Domain-specific mechanosensory transmission of osmotic and enzymatic cell wall disturbances to the actin cytoskeleton

Protoplasma

Volumn 230, Issue 3-4, 2007, Pages 217-230

  Wojtaszek, Przemysław ^a,b,c   Baluška, František ^a,d   Kasprowicz, Anna ^b   Łuczak, Magdalena ^b,c   Volkmann, Dieter ^a  

^a UNIVERSITY OF BONN   (Germany)

^b ADAM MICKIEWICZ UNIVERSITY   (Poland)

^c INSTITUTE OF BIOORGANIC CHEMISTRY   (Poland)

^d INSTITUTE OF BOTANY   (Slovakia)

Author keywords

Actin; Cell wall cytoskeleton interaction; Enzymatic digestion; Lupinus albus; Mechanosensing; Plasmolysis; Zea mays

Indexed keywords

ACTIN; CELLULOSE; ENZYME; PECTIN; POLYSACCHARIDE;

ARTICLE; CELL ADHESION; CELL JUNCTION; CELL WALL; CYTOSKELETON; DRUG EFFECT; ELECTROLYTE BALANCE; MECHANOTRANSDUCTION; METABOLISM; MICROFILAMENT; OSMOTIC PRESSURE; PHYSIOLOGY; PLANT; PLANT ROOT; PROTOPLAST; ULTRASTRUCTURE;

ACTINS; CELL ADHESION; CELL WALL; CELLULOSE; CYTOSKELETON; ENZYMES; INTERCELLULAR JUNCTIONS; MECHANOTRANSDUCTION, CELLULAR; MICROFILAMENTS; OSMOTIC PRESSURE; PECTINS; PLANT ROOTS; PLANTS; POLYSACCHARIDES; PROTOPLASTS; WATER-ELECTROLYTE BALANCE;

LUPINUS ALBUS; ZEA MAYS;

EID: 34247615444     PISSN: 0033183X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00709-006-0235-6     Document Type: Article

References (94)

