Regulation Of Root Hair Tip Growth: Can Mitogen-Activated Protein Kinases Be Taken Into Account?

  • Miroslav OveČka
  • Irene K. Lichtscheidl
  • FrantiŠek BaluŠka
  • Jozef Šamaj
  • Dieter Volkmann
  • Heribert Hirt
Conference paper
Part of the NATO Science for Peace and Security Series C: Environmental Security book series (NAPSC)

Plant growth and development are complex processes modulated by multi-level regulation mechanisms that depend on both internal and external signals. Such signals with the capacity to alter the morphogenesis of plant cells are perceived at the cellular level. Based on mitogen-activated protein kinase (MAPK) cascades, signalling of diverse stress-related factors is responsible for the generation of cell- and tissue-specific responses, and can be expected to participate also in the signal-mediated growth of plant cells, like tip growth of root hairs. Investigating stress-induced MAPKs in growing root hairs revealed a new field of complexity in plant signalling networks, and thus, MAPKs supplemented the collection of tip growth-specific factors with putative regulatory functions. The emerging scenario appears to be more complex; MAPK signalling pathways can support the reorganization of root epidermal cells during formation of tip growing hairs, but can also participate in the harmony of root hair tip growth with the changing environment.

Keywords

Biotic and abiotic stresses MAPKs plant development root hairs signal transduction SIMK tip growth 

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References

  1. 1.
    J. S. Parker, A. C. Cavell, L. Dolan, K. Roberts and C. S. Grierson, Genetic interactions during root hair morphogenesis in Arabidopsis, Plant Cell 12, 1961–1974 (2000).PubMedCrossRefGoogle Scholar
  2. 2.
    C. S. Grierson, J. S. Parker and A. C. Kemp, Arabidopsis genes with roles in root hair development, J. Plant Nutr. Soil. Sci. 164, 131–140 (2001).CrossRefGoogle Scholar
  3. 3.
    C. Grierson and J. Schiefelbein, Root hairs. In: The Arabidopsis Book, edited by C. R. Somerville and E. M. Meyerowitz (Rockville, Maryland, American Society of Plant Biologists), aspb.org/publications/arabidopsis/ doi: 10.1199/tab.0060, pp. 1–22 (2002).Google Scholar
  4. 4.
    J. Šamaj, M. OveČka, A. Hlavačka, F. Lecourieux, I. Meskiene, I. Lichtscheidl, P.Lenart, J. Salaj, D. Volkmann, L. Bogre, F. Baluska and H. Hirt, Involvement of the mitogen-activated protein kinase SIMK in regulation of root hair tip growth, EMBO J.21, 3296–3306 (2002).PubMedCrossRefGoogle Scholar
  5. 5.
    L. Bögre, I. Meskiene, E. Heberle-Bors and H. Hirt, Stressing the role of MAP kinases in mitogenic stimulation, Plant Mol. Biol. 43, 705–718 (2000).PubMedCrossRefGoogle Scholar
  6. 6.
    P. Zarzov, C. Mazzoni and C. Mann, The SLT2 (MPK1) MAP kinase is activated during periods of polarized cell growth in yeast, EMBO J. 15, 83–91 (1996).PubMedGoogle Scholar
  7. 7.
    T. Matsumoto, K. Yokote, K. Tamura, M. Takemoto, H. Ueno, Y. Saito and S. Mori, Platelet-derived growth factor activates p38 mitogen-activated protein kinase through a Ras-dependent pathway that is important for actin reorganization and cell migration, J.Biol. Chem. 274, 13954–13960 (1999).PubMedCrossRefGoogle Scholar
  8. 8.
    G. Jürgens, Cell division and morphogenesis in angiosperm embryogenesis, Seminars Cell Dev. Biol. 7, 867–872 (1996).CrossRefGoogle Scholar
  9. 9.
    B. Scheres, H. Wolkenfelt, V. Willemsen, M. Terlouw, E. Lawson, C. Dean and P.Weisbeek, Embryonic origin of the Arabidopsis primary root and root meristem initials,Development 120, 2475–2487 (1994).Google Scholar
  10. 10.
    W. F. Sheridan, Genes and embryo morphogenesis in Angiosperms, Dev. Gen. 16, 291–297 (1995).CrossRefGoogle Scholar
  11. 11.
    G. Jürgens, Axis formation in plant embryogenesis: cues and clues, Cell 81, 467–470(1995).PubMedCrossRefGoogle Scholar
  12. 12.
    L. Dolan and K. Roberts, Plant development: pulled up by the roots, Curr. Opin. Genet.Dev. 5, 432–438 (1995).PubMedCrossRefGoogle Scholar
  13. 13.
    F. Baluška, Š. Kubica and M. Hauskrecht, Postmitotic ‘isodiametric’ cell growth in the maize root apex, Planta 181, 269–274 (1990).CrossRefGoogle Scholar
  14. 14.
    F. Baluška, D. Volkmann and P. W. Barlow, Specialized zones of development in roots: view from the cellular level, Plant Physiol. 112, 3–4 (1996).PubMedGoogle Scholar
  15. 15.
    H. Ishikawa and M. L. Evans, The role of the distal elongation zone in the response of maize roots to auxin and gravity, Plant Physiol. 102, 1203–1210 (1993).PubMedGoogle Scholar
  16. 16.
    L. Dolan, K. Janmaat, V. Willemsen, P. Linstead, S. Poethig, K. Roberts and B. Scheres,Cellular organisation of the Arabidopsis thaliana root, Development 119, 71–84 (1993).PubMedGoogle Scholar
  17. 17.
    L. Dolan, C. M. Duckett, C. Grierson, P. Linstead, K. Schneider, E. Lawson, C. Dean, S.Poethig and K. Roberts, Clonal relationships and cell patterning in the root epidermis of Arabidopsis, Development 120, 2465–2474 (1994).Google Scholar
  18. 18.
    Y. Lin and J. Schiefelbein, Embryonic control of epidermal cell patterning in the root and hypocotyl of Arabidopsis, Development 128, 3697–3705 (2001).PubMedGoogle Scholar
  19. 19.
    E. D. L. Schmidt, A. J. De Jong and S. C. De Vries, Signal molecules involved in plant embryogenesis, Plant Mol. Biol. 26, 1305–1313 (1994).PubMedCrossRefGoogle Scholar
  20. 20.
    S. Hake and B. R. Char, Cell-cell interactions during plant development, Gen. Dev. 11,1087–1097 (1997).CrossRefGoogle Scholar
  21. 21.
    L. Dolan, Pattern in the root epidermis: an interplay of diffusible signals and cellular geometry, Ann. Bot. 77, 547–553 (1996).CrossRefGoogle Scholar
  22. 22.
    F. Berger, J. Haselhoff, J. Schiefelbein and L. Dolan, Positional information in root epidermis is defined during embryogenesis and acts in domains with strict boundaries,Curr. Biol. 8, 421–430 (1998).PubMedCrossRefGoogle Scholar
  23. 23.
    F. Baluška, J. Šamaj and D. Volkmann, Proteins reacting with cadherin and catenin antibodies are present in maize showing tissue-, domain-, and development-specific associations with ER membranes and actin microfilaments in root cells, Protoplasma 206, 174–187 (1999).CrossRefGoogle Scholar
  24. 24.
    F. BaluŠka, D. Volkmann and P. W. Barlow, Actin-based domains of the ‘cell periphery complex’ and their associations with polarized ‘cell bodies’ in higher plants, Plant Biol.2, 253–267 (2000).CrossRefGoogle Scholar
  25. 25.
