Mechanics of the Cytoskeleton

Chapter
Part of the Signaling and Communication in Plants book series (SIGCOMM, volume 9)

Abstract

This chapter summarizes evidence for a cytoskeletal function in tensegral integration on both the organismal and the cellular levels. The plant cytoskeleton consists of two major elements, microtubules and actin filaments. The spatial organization of these elements is highly dynamic and changes fundamentally during the cell cycle, with conspicuous effects on the predicted stress–strain patterns. In interphase cells, microtubule bundles are thought to control the direction of cellulose deposition and thus to reinforce the axiality of cell growth. By microtubule–actin linkers such as the novel class of plant-specific kinesins with a calponin-homology domain, the rigid microtubules and the flexible actin bundles can be integrated into a system endowed with mechanical tensegrity. Because the plant cytoskeleton is relieved of the load-bearing task it fulfils in the non-walled animal cells, it has adopted sensory functions. Stretch-induced changes of protein conformation and stretch-activated ion channels seem to act in concert with the cytoskeleton, which acts either as a stress-focussing susceptor of mechanical force upon mechanosensitive ion channels or as a primary sensor that transduces mechanical force into differential growth of microtubule plus ends. This cytoskeletal tensegrity sensor is used both to integrate the growth of individual cells with mechanical load of tissues and organs and as an intracellular sensor used to control holistic properties of a cell such as organelle positioning. The distinct nonlinearity of microtubules in particular renders them an ideal tool for self-organization in response to mechanical input from the exterior.

References

  1. Abdrakhamanova A, Wang QY, Khokhlova L, Nick P (2003) Is microtubule assembly a trigger for cold acclimation? Plant Cell Physiol 44:676–686PubMedGoogle Scholar
  2. Adames NR, Cooper JA (2000) Microtubule interactions with the cell cortex causing nuclear movements in Saccharomyces cerevisiae. J Cell Biol 149:863–874PubMedGoogle Scholar
  3. Ahad A, Wolf J, Nick P (2003) Activation-tagged tobacco mutants that are tolerant to antimicrotubular herbicides are cross-resistant to chilling stress. Transgenic Res 12:615–629PubMedGoogle Scholar
  4. Akashi T, Shibaoka H (1987) Effects of gibberellin on the arrangement and the cold stability of cortical microtubules in epidermal cells of pea internodes. Plant Cell Physiol 28:339–348Google Scholar
  5. Akashi T, Kawasaki S, Shibaoka H (1990) Stabilization of cortical microtubules by the cell wall in cultured tobacco cells. Effect of extensin on the cold stability of cortical microtubules. Planta 182:363–369Google Scholar
  6. Akhmanova A, Steinmetz MO (2008) Tracking the ends: a dynamic protein network controls the fate of microtubule tips. Nat Rev Mol Cell Biol 9:309–322PubMedGoogle Scholar
  7. Baluška F, Hlavačka A (2005) Plant formins come of age: something special about cross-walls. New Phytol 168:499–503PubMedGoogle Scholar
  8. Baluška F, Jasik J, Edelmann HG, Salajová T, Volkmann D (2001) Latrunculin B-induced plant dwarfism: plant cell elongation is F-actin-dependent. Dev Biol 231:113–124PubMedGoogle Scholar
  9. Baluška F, Šamaj J, Wojtaszek P, Volkmann D, Menzel D (2003) Cytoskeleton-plasma membrane-cell wall continuum in plants. Emerging links revisited. Plant Physiol 133:482–491PubMedGoogle Scholar
  10. Bannigan A, Wiedemeier AMD, Williamson RE, Overall RL, Baskin TI (2006) Cortical microtubule arrays lose uniform alignment between cells and are oryzalin resistant in the Arabidopsis mutant, radially swollen 6. Plant Cell Physiol 47:949–958PubMedGoogle Scholar
  11. Bartolo ME, Carter JV (1991a) Microtubules in the mesophyll cells of nonacclimated and cold-acclimated spinach. Plant Physiol 97:175–181PubMedGoogle Scholar
  12. Bartolo ME, Carter JV (1991b) Effect of microtubule stabilization on the freezing tolerance of mesophyll cells of spinach. Plant Physiol 97:182–187PubMedGoogle Scholar
  13. Bartolo ME, Carter JV (1992) Lithium decreases cold-induced microtubule depolymerization in mesophyll cells of spinach. Plant Physiol 99:1716–1718PubMedGoogle Scholar
  14. Baskin TI (2001) On the alignment of cellulose microfibrils by cortical microtubules: a review and a model. Protoplasma 215:150–171PubMedGoogle Scholar
  15. Baskin TI, 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 197:514–521PubMedGoogle Scholar
  16. Baskin TI, Wilson JE (1997) Inhibitors of protein kinases and phosphatases alter root morphology and disorganize cortical microtubules. Plant Physiol 113:493–502PubMedGoogle Scholar
