar
  28. Gerke V and Moss SE (1997) Annexins and membrane dynamics. Biochim Biophys Acta 1357:129–154PubMedCrossRefGoogle Scholar
  29. Gibbon BC, Kovar DR and Staiger CJ (1999) Latrunculin B has different effects on pollen germination and tube growth. Plant Cell 11: 2349–2363PubMedGoogle Scholar
  30. Griffith LM and Pollard TD (1978) Evidence for actin filament-microtubule interaction mediated by microtubule-associated proteins. J Cell Biol 78: 958–965PubMedCrossRefGoogle Scholar
  31. Hahne G and Hoffmann F (1984) The effect of laser microsurgery on cytoplasmic strands and cytoplasmic streaming in isolated plant protoplasts. Eur J Cell Biol 33: 175–179PubMedGoogle Scholar
  32. Hasezawa S, Sano T and Nagata T (1998) The role of microfilaments in the reoganization and orientation of microtubules during the cell cycle transition from M phase to G1 phase in tobacco BY-2 cells. Protoplasma 202: 105–114CrossRefGoogle Scholar
  33. Himmelspach R, Wymer CL, Lloyd CW and Nick P (1999) Gravity-induced reorientation of cortical microtubules observed in vivo. Plant J 18: 449–453PubMedCrossRefGoogle Scholar
  34. Hitt AL and Luna EJ (1994) Membrane interactions with the actin cytoskeleton. Curr Opin Cell Biol 6: 120–130PubMedCrossRefGoogle Scholar
  35. Huang J, Brady ST, Richards BW, Stenoien D, Resau JH, Copeland NG and Jenkins NA (1999) Direct interaction of microtubule- and actin-based transport motors. Nature 397: 267–270PubMedCrossRefGoogle Scholar
  36. Hush JM and Overall RL (1992) Re-oreintation of cortical F-actin is not necessary for wound-induced microtubule re-orientation and cell polarity establishment. Protoplasma 169: 97–106CrossRefGoogle Scholar
  37. Hussey PJ, Yuan M, Calder G, Khan S and Lloyd CW (1998) Microinjection of pollen-specific actin-depolymerizing factor, ZmADFl, reorientates F-actin strands in Tradescantia stamen hair cells. Plant J 14: 353–357CrossRefGoogle Scholar
  38. Hwang J, Suh S, Yi H, Kim J and Lee Y (1997) Actin filaments modulate both stomatal opening and inward K+-channel activities in guard cells of Vicia faba L. Plant Physiol 115: 335–342PubMedGoogle Scholar
  39. Ingber DE (1997) Tensegrity: the architectural basis of cellular mechanotransduction. Annu Rev Physiol 59: 575–599PubMedCrossRefGoogle Scholar
  40. Itano N and Hatano S (1991) F-actin bundling protein from Physarum polycephalum: purification and its capacity for co-bundling of actin filaments and microtubules. Cell Motil Cytoskel 19: 244–254CrossRefGoogle Scholar
  41. Janßen M, Hunte C, Schulz M and Schnabl H (1996) Tissue specification and intracellular distribution of actin isoforms in Vicia faba L. Protoplasma 191: 158–163CrossRefGoogle Scholar
  42. Kadota A and Wada M (1992) The circular arrangement of cortical microtubules around the subapex of tip-growing fern protonemata is sensitive to cytochalasin B. Plant Cell Physiol 33: 99–102Google Scholar
  43. Katsuta J, Hashiguchi Y and Shibaoka H (1992) The role of the cytoskeleton in positioning of the nucleus is premitotic tobacco BY-2 cells. J Cell Sci 95: 413–422Google Scholar
  44. Katsuta J and Shibaoka H (1992) Inhibition by kinase inhibitors of the development and the disappearance of the preprophase band of microtubules in tobacco BY-2 cells. J Cell Sci 103: 397–405Google Scholar
  45. Kobayashi H (1996) Changes in the relationship between actin filaments and the plasma membrane in cultured Zinnia cells during tracheary element differentiation investigated by using plasma membrane ghosts. J Plant Res 109: 61–65CrossRefGoogle Scholar