    K. Roberts, The plant extracellular matrix: in a new expansive mood, Curr. Opin. Cell Biol. 6, 688–694 (1994).PubMedCrossRefGoogle Scholar
  26. 26.
    C. Martin, K. Bhatt and K. Baumann, Shaping in plant cells, Curr. Opin. Plant Biol. 4,540–549 (2001).PubMedCrossRefGoogle Scholar
  27. 27.
    K. Vissenberg, S. C. Fry and J.-P. Verbelen, Root hair initiation is coupled to a highly localized increase of xyloglucan endotransglycosylase action in Arabidopsis roots, Plant Physiol. 127, 1125–1135 (2001).PubMedCrossRefGoogle Scholar
  28. 28.
    F. BaluŠka, J. Salaj, J. Mathur, M. Braun, F. Jasper, J. Šamaj, N.-H. Chua, P. W. Barlow and D. Volkmann, Root hair formation: F-actin-dependent tip growth is initiated by local assembly of profilin-supported F-actin meshworks accumulated within expansin-enriched bulges, Dev. Biol. 227, 618–632 (2000).PubMedCrossRefGoogle Scholar
  29. 29.
    T. N. Bibikova, T. Jacob, I. Dahse and S. Gilroy, Localized changes in apoplastic and cytoplasmic pH are associated with root hair development in Arabidopsis thaliana,Development 125, 2925–2934 (1998).PubMedGoogle Scholar
  30. 30.
    D. J. Cosgrove, Plant cell enlargement and the action of expansins, BioEssays 18, 533–540 (1996).PubMedCrossRefGoogle Scholar
  31. 31.
    M. Čiamporová, K. Dekánková, Z. Hanáčková, P. Peters, M. Ovečka and F. Baluška,Structural aspects of bulge formation during root hair initiation, Plant Soil 255, 1–7(2003).CrossRefGoogle Scholar
  32. 32.
    O. Šamajová, J. Šamaj, D. Volkmann and H. Edelmann, Occurrence of osmiophilic particles is correlated to elongation growth of higher plants. Protoplasma 202, 185–191 (1998).CrossRefGoogle Scholar
  33. 33.
    J. Šamaj, M. Braun, F. Baluška, H.-J. Ensikat, Y. Tsumuraya and D. Volkmann, Specific localization of arabinogalactan-protein epitopes at the surface of maize root hairs, Plant Cell Physiol. 40, 874–883 (1999).Google Scholar
  34. 34.
    B. Favery, E. Ryan, J. Foreman, P. Linstead, K. Boudonck, M. Steer, P. Shaw and L.Dolan, KOJAK encodes a cellulose synthase-like protein required for root hair cellmorphogenesis in Arabidopsis, Gen. Dev. 15, 79–89 (2001).CrossRefGoogle Scholar
  35. 35.
    M. Bucher, S. Brunner, P. Zimmermann, G. I. Zardi, N. Amrhein, L. Willmitzer and J.W. Riesmeier, The Expression of an extensin-like protein correlates with cellular tip growth in tomato, Plant Physiol. 128, 911–923 (2002).PubMedCrossRefGoogle Scholar
  36. 36.
    C. Bernhardt and M. L. Tierney, Expression of AtPRP3, a proline-rich structural cell wall protein from Arabidopsis, is regulated by cell-type-specific developmental pathways involved in root hair formation, Plant Physiol. 122, 705–714 (2000).PubMedCrossRefGoogle Scholar
  37. 37.
    N. Baumberger, C. Ringli and B. Keller, The chimeric leucine-rich repeat/extensin cell wall protein LRX1 is required for root hair morphogenesis in Arabidopsis thaliana, Gen.Dev. 15, 1128–1139 (2001).CrossRefGoogle Scholar
  38. 38.
    F. BaluŠka, J. S. Parker and P. W. Barlow, Specific patterns of cortical and endoplasmic microtubules associated with cell growth and tissue differentiation in roots of maize (Zeamays L.), J. Cell Sci. 103, 191–200 (1992).Google Scholar
  39. 39.
    P. K. Hepler, A. L. Cleary, B. E. S. Gunning, P. Wadsworth, G. O. Wasteneys and D. H.Zhang, Cytoskeletal dynamics in living plant cells, Cell Biol. Int. 17, 127–142 (1993).CrossRefGoogle Scholar
  40. 40.
    H. Shibaoka and R. Nagai, The plant cytoskeleton, Curr. Opin. Cell Biol. 6, 10–15 (1994).PubMedCrossRefGoogle Scholar
  41. 41.
    F. Baluška, S. Vitha, P. W. Barlow and D. Volkmann, 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, 113–121 (1997).PubMedGoogle Scholar
  42. 42.
    D. D. Miller, N. C. A. de Ruijter, T. Bisseling and A. M. C. Emons, The role of actin in root hair morphogenesis: studies with lipochito-oligosaccharide as a growth stimulator and cytochalasin as an actin perturbing drug, Plant J. 17, 141–154 (1999).CrossRefGoogle Scholar
  43. 43.
    T. Ketelaar, N. C. A. de Ruijter and A. M. C. Emons, Unstable F-actin specifies the area and microtubule direction of cell expansion in Arabidopsis root hairs, Plant Cell 15,285–292 (2003).PubMedCrossRefGoogle Scholar
  44. 44.
    B. Voigt, A. C. Timmers, J. Šamaj, J. Müller, F. Baluška and D. Menzel, GFP-FABD2 fusion construct allows in vivo visualization of the dynamic actin cytoskeleton in all cells of Arabidopsis seedlings, Eur. J. Cell Biol. 84, 595–608 (2005).PubMedCrossRefGoogle Scholar
  45. 45.
    M. Braun, F. Baluška, M. von Witsch and D. Menzel, Redistribution of actin, profilin and phosphatidylinositol-4,5-bisphosphate (PIP2) in growing and maturing root hairs,Planta 209, 435–443 (1999).PubMedCrossRefGoogle Scholar
  46. 46.
    F. Baluška, J. Jásik, H. G. Edelmann, T. Salajová and D. Volkmann, Latrunculin B induced plant dwarfism: plant cell elongation is F-actin dependent, Dev. Biol. 231, 113–124 (2001).PubMedCrossRefGoogle Scholar
  47. 47.
    B. Voigt, A. C. Timmers, J. Šamaj, A. Hlavačka, T. Ueda, M. Preuss, E. Nielsen, J. Mathur,N. Emans, H. Stenmark, A. Nakano, F. Baluška and D. Menzel, Actin-based motility of endosomes is linked to the polar tip growth of root hairs, Eur. J. Cell Biol. 84, 609–621 (2005).PubMedCrossRefGoogle Scholar
  48. 48.
    T. Ketelaar, C. Faivre-Moskalenko, J. J. Esseling, N. C. A. de Ruijter, C. S. Grierson, M.Dogterom and A. M. C. Emons, Positioning of nuclei in Arabidopsis root hairs: an actin-regulated process of tip growth, Plant Cell 14, 2941–2955 (2002).PubMedCrossRefGoogle Scholar
  49. 49.
    A. M. C. Emons: the cytoskeleton and secretory vesicles in root hairs of Equisetum and Limnobium and cytoplasmic streaming in root hairs of Equisetum, Ann. Bot. 60, 625–632 (1987).Google Scholar
  50. 50.