  17. Bichet A, Desnos T, Turner S, Grandjean O, Höfte H (2001) BOTERO1 is required for normal orientation of cortical microtubules and anisotropic cell expansion in Arabidopsis. Plant J 25:137–148PubMedGoogle Scholar
  18. Bisgrove SR, Lee YRJ, Liu B, Peters NT, Kropf DL (2008) The microtubule plus-end binding protein EB1 functions in root responses to touch and gravity signals in Arabidopsis. Plant Cell 20:396–410PubMedGoogle Scholar
  19. Björkman T (1988) Perception of gravity by plants. Adv Bot Res 15:1–4Google Scholar
  20. Blancaflor EB (2000) Cortical actin filaments potentially interact with cortical microtubules in regulating polarity of cell expansion in primary roots of maize (Zea mays L.). J Plant Growth Regul 19:406–414PubMedGoogle Scholar
  21. Blancaflor EB, Hasenstein KH (1993) Organization of cortical microtubules in graviresponding maize roots. Planta 191:230–237Google Scholar
  22. Bokros CL, Hugdahl JD, Blumenthal SSD, Morejohn LC (1996) Proteolytic analysis of polymerized maize tubulin: regulation of microtubule stability to low temperature and Ca2+ by the carboxyl terminus of β-tubulin. Plant Cell Environ 19:539–548Google Scholar
  23. Braam J, Davis RW (1990) Rain-, wind-, and touch-induced expression of calmodulin and calmodulin-related genes in Arabidopsis. Cell 60:357–364PubMedGoogle Scholar
  24. Breviario D (2008) Plant tubulin genes: regulatory and evolutionary aspects. Plant Cell Monogr 11:207–232Google Scholar
  25. Brown RC, Lemmon BE (2007) The pleiomorphic plant MTOC: An evolutionary perspective. J Int Plant Biol 49:1142–1153Google Scholar
  26. Buder J (1920) Neue phototropische Fundamentalversuche. Ber Dtsch Bot Ges 38:10–19Google Scholar
  27. Buder J (1961) Der Geotropismus der Characeenrhizoide. Ber Dtsch Bot Ges 74:14–23Google Scholar
  28. Burk DH, Ye ZH (2002) Alteration of oriented deposition of cellulose microfibrils by mutation of a katanin-like microtubule severing protein. Plant Cell 14:2145–2160PubMedGoogle Scholar
  29. Burk DH, Liu B, Zhong R, Morrison WH, Ye ZH (2001) A katanin-like protein regulates normal cell wall biosynthesis and cell elongation. Plant Cell 13:807–827PubMedGoogle Scholar
  30. Buschmann H, Fabri CO, Hauptmann M, Hutzler P, Laux T, Lloyd CW, Schäffner AR (2004) Helical growth of the Arabidopsis mutant tortifolia1 reveals a plant-specific microtubule-associated protein. Curr Biol 14:1515–1521PubMedGoogle Scholar
  31. Camilleri C, Azimzadeh J, Pastuglia M, Bellini C, Grandjean O, Bouchez D (2002) The Arabidopsis TONNEAU2 gene encodes a putative novel PP2A regulatory subunit essential for the control of cortical cytoskeleton. Plant Cell 14:833–845PubMedGoogle Scholar
  32. Campanoni P, Blasius B, Nick P (2003) Auxin transport synchronizes the pattern of cell division in a tobacco cell line. Plant Physiol 133:1251–1260PubMedGoogle Scholar
  33. Canut H, Carrasco A, Galaud J-P, Cassan C, Bouyssou H, Vita N, Ferrara P, Pont-Lezica R (1998) High affinity RGD-binding sites at the plasma membrane of Arabidopsis thaliana links the cell wall. Plant J 16:63–71PubMedGoogle Scholar
  34. Cárdenas L, Lovy-Wheeler A, Kunkel JG, Hepler PK (2008) Pollen tube growth oscillations and intracellular calcium levels are reversibly modulated by actin polymerization. Plant Physiol 146:1611–1621PubMedGoogle Scholar
  35. Chan J, Calder G, Fox S, Lloyd C (2007) Cortical microtubule arrays undergo rotary movements in Arabidopsis hypocotyl epidermal cells. Nat Cell Biol 9:171–175PubMedGoogle Scholar
  36. Collings DA (2008) Crossed-wires: interactions and cross-talk between the microtubule and micro. lament networks in plants. Plant Cell Monogr 11:47–79Google Scholar
  37. Collings DA, Lill AW, Himmelspach R, Wasteneys GO (2006) Hypersensitivity to cytoskeletal antagonists demonstrates microtubule-microfilament cross-talk in the control of root elongation in Arabidopsis thaliana. New Phytol 170:275–290PubMedGoogle Scholar
  38. Dhonukshe P, Mathur J, Hülskamp M, Gadella TWJ (2005) Microtubule plus-ends reveal essential links between intracellular polarization and localized modulation of endocytosis during division-plane establishment in plant cells. BMC Biol 3:11PubMedGoogle Scholar
  39. Ding JP, Pickard BG (1993) Mechanosensory calcium-selective cation channels in epidermal cells. Plant J 3:83–110Google Scholar
  40. Durso NA, Cyr RJ (1994) A calmodulin-sensitive interaction between microtubules and a higher plant homolog of elongation factor 1α. Plant Cell 6:893–905PubMedGoogle Scholar
  41. Eckert BS, Yeagle PL (1988) Acrylamide treatment of PtK1 cells causes dephosphorylation of keratin polypeptides. Cell Motil Cytoskelet 11:24–30Google Scholar
