Advertisement

Protoplasma

, Volume 230, Issue 3–4, pp 217–230 | Cite as

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

  • Przemysław WojtaszekEmail author
  • František Baluška
  • Anna Kasprowicz
  • Magdalena Łuczak
  • Dieter Volkmann
Article

Summary.

Plant protoplasts are embedded within surrounding cell walls and the cell wall–plasma membrane–cytoskeleton (WMC) structural continuum seems to be crucial for the proper functioning of plant cells. We have utilised the protoplast preparation methodology to study the organisation and the putative components of the WMC continuum. Application of an osmotic agent evoked plasmolysis of the Zea mays root apex cells which appeared to be cell type- and growth stage-specific. Simultaneous use of wall polysaccharide-digesting enzymes selectively severed linkages between the components of the WMC continuum which changed the plasmolytic patterns in various cell types. This was followed by a reorganisation of filamentous actin aimed to reinforce protoplast boundaries and maintain the functioning of intercellular contact sites, especially at the cross walls. Particularly strong effects were evoked by pectin-degrading enzymes. Such treatments demonstrated directly the differentiated composition of various wall domains surrounding individual cells with the pectin-enriched cross walls (synapses), and the cellulose-hemicellulose network dominating the side walls. The same wall-degrading enzymes were used for in vitro digestion of isolated Lupinus albus cell walls followed by the extraction of wall proteins. Selective release of proteins suggested the importance of wall polysaccharide–protein interactions in the maintenance of the functioning and mechanical stability of root cell walls.

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

Abbreviations:

ECM

extracellular matrix

WAK

wall-associated kinase

WMC

cell wall–plasma membrane–cytoskeleton continuum

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Anderson, C, Wagner, T, Perret, M, He, Z, He, D, Kohorn, B 2001WAKs: cell wall-associated kinases linking the cytoplasm to the extracellular matrixPlant Mol Biol47197206PubMedCrossRefGoogle Scholar
  2. Bachewich, CL, Heath, IB 1997Differential cytoplasm-plasma membrane-cell wall adhesion patterns and their relationships to hyphal tip growth and organelle motilityProtoplasma2007186CrossRefGoogle Scholar
  3. Baluška, F, Hlavačka, A 2005Plant formins come to age: something special about cross-wallsNew Phytol168499503PubMedCrossRefGoogle Scholar
  4. Baluška, F, Parker, JS, Barlow, PW 1992Specific 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 regionEur J Cell Biol72113121Google Scholar
  5. Baluška, F, Volkmann, D, Barlow, PW 2001A polarity crossroad in the transition growth zone of maize root apices: cytoskeletal and developmental implicationsJ Plant Growth Regul20170181CrossRefGoogle Scholar
  6. Baluška, F, Hlavačka, A, Šamaj, J, Palme, K, Robinson, DG, Matoh, T, McCurdy, DW, Menzel, D, Volkmann, D 2002F-actin-dependent endocytosis of cell wall pectins in meristematic root cells. Insights from brefeldin A-induced compartmentsPlant Physiol130422431PubMedCrossRefGoogle Scholar
  7. Baluška, F, Šamaj, J, Wojtaszek, P, Volkmann, D, Menzel, D 2003aCytoskeleton-plasma membrane-cell wall continuum in plants. Emerging links revisitedPlant Physiol133482491CrossRefGoogle Scholar
  8. Baluška, F, Wojtaszek, P, Volkmann, D 2003bThe architecture of polarized cell growth: the unique status of elongating plant cellsBioEssays25569576CrossRefGoogle Scholar
  9. Baluška, F, Hlavačka, A, Volkmann, D, Menzel, D 2004aGetting connected: actin-based cell-to-cell channels in plants and animalsTrends Cell Biol14404408CrossRefGoogle Scholar
  10. Baluška, F, Šamaj, J, Hlavačka, A, Kendrick-Jones, J, Volkmann, D 2004bMyosin VIII and F-actin enriched plasmodesmata in maize root inner cortex cells accomplish fluid-phase endocytosis via an actomyosin-dependent processJ Exp Bot55463473CrossRefGoogle Scholar
  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 2005aWhat is apical and what is basal in plant root development?Trends Plant Sci10409411CrossRefGoogle Scholar
  12. Baluška, F, Liners, F, Hlavačka, A, Schlicht, M, Van Cutsem, P, McCurdy, D, Menzel, D 2005bCell wall pectins and xyloglucans are internalized into dividing root cells and accumulate within cell plates during cytokinesisProtoplasma225141151CrossRefGoogle Scholar
  13. Baluška, F, Volkmann, D, Menzel, D 2005cPlant synapses: actin-based adhesion domains for cell-to-cell communicationTrends Plant Sci10106111Google Scholar
  14. Barlow, PW, Volkmann, D, Baluška, F 2004Polarity in rootsLindsey, K eds. Polarity in plantsBlackwellOxford192241Google Scholar
  15. Borner, GHH, Sherrier, DJ, Stevens, JT, Arkin, IT, Dupree, P 2002Prediction of glycosylphosphatidylinositol-anchored proteins in Arabidopsis: a genomic analysisPlant Physiol129486499PubMedCrossRefGoogle Scholar
  16. Boutté, Y, Crosnier, M-T, Carraro, N, Traas, J, Satiat-Jeunemaitre, B 2006The plasma membrane recycling pathway and cell polarity in plants: studies on PIN proteinsJ Cell Sci11912551265PubMedCrossRefGoogle Scholar
  17. Bradford, MM 1976A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye bindingAnal Biochem72248254PubMedCrossRefGoogle Scholar
  18. Brüdern, A, Thiel, G 1999Effect of cell-wall-digesting enzymes on physiological state and competence of maize coleoptile cellsProtoplasma209246255CrossRefGoogle Scholar
  19. Cleary, AL 2001Plasma membrane-cell wall connections: roles in mitosis and cytokinesis revealed by plasmolysis of Tradescantia virginiana leaf epidermal cellsProtoplasma2152134PubMedCrossRefGoogle Scholar
  20. Coelho, SM, Taylor, AR, Ryan, KP, Sousa-Pinto, I, Brown, MT, Brownlee, C 2002Spatiotemporal patterning of reactive oxygen production and Ca2+ wave propagation in Fucus rhizoid cellsPlant Cell1423692381PubMedCrossRefGoogle Scholar
  21. Cosgrove, DJ 2005Growth of the plant cell wallNat Rev Mol Cell Biol6850861PubMedCrossRefGoogle Scholar
  22. Decreux, A, Messiaen, J 2005Wall-associated kinase WAK1 interacts with cell wall pectins in a calcium-induced conformationPlant Cell Physiol46268278PubMedCrossRefGoogle Scholar