    C. W. Lloyd, K. J. Pearce, D. J. Rawlins, R. W. Ridge and P. J. Shaw, Endoplasmic microtubules connect the advancing nucleus to the tip of legume root hairs, but F-actin is involved in basipetal migration, Cell Motil. Cytoskelet. 8, 27–36 (1987).CrossRefGoogle Scholar
  51. 51.
    B. J. Sieberer, A. C. J. Timmers, F. G. P. Lhuissier and A. M. C. Emons, Endoplasmic microtubules configure the subapical cytoplasm and are required for fast growth of Medicago truncatula root hairs, Plant Physiol. 130, 977–988 (2002).PubMedCrossRefGoogle Scholar
  52. 52.
    A. C. Timmers, P. Vallotton, C. Heym and D. Menzel, Microtubule dynamics in root hairs of Medicago truncatula, Eur. J. Cell Biol. 86, 69–83 (2007).PubMedCrossRefGoogle Scholar
  53. 53.
    T. N. Bibikova, E. B. Blancaflor and S. Gilroy, Microtubules regulate tip growth and orientation of root hairs of Arabidopsis thaliana, Plant J. 17, 657–665 (1999).PubMedCrossRefGoogle Scholar
  54. 54.
    A. T. Whittington, O. Vugrek, K. J. Wei, N. G. Hasenbein, K. Sugimoto, M. C.Rashbrooke and G. O. Wasteneys, MOR1 is essential for organizing cortical microtubules in plants, Nature 411, 610–613 (2001).PubMedCrossRefGoogle Scholar
  55. 55.
    C. Ringli, N. Baumberger, A. Diet, B. Frey and B. Keller, ACTIN2 is essential for bulge site selection and tip growth during root hair development of Arabidopsis, Plant Physiol.129, 1464–1472 (2002).PubMedCrossRefGoogle Scholar
  56. 56.
    M. A. Jones, M. J. Raymond and N. Smirnoff, Analysis of the root-hair morphogenesis transcriptome reveals the molecular identity of six genes with roles in root-hair development in Arabidopsis, Plant J. 45, 83–100 (2006).PubMedCrossRefGoogle Scholar
  57. 57.
    T. Sakai, H. van der Honing, M. Nishioka, Y. Uehara, M. Takahashi, N. Fujisawa, K.Saji, M. Seki, K. Shinozaki, M. A. Jones, N. Smirnoff, K. Okada and G. O. Wasteneys,Armadillo repeat-containing kinesins and a NIMA-related kinase are required for epidermal-cell morphogenesis in Arabidopsis, Plant J. 53, 157–171 (2008).PubMedCrossRefGoogle Scholar
  58. 58.
    E.-L. Ojangu, K. Järve, H. Paves and E. Truve, Arabidopsis thaliana myosin XIK is involved in root hair as well as trichome morphogenesis on stems and leaves,Protoplasma 230, 193ä202 (2007).PubMedCrossRefGoogle Scholar
  59. 59.
    J. Mathur, N. Mathur, V. Kirik, B. Kernebeck, B. P. Srinivas and M. Hülskamp,Arabidopsis CROOKED encodes for the smallest subunit of the ARP2/3 complex and controls cell shape by region specific fine F-actin formation, Development 130, 3137–3146 (2003).PubMedCrossRefGoogle Scholar
  60. 60.
    M. Ovečka, I. Lang, F. Baluška, A. Ismail, P. Illéš and I. K. Lichtscheidl, Endocytosis and vesicle trafficking during tip growth of root hairs, Protoplasma 226, 39–54 (2005).PubMedCrossRefGoogle Scholar
  61. 61.
    S. L. Shaw, J. Dumais and S. R. Long, Cell surface expansion in polarly growing root hairs of Medicago truncatula,Plant Physiol. 124, 959–969 (2000).PubMedCrossRefGoogle Scholar
  62. 62.
    J. Schiefelbein, A. Shipley and P. Rowse, Calcium influx at the tips of growing root-hair cells of Arabidopsis thaliana, Planta 187, 455–459 (1992).CrossRefGoogle Scholar
  63. 63.
    A. Very and J. M. Davies, Hyperpolarization — activated calcium channels at the tip of Arabidopsis root hairs, Proc. Natl. Acad. Sci. USA 97, 9801–9806 (2000).PubMedCrossRefGoogle Scholar
  64. 64.
    T. N. Bibikova, A. Zhigilei and S. Gilroy, Root hair growth in Arabidopsis thaliana is directed by calcium and an endogenous polarity, Planta 203, 495–505 (1997).PubMedCrossRefGoogle Scholar
  65. 65.
    C. Wymer, T. Bibikova and S. Gilroy, Cytoplasmic free calcium distributions during the development of root hairs of Arabidopsis thaliana, Plant J. 12, 427–439 (1997).PubMedCrossRefGoogle Scholar
  66. 66.
    J. Foreman, V. Demidchik, J. H. F. Bothwell, P. Mylona, H. Miedema, M. Angel Torresk, P. Linstead, S. Costa, C. Brownlee, J. D. G. Jonesk, J. M. Davies and L. Dolan,Reactive oxygen species produced by NADPH oxidase regulate plant cell growth,Nature 422, 442–446 (2003).PubMedCrossRefGoogle Scholar
  67. 67.
    V. Demidchik, V. S. Shabala and J. M. Davies, Spatial variation in H2O2 response of Arabidopsis thaliana root epidermal Ca2þ flux and plasma membrane Ca2þ channels,Plant J. 49, 377–386 (2007).PubMedCrossRefGoogle Scholar
  68. 68.
    S. Gilroy and D. L. Jones, Through form to function: root hair development and nutrient uptake, Trends Plant Sci. 5, 56–60 (2000).PubMedCrossRefGoogle Scholar
  69. 69.
    R. Sánchez-Fernández, M. Fricker, L. B. Corben, N. S. White, N. Sheard, C. J. Leaver,M. Van Montagu, D. Inzé and M. J. May, Cell proliferation and hair tip growth in the Arabidopsis root are under mechanistically different forms of redox control, Proc. Natl.Acad. Sci. USA 94, 2745–2750 (1997).PubMedCrossRefGoogle Scholar
  70. 70.
    T. Bates and J. Lynch, Stimulation of root hair elongation in Arabidopsis thaliana by low hosphorous availability, Plant Cell Environ. 19, 529–538 (1996).CrossRefGoogle Scholar
  71. 71.
    Z. Ma, T. C. Walk, A. Marcus and J. P. Lynch, Morphological synergism in root hair length, density, initiation and geometry for phosphorus acquisition in Arabidopsis thaliana: a modeling approach, Plant Soil 236, 221–235 (2001).CrossRefGoogle Scholar
  72. 72.
    A. Jungk, Root hairs and the acquisition of plant nutrients from soil, J. Plant Nutr. SoilSci. 164, 121–129 (2001).CrossRefGoogle Scholar
  73. 73.
    R. Shin, R. H. Berg and D. P. Schachtman, Reactive oxygen species and root hairs in Arabidopsis root response to nitrogen, phosphorus and potassium deficiency, Plant Cell Physiol. 46, 1350–1357 (2005).PubMedCrossRefGoogle Scholar
  74. 74.
    S. Rigas, G. Debrosses, K. Haralampidis, F. Vicente-Agullo, K. A. Feldmann, A.Grabov, L. Dolan and P. Hatzopoulos, TRH1 encodes a potassium transporter required for tip growth in Arabidopsis root hairs, Plant Cell 13, 139–151 (2001).PubMedCrossRefGoogle Scholar
  75. 75.