  42. Edwards ES, Roux SJ (1994) Limited period of graviresponsiveness in germinating spores of Ceratopteris richardii. Planta 195:150–152PubMedGoogle Scholar
  43. Edwards ES, Roux SJ (1997) The influence of gravity and light on developmental polarity of single cells of Ceratopteris richardii gametophytes. Biol Bull 192:139–140PubMedGoogle Scholar
  44. Elinson RP, Rowning B (1988) Transient array of parallel microtubules in frog eggs: potential tracks for a cytoplasmic rotation that specifies the dorso-ventral axis. Dev Biol 128:185–197PubMedGoogle Scholar
  45. Fisher DD, Cyr RJ (1993) Calcium levels affect the ability to immunolocalize calmodulin to cortical microtubules. Plant Physiol 10:543–551Google Scholar
  46. Frey N, Klotz J, Nick P (2009) Dynamic bridges – a calponin-domain kinesin from rice links actin filaments and microtubules in both cycling and non-cycling cells. Plant Cell Physiol 50:1493–1506PubMedGoogle Scholar
  47. Frey N, Klotz J, Nick P (2010) A kinesin with calponin-homology domain is involved in premitotic nuclear migration. J Exp Bot 61:3423–3437PubMedGoogle Scholar
  48. Funada R (2008) Microtubules and the control of wood formation. Plant Cell Monogr 11:83–119Google Scholar
  49. Furutani I, Watanabe Y, Prieto R, Masukawa M, Suzuki K, Naoi K, Thitamadee S, Shikanai T, Hashimoto T (2000) The SPIRAL genes are required for directional control of cell plates elongation in Arabidopsis thaliana. Development 127:4443–4453PubMedGoogle Scholar
  50. Gardiner JC, Harper JDI, Weerakoon ND, Collings DA, Ritchie S, Gilroy S, Cyr RJ, Marc J (2001) A 90-kD phospholipase D from tobacco binds to microtubules and the plasma membrane. Plant Cell 13:2143–2158PubMedGoogle Scholar
  51. Geiger B, Bershadsky A (2001) Assembly and mechanosensory function of focal contacts. Curr Opin Cell Biol 13:584–592PubMedGoogle Scholar
  52. Gens JS, Fujiki M, Pickard BG (2000) Arabinogalactan protein and wall-associated kinase in a plasmalemmal reticulum with specialized vertices. Protoplasma 212:115–134PubMedGoogle Scholar
  53. Gerhart J, Ubbeles G, Black S, Hara K, Kirschner M (1981) A reinvestigation of the role of the grey crescent in axis formation in Xenopus laevis. Nature 292:511–516PubMedGoogle Scholar
  54. Giancotti FG, Ruoslahti E (1999) Integrin signaling. Science 285:1028–1032PubMedGoogle Scholar
  55. Gianí S, Qin X, Faoro F, Breviario D (1998) In rice, oryzalin and abscisic acid differentially affect tubulin mRNA and protein levels. Planta 205:334–341PubMedGoogle Scholar
  56. Giddings TH, Staehelin A (1988) Spatial relationship between microtubules and plasmamembrane rosettes during the deposition of primary wall microfibrils in Closterium spec. Planta 173:22–30Google Scholar
  57. Giddings TH, Staehelin A (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. Academic, London, pp 85–99Google Scholar
  58. Gierer A (1981) Generation of biological patterns and form: some physical, mathematical, and logical aspects. Progr Biophys Mol Biol 37:1–47Google Scholar
  59. Gittes F, Mickey B, Nettleton J, Howard J (1993) Flexual rigidity of microtubules and actin filaments measured from thermal fluctuations in shape. J Cell Biol 120:923–934PubMedGoogle Scholar
  60. Godbolé R, Michalke W, Nick P, Hertel R (2000) Cytoskeletal drugs and gravity-induced lateral auxin transport in rice coleoptiles. Plant Biol 2:176–181Google Scholar
  61. Goebel K (1908) Einleitung in die experimentelle Morphologie der Pflanzen. Teubner, Leipzig, pp 218–251Google Scholar
  62. Goode BL, Drubin DG, Barnes G (2000) Functional cooperation between the microtubule and actin cytoskeletons. Curr Opin Cell Biol 12:63–71PubMedGoogle Scholar
  63. Gossot O, Geitmann A (2007) Pollen tube growth: coping with mechanical obstacles involves the cytoskeleton. Planta 226:405–416PubMedGoogle Scholar
  64. Grabski S, Schindler M (1996) Auxins and cytokinins as antipodal modulators of elasticity within the actin network of plant cells. Plant Physiol 110:965–970PubMedGoogle Scholar
  65. Grabski S, Arnoys E, Busch B, Schindler M (1998) Regulation of actin tension in plant cells by kinases and phosphatases. Plant Physiol 116:279–290Google Scholar
  66. Green PB (1962) Mechanism for plant cellular morphogenesis. Science 138:1404–1405PubMedGoogle Scholar
  67. Green PB (1980) Organogenesis – a biophysical view. Annu Rev Plant Physiol 31:51–82Google Scholar
  68. Gus-Mayer S, Naton B, Hahlbrock K, Schmelzer E (1998) Local mechanical stimulation induces components of the pathogen defense response in parsley. Proc Natl Acad Sci USA 95:8398–8403PubMedGoogle Scholar
  69. Gustin MC, Sachs F, Sigurdson WJ, Ruknudin A, Bowman C (1991) Technical comments. Single channel mechanosensitive currents. Science 253:1195–1197Google Scholar