  46. Kobayashi H, Fukuda H and Shibaoka H (1988) Interrelation between the spatial disposition of actin filaments and microtubules during the differentiation of tracheary elements in cultured Zinnia cells. Protoplasma 143: 29–37CrossRefGoogle Scholar
  47. Kost B, Spielhofer P and Chua N-H (1998) A GFP-mouse talin fusion protein labels plant actin filaments in vivo and visualizes the actin cytoskeleton in growing pollen tubes. Plant J 16: 393–401PubMedCrossRefGoogle Scholar
  48. Kusumi A and Sako Y (1996) Cell surface organization by the membrane skeleton. Curr Opin Cell Biol 8: 566–574PubMedCrossRefGoogle Scholar
  49. Labouré A, Faik A, Mandaron P and Falconet D (1999) RGD-dependent growth of maize calluses and immunodetection of an integrin-like protein. FEBS Lett 442:123–128PubMedCrossRefGoogle Scholar
  50. Lancelle SA, Cresti M and Hepler PK (1987) Ultrastructure of the cytoskeleton in freeze-substituted pollen tubes of Nicotiana alata. Protoplasma 140: 141–150CrossRefGoogle Scholar
  51. Lancelle SA and Hepler PK (1991) Association of actin with cortical microtubules revealed by immunogold localization in Nicotiana pollen tubes. Protoplasma 165: 167–172CrossRefGoogle Scholar
  52. Lantz VA and Miller KG (1998) A class VI unconventional myosin is associated with a homologue of a microtubule-binding protein, cytoplasmic linker protein-170, in neurons and at the posterior pole of Drosophila embryos. J Cell Biol 140: 897–910PubMedCrossRefGoogle Scholar
  53. Lloyd CW, Drøbak BK, Dove SK and Staiger CJ (1996) Interactions between the plasma membrane and the cytoskeleton in plants. In: Small wood M, Knox JP, Bowles DJ (eds) Membranes: Specialized Functions in Plants. Oxford: BIOS Scientific, pp 1–20Google Scholar
  54. Leung CL, Sun D, Zheng M, Knowles DR and Liem RKH (1999) Microtubule actin cross-linking factor (MACF): a hybrid of dystonin and dystrophin that can interact with the actin and microtubule cytoskeletons. J Cell Biol 147: 1275–1285PubMedCrossRefGoogle Scholar
  55. Marc J, Granger CL, Brincat J, Fisher DD, Kao T, McGrubbin AG and Cyr RJ (1998) A GFP-MAP4 reporter gene for visualizing cortical microtubule rearrangements in living epidermal cells. Plant Cell 10: 1927–1939PubMedGoogle Scholar
  56. Marchesi VT and Ngo N (1993) In vitro assembly of multiprotein complexes containing alpha, beta and gamma tubulins, heat shock protein HSP70, and elongation factor la. Proc Natl Acad Sci USA 90: 3028–3032PubMedCrossRefGoogle Scholar
  57. Mathur J, Spielhofer P, Kost B and Chua N-H (1999) The actin cytoskeleton is required to elaborate and maintain spatial patterning during trichome cell morphogenesis in Arabidopsis thaliana. Development 126: 5559–5568PubMedGoogle Scholar
  58. Michaud D, Guillet G, Rogers PA and Charest PM (1991) Identification of a 220 kDa membrane-associated plant cell protein immunologically related to human β-spectrin. FEBS Lett 294: 77–80PubMedCrossRefGoogle Scholar
  59. Miller DD, de Ruijter NCA and Emons AMC (1997) From signal to form: aspects of the cytoskeleton-plasma membrane-cell wall continuum in root hair tips. J Exp Bot 48: 1881–1886Google Scholar
  60. Mineyuki Y and Palevitz BA (1990) Relationship between preprophase band organization, F-actin and the division site in Allium. J Cell Sci 97: 283–295Google Scholar
  61. Mollenhauer HH and Morré DJ (1976) Cytochalasin B, but not colchicine, inhibits migration of secretory vesicles in root tips of maize. Protoplasma 87: 39–48PubMedCrossRefGoogle Scholar
  62. Moore RC, Durso NA and Cyr RJ (1998) Elongation factor-la stabilizes microtubules in a calcium/calmodulin-dependent manner. Cell Motil Cytoskel 41: 168–180CrossRefGoogle Scholar