  23. Deeks, MJ, Cvrcková, F, Machesky, LM, Mikitová, V, Ketelaar, T, Zársky, V, Davies, B, Hussey, PJ 2005Arabidopsis group Ie formins localize to specific cell membrane domains, interact with actin-binding proteins and cause defects in cell expansion upon aberrant expressionNew Phytol168529540PubMedCrossRefGoogle Scholar
  24. Delmer, DP 1999Cellulose biosynthesis: exciting times for a difficult field of studyAnnu Rev Plant Physiol Plant Mol Biol50245276PubMedCrossRefGoogle Scholar
  25. DeWitt, G, Richards, J, Mohnen, D, Jones, AM 1999Comparative compositional analysis of walls with two different morphologies: archetypical versus transfer-cell-likeProtoplasma209238245CrossRefGoogle Scholar
  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 nematodesPlant Cell1625292540PubMedCrossRefGoogle Scholar
  27. Fincher, GB, Stone, BA, Clarke, AE 1983Arabinogalactan-proteins: structure, biosynthesis, and functionAnnu Rev Plant Physiol344770CrossRefGoogle Scholar
  28. Freshour, G, Bonin, CP, Reiter, W-D, Albersheim, P, Darvill, AD, Hahn, MG 2003Distribution of fucose-containing xyloglucans in cell walls of the mur1 mutant of Arabidopsis Plant Physiol13116021612PubMedCrossRefGoogle Scholar
  29. Gens, JS, Fujiki, M, Pickard, BG 2000Arabinogalactan protein and wall-associated kinase in a plasmalemmal reticulum with specialized verticesProtoplasma212115134PubMedCrossRefGoogle Scholar
  30. Gouget, A, Senchou, V, Govers, F, Sanson, A, Barre, A, Rouge, P, Pont-Lezica, R, Canut, H 2006Lectin receptor kinases participate in protein-protein interactions to mediate plasma membrane-cell wall adhesions in Arabidopsis Plant Physiol1408190PubMedCrossRefGoogle Scholar
  31. Hayashi, T, Takagi, S 2003Ca2+-dependent cessation of cytoplasmic streaming induced by hypertonic treatment in Vallisneria mesophyll cells: possible role of cell wall–plasma membrane adhesionPlant Cell Physiol4410271036PubMedCrossRefGoogle Scholar
  32. He, Z-H, Fujiki, M, Kohorn, BD 1996A cell wall-associated, receptor-like protein kinaseJ Biol Chem2711978919793PubMedCrossRefGoogle Scholar
  33. He, Z-H, Cheeseman, I, He, D, Kohorn, BD 1999A cluster of five cell wall-associated receptor kinase genes, Wak1–5, are expressed in specific organs of Arabidopsis Plant Mol Biol3911891196PubMedCrossRefGoogle Scholar
  34. Henry, CA, Jordan, JR, Kropf, DL 1996Localized membrane-wall adhesions in Pelvetia zygotesProtoplasma1903952CrossRefGoogle Scholar
  35. Herve, C, Dabos, P, Galaud, JP, Rouge, P, Lescure, B 1996Characterization of an Arabidopsis thaliana gene that defines a new class of putative plant receptor kinases with an extracellular lectin-like domainJ Mol Biol258778788PubMedCrossRefGoogle Scholar
  36. Hohl, M, Schopfer, P 1991Water relations of growing maize coleoptiles: comparison between mannitol and polyethylene glycol 6000 as external osmotica for adjusting turgor pressurePlant Physiol95716722PubMedGoogle Scholar
  37. Huang, S, Gao, L, Blanchoin, L, Staiger, CJ 2006Heterodimeric capping protein from Arabidopsis is regulated by phosphatidic acidMol Biol Cell1719461958PubMedCrossRefGoogle Scholar
  38. Hussey, PJ eds. 2004The plant cytoskeleton in cell differentiation and developmentBackwellOxfordGoogle Scholar
  39. Ingber, DE 2003aTensegrity. I. Cell structure and hierarchical systems biologyJ Cell Sci11611571173CrossRefGoogle Scholar
  40. Ingber, DE 2003bTensegrity. II. How structural networks influence cellular information-processing networksJ Cell Sci11613971408CrossRefGoogle Scholar
  41. Jamet, E, Canut, H, Boudart, G, Pont-Lezica, RF 2005Cell wall proteins: a new insight through proteomicsTrends Plant Sci113339PubMedCrossRefGoogle Scholar
  42. Jarvis, MC, McCann, MC 2000Macromolecular biophysics of plant cell wall. Concepts and methodologyPlant Physiol Biochem38113CrossRefGoogle Scholar
  43. Knox, JP, Linstead, PJ, King, J, Cooper, C, Roberts, K 1990Pectin esterification is spatially regulated both within cell walls and between developing tissues of root apicesPlanta181512521CrossRefGoogle Scholar
  44. Kohorn, BD 2000Plasma membrane-cell wall contactsPlant Physiol1243138PubMedCrossRefGoogle Scholar
  45. Kohorn, BD 2001WAKs; cell wall associated kinasesCurr Opin Cell Biol13529533PubMedCrossRefGoogle Scholar