    V. Vicente-Agullo, S. Rigas, G. Desbrosses, L. Dolan, P. Hatzopoulos and A. Grabov,Potassium carrier TRH1 is required for auxin transport in Arabidopsis roots, Plant J. 40,523–535 (2004).PubMedCrossRefGoogle Scholar
  76. 76.
    N. Geldner, J. Friml, Y.-D. Stierhof, G. Jürgens and K. Palme, PIN1 cycling and vesicle trafficking, Nature 413, 425–428 (2001).PubMedCrossRefGoogle Scholar
  77. 77.
    P. Nagpal, L. M. Walker, J. S. Young, A. Sonawala, C. Timpte, M. Estelle and J. W.Reed, AXR2 encodes a member of the Aux/IAA protein family, Plant Physiol. 123, 563–573 (2000).PubMedCrossRefGoogle Scholar
  78. 78.
    M. Tanimoto, K. Roberts and L. Dolan, Ethylene is a positive regulator of root hair development in Arabidopsis thaliana, Plant J. 8, 943–948 (1995).PubMedGoogle Scholar
  79. 79.
    J. D. Masucci and J. W. Schiefelbein, Hormones act downstream of TTG and GL2 to promote root hair outgrowth during epidermis development in the Arabidopsis root,Plant Cell 8, 1505–1517 (1996).PubMedCrossRefGoogle Scholar
  80. 80.
    J. D. Masucci and J. W. Schiefelbein, The rhd6 mutation of Arabidopsis thaliana alters root-hair initiation through an auxin- and ethylene-associated process, Plant Physiol.106, 1335–1346 (1994).PubMedGoogle Scholar
  81. 81.
    R. J. Pitts, A. Cernac and M. Estelle, Auxin end ethylene promote root hair elongation in Arabidopsis, Plant J. 16, 553–560 (1998).PubMedCrossRefGoogle Scholar
  82. 82.
    A. Rahman, S. Hosokawa, Y. Oono, T. Amakawa, N. Goto and S. Tsurumi, Auxin and ethylene response interactions during Arabidopsis root hair development dissected by auxin influx modulators, Plant Physiol. 130, 1908–1917 (2002).PubMedCrossRefGoogle Scholar
  83. 83.
    S. K. Soropy and M. Munshi, Protein kinases and phosphatases and their role in cellular signaling in plants, Crit. Rev. Plant Sci. 17, 245–318 (1998).CrossRefGoogle Scholar
  84. 84.
    S. G. Møller and N.-H. Chua, Interaction and intersections of plant signaling pathways,J. Mol. Biol. 293, 219–234 (1999).PubMedCrossRefGoogle Scholar
  85. 85.
    R. Seger and E. G. Krebs, The MAPK signaling cascade,FASEB J. 9, 726–735 (1995).PubMedGoogle Scholar
  86. 86.
    M. J. Robinson and M. H. Cobb, Mitogen-activated protein kinase pathways, Curr. Opin.Cell Biol. 9, 180–186 (1997).PubMedCrossRefGoogle Scholar
  87. 87.
    T. P. Garrington and G. L. Johnson, Organization and regulation of mitogen-activated protein kinase signaling pathway, Curr. Opin. Cell Biol. 11, 211–218 (1999).PubMedCrossRefGoogle Scholar
  88. 88.
    A. J. Whitmarsh and R. Davis, Structural organization of MAP kinase signaling modules by scaffold proteins in yeast and mammals, Trends Biochem. Sci. 23, 481–485 (1998).PubMedCrossRefGoogle Scholar
  89. 89.
    K. Harris, R. E. Lamson, B. Nelson, T. R. Hughes, M. J. Marton, C. J. Roberts, C. Boone and P. M. Pryciak, Role of scaffolds in MAP kinase pathway specificity revealed by custom design of pathway-dedicated signaling proteins, Curr. Biol. 11, 1815–1824(2001).PubMedCrossRefGoogle Scholar
  90. 90.
    S. Luan, Protein phosphatases and signaling cascades in higher plants, Trends Plant Sci.3, 271–275 (1998).CrossRefGoogle Scholar
  91. 91.
    G. C. Brown, J. B. Hoek and B. N. Kholodenko, Why do protein kinase cascades have more then one level? Trends Biochem. Sci. 22, 288 (1997).PubMedCrossRefGoogle Scholar
  92. 92.
    P. Cohen, The structure and regulation of protein phosphatases, Annu. Rev. Biochem.58, 453–508 (1989).PubMedCrossRefGoogle Scholar
  93. 93.
    A. J. Waskiewicz and J. A. Cooper, Mitogen and stress response pathways: MAP kinase cascades and phosphatase regulation in mammals and yeast, Curr. Opin. Cell Biol. 7,798–805 (1995).PubMedCrossRefGoogle Scholar
  94. 94.
    N. Inagaki, M. Ito, T. Nakano and M. Inagaki, Spatiotemporal distribution of protein kinase and phosphatase activities, Trends Biochem. Sci. 19, 448–452 (1994).PubMedCrossRefGoogle Scholar
  95. 95.
    S. M. Keyse, The role of protein phosphatases in the regulation of mitogen and stress-activated protein kinases, Free Rad. Res. 31, 341–349 (1999).CrossRefGoogle Scholar
  96. 96.
    L. A. Tibbles and J. R. Woodgett, The stress-activated protein kinase pathways, Cell.Molec. Life Sci. 55, 1230–1254 (1999).PubMedCrossRefGoogle Scholar
  97. 97.
    H. Hirt, Multiple roles of MAP kinases in plant signal transduction, Trends Plant Sci. 2,11–15 (1997).CrossRefGoogle Scholar
  98. 98.
    M. Wrzaczek and H. Hirt, Plant MAP kinase pathways: how many and what for? Biol.Cell 93, 81–87 (2001).PubMedCrossRefGoogle Scholar
  99. 99.
    K. Ichimura, K. Shinozaki, G. Tena, J. Sheen, Y. Henry, A. Champion, M. Kreis, S.Zhang, H. Hirt, C. Wilson, E. Heberle-Bors, B. E. Ellis, P. C. Morris, R. W. Innes, J. R.Ecker, D. Scheel, D. F. Klessig, Y. Machida, J. Mundy, Y. Ohashi and J. C. Walker,Mitogen-activated protein kinase cascades in plants: a new nomenclature, Trends Plant Sci. 7, 301–308 (2002).CrossRefGoogle Scholar
  100. 100.
    L.-P. Hamel, M.-C. Nicole, S. Sritubtim, M.-J. Morency, M. Ellis, J. Ehlting, N.Beaudoin, B. Barbazuk, D. Klessig, J. Lee, G. Martin, J. Mundy, Y. Ohashi, D. Scheel,J. Sheen, T. Xing, S. Zhang, A. Seguin and B. E. Ellis, Ancient signals: comparative genomics of plant MAPK and MAPKK gene families, Trends Plant Sci. 11, 192–198(2006).PubMedCrossRefGoogle Scholar
  101. 101.
    H. Hirt, Connecting oxidative stress, auxin, and cell cycle regulation through a plant mitogen-activated protein kinase pathwayProc. Natl. Acad. Sci. USA 97, 2405–2407(2000).PubMedCrossRefGoogle Scholar
  102. 102.
    T. Asai, G. Tena, J. Plotnikova, M. R. Willmann, W.-L. Chiu, L. Gomez-Gomez, T.Boller, F. M. Ausubel and J. Sheen, MAP kinase signalling cascade inArabidopsis innate immunityNature 415, 977–983 (2002).PubMedCrossRefGoogle Scholar
  103. 103.