1. Anderson C, Wagner T, Perret M, He Z, He D, Kohorn B (2001) WAKs: cell wall-associated kinases linking the cytoplasm to the extracellular matrix. Plant Mol Biol 47: 197-206
2. Bachewich CL, Heath IB (1997) Differential cytoplasm-plasma membrane-cell wall adhesion patterns and their relationships to hyphal tip growth and organelle motility. Protoplasma 200: 71-86
3. Baluška F, Hlavačka A (2005) Plant formins come to age: something special about cross-walls. New Phytol 168: 499-503
4. Baluška F, Parker JS, Barlow PW (1992) Specific patterns of cortical and endoplasmic microtubules associated with cell growth. 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
5. Baluška F, Volkmann D, Barlow PW (2001) A polarity crossroad in the transition growth zone of maize root apices: cytoskeletal and developmental implications. J Plant Growth Regul 20: 170-181
6. Baluška F, Hlavačka A, Šamaj J, Palme K, Robinson DG, Matoh T, McCurdy DW, Menzel D, Volkmann D (2002) F-actin-dependent endocytosis of cell wall pectins in meristematic root cells. Insights from brefeldin A-induced compartments. Plant Physiol 130: 422-431
7. Baluška F, Šamaj J, Wojtaszek P, Volkmann D, Menzel D (2003a) Cytoskeleton-plasma membrane-cell wall continuum in plants. Emerging links revisited. Plant Physiol 133: 482-491
8. Baluška F, Wojtaszek P, Volkmann D (2003b) The architecture of polarized cell growth: the unique status of elongating plant cells. BioEssays 25: 569-576
9. Baluška F, Hlavačka A, Volkmann D, Menzel D (2004a) Getting connected: actin-based cell-to-cell channels in plants and animals. Trends Cell Biol 14: 404-408
10. Baluška F, Šamaj J, Hlavačka A, Kendrick-Jones J, Volkmann D (2004b) Myosin VIII and F-actin enriched plasmodesmata in maize root inner cortex cells accomplish fluid-phase endocytosis via an actomyosin-dependent process. J Exp Bot 55: 463-473
11. Baluška F, Barlow P, Baskin T, Chen R, Feldman L, Forde BG, Geisler M, Jernstedt J, Menzel D, Muday G, Murphy A, Šamaj J, Volkmann D (2005a) What is apical and what is basal in plant root development? Trends Plant Sci 10: 409-411
12. Baluška F, Liners F, Hlavačka A, Schlicht M, Van Cutsem P, McCurdy D, Menzel D (2005b) Cell wall pectins and xyloglucans are internalized into dividing root cells and accumulate within cell plates during cytokinesis. Protoplasma 225: 141-151
13. Baluška F, Volkmann D, Menzel D (2005c) Plant synapses: actin-based adhesion domains for cell-to-cell communication. Trends Plant Sci 10: 106-111
14. Barlow PW, Volkmann D, Baluška F (2004) Polarity in roots. In: Lindsey K (ed) Polarity in plants. Blackwell, Oxford, pp 192-241
15. Borner GHH, Sherrier DJ, Stevens JT, Arkin IT, Dupree P (2002) Prediction of glycosylphosphatidylinositol-anchored proteins in Arabidopsis: a genomic analysis. Plant Physiol 129: 486-499
16. Boutté Y, Crosnier M-T, Carraro N, Traas J, Satiat-Jeunemaitre B (2006) The plasma membrane recycling pathway and cell polarity in plants: studies on PIN proteins. J Cell Sci 119: 1255-1265
17. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of proteindye binding. Anal Biochem 72: 248-254
18. Brüdern A, Thiel G (1999) Effect of cell-wall-digesting enzymes on physiological state and competence of maize coleoptile cells. Protoplasma 209: 246-255
19. Cleary AL (2001) Plasma membrane-cell wall connections: roles in mitosis and cytokinesis revealed by plasmolysis of Tradescantia virginiana leaf epidermal cells. Protoplasma 215: 21-34
20. 2+ wave propagation in Fucus rhizoid cells. Plant Cell 14: 2369-2381
21. Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6: 850-861
22. Decreux A, Messiaen J (2005) Wall-associated kinase WAK1 interacts with cell wall pectins in a calcium-induced conformation. Plant Cell Physiol 46: 268-278
23. Deeks MJ, Cvrcková F, Machesky LM, Mikitová V, Ketelaar T, Zársky V, Davies B, Hussey PJ (2005) Arabidopsis group Ie formins localize to specific cell membrane domains, interact with actin-binding proteins and cause defects in cell expansion upon aberrant expression. New Phytol 168: 529-540