  70. Gutjahr C, Nick P (2006) Acrylamide inhibits gravitropism and destroys microtubules in rice coleoptiles. Protoplasma 227:211–222PubMedGoogle Scholar
  71. Haberland G (1900) Über die Perzeption des geotropischen Reizes. Ber Dtsch Bot Ges 18:261–272Google Scholar
  72. Hamada T (2007) Microtubule-associated proteins in higher plants. J Plant Res 120:79–98PubMedGoogle Scholar
  73. Hamant O, Heisler MG, Jönsson H, Krupinski P, Uyttewaal M, Bokov P, Corson F, Sahlin P, Boudaoud A, Meyerowitz EM, Couder Y, Traas J (2008) Developmental patterning by mechanical signals in Arabidopsis. Science 322:1650–1655PubMedGoogle Scholar
  74. Hardham AR, Green PB, Lang JM (1980) Reorganization of cortical microtubules and cellulose deposition during leaf formation of Graptopetalum paraguayense. Planta 149:181–195Google Scholar
  75. Hasezawa S, Nozaki H (1999) Role of cortical microtubules in the orientation of cellulose microfibril deposition in higher-plant cells. Protoplasma 209:98–104PubMedGoogle Scholar
  76. Hashimoto T, Kato T (2006) Cortical control of plant microtubules. Curr Opin Plant Biol 9:5–11PubMedGoogle Scholar
  77. Heath IB (1974) A unified hypothesis for the role of membrane bound enzyme complexes and microtubules in plant cell wall synthesis. J Theor Biol 48:445–449PubMedGoogle Scholar
  78. Hepler PK, Vidali L, Cheung AY (2001) Polarized cell growth in higher plants. Annu Rev Cell Dev Biol 17:159–187PubMedGoogle Scholar
  79. Hertel R, Friedrich U (1973) Abhängigkeit der geotropischen Krümmung der Chara-Rhizoide von der Zentrifugalbeschleunigung. Z Pflanzenphysiol 70:173–184Google Scholar
  80. Himmelspach R, Wymer CL, Lloyd CW, Nick P (1999) Gravity-induced reorientation of cortical microtubules observed in vivo. Plant J 18:449–453PubMedGoogle Scholar
  81. Himmelspach R, Nick P (2001) Gravitropic microtubule reorientation can be uncoupled from growth. Planta 212:184–189PubMedGoogle Scholar
  82. Hodick D (1994) Negative gravitropism in Chara protonemata: a model integrating the opposite gravitropic responses of protonemata and rhizoids. Planta 195:43–49PubMedGoogle Scholar
  83. Holubowicz T, Boe AA (1969) Development of cold hardiness in apple seedlings treated with gibberellic acid and abscisic acid. J Am Soc Hortic Sci 94:661–664Google Scholar
  84. Holweg C, Süßlin C, Nick P (2004) Capturing in-vivo dynamics of the actin cytoskeleton. Plant Cell Physiol 45:855–863PubMedGoogle Scholar
  85. Hush JM, Hawes CR, Overall RL (1990) Interphase microtubule re-orientation predicts a new cell polarity in wounded pea roots. J Cell Sci 96:47–61Google Scholar
  86. Igarashi H, Orii H, Mori H, Shimmen T, Sonobe S (2000) Isolation of a novel 190 kDa protein from tobacco BY-2 cells: possible involvement in the interaction between actin filaments and microtubules. Plant Cell Physiol 41:920–931PubMedGoogle Scholar
  87. Ikushima T, Shimmen T (2005) Mechano-sensitive orientation of cortical microtubules during gravitropism in azuki bean epicotyls. J Plant Res 118:19–26PubMedGoogle Scholar
  88. Ingber DE (2003a) Tensegrity I: cell structure and hierarchical systems biology. J Cell Sci 116:1157–1173PubMedGoogle Scholar
  89. Ingber DE (2003b) Tensegrity II: how structural networks influence cellular information processing networks. J Cell Sci 116:1397–1408PubMedGoogle Scholar
  90. Irving RM (1969) Characterization and role of an endogenous inhibitor in the induction of cold hardiness in Acer negundo. Plant Physiol 44:801–805PubMedGoogle Scholar
  91. Irving RM, Lanphear FO (1968) Regulation of cold hardiness in Acer negundo. Plant Physiol 43:9–13PubMedGoogle Scholar
  92. Jacob F (1977) Evolution and tinkering. Science 196:1161–1166PubMedGoogle Scholar
  93. Jaffe MJ, Leopold AC, Staples RA (2002) Thigmo responses in plants and fungi. Am J Bot 89:375–382PubMedGoogle Scholar
  94. Janmey PA, Weitz DA (2004) Dealing with mechanics: mechanisms of force transduction in cells. Trends Biochem Sci 29:364–370PubMedGoogle Scholar
  95. Jian LC, Sun LH, Lin ZP (1989) Studies on microtubule cold stability in relation to plant cold hardiness. Acta Bot Sin 31:737–741Google Scholar
  96. Jones RS, Mitchell CA (1989) Calcium ion involvement in growth inhibition of mechanically stressed soybean Glycine max seedlings. Physiol Plant 76:598–602PubMedGoogle Scholar
  97. Kakimoto T, Shibaoka H (1987) Actin filaments in the preprophase band and phragmoplast of tobacco cells. Protoplasma 140:151–156Google Scholar
  98. Karki S, Holzbaur EL (1999) Cytoplasmic dynein and dynactin in cell division and intracellular transport. Curr Opin Cell Biol 1:45–53Google Scholar