  46. Kollmeier, M, Dietrich, P, Bauer, CS, Horst, WJ, Hedrich, R 2001Aluminium activates citrate-permeable anion channel in the aluminium-sensitive zone of the maize root apex. A comparison between an aluminium-sensitive and an aluminium-insensitive cultivarPlant Physiol126397410PubMedCrossRefGoogle Scholar
  47. Komis, G, Apostolakos, P, Galatis, B 2002Hyperosmotic stress-induced actin filament reorganization in leaf cells of Chlorophyton comosum J Exp Bot5316991710PubMedCrossRefGoogle Scholar
  48. Komis, G, Apostolakos, P, Galatis, B 2003Actomyosin is involved in the plasmolytic cycle: gliding movement of the deplasmolyzing protoplastProtoplasma221245256PubMedGoogle Scholar
  49. Komis, G, Apostolakos, P, Gaitanaki, C, Galatis, B 2004Hyperosmotically induced accumulation of a phosphorylated p38-like MAPK involved in protoplast volume regulation of plasmolyzed wheat root cellsFEBS Lett573168174PubMedCrossRefGoogle Scholar
  50. Laemmli, UK 1970Cleavage of structural proteins during the assembly of the head of bacteriophage T4Nature227680685PubMedCrossRefGoogle Scholar
  51. Lang, I, Barton, DA, Overall, RL 2004Membrane-wall attachments in plasmolysed plant cellsProtoplasma224231243PubMedCrossRefGoogle Scholar
  52. Lang-Pauluzzi, I 2000The behaviour of the plasma membrane during plasmolysis: a study by UV microscopyJ Microsc198188198PubMedCrossRefGoogle Scholar
  53. Lang-Pauluzzi, I, Gunning, BES 2000A plasmolytic cycle: the fate of cytoskeletal elementsProtoplasma212174185CrossRefGoogle Scholar
  54. Mancuso, S, Marras, AM, Volker, M, Baluška, F 2005Non-invasive and continuous recordings of auxin fluxes in intact root apex with a carbon-nanotube-modified and self-referencing microelectrodeAnal Biochem341344351PubMedCrossRefGoogle Scholar
  55. Maniotis, AJ, Chen, CS, Ingber, DE 1997Demonstration of mechanical connections between integrins, cytoskeletal filaments, and nucleoplasm that stabilize nuclear structureProc Natl Acad Sci USA94849854PubMedCrossRefGoogle Scholar
  56. Masuda, Y, Takagi, S, Nagai, R 1991Protease-sensitive anchoring of microfilament bundles provides tracks for cytoplasmic streaming in Vallisneria Protoplasma162151159CrossRefGoogle Scholar
  57. Mathur, J 2006Local interactions shape plant cellsCurr Opin Cell Biol184046PubMedCrossRefGoogle Scholar
  58. McLusky, SR, Bennett, MH, Beale, MH, Lewis, MJ, Gaskin, P, Mansfield, JW 1999Cell 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 biosynthesisPlant J17523534CrossRefGoogle Scholar
  59. Munnik, T, Meijer, HJG, ter Riet, B, Hirt, H, Frank, W, Bartels, D, Musgrave, A 2000Hyperosmotic stress stimulates phospholipase D activity and elevates the levels of phosphatidic acid and diacylglycerol pyrophosphatePlant J22147154PubMedCrossRefGoogle Scholar
  60. Niklas, KJ 2000The evolution of plant body plans – a biomechanical perspectiveAnn Bot85411438CrossRefGoogle Scholar
  61. Nothnagel, EA 1997Proteoglycans and related components in plant cellsInt Rev Cytol174195291PubMedGoogle Scholar
  62. Oparka, KJ 1994Plasmolysis: new insights into an old processNew Phytol126571591CrossRefGoogle Scholar
  63. Orr, AW, Helmke, BP, Blackman, BR, Schwartz, MA 2006Mechanisms of mechanotransductionDev Cell101120PubMedCrossRefGoogle Scholar
  64. Park, AR, Cho, SK, Yun, UJ, Jin, MY, Lee, SH, Sachetto-Martins, G, Park, OK 2001Interaction of the Arabidopsis receptor protein kinase Wak1 with a glycine rich protein AtGRP-3J Biol Chem2762668826693PubMedCrossRefGoogle Scholar
  65. Peters, WS, Hagemann, W, Tomos, DA 2000What makes plants different? Principles of extracellular matrix function in “soft” plant tissuesComp Biochem Physiol Part A125151167CrossRefGoogle Scholar
  66. Pollock, FM, Pickett-Heaps, JD 2005Spatial determinants in morphogenesis: recovery from plasmolysis in the diatom Ditylum Cell Motil Cytoskeleton607182PubMedCrossRefGoogle Scholar
  67. Pont-Lezica, RF, McNally, JG, Pickard, BG 1993Wall-to-membrane linkers in onion epidermis: some hypothesesPlant Cell Environ16111123CrossRefGoogle Scholar
  68. Reinhardt, D, Kuhlemeier, C 2002Plant architectureEMBO Rep3846851PubMedCrossRefGoogle Scholar
  69. Richmond, TA, Somerville, CR 2001Integrative approaches to determining Csl functionPlant Mol Biol47131143PubMedCrossRefGoogle Scholar