24. Delmer DP (1999) Cellulose biosynthesis: exciting times for a difficult field of study. Annu Rev Plant Physiol Plant Mol Biol 50: 245-276
25. DeWitt G, Richards J, Mohnen D, Jones AM (1999) Comparative compositional analysis of walls with two different morphologies: archetypical versus transfer-cell-like. Protoplasma 209: 238-245
26. Favery B, Chelysheva LA, Lebris M, Jammes F, Marmagne A, Almeida-Engler J, Lecomte P, Vaury C, Arkowitz RA, Abada P (2004) Arabidopsis formin AtFH6 is a plasma membrane-associated protein upregulated in giant cells induced by parasitic nematodes. Plant Cell 16: 2529-2540
27. Fincher GB, Stone BA, Clarke AE (1983) Arabinogalactan-proteins: structure, biosynthesis, and function. Annu Rev Plant Physiol 34: 47-70
28. Freshour G, Bonin CP, Reiter W-D, Albersheim P, Darvill AD, Hahn MG (2003) Distribution of fucose-containing xyloglucans in cell walls of the mur1 mutant of Arabidopsis. Plant Physiol 131: 1602-1612
29. Gens JS, Fujiki M, Pickard BG (2000) Arabinogalactan protein and wall-associated kinase in a plasmalemmal reticulum with specialized vertices. Protoplasma 212: 115-134
30. Gouget A, Senchou V, Govers F, Sanson A, Barre A, Rouge P, Pont-Lezica R, Canut H (2006) Lectin receptor kinases participate in protein-protein interactions to mediate plasma membrane-cell wall adhesions in Arabidopsis. Plant Physiol 140: 81-90
31. 2+-dependent cessation of cytoplasmic streaming induced by hypertonic treatment in Vallisneria mesophyll cells: possible role of cell wall-plasma membrane adhesion. Plant Cell Physiol 44: 1027-1036
32. He Z-H, Fujiki M, Kohorn BD (1996) A cell wall-associated, receptorlike protein kinase. J Biol Chem 271: 19789-19793
33. He Z-H, Cheeseman I, He D, Kohorn BD (1999) A cluster of five cell wall-associated receptor kinase genes, Wak1-5, are expressed in specific organs of Arabidopsis. Plant Mol Biol 39: 1189-1196
34. Henry CA, Jordan JR, Kropf DL (1996) Localized membrane-wall adhesions in Pelvetia zygotes. Protoplasma 190: 39-52
35. Herve C, Dabos P, Galaud JP, Rouge P, Lescure B (1996) Characterization of an Arabidopsis thaliana gene that defines a new class of putative plant receptor kinases with an extracellular lectin-like domain. J Mol Biol 258: 778-788
36. Hohl M, Schopfer P (1991) Water relations of growing maize coleoptiles: comparison between mannitol and polyethylene glycol 6000 as external osmotica for adjusting turgor pressure. Plant Physiol 95: 716-722
37. Huang S, Gao L, Blanchoin L, Staiger CJ (2006) Heterodimeric capping protein from Arabidopsis is regulated by phosphatidic acid. Mol Biol Cell: 17: 1946-1958
38. Hussey PJ (ed) (2004) The plant cytoskeleton in cell differentiation and development. Backwell, Oxford
39. Ingber DE (2003a) Tensegrity. I. Cell structure and hierarchical systems biology. J Cell Sci 116: 1157-1173
40. Ingber DE (2003b) Tensegrity. II. How structural networks influence cellular information-processing networks. J Cell Sci 116: 1397-1408
41. Jamet E, Canut H, Boudart G, Pont-Lezica RF (2005) Cell wall proteins: a new insight through proteomics. Trends Plant Sci 11: 33-39
42. Jarvis MC, McCann MC (2000) Macromolecular biophysics of plant cell wall. Concepts and methodology. Plant Physiol Biochem 38: 1-13
43. Knox JP, Linstead PJ, King J, Cooper C, Roberts K (1990) Pectin esterification is spatially regulated both within cell walls and between developing tissues of root apices. Planta 181: 512-521
44. Kohorn BD (2000) Plasma membrane-cell wall contacts. Plant Physiol 124: 31-38
45. Kohorn BD (2001) WAKs; cell wall associated kinases. Curr Opin Cell Biol 13: 529-533
46. Kollmeier M, Dietrich P, Bauer CS, Horst WJ, Hedrich R (2001) Aluminium activates citrate-permeable anion channel in the aluminiumsensitive zone of the maize root apex. A comparison between an aluminium-sensitive and an aluminium-insensitive cultivar. Plant Physiol 126: 397-410