  63. Nebenfuhr A, Gallagher LA, Dunahy TG, Frohlick JA, Mazurkiewicz AM, Meehl JB and Staehelin LA (1999) Stop-and-go movements of plant Golgi stacks are mediated by the acto-myosin system. Plant Physiol 121: 1127–1141PubMedCrossRefGoogle Scholar
  64. Niggli V (1996) Membrane-cytoskeleton. In: Hesketh JE, Pryme IF (eds) The Cytoskeleton. Structure and Assembly. Greenwich: JAI Press, pp 123–168Google Scholar
  65. Peterman K and Luna EJ (1999) p125, a plasma membrane-associated F-actin-binding protein. Plant Physiol 120: s71Google Scholar
  66. Quader H, Hormann A and Schnepf E (1989) Reorganization of the endoplasmic reticulum in epidermal cells of onion bulb scales after cold stress: involvement of cytoskeletal elements. Planta 177: 273–280CrossRefGoogle Scholar
  67. Reichelt S, Knight AE, Hodge TP, Baluska F, Samaj J, Volkmann D and Kendrick-Jones J (1999) Characterization of the unconventional myosin VIII in plant cells and its localization at the post-cytokinetic cell wall. Plant J 19: 555–567PubMedCrossRefGoogle Scholar
  68. Ruoslahti E (1996) RGD and other recognition sequences for integrins. Annu Rev Cell Dev Biol 12: 697–715PubMedCrossRefGoogle Scholar
  69. Ryu J-H, Mizuno K, Takagi S and Nagai R (1997) Extracellular components implicated in the stationary organization of the actin cytoskeleton in mesophyll cells of Vallisneria. Plant Cell Physiol 38: 420–432PubMedCrossRefGoogle Scholar
  70. Ryu J, Takagi S and Nagai R (1995) Stationary organization of the actin cytoskeleton in Vallisneria: the role of stable microfilaments at the end walls. J Cell Sci 108: 1531–1539PubMedGoogle Scholar
  71. Satiat-Jeunemaitre B, Steele C and Hawes C (1996) Golgi-membrane dynamics are cytoskeleton dependent: a study on golgi stack movement induced by brefeldin A. Protoplasma 191: 21–33CrossRefGoogle Scholar
  72. Schindler M, Meiners M and Cheresh DA (1989) RGD-dependent linkage between cell wall and plasma membrane: consequences for growth. J Cell Biol 108: 1955–1965PubMedCrossRefGoogle Scholar
  73. Seagull RW (1990) The effects of microtubule and microfilament disrupting agents on cytoskeletal arrays and wall deposition in developing cotton fibres. Protoplasma 159: 44–59CrossRefGoogle Scholar
  74. Sider JR, Mandate CA, Weber KL, Zandy AJ, Beach D, Finst RJ, Skoble J and Bernent WM (1999) Direct observation of microtubule-f-actin interaction in cell free lysates. J Cell Sci 112:1947–1956PubMedGoogle Scholar
  75. Small JV, Clemens R and Kaverina I (1999) Functional design in the actin cytoskeleton, Curr Opin Cell Biol 11:54–60PubMedCrossRefGoogle Scholar
  76. Sonesson A and Widell S (1993) Cytoskeleton components of inside-out and right-side-out plasma membrane vesicles from plants. Protoplasma 177: 45–52CrossRefGoogle Scholar
  77. Sonobe S and Shibaoka H (1989) Cortical fine actin filaments in higher plant cells visualized by rhodamine-phalloidin after pretreatment with m-maleimidobenzoyl N-hydroxysuccinimide ester. Protoplasma 148: 80–86CrossRefGoogle Scholar
  78. Sonobe S and Takahashi S (1994) Association of microtubules with the plasma membrane of tobacco BY-2 cells in vitro. Plant Cell Physiol 35: 451–460Google Scholar
  79. Staiger CJ (2000) Signaling to the actin cytoskeleton in plants. Annu Rev Plant Physiol Plant Mol Biol 51: 257–288PubMedCrossRefGoogle Scholar
  80. Staiger CJ and Cande WZ (1991) Microfilament distribution in maize meiotic mutants correlates with microtubule organization. Plant Cell 3: 637–644PubMedGoogle Scholar
  81. Szymanski DB, Marks DM and Wick SM (1999) Organized F-actin is essential for normal trichome morphogenesis in Arabidopsis. Plant Cell 11: 2331–2347PubMedGoogle Scholar