    T. S. Nühse, S. C. Peck, H. Hirt and T. Boller, Microbial elicitors induce activation and dual phosphorylation of theArabidopsis thaliana MAPK 6J. Biol. Chem. 275, 7521–7526 (2000).PubMedCrossRefGoogle Scholar
  104. 104.
    T. Mészáros, A. Helfer, E. Hatzimasoura, Z. Magyar, L. Serazetdinova, G. Rios, V.Bardóczy, M. Teige, C. Koncz, S. Peck and L. Bögre, TheArabidopsis MAP kinase kinase MKK1 participates in defence responses to the bacterial elicitor flagellinPlant J. 48, 485–498 (2006).PubMedCrossRefGoogle Scholar
  105. 105.
    M. C. Suarez-Rodriguez, L. Adams-Phillips, Y. Liu, H. Wang, S. H. Su, P. J. Jester, S.Zhang, A. F. Bent and P. J. Krysan, MEKK1 is required for flg22-induced MPK4activation inArabidopsis plantsPlant Physiol. 143, 661–669 (2007).PubMedCrossRefGoogle Scholar
  106. 106.
    H. Nakagami, H. Soukupová, A. Schikora, V. Žárský and H. Hirt, A mitogen-activated protein kinase kinase kinase mediates reactive oxygen species homeostasis inArabidopsis J. Biol. Chem. 281, 38697–38704 (2006).PubMedCrossRefGoogle Scholar
  107. 107.
    A. Djamei, A. Pitzschke, H. Nakagami, I. Rajh and H. Hirt, Trojan horse strategy inAgrobacterium transformation: abusing MAPK defense signalingScience 318, 453–456 (2007).PubMedCrossRefGoogle Scholar
  108. 108.
    R. Dóczi, G. Brader, A. Pettkó-Szandtner, I. Rajh, A. Djamei, A. Pitzschke, M. Teige and H. Hirt, TheArabidopsis mitogen-activated protein kinase kinase MKK3 is upstream of group C mitogen-activated protein kinases and participates in pathogen signallingPlant Cell 19, 3266–3279 (2007).PubMedCrossRefGoogle Scholar
  109. 109.
    M. Fernandez-Pascual, M. M. Lucas, M. R. de Felipe, L. Boscá, H. Hirt and M. P.Golvano, Involvement of mitogen-activated protein kinases in the symbiosisBradyrhizobium—Lupinus J Exp. Bot. 57, 2735–2742 (2006).PubMedCrossRefGoogle Scholar
  110. 110.
    Y. Liu, S. Zhang and D. F. Klessig, Molecular cloning and characterization of a tobacco MAP Kinase Kinase that interacts with SIPKMolec. Plant Micr. Inter. 13, 118–124(2000).CrossRefGoogle Scholar
  111. 111.
    K.-Y. Yang, Y. Liu and S. Zhang, Activation of a mitogen-activated protein kinase pathway is involved in disease resistance in tobaccoProc. Natl. Acad. Sci. USA 98,741–746 (2001).PubMedCrossRefGoogle Scholar
  112. 112.
    C. Chang, S. F. Kwok, A. B. Bleecker and E. M. MeyerowitzArabidopsis ethylene-response gene ETR1: similarity of product to two-component regulatorsScience 262,539–544 (1993).PubMedCrossRefGoogle Scholar
  113. 113.
    J. Hua and E. M. Meyerowitz, Ethylene responses are negatively regulated by a receptor gene family inArabidopsis thaliana Cell 94, 261–271 (1998).PubMedCrossRefGoogle Scholar
  114. 114.
    J. J. Kieber, M. Rothenberg, G. Roman, K. A. Feldmann and J. R. Ecker, CTR1, a negative regulator of the ethylene response pathway inArabidopsis, encodes a member of the Raf family of protein kinasesCell 72, 427–441 (1993).PubMedCrossRefGoogle Scholar
  115. 115.
    O. Leyser, Auxin signalling: the beginning, the middle and the endCurr. Opin. Plant Biol. 4, 382–386 (2001).PubMedCrossRefGoogle Scholar
  116. 116.
    Y. Kovtun, W.-L. Chiu, W. Zeng and J. Sheen, Suppression of auxin signal transduction by a MAPK cascade in higher plantsNature 395, 716–720 (1998).PubMedCrossRefGoogle Scholar
  117. 117.
    Y. Kovtun, W. L. Chiu, G. Tena and J. Sheen, Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plantsProc. Natl. Acad. Sci. USA97, 2940–2945 (2000).PubMedCrossRefGoogle Scholar
  118. 118.
    R. Nishihama, M. Ishikawa, S. Araki, T. Soyano, T. Asada and Y. Machida, The NPK1 mitogen-activated protein kinase kinase kinase is a regulator of cell-plate formation in plant cytokinesisGen. Dev. 15, 352–363 (2001).CrossRefGoogle Scholar
  119. 119.
    R. Nishihama, T. Soyano, M. Ishikawa, S. Araki, H. Tanaka, T. Asada, K. Irie, M. Ito,M. Terada, H. Banno, Y. Yamazaki and Y. Machida, Expansion of the cell plate in plant cytokinesis requires a kinesin-like protein/MAPKKK complexCell 109, 87–99 (2002).PubMedCrossRefGoogle Scholar
  120. 120.
    P. J. Krysan, P. J. Jester, J. R. Gottwald and M. R. Sussman, AnArabidopsis mitogen-activated protein kinase kinase kinase gene family encodes essential positive regulators of cytokinesisPlant Cell 14, 1109–1120 (2002).PubMedCrossRefGoogle Scholar
  121. 121.
    L. Bögre, O. Calderini, P. Binarova, M. Mattauch, S. Till, S. Kiegerl, C. Jonak, C.Pollaschek, P. Barker, N. S. Huskisson, H. Hirt and E. Heberle-Bors, A MAP kinase is activated late in plant mitosis and becomes localised to the plane of cell divisionPlant Cell 11, 101–113 (1999).PubMedCrossRefGoogle Scholar
  122. 122.
    O. Calderini, L. Bögre, O. Vicente, P. Binarova, E. Heberle-Bors and C. Wilson, A cell cycle regulated MAP kinase with a possible role in cytokinesis in tobacco cellsJ. Cell Sci. 111, 3091–3100 (1998).PubMedGoogle Scholar
  123. 123.
    S. M. Bush and P. J. Krysan, Mutational evidence that theArabidopsis MAP kinase MPK6 is involved in anther, inflorescence, and embryo developmentJ. Exp. Bot. 58,2181–2191 (2007).PubMedCrossRefGoogle Scholar
  124. 124.
    Y. Dai, H. Wang, B. Li, J. Huang, X. Liu, Y. Zhou, Z. Mou and J. Lia, Increased expression of MAP KINASE KINASE7 causes deficiency in polar auxin transport and leads to plant architectural abnormality inArabidopsis Plant Cell 18, 308–320 (2006).PubMedCrossRefGoogle Scholar
  125. 125.
    W. Lukowitz, A. Roeder, D. Parmenter and C. Somerville, A MAPKK Kinase gene regulates extra-embryonic cell fate inArabidopsis Cell 116, 109–119 (2004).PubMedCrossRefGoogle Scholar
  126. 126.
    D. C. Bergmann, W. Lukowitz and C. R. Somerville: pattern controlled by a MAPKK kinaseScience 304, 1494–1497 (2004).PubMedCrossRefGoogle Scholar
  127. 127.