47. Komis G, Apostolakos P, Galatis B (2002) Hyperosmotic stress-induced actin filament reorganization in leaf cells of Chlorophyton comosum. J Exp Bot 53: 1699-1710
48. Komis G, Apostolakos P, Galatis B (2003) Actomyosin is involved in the plasmolytic cycle: gliding movement of the deplasmolyzing protoplast. Protoplasma 221: 245-256
49. Komis G, Apostolakos P, Gaitanaki C, Galatis B (2004) Hyperosmotically induced accumulation of a phosphorylated p38-like MAPK involved in protoplast volume regulation of plasmolyzed wheat root cells. FEBS Lett 573: 168-174
50. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685
51. Lang I, Barton DA, Overall RL (2004) Membrane-wall attachments in plasmolysed plant cells. Protoplasma 224: 231-243
52. Lang-Pauluzzi I (2000) The behaviour of the plasma membrane during plasmolysis: a study by UV microscopy. J Microsc 198: 188-198
53. Lang-Pauluzzi I, Gunning BES (2000) A plasmolytic cycle: the fate of cytoskeletal elements. Protoplasma 212: 174-185
54. Mancuso S, Marras AM, Volker M, Baluška F (2005) Non-invasive and continuous recordings of auxin fluxes in intact root apex with a carbon-nanotube-modified and self-referencing microelectrode. Anal Biochem 341: 344-351
55. Maniotis AJ, Chen CS, Ingber DE (1997) Demonstration of mechanical connections between integrins, cytoskeletal filaments, and nucleoplasm that stabilize nuclear structure. Proc Natl Acad Sci USA 94: 849-854
56. Masuda Y, Takagi S, Nagai R (1991) Protease-sensitive anchoring of microfilament bundles provides tracks for cytoplasmic streaming in Vallisneria. Protoplasma 162: 151-159
57. Mathur J (2006) Local interactions shape plant cells. Curr Opin Cell Biol 18: 40-46
58. McLusky SR, Bennett MH, Beale MH, Lewis MJ, Gaskin P, Mansfield JW (1999) Cell wall alterations and localized accumulation of feruloyl-3′- methoxytyramine in onion epidermis at sites of attempted penetration by Botrytis allii are associated with actin polarisation, peroxidase activity and suppression of flavonoid biosynthesis. Plant J 17: 523-534
59. Munnik T, Meijer HJG, ter Riet B, Hirt H, Frank W, Bartels D, Musgrave A (2000) Hyperosmotic stress stimulates phospholipase D activity and elevates the levels of phosphatidic acid and diacylglycerol pyrophosphate. Plant J 22: 147-154
60. Niklas KJ (2000) The evolution of plant body plans - a biomechanical perspective. Ann Bot 85: 411-438
61. Nothnagel EA (1997) Proteoglycans and related components in plant cells. Int Rev Cytol 174: 195-291
62. Oparka KJ (1994) Plasmolysis: new insights into an old process. New Phytol 126: 571-591
63. Orr AW, Helmke BP, Blackman BR, Schwartz MA (2006) Mechanisms of mechanotransduction. Dev Cell 10: 11-20
64. Park AR, Cho SK, Yun UJ, Jin MY, Lee SH, Sachetto-Martins G, Park OK (2001) Interaction of the Arabidopsis receptor protein kinase Wak1 with a glycine rich protein AtGRP-3. J Biol Chem 276: 26688-26693
65. Peters WS, Hagemann W, Tomos DA (2000) What makes plants different? Principles of extracellular matrix function in "soft" plant tissues. Comp Biochem Physiol Part A 125: 151-167
66. Pollock FM, Pickett-Heaps JD (2005) Spatial determinants in morphogenesis: recovery from plasmolysis in the diatom Ditylum. Cell Motil Cytoskeleton 60: 71-82
67. Pont-Lezica RF, McNally JG, Pickard BG (1993) Wall-to-membrane linkers in onion epidermis: some hypotheses. Plant Cell Environ 16: 111-123
68. Reinhardt D, Kuhlemeier C (2002) Plant architecture. EMBO Rep 3: 846-851
69. Richmond TA, Somerville CR (2001) Integrative approaches to determining Csl function. Plant Mol Biol 47: 131-143
70. Ryu J-H, Takagi S, Nagai R (1995) Stationary organization of the actin cytoskeleton in Vallisneria: the role of stable microfilaments and the end walls. J Cell Sci 108: 1531-1539
71. Šamaj J, Braun M, Baluška F, Ensikat H-J, Tsumuraya Y, Volkmann D (1999a) Specific localization of arabinogalactan-protein epitopes at the surface of maize root hairs. Plant Cell Physiol 40: 874-883