  99. Katsuta J, Shibaoka H (1988) The roles of the cytoskeleton and the cell wall in nuclear positioning in tobacco BY-2 cells. Plant Cell Physiol 29:403–413Google Scholar
  100. Kell A, Glaser RW (1993) On the mechanical and dynamic properties of plant-cell membranes: their role in growth, direct gene transfer and protoplast fusion. J Theor Biol 160:41–62Google Scholar
  101. Kennard JL, Cleary AL (1997) Pre-mitotic nuclear migration in subsidiary mother cells of Tradescantia occurs in G1 of the cell cycle and requires F-actin. Cell Motil Cytoskelet 36:55–67Google Scholar
  102. Kerr GP, Carter JV (1990) Relationship between freezing tolerance of root-tip cells and cold stability ofmicrotubules in rye (Secale cereale L. Cv. Puma). Plant Physiol 93:77–82PubMedGoogle Scholar
  103. Kimura S, Laosinchai W, Itoh T, Cui X, Linder CR, Brown RM (1999) Immunogold labeling of rosette terminal cellulose-synthesizing complexes in the vascular plant Vigna angularis. Plant Cell 11:2075–2086PubMedGoogle Scholar
  104. Kishimoto U (1968) Response of Chara internodes to mechanical stimulation. Ann Rep Biol Works Fac Sci Osaka Univ 16:61–66Google Scholar
  105. Knight MR, Campbell AK, Smith SM, Trewavas AJ (1991) Transgenic plant aequorin reports the effects of touch and cold-shock and elicitors on cytoplasmic calcium. Nature 352:524–526PubMedGoogle Scholar
  106. Kobayashi I, Kobayashi Y (2008) Microtubules and pathogen defence. Plant Cell Monogr 11:121–140Google Scholar
  107. Komis G, Apostolakos P, Galatis B (2002) Hyperosmotic stress induces formation of tubulin macrotubules in root-tip cells of Triticum turgidum: their probable involvement in protoplast volume control. Plant Cell Physiol 43:911–922PubMedGoogle Scholar
  108. Komis G, Quader H, Galatis B, Apostolakos P (2006) Macrotubule-dependent protoplast volume regulation in plasmolysed root-tip cells of Triticum turgidum: involvement of phospholipase D. New Phytol 171:737–750PubMedGoogle Scholar
  109. Kung C (2005) A possible unifying principle for mechanosensation. Nature 436:647–654PubMedGoogle Scholar
  110. Kutschera U (2008) The outer epidermal wall: design and physiological role of a composite structure. Ann Bot 101:615–621PubMedGoogle Scholar
  111. Kuznetsov OA, Hasenstein KH (1996) Magnetophoretic induction of root curvature. Planta 198:87–94PubMedGoogle Scholar
  112. Lawrence CJ, Morris NR, Meagher RB, Dawe RK (2001) Dyneins have run their course in plant lineage. Traffic 2:362–363PubMedGoogle Scholar
  113. Ledbetter MC, Porter KR (1963) A microtubule in plant cell fine structure. J Cell Biol 12:239–250Google Scholar
  114. Lintilhac PM, Vesecky TB (1984) Stress-induced alignment of division plane in plant tissues grown in vitro. Nature 307:363–364Google Scholar
  115. Lloyd CW, Traas JA (1988) The role of F-actin in determining the division plane of carrot suspension cells. Drug Stud Dev 102:211–221Google Scholar
  116. Los DA, Murata N (2004) Membrane fluidity and its roles in the perception of environmental signals. Biochim Biophys Acta 1666:142–157PubMedGoogle Scholar
  117. Lucas J, Shaw SL (2008) Cortical microtubule arrays in the Arabidopsis seedling. Curr Opin Plant Biol 11:94–98PubMedGoogle Scholar
  118. Lyons JM (1973) Chilling injury in plants. Annu Rev Plant Physiol 24:445–466Google Scholar
  119. Maisch J, Nick P (2007) Actin is involved in auxin-dependent patterning. Plant Physiol., Plant Physiol 143:1695–1704.PubMedGoogle Scholar
  120. McClinton RS, Sung ZR (1997) Organization of cortical microtubules at the plasma membrane in Arabidopsis. Planta 201:252–260PubMedGoogle Scholar
  121. Modig C, Strömberg E, Wallin M (1994) Different stability of posttranslationally modified brain microtubules isolated from cold-temperate fish. Mol Cell Biochem 130:137–147PubMedGoogle Scholar
  122. Monroy AF, Sarhan F, Dhindsa RS (1993) Cold-induced changes in freezing tolerance, protein phosphorylation, and gene expression. Plant Physiol 102:1227–1235PubMedGoogle Scholar
  123. Morris NR (2003) Nuclear positioning: the means is at the ends. Curr Opin Cell Biol 15:54–59PubMedGoogle Scholar
  124. Moseley JB, Bartolini F, Okada K, Wen Y, Gundersen GG, Goode BL (2007) Regulated binding of adenomatous polyposis coli protein to actin. J Biol Chem 282:12661–12668PubMedGoogle Scholar
  125. Mulder B, Schell J, Emons AM (2004) How the geometrical model for plant cell wall formation enables the production of a random texture. Cellulose 11:395–401Google Scholar
  126. Murata T, Wada M (1991) Effects of centrifugation on preprophase-band formation in Adiantum protonemata. Planta 183:391–398Google Scholar
  127. Murata N, Ishizaki-Nishizawa O, Higashi H, Tasaka Y, Nishida I (1992) Genetically engineered alteration in chilling sensitivity of plants. Nature 356:710–713Google Scholar