    H. Wang, N. Ngwenyama, Y. Liu, J. C. Walker and S. Zhang, Stomatal development and patterning are regulated by environmentally responsive mitogen-activated protein kinases inArabidopsis Plant Cell 19, 63–73 (2007).PubMedCrossRefGoogle Scholar
  128. 128.
    K. Zwerger and H. Hirt, Recent advances in plant MAP kinase signallingBiol Chem.382, 1123–1131 (2001).PubMedCrossRefGoogle Scholar
  129. 129.
    G. Tena, T. Asai, W.-L. Chiu and J. Sheen, Plant mitogen-activated protein kinase signaling cascadesCurr. Opin. Plant Biol. 4, 392–400 (2001).PubMedCrossRefGoogle Scholar
  130. 130.
    C. Jonak, L. Ökrész, L. Bögre and H. Hirt, Complexity, cross talk and integration of plant MAP kinase signallingCurr. Opin. Plant Biol. 5, 415–424 (2002).PubMedCrossRefGoogle Scholar
  131. 131.
    J. Šamaj, F. Baluška and H. Hirt, From signal to cell polarity: mitogen-activated protein kinases as sensors and effectors of cytoskeleton dynamicityJ. Exp. Bot. 55, 189–198(2004).PubMedCrossRefGoogle Scholar
  132. 132.
    H. Nakagami, A. Pitzschke and H. Hirt, Emerging MAP kinase pathways in plant stress signallingTrends Plant Sci. 10, 339–346 (2005).PubMedCrossRefGoogle Scholar
  133. 133.
    N. S. Mishra, R. Tuteja and N. Tuteja, Signaling through MAP kinase networks in plants.Arch. Biochem. Biophys. 452, 55–68 (2006).PubMedCrossRefGoogle Scholar
  134. 134.
    T. Zhang, Y. Liuc, T. Yanga, L. Zhanga, S. Xua, L. Xuea and L. Ana, Diverse signals converge at MAPK cascades in plantPlant Physiol. Biochem. 44, 274–283 (2006).PubMedCrossRefGoogle Scholar
  135. 135.
    T. Munnik, W. Ligterink, I. Meskiene, O. Calderini, J. Beyerly, A. Musgrave and H.Hirt, Distinct osmo-sensing protein kinase pathways are involved in signalling moderate and severe hyper-osmotic stressPlant J. 20, 381–388 (1999).PubMedCrossRefGoogle Scholar
  136. 136.
    S. Kiegerl, F. Cardinale, C. Siligan, A. Gross, E. Baudouin, A. Liwosz, S. Eklöf, S. Till,L. Bögre, H. Hirt and I. Meskiene, SIMKK, a mitogen-activated protein kinase (MAPK) kinase, is a specific activator of the salt stress—induced MAPK, SIMKPlant Cell 12, 2247–2258 (2000).PubMedCrossRefGoogle Scholar
  137. 137.
    I. E. Baudouin, A. Schweighofer, A. Liwosz, C. Jonak, P. L. Rodriguez, H.Jelinek and H. HirtJ. Biol. Chem. 278, 18945–18952 (2003).PubMedCrossRefGoogle Scholar
  138. 138.
    F. Cardinale, C. Jonak, W. Ligterink, K. Niehaus, T. Boller and H. Hirt, Differential activation of four specific MAPK pathways by distinct elicitorsJ. Biol. Chem. 275,36734–36740 (2000).PubMedCrossRefGoogle Scholar
  139. 139.
    F. Cardinale, I. Meskiene, F. Ouaked and H. Hirt, Convergence and divergence of stress-induced mitogen-activated protein kinase signaling pathways at the level of two distinct mitogen-activated protein kinase kinasesPlant Cell 14, 703–711 (2002).PubMedGoogle Scholar
  140. 140.
    K. Ichimura, T. Mizoguchi, R. Yoshida, T. Yuasa and K. Shinozaki, Various abiotic stresses rapidly activateArabidopsis MAP kinases AtMPK4 and AtMPK6Plant J. 24,655–665 (2000).PubMedCrossRefGoogle Scholar
  141. 141.
    M. Teige, E. Scheikl, T. Eulgem, R. Dóczi, K. Ichimura, K. Shinozaki, J. L. Dangl and H. Hirt, The MKK2 pathway mediates cold and salt stress signaling inArabidopsis,Molec. Cell 15, 141–152 (2004).PubMedCrossRefGoogle Scholar
  142. 142.
    C. Jonak, H. Nakagami and H. Hirt, Heavy metal stress. Activation of distinct mitogen-activated protein kinase pathways by copper and cadmiumPlant Physiol. 136, 3276–3283 (2004).PubMedCrossRefGoogle Scholar
  143. 143.
    C.-M. Yeh, P.-S. Chien and H.-J. Huang, Distinct signalling pathways for induction of MAP kinase activities by cadmium and copper in rice rootsJ. Exp. Bot. 58, 659–671(2007).PubMedCrossRefGoogle Scholar
  144. 144.
    F. Ouaked, W. Rozhon, D. Lecourieux and H. Hirt, A MAPK pathway mediates ethylene signaling in plantsEMBO J. 22, 1282–1288 (2003).PubMedCrossRefGoogle Scholar
  145. 145.
    F. Baluška, M. Ovečka and H. Hirt, Salt stress induced changes in amounts and localisation of the mitogen-activated protein kinase SIMK in alfalfa rootsProtoplasma 212, 262–267 (2000).CrossRefGoogle Scholar
  146. 146.
    C. Jonak, A. Páy, L. Bögre, H. Hirt and E. Heberle-Bors, The plant homoloque of MAP kinase is expressed in a cell cycle-dependent and organ-specific mannerPlant J. 3,611–617 (1993).PubMedCrossRefGoogle Scholar
  147. 147.
    J. Šamaj, M. Ovečka, A. Hlavačka, F. Lecourieux, I. Meskiene, I. Lichtscheidl, P.Lenart, J. Salaj, D. Volkmann, L. Bogre, F. BaluŠka and H. Hirt, Involvement of MAP kinase SIMK and actin cytoskeleton in the regulation of root hair tip growthCell Biol.Int. 27, 257–259 (2003).PubMedCrossRefGoogle Scholar
  148. 148.
    C. J. Staiger, B. C. Gibbon, D. R. Kovar and L. E. Zonia, Profilin and actin depolymerizing factor: modulators of actin organization in plantsTrends Plant Sci. 2,275–281 (1997).CrossRefGoogle Scholar
  149. 149.
    D. Didry, M.-F. Carlier and D. Pantaloni, Synergy between actin depolymerizing factor/cofilin and profilin in increasing actin filament turnoverJ. Biol. Chem. 273,25602–25611 (1998).PubMedCrossRefGoogle Scholar
  150. 150.
    K. Schlüter, B. M. Jockusch and M. Rothkegel, Profilins as regulators of actin dynamicsBiochim. Biophys. Acta 1359, 97–109 (1997).PubMedCrossRefGoogle Scholar
  151. 151.
    M.-F. Carlier, V. Laurent, J. Santolini, R. Melki, D. Didry, G.-X. Xia, Y. Hong, N.-H.Chua, and D. Pantaloni, Actin depolymerizing factor (ADF/cofilin) enhances the rate of filament turnover: implication in actin-based motilityJ. Cell Biol. 136, 1307–1323(1997).PubMedCrossRefGoogle Scholar
  152. 152.
    A. Wada, M. Fukuda, M. Mishima and E. Nishida, Nuclear export of actin: a novel mechanism regulating the subcellular localization of a major cytoskeletal proteinEMBO J. 17, 1635–1641 (1998).PubMedCrossRefGoogle Scholar
  153. 153.