72. Šamaj J, Ensikat H-J, Baluška F, Knox JP, Barthlott W, Volkmann D (1999b) Immunogold localization of plant surface arabinogalactanproteins using glycerol liquid substitution and scanning electron microscopy. J Microsc 193: 150-157
73. Šamaj J, Ovecka M, Hlavačka A, Lecourieux F, Meskiene I, Lichtscheidl I, Lenart P, Salaj J, Volkmann D, Bögre L, Baluška F, Hirt H (2002) Involvement of the mitogen-activated protein kinase SIMK in regulation of root hair tip-growth EMBO J 21: 3296-3306
74. Schultz C, Gilson P, Oxley D, Youl J, Bacic A (1998) GPI-anchors on arabinogalactan-proteins: implications for signalling in plants. Trends Plant Sci 3: 426-431
75. Schultz C, Johnson KL, Currie G, Bacic A (2000) The classical arabinogalactan protein gene family of Arabidopsis. Plant Cell 12: 1751-1768
76. Sivaguru M, Baluška F, Volkmann D, Felle H, Horst WJ (1999) Impacts of aluminum on cytoskeleton of maize root apex: short-term effects on distal part of transition zone. Plant Physiol 119: 1073-1082
77. Sivaguru M, Ezaki B, He Z-H, Tong H, Osawa H, Baluška F, Volkmann D, Matsumoto H (2003) Aluminum induced gene expression and protein localization of cell wall-associated receptor kinase in Arabidopsis thaliana. Plant Physiol 132: 2256-2266
78. Somerville C, Bauer S, Brininstool G, Facette M, Hamann T, Milne J, Osborne E, Paredez A, Persson S, Raab T, Vorwerk S, Youngs H (2004) Toward a system approach to understanding plant cell walls. Science 306: 2206-2211
79. 31P nuclear magnetic resonance study. Plant Physiol 99: 856-863
80. Suzuki K, Amino S-I, Takeuchi Y, Komamine A (1990) Differences in the composition of the cell walls of two morphologically different lines of suspension-cultured Catharanthus roseus cells. Plant Cell Physiol 31: 7-14
81. Verica JA, He ZH (2002) The cell wall-associated kinase (WAK) and WAK-like kinase gene family1. Plant Physiol 129: 455-459
82. Vorwerk S, Somerville S, Somerville C (2004) The role of plant cell wall polysaccharide composition in disease resistance. Trends Plant Sci 9: 203-209
83. Wang N, Naruse K, Stamenovic D, Fredberg JJ, Mijailovich SM, Tolic-Nørrelykke IM, Polte T, Mannix R, Ingber DE (2001) Mechanical behavior in living cells consistent with the tensegrity model. Proc Natl Acad Sci USA 98: 7765-7770
84. Wayne R, Staves MP, Leopold AC (1992) The contribution of the extracellular matrix to gravisensing in characean cells. J Cell Sci 101: 611-623
85. Willats WGT, McCartney L, Mackie W, Knox JP (2001) Pectin: cell biology and prospects for functional analysis. Plant Mol Biol 47: 9-27
86. Williams M, Freshour G, Darvill A, Albersheim P, Hahn M (1996) An antibody Fab selected from a recombinant phage display library detects deesterified pectic polysaccharide rhamnogalacturonan II in plant cells. Plant Cell 8: 673-685
87. Wojtaszek P (2000) Genes and plant cell walls: a difficult relationship. Biol Rev (Cambridge) 75: 437-475
88. Wojtaszek P (2001) Organismal view of a plant and a plant cell. Acta Biochim Pol 48: 443-451
89. Wojtaszek P, Bolwell GP (1995) Secondary cell-wall-specific glycoprotein( s) from French bean hypocotyls. Plant Physiol 108: 1001-1012
90. Wojtaszek P, Volkmann D, Baluška F (2004) Polarity and cell walls. In: Lindsey K (ed) Polarity in plants. Blackwell, Oxford, pp 72-121
91. Wojtaszek P, Anielska-Mazur A, Gabryś H, Baluška F, Volkmann D (2005) Rapid relocation of myosin VIII between cell periphery and plastid surfaces are root-specific and provide the evidence for actomyosin involvement in osmosensing. Funct Plant Biol 32: 721-736
92. Wyatt SE, Carpita NC (1993) The plant cytoskeleton-cell wall continuum. Trends Cell Biol 3: 413-417
93. Yu Q, Hlavačka A, Matoh T, Volkmann D, Menzel D, Goldbach HE, Baluška F (2002) Short-term boron deprivation inhibits endocytosis of cell wall pectins in meristematic cells of maize and wheat root apices. Plant Physiol 130: 415-421
94. Yu Q, Baluška F, Jasper F, Menzel D, Volkmann D, Goldbach HE (2003) Short-term boron deprivation enhances levels of cytoskeletal proteins in maize, but not zucchini, root apices. Physiol Plant 117: 1-9