  128. Nemec B (1900) Über die Art der Wahrnehmung des Schwerkraftreizes bei den Pflanzen. Ber Dtsch Bot Ges 18:241–245Google Scholar
  129. Nick P (2008a) Control of cell axis. Plant Cell Monogr 11:3–46Google Scholar
  130. Nick P (2008b) Microtubules as sensors for abiotic stimuli. Plant Cell Monogr 11:175–203Google Scholar
  131. Nick P, Furuya M (1996) Buder revisited – cell and organ polarity during phototropism. Plant Cell Environ 19:1179–1187PubMedGoogle Scholar
  132. Nick P, Schäfer E, Hertel R, Furuya M (1991) On the putative role of microtubules in gravitropism of maize coleoptiles. Plant Cell Physiol 32:873–880Google Scholar
  133. Nick P, Yatou O, Furuya M, Lambert AM (1994) Auxin-dependent microtubule responses and seedling development are affected in a rice mutant resistant to EPC. Plant J 6:651–663Google Scholar
  134. Nick P, Godbolé R, Wang QY (1997) Probing rice gravitropism with cytoskeletal drugs and cytoskeletal mutants. Biol Bull 192:141–143PubMedGoogle Scholar
  135. Nick P, Han M, An G (2009) Auxin stimulates its own transport by actin reorganization. Plant Physiol 151:155–167PubMedGoogle Scholar
  136. Niklas KJ (1992) Plant biomechanics. An engineering approach to plant form and function. University of Chicago Press, ChicagoGoogle Scholar
  137. Orr AW, Helmke BP, Blackman BR, Schwartz MA (2006) Mechanisms of mechanotransduction. Dev Cell 10:11–20PubMedGoogle Scholar
  138. Panteris E (2008) Cortical actin filaments at the division site of mitotic plant cells: a reconsideration of the ‘actin-depleted zone’. New Phytol 179:334–341PubMedGoogle Scholar
  139. Paredez AR, Somerville CR, Ehrhardt DW (2006) Visualization of cellulose synthase demonstrates functional association with microtubules. Science 312:1491–1495PubMedGoogle Scholar
  140. Parthasarathy MV, Perdue TD, Witztum A, Alvernaz J (1985) Actin network as a normal component of the cytoskeleton in many vascular plant cells. Am J Bot 72:1318–1323Google Scholar
  141. Pickard BG (2008) “Second extrinsic organizational mechanism” for orienting cellulose: modeling a role for the plasmalemmal reticulum. Protoplasma 233:7–29PubMedGoogle Scholar
  142. Pickard BG, Fujiki M (2005) Ca2+ pulsation in BY-2 cells and evidence for control of mechanosensory Ca2+-selective channels by the plasmalemmal reticulum. Funct Plant Biol 32:863–879Google Scholar
  143. Pihakaski-Maunsbach K, Puhakainen T (1995) Effect of cold exposure on cortical microtubules of rye (Secale cereale) as observed by immunocytochemistry. Physiol Plant 93:563–571Google Scholar
  144. Preston RD (1988) Cellulose-microfibril-orienting mechanisms in plant cell walls. Planta 174:67–74Google Scholar
  145. Preuss ML, Kovar DR, Lee YR, Staiger CJ, Delmer DP, Liu B (2004) A plant-specific kinesin binds to actin microfilaments and interacts with cortical microtubules in cotton fibers. Plant Physiol 136:3945–3955PubMedGoogle Scholar
  146. Rawitscher F (1932) Der Geotropismus der Pflanzen. Fischer, JenaGoogle Scholar
  147. Richardson D, Simmons M, Reddy A (2006) Comprehensive comparative analysis of kinesins in photosynthetic eukaryotes. BMC Genomics 7:18PubMedGoogle Scholar
  148. Rikin A, Richmond AE (1976) Amelioration of chilling injuries in cucumber seedlings by abscisic acid. Physiol Plant 38:95–97Google Scholar
  149. Rikin A, Waldman M, Richmond AE, Dovrat A (1975) Hormonal regulation of morphogenesis and cold resistance. I. Modifications by abscisic acid and gibberellic acid in alfalfa (Medicago sativa L.) seedlings. J Exp Bot 26:175–183Google Scholar
  150. Rikin A, Atsmon D, Gitler C (1980) Chilling injury in cotton (Gossypium hirsutum L.): effects of antimicrotubular drugs. Plant Cell Physiol 21:829–837Google Scholar
  151. Riveline D, Zamir E, Balaban NQ, Schwarz US, Ishizaki T, Narumiya S, Kam Z, Geiger B, Bershadsky AD (2001) Focal contacts as mechanosensors: externally applied local mechanical force induces growth of focal contacts by an mDia1-dependent and ROCK-independent mechanism. J Cell Biol 153:1175–1185PubMedGoogle Scholar
  152. Robby T (1996) A new architecture. Yale Academic Press, New HavenGoogle Scholar
  153. Rodriguez OC, Schaefer AW, Mandato CA, Forscher P, Bement WM, Waterman-Storer CM (2003) Conserved microtubule-actin interactions in cell movement and morphogenesis. Nat Cell Biol 5:599–609PubMedGoogle Scholar
  154. Sachs J (1880) Stoff und Form der Pflanzenorgane. Arb Bot Inst Würzburg 2:469–479Google Scholar
  155. Sachs F, Morris CE (1998) Mechanosensitive ion channels in nonspecialized cells. Rev Physiol Biochem Pharmacol 132:1–77PubMedGoogle Scholar