    S. R. Clarke, C. J. Staiger, B. C. Gibbon and V. E. Franklin-Tong, A potential signaling role for profilin in pollen ofPapaver rhoeas Plant Cell 10, 967–979 (1998).PubMedCrossRefGoogle Scholar
  154. 154.
    C.-J. Jiang, A. G. Weeds and P. J. Hussey, The maize actin-depolymerizing factor,ZmADF3, redistributes to the growing tip of elongating root hairs and can be induced to translocate into the nucleus with actinPlant J. 12, 1035–1043 (1997).PubMedCrossRefGoogle Scholar
  155. 155.
    A. P. Smertenko, C.-J. Jiang, N. J. Simmons, A. G. Weeds, D. R. Davies and P. J.Hussey, Ser6 in the maize actin-depolymerizing factor, ZmADF3, is phosphorylated by a calcium-stimulated protein kinase and is essential for the control of functional activityPlant J. 14, 187–193 (1997).CrossRefGoogle Scholar
  156. 156.
    F. Ressad, D. Didry, G. X. Xia, Y. Hong, N.-H. Chua, D. Pantaloni and M. F. Carlier,Kinetic analysis of the interaction of actin-depolymerizing factor (ADF)/cofilin with G-and F-actins. Comparison of plant and human ADFs and effect of phosphorylationJ.Biol. Chem. 273, 20894–20902 (1998).PubMedCrossRefGoogle Scholar
  157. 157.
    M. L. Preuss, J. Serna, T. G. Falbel, S. Y. Bednarek and E. Nielsen, TheArabidopsisRab GTPase RabA4b localizes to the tips of growing root hair cellsPlant Cell 16,1589–1603 (2004).PubMedCrossRefGoogle Scholar
  158. 158.
    M. L. Preuss, A. J. Schmitz, J. M. Thole, H. K. S. Bonner, M. S. Otegui and E. Nielsen,A role for the RabA4b effector protein PI-4Kb1 in polarized expansion of root hair cells inArabidopsis thaliana J. Cell Biol. 172, 991–998 (2006).PubMedCrossRefGoogle Scholar
  159. 159.
    J. Xu and B. Scheres, Dissection ofArabidopsis ADP-RIBOSYLATION FACTOR 1function in epidermal cell polarityPlant Cell 17, 525–536 (2005).PubMedCrossRefGoogle Scholar
  160. 160.
    X.-F. Song, C.-Y. Yang, J. Liu and W.-C. Yang, RPA, a class II ARFGAP protein,activates ARF1 and U5 and plays a role in root hair development inArabidopsis Plant Physiol. 141, 966–976 (2006).PubMedCrossRefGoogle Scholar
  161. 161.
    M. A. Jones, J.-J. Shen, Y. Fu, H. Li, Z. Yang and C. S. Grierson, TheArabidopsisRop2 GTPase is a positive regulator of both root hair initiation and tip growthPlant Cell 14, 763–776 (2002).PubMedCrossRefGoogle Scholar
  162. 162.
    Z. L. Zheng and Z. Yang, The Rop GTPase switch turns on polar growth in pollen,Trends Plant Sci. 5, 298–303 (2000).PubMedCrossRefGoogle Scholar
  163. 163.
    Y. Fu, G. Wu and Z. Yang, Rop GTPase-dependent dynamics of tip-localised F-actin controls tip growth in pollen tubesJ. Cell Biol. 152, 1019–1032 (2001).PubMedCrossRefGoogle Scholar
  164. 164.
    Y. Fu and Z. Yang, Rop GTPase: a master switch of cell polarity developments in plantsTrends Plant Sci. 6, 545–547 (2001).PubMedCrossRefGoogle Scholar
  165. 165.
    A. J. Molendijk, F. Bischoff, C. S. V. Rajendrakumar, J. Friml, M. Braun, S. Gilroy and K. Palme:Arabidopsis thaliana Rop GTPases are localized to tips of root hairs and control polar growthEMBO J. 20, 2779–2788 (2001).PubMedCrossRefGoogle Scholar
  166. 166.
    R. J. Carol, S. Takeda, P. Linstead, M. C. Durrant, H. Kakesová, P. Derbyshire, S. Drea,V. Zárský and L. Dolan, RhoGDP dissociation inhibitor spatially regulates growth in root hair cellsNature 438, 1013–1016 (2005).PubMedCrossRefGoogle Scholar
  167. 167.
    A. Pitzschke and H. Hirt, Mitogen-activated protein kinases and reactive oxygen species signaling in plants.Plant Physiol. 141, 351–356 (2006).PubMedCrossRefGoogle Scholar
  168. 168.
    M. C. Rentel, D. Lecourieux, F. Ouaked, S. L. Usher, L. Petersen, H. Okamoto, H.Knight, S. C. Peck, C. S. Grierson, H. Hirt and M. R. Knight, OXI1 kinase is necessaryfor oxidative burst-mediated signalling inArabidopsis Nature 427, 858–861 (2004).PubMedCrossRefGoogle Scholar
  169. 169.
    C. Gapper and L. Dolan, Control of plant development by reactive oxygen species,Plant Physiol. 141, 341–345 (2006).PubMedCrossRefGoogle Scholar
  170. 170.
    R. G. Anthony, R. Henriques, A. Helfer, T. Mészáros, G. Rios, C. Testerink, T.Munnik, M. Deák, C. Koncz and L.Bögre, A protein kinase target of a PDK1 signallingpathway is involved in root hair growth inArabidopsis EMBO J. 23, 572–581 (2004).PubMedCrossRefGoogle Scholar
  171. 171.
    Y. Ohashi, A. Oka, R. Rodrigues-Pousada, M. Possenti, I. Ruberti, G. Morelli and T.Aoyama: modulation of phospholipid signaling by GLABRA2 in root-hair pattern formationScience 300, 1427–1430 (2003).PubMedCrossRefGoogle Scholar
  172. 172.
    S. H. Lee and H. T. Choa, PINOID positively regulates auxin efflux inArabidopsis root hair cells and tobacco cellsPlant Cell 18, 1604–1616 (2006).PubMedCrossRefGoogle Scholar
  173. 173.
    T. Oyama, Y. Shimura and K. Okada, The IRE gene encodes a protein kinase homologue and modulates root hair growth inArabidopsis Plant J. 30, 289–299(2002).PubMedCrossRefGoogle Scholar
  174. 174.
    H. Shi and J.-K. Zhu, SOS4, A pyridoxal kinase gene, is required for root hair development inArabidopsis Plant Physiol. 129, 585–593 (2002).PubMedCrossRefGoogle Scholar
  175. 175.
    R. D. Smith, J. E. Wilson, J. C. Walker and T. I. Baskin, Protein-phosphatase inhibitorsblock root hair growth and alter cortical cell shape ofArabidopsis rootsPlanta 194,516–524 (1994).CrossRefGoogle Scholar
  176. 176.
    S. Rousseau, F. Houle, J. Landry and J. Huot, p38 MAP kinase activation by vascular endothelial growth factor mediates actin reorganization and cell migration in human endotelial cellsOncogene 15, 2169–2177 (1997).PubMedCrossRefGoogle Scholar
  177. 177.
    C. Mazzoni, P. Zarzov, A. Rambourg and C. Mann, The SLT2 (MPK1) MAP kinase homolog is involved in polarized cell growth inSaccharomyces cerevisiae J. Cell Biol.123, 1821–1833 (1993).PubMedCrossRefGoogle Scholar
  178. 178.