  82. Takesue K and Shibaoka H (1998) The cyclic reorientation of cortical microtubules in epidermal cells of azuki bean epicotyls: the role of actin filaments in the progression of the cycle. Planta 205: 539–546PubMedCrossRefGoogle Scholar
  83. Thimann KV, Reese K and Nachmias VT (1992) Actin and the elongation of plant cells. Protoplasma 171: 153–166CrossRefGoogle Scholar
  84. Tominaga M, Morita K, Sonobe S, Yokota E and Shimmen T (1997) Microtubules regulate the organization of actin filaments at the cortical region in root hair cells of Hydrocharis. Protoplasma 199: 83–92CrossRefGoogle Scholar
  85. Traas J (1984) Visualization of the membrane bound cytoskeleton and coated pits of plant cells by means of dry cleaving. Protoplasma 119: 212–218CrossRefGoogle Scholar
  86. Traas JA, Doonan JH, Rawlins DJ, Shaw PJ, Watts J and Lloyd CW (1987) An actin network is present in the cytoplasm throughout the cell cycle of carrot cells and associates with the dividing nucleus. J Cell Biol 105: 387–395PubMedCrossRefGoogle Scholar
  87. Traas J, Bellini C, Nacry P, Kronenberger J, Bouchez D and Caboche M (1995) Normal differentiation patterns in plants lacking microtubular preprophase bands. Nature 375: 676–677CrossRefGoogle Scholar
  88. Ueda K, Matsuyama T and Hashimoto T (1999) Visualization of microtubules in living cells of transgenic Arabidopsis thaliana. Protoplasma 206: 201–206CrossRefGoogle Scholar
  89. van der Valk P, Rennie PJ, Connolly JA and Fowke LC (1980) Distribution of cortical microtubules in tobacco protoplasts. An immunofluorescence microscopic and ultrastructural study. Protoplasma 105: 27–43CrossRefGoogle Scholar
  90. Vaughan MA and Vaughn KC (1987) Effects of microfilament disrupters on microfilament distribution and morphology in maize root cells. Histochemistry 87: 129–137PubMedCrossRefGoogle Scholar
  91. Volkmann D and Baluska F (1999) Actin cytoskeleton in plants: from transport networks to signaling networks. Microsc Res Tech 47: 135–154PubMedCrossRefGoogle Scholar
  92. Wang Q and Nick P (1998) The auxin response of actin is altered in the rice mutant Yin-Yang. Protoplasma 204: 22–33PubMedCrossRefGoogle Scholar
  93. Wasteneys GO and Williamson RE (1991) Endoplasmic microtubules and nucleus-associated actin rings in Nitella internodal cells. Protoplasma 162: 86–98CrossRefGoogle Scholar
  94. Waterman-Storer CM and Salmon ED (1999) Positive feedback interactions between microtubule and actin dynamics during cell motility. Curr Opin Cell Biol 11: 61–67PubMedCrossRefGoogle Scholar
  95. Wayne R, Staves MP and Leopold AC (1992) The contribution of the extracellular matrix to gravisensing in characean cells. J Cell Sci 101: 611–623PubMedGoogle Scholar
  96. Wernicke W and Jung G (1992) Role of cytoskeleton in cell shaping of developing mesophyll of wheat (Triticum aestivum L.). Eur J Cell Biol 57: 88–94PubMedGoogle Scholar
  97. Yang F, Demma M, Warren V, Dharmawardhane S and Condeelis J (1990) Identification of an actin-binding protein from Dictyostelium as elongation factor 1α. Nature 347: 494–496PubMedCrossRefGoogle Scholar
  98. Yang W, Burkhart W, Cavallius WC and Boss WF (1993) Purification and characterization of a phosphatidylinositol 4-kinase activator in carrot cells. J Biol Chem 268: 392–398PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2000

Authors and Affiliations

  • David A. Collings
    • 1
    • 2
  • Nina S. Allen
    • 1
  1. 1.Department of BotanyNorth Carolina State UniversityRaleighUSA
  2. 2.Department of Biological SciencesPurdue UniversityWest LafayetteUSA

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