  70. Ryu, J-H, Takagi, S, Nagai, R 1995Stationary organization of the actin cytoskeleton in Vallisneria: the role of stable microfilaments and the end wallsJ Cell Sci10815311539PubMedGoogle Scholar
  71. Šamaj, J, Braun, M, Baluška, F, Ensikat, H-J, Tsumuraya, Y, Volkmann, D 1999aSpecific localization of arabinogalactan-protein epitopes at the surface of maize root hairsPlant Cell Physiol40874883Google Scholar
  72. Šamaj, J, Ensikat, H-J, Baluška, F, Knox, JP, Barthlott, W, Volkmann, D 1999bImmunogold localization of plant surface arabinogalactan-proteins using glycerol liquid substitution and scanning electron microscopyJ Microsc193150157CrossRefGoogle Scholar
  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 2002Involvement of the mitogen-activated protein kinase SIMK in regulation of root hair tip-growthEMBO J2132963306PubMedCrossRefGoogle Scholar
  74. Schultz, C, Gilson, P, Oxley, D, Youl, J, Bacic, A 1998GPI-anchors on arabinogalactan-proteins: implications for signalling in plantsTrends Plant Sci3426431CrossRefGoogle Scholar
  75. Schultz, C, Johnson, KL, Currie, G, Bacic, A 2000The classical arabinogalactan protein gene family of Arabidopsis Plant Cell1217511768PubMedCrossRefGoogle Scholar
  76. Sivaguru, M, Baluška, F, Volkmann, D, Felle, H, Horst, WJ 1999Impacts of aluminum on cytoskeleton of maize root apex: short-term effects on distal part of transition zonePlant Physiol11910731082PubMedCrossRefGoogle Scholar
  77. Sivaguru, M, Ezaki, B, He, Z-H, Tong, H, Osawa, H, Baluška, F, Volkmann, D, Matsumoto, H 2003Aluminum induced gene expression and protein localization of cell wall-associated receptor kinase in Arabidopsis thaliana Plant Physiol13222562266PubMedCrossRefGoogle Scholar
  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 2004Toward a system approach to understanding plant cell wallsScience30622062211PubMedCrossRefGoogle Scholar
  79. Spickett, CM, Smirnoff, N, Ratcliffe, RG 1992Metabolic response of maize roots to hyperosmotic shock: an in vivo 31P nuclear magnetic resonance studyPlant Physiol99856863PubMedGoogle Scholar
  80. Suzuki, K, Amino, S-I, Takeuchi, Y, Komamine, A 1990Differences in the composition of the cell walls of two morphologically different lines of suspension-cultured Catharanthus roseus cellsPlant Cell Physiol31714Google Scholar
  81. Verica, JA, He, ZH 2002The cell wall-associated kinase (WAK) and WAK-like kinase gene family1Plant Physiol129455459PubMedCrossRefGoogle Scholar
  82. Vorwerk, S, Somerville, S, Somerville, C 2004The role of plant cell wall polysaccharide composition in disease resistanceTrends Plant Sci9203209PubMedCrossRefGoogle Scholar
  83. Wang, N, Naruse, K, Stamenovic, D, Fredberg, JJ, Mijailovich, SM, Tolic-Nørrelykke, IM, Polte, T, Mannix, R, Ingber, DE 2001Mechanical behavior in living cells consistent with the tensegrity modelProc Natl Acad Sci USA9877657770PubMedCrossRefGoogle Scholar
  84. Wayne, R, Staves, MP, Leopold, AC 1992The contribution of the extracellular matrix to gravisensing in characean cellsJ Cell Sci101611623PubMedGoogle Scholar
  85. Willats, WGT, McCartney, L, Mackie, W, Knox, JP 2001Pectin: cell biology and prospects for functional analysisPlant Mol Biol47927PubMedCrossRefGoogle Scholar
  86. Williams, M, Freshour, G, Darvill, A, Albersheim, P, Hahn, M 1996An antibody Fab selected from a recombinant phage display library detects deesterified pectic polysaccharide rhamnogalacturonan II in plant cellsPlant Cell8673685PubMedCrossRefGoogle Scholar
  87. Wojtaszek, P 2000Genes and plant cell walls: a difficult relationshipBiol Rev (Cambridge)75437475Google Scholar
  88. Wojtaszek, P 2001Organismal view of a plant and a plant cellActa Biochim Pol48443451PubMedGoogle Scholar
  89. Wojtaszek, P, Bolwell, GP 1995Secondary cell-wall-specific glycoprotein(s) from French bean hypocotylsPlant Physiol10810011012PubMedCrossRefGoogle Scholar
  90. Wojtaszek, P, Volkmann, D, Baluška, F 2004Polarity and cell wallsLindsey, K eds. Polarity in plantsBlackwellOxford72121Google Scholar
  91. Wojtaszek, P, Anielska-Mazur, A, Gabryś, H, Baluška, F, Volkmann, D 2005Rapid relocation of myosin VIII between cell periphery and plastid surfaces are root-specific and provide the evidence for actomyosin involvement in osmosensingFunct Plant Biol32721736CrossRefGoogle Scholar
  92. Wyatt, SE, Carpita, NC