  156. Sainsbury F, Collings DA, Mackun K, Gardiner J, Harper JDI, Marc J (2008) Developmental reorientation of transverse cortical microtubules to longitudinal directions: a role for actomyosin-based streaming and partial microtubule-membrane detachment. Plant J 56:116–131PubMedGoogle Scholar
  157. Sakiyama M, Shibaoka H (1990) Effects of abscisic acid on the orientation and cold stability of cortical microtubules in epicotyl cells of the dwarf pea. Protoplasma 157:165–171Google Scholar
  158. Samuels AL, Giddings TH, Staehelin LA (1995) Cytokinesis in tobacco BY-2 and root tip cells – a new model of cell plate formation in higher plants. J Cell Biol 130:1345–1357PubMedGoogle Scholar
  159. Sandblad L, Busch KE, Tittmann P, Gross H, Brunner D, Hoenger A (2006) The Schizosaccharomyces pombe EB1 homolog Mal3p binds and stabilizes the microtubule lattice seam. Cell 127:1415–1424PubMedGoogle Scholar
  160. Sangwan V, Foulds I, Singh J, Dhindsa RS (2001) Cold-activation of Brassica napus BN115 promoter is mediated by structural changes in membranes and cytoskeleton, and requires Ca2+ influx. Plant J 27:1–12PubMedGoogle Scholar
  161. Sano T, Higaki T, Oda Y, Hayashi T, Hasezawa S (2005) Appearance of actin microfilament ‘twin peaks’ in mitosis and their function in cell plate formation, as imaged in tobacco BY-2 cells expressing GFP-fimbrin. Plant J 44:595–605PubMedGoogle Scholar
  162. Sato Y, Kadota A, Wada M (1999) Mechanically Induced Avoidance Response of Chloroplasts in Fern Protonemal Cells. Plant Physiol 121:37–44PubMedGoogle Scholar
  163. Schmelzer E (2002) Cell polarization, a crucial process in fungal defence. Trends Plant Sci 7:411–415PubMedGoogle Scholar
  164. Schmit AC, Nick P (2008) Microtubules and the evolution of mitosis. Plant Cell Monogr 11: 1500 233–266Google Scholar
  165. Schwuchow J, Sack FD, Hartmann E (1990) Microtubule disruption in gravitropic protonemata of the moss Ceratodon. Protoplasma 159:60–69PubMedGoogle Scholar
  166. Seagull R (1990) The effects of microtubule and microfilament disrupting agents on cytoskeletal arrays and wall deposition in developing cotton fibers. Protoplasma 159:44–59Google Scholar
  167. Sedbrook JC, Kaloriti D (2008) Microtubules, MAPs and plant directional cell expansion. Trends Plant Sci 13:303–310PubMedGoogle Scholar
  168. Shibaoka T (1966) Action potentials in plant organs. Symp Soc Exp Biol 20:165–184Google Scholar
  169. Sievers A, Schröter K (1971) Versuch einer Kausalanalyse der geotropischen Reaktionskette im Chara-Rhizoid. Planta 96:339–353Google Scholar
  170. Sonobe S, Shibaoka H (1989) Cortical fine actin filaments in higher plant cells visualized by rhodamine-phalloidin after pretreatment with m-maleimidobenzoyl-N-hydrosuccinimide ester. Protoplasma 148:80–86Google Scholar
  171. Tabony J, Glade N, Papaseit C, Demongeot J (2004) Microtubule self-organization as an example of the development of order in living systems. J Biol Phys Chem 4:50–63Google Scholar
  172. Takemoto D, Hardham AR (2004) The cytoskeleton as a regulator and target of biotic interactions in plants. Plant Physiol 136:3864–3876PubMedGoogle Scholar
  173. Tamura K, Nakatani K, Mitsui H, Ohashi Y, Takahashi H (1999) Characterization of katD, a kinesin-like protein gene specifically expressed in floral tissues of Arabidopsis thaliana. Gene 230:23–32PubMedGoogle Scholar
  174. Taylor DP, Leopold AC (1992) Offset of gravitropism in maize roots by low temperature. ASGSB Bull 6:75Google Scholar
  175. Telewski FW (2006) A unified hypothesis of mechanoperception in plants. Am J Bot 93:1466–1476PubMedGoogle Scholar
  176. Thimann KV, Reese K, Nachmikas VT (1992) Actin and the elongation of plant cells. Protoplasma 171:151–166Google Scholar
  177. Thitamadee S, Tuchihara K, Hashimoto T (2002) Microtubule basis for left-handed helical growth in Arabidopsis. Nature 417:193–196PubMedGoogle Scholar
  178. Thomas DDS, Dunn DM, Seagull RW (1977) Rapid cytoplasmic responses of oat coleoptiles to cytochalasin B, auxin, and colchicine. Can J Bot 55:1797–1800Google Scholar
  179. Thompson DW (1959) On growth and form. Cambridge University Press, Cambridge, pp 465–644Google Scholar
  180. Tirnauer JS, Bierer BE (2000) EB1 proteins regulate microtubule dynamics, cell polarity, and chromosome stability. J Cell Biol 149:761–766PubMedGoogle Scholar
  181. Toriyama H, Jaffe MJ (1972) Migration of calcium and its role in the regulation of seismonasty in the motor cell of Mimosa pudica D. Plant Physiol 49:72–81PubMedGoogle Scholar
  182. Traas J, Bellini C, Nacry P, Kronenberger J, Bouchez D, Caboche M (1995) Normal differentiation patterns in plants lacking microtubular preprophase bands. Nature 375:676–677Google Scholar