    T. Roemer, L. Vallier, Y.-J. Sheu and M. Snyder, The Spa2-related protein, Sph1, is important for polarized growth in yeast.J. Cell Sci 111, 479–494 (1998).PubMedGoogle Scholar
  179. 179.
    S. K. Mahanty, Y. Wang, F. W. Farley and E. A. Elion, Nuclear shuttling of yeast scaffold Ste5 is required for its recruitment to the plasma membrane and activation of the mating MAPK cascadeCell 98, 501–512 (1999).PubMedCrossRefGoogle Scholar
  180. 180.
    Z. Changwei, X. Mingyong and W. Ranran, Afr1p has a role in regulating the localization of Mpk1p at the shmoo tip inSaccharomyces cerevisiae FEBS Letters 581,2670–2674 (2007).PubMedCrossRefGoogle Scholar
  181. 181.
    D. G. Drubin and W. J. Nelson, Origins of cell polarityCell 84, 335–344 (1996).PubMedCrossRefGoogle Scholar
  182. 182.
    D. Pruyne and A. Bretscher, Polarization of cell growth in yeast. I. Establishment and maintenance of polarity statesJ. Cell Sci. 113, 365–375 (2000).PubMedGoogle Scholar
  183. 183.
    M. Ziman, D. Preuss, J. Mulholland, J. O'Brien, D. Botstein and D. Johnson, Subcellular localization of Cdc42p, aSaccharomyces cerevisiae GTP-binding protein involved in the control of cell polarityMol. Biol. Cell 4, 1307–1316 (1993).PubMedGoogle Scholar
  184. 184.
    B. L. Drees, B. Sundin, E. Brazeau, J. P. Caviston, G.-C. Chen, W. Guo, K. G. Kozminski, M. W. Lau, J. J. Moskow, A. Tong, L. R. Schenkman, A. McKenzie, P. Brennwald, M. Longtine, E. Bi, C. Chan, P. Novick, C. Boone, J. R. Pringle, T. N,Davis, S. Fields and D. G. Drubin, A protein interaction map for cell polarity developmentJ. Cell Biol. 154, 549–576 (2001).PubMedCrossRefGoogle Scholar
  185. 185.
    S. Halpain, Actin in a supporting roleNature Neurosci. 6, 101–102 (2003).PubMedCrossRefGoogle Scholar
  186. 186.
    S. Sankaranarayanan, P. P. Alturi and T. A. Ryan, Actin has a molecular scaffolding, not propulsive, role in presynaptic functionNature Neurosci. 6, 127–135 (2003).PubMedCrossRefGoogle Scholar
  187. 187.
    P. S. McPherson, B. K. Kay and N. K. Hussain, Signaling on the endocytic pathway,Traffic 2, 375–384 (2001).PubMedCrossRefGoogle Scholar
  188. 188.
    N. Geldner, D. L. Hyman, X. Wang, K. Schumacher and J. Chory, Endosomal signaling of plant steroid receptor kinase BRI1Gen. Dev. 21, 1598–1602 (2007).CrossRefGoogle Scholar
  189. 189.
    A. J. Ingram, L. James, L. Cai, K. Thai, H. Ly and J. W. Scholey, NO inhibits stretch-induced MAPK activity by cytoskeletal disruptionJ. Biol. Chem. 275, 40301–40306(2000).PubMedCrossRefGoogle Scholar
  190. 190.
    Y. Kamada, U. S. Jung, J. Piotrowski and D. E. Levin, The protein kinase C-activated MAP kinase pathway ofSaccharomyces cerevisiae mediates a novel aspect of the heath shock responseGen. Dev. 9, 1559–1571 (1995).CrossRefGoogle Scholar
  191. 191.
    A. Kell and R. W. Glaser, On the mechanical and dynamic properties of plant cell membranes: their role in growth, direct gene transfer and protoplast fusionJ. Theor.Biol. 160, 41–62 (1993).CrossRefGoogle Scholar
  192. 192.
    W. Fricker, M. C. Jarvis and C. T. Brett, Turgor pressure, membrane tension and the control of exocytosis in higher plantsPlant Cell Environ. 23, 999–1003 (2000).CrossRefGoogle Scholar
  193. 193.
    J. Šamaj, J. Müller, M. Beck, N. Böhm and D. Menzel, Vesicular trafficking,cytoskeleton and signalling in root hairs and pollen tubesTrends Plant Sci. 11, 594–600 (2006).PubMedCrossRefGoogle Scholar
  194. 194.
    R. A. Cole and J. E. Fowler, Polarized growth: maintaining focus on the tipCurr. Opin.Plant Biol. 9, 579–588 (2006).PubMedCrossRefGoogle Scholar
  195. 195.
    P. Campanoni and M. R. Blatt, Membrane trafficking and polar growth in root hairs and pollen tubesJ. Exp. Bot. 58, 65–74 (2007).PubMedCrossRefGoogle Scholar
  196. 196.
    M. Potocký, M. A. Jones, R. Bezvoda, N. Smirnoff and V. Žárský, Reactive oxygen species produced by NADPH oxidase are involved in pollen tube growthNew Phytol.174, 742–751 (2007).PubMedCrossRefGoogle Scholar
  197. 197.
    B. A. McClure and V. E. Franklin-Tong, Gametophytic self-incompatibility:understanding the cellular mechanisms involved in “self” pollen tube inhibitionPlanta 224, 233–245 (2006).PubMedCrossRefGoogle Scholar
  198. 198.
    S. Li, J. Šamaj and V. E. Franklin-Tong, A mitogen-activated protein kinase signals to programmed cell death induced by self-incompatibility inPapaver PollenPlant Physiol. 145, 236–245 (2007).PubMedCrossRefGoogle Scholar
  199. 199.
    Y. Chen, T. Chen, S. Shen, M. Zheng, Y. Guo, J. Lin, F. Baluška, and J. Šamaj,Differential display proteomic analysis ofPicea meyeri pollen germination and pollen-tube growth after inhibition of actin polymerization by latrunculin BPlant J. 47, 174–195 (2006).PubMedCrossRefGoogle Scholar
  200. 200.
    J. A. Feijó, S. S. Costa, A. M. Prado, J. D. Becker and A. C. Certal, Signalling by tips,Curr. Opin. Plant Biol. 7, 589–598 (2004).PubMedCrossRefGoogle Scholar
  201. 201.
    J. Šamaj, F. Baluška, B. Voigt, M. Schlicht, D. Volkmann and D. Menzel, Endocytosis,actin cytoskeleton and signalingPlant Physiol. 135, 1150–1161 (2004).PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science + Business Media B.V. 2008

Authors and Affiliations

  • Miroslav OveČka
    • 1
  • Irene K. Lichtscheidl
    • 2
  • FrantiŠek BaluŠka
    • 1
  • Jozef Šamaj
    • 3
  • Dieter Volkmann
    • 4
  • Heribert Hirt
    • 5
  1. 1.Institute of BotanySlovak Academy of SciencesBratislavaSlovak Republic
  2. 2.Institution of Cell imaging and Ultrastructure ResearchUniversity of ViennaViennaAustria
  3. 3.Institute of Plant Genetics and BiotechnologySlovak Academy of SciencesNitraSlovak Republic
  4. 4.Institute of Cellular and Molecular BotanyUniversity of BonnBonnGermany
  5. 5.Department of Plant Molecular BiologyMax F. Perutz Laboratories, University of ViennaViennaAustria

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