  183. Tsvetkov AS, Samsonov A, Akhmanova A, Galjart N, Popov SV (2007) Microtubule-binding proteins CLASP1 and CLASP2 interact with actin filaments. Cell Motil Cytoskelet 64:519–530Google Scholar
  184. Turing AM (1952) The chemical basis of morphogenesis. Philos Trans R Soc Lond Ser B 237:37–72Google Scholar
  185. Vantard M, Leviliiers N, Hill AM, Adoutte A, Lambert AM (1990) Incorporation of Paramecium axonemal tubulin into higher plant cells reveals functional sites of microtubule assembly. Proc Natl Acad Sci USA 87:8825–8829PubMedGoogle Scholar
  186. Vitha S, Froehlich JE, Koksharova O, Pyke KA, van Erp H, Osteryoung KW (2003) ARC6 is a J-domain plastid division protein and an evolutionary descendant of the cyanobacterial cell division protein Ftn2. Plant Cell 15:1918–1933PubMedGoogle Scholar
  187. Vöchting H (1878) Über Organbildung im Pflanzenreich. Cohen, BonnGoogle Scholar
  188. Vogelmann TC, Bassel AR, Miller JH (1981) Effects of microtubule-inhibitors on nuclear migration and rhizoid formation in germinating fern spores (Onoclea sensibilis). Protoplasma 109:295–316Google Scholar
  189. Voigt B, Timmers ACJ, Šamaj J, Müller J, Baluška F, Menzel D (2005) GFP-FABD2 fusion construct allows in vivo visualization of the dynamic actin cytoskeleton in all cells of Arabidopsis seedlings. Eur J Cell Biol 84:595–608PubMedGoogle Scholar
  190. Walker LM, Sack FD (1990) Amyloplasts as possible statoliths in gravitropic protonemata of the moss Ceratodon purpureus. Planta 181:71–77PubMedGoogle Scholar
  191. Waller F, Nick P (1997) Response of actin microfilaments during phytochrome-controlled growth of maize seedlings. Protoplasma 200:154–162Google Scholar
  192. Waller F, Riemann M, Nick P (2002) A role for actin-driven secretion in auxin-induced growth. Protoplasma 219:72–81PubMedGoogle Scholar
  193. Wang QY, Nick P (1998) The auxin response of actin is altered in the rice mutant Yin-Yang. Protoplasma 204:22–33PubMedGoogle Scholar
  194. Wang QY, Nick P (2001) Cold acclimation can induce microtubular cold stability in a manner distinct from abscisic acid. Plant Cell Physiol 42:999–1005PubMedGoogle Scholar
  195. Wang YS, Motes CM, Mohamalawari DR, Blancaflor EB (2004) Green fluorescent protein fusions to Arabidopsis fimbrin 1 for spatio-temporal imaging of F-actin dynamics in roots. Cell Motil Cytoskelet 59:79–93Google Scholar
  196. Wang X, Zhua L, Liu B, Wang C, Jin L, Zhao Q, Yuan M (2007) Arabidopsis microtubule-associated protein18 functions in directional cell growth by destabilizing cortical microtubules. Plant Cell 19:877–889PubMedGoogle Scholar
  197. Wasteneys GO (2004) Progress in understanding the role of microtubules in plant cells. Curr Opin Plant Biol 7:651–660PubMedGoogle Scholar
  198. Wasteneys GO, Galway ME (2003) Remodeling the cytoskeleton for growth and form: an overview with some new views. Annu Rev Plant Biol 54:691–722PubMedGoogle Scholar
  199. Whittington AT, Vugrek O, Wei KJ, Hasenbein NG, Sugimoto K, Rashbrooke MC, Wasteneys GO (2001) MOR1 is essential for organizing cortical microtubules in plants. Nature 411:610–613PubMedGoogle Scholar
  200. Wiesler B, Wang QY, Nick P (2002) The stability of cortical microtubules depends on their orientation. Plant J 32:1023–1032PubMedGoogle Scholar
  201. Wymer C, Wymer SA, Cosgrove DJ, Cyr RJ (1996) Plant cell growth responds to external forces and the response requires intact microtubules. Plant Physiol 110:425–430PubMedGoogle Scholar
  202. Xu T, Qu Z, Yang X, Qin X, Xiong J, Wang Y, Ren D, Liu G (2009) A cotton kinesin GhKCH2 interacts with both microtubules and microfilaments. Biochem J 421:171–180PubMedGoogle Scholar
  203. Yamamoto A, Hiraoka Y (2003) Cytoplasmic dynein in fungi: insights from nuclear migration. J Cell Sci 116:4501–4512PubMedGoogle Scholar
  204. Zandomeni K, Schopfer P (1994) Mechanosensory microtubule reorientation in the epidermis of maize coleoptiles subjected to bending stress. Protoplasma 182:96–101PubMedGoogle Scholar
  205. Zhou J, Wang B, Li Y, Wang Y, Zhu L (2007) Responses of Chrysanthemum cells to mechanical stimulation require intact microtubules and plasma membrane-cell wall adhesion. J Plant Growth Regul 26:55–68Google Scholar
  206. Zimmermann W (1965) Die Telomtheorie. Fischer, StuttgartGoogle Scholar
  207. Zimmermann S, Nürnberger T, Frachisse JM, Wirtz W, Guern J, Hedrich R, Scheel D (1997) Receptor-mediated activation of a plant Ca2+-permeable ion channel involved in pathogen defense. Proc Natl Acad Sci USA 94:2751–2755PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2011

Authors and Affiliations

  1. 1.Botanical Institute and Center of Functional NanostructuresKarlsruhe Institute of TechnologyKarlsruheGermany

Personalised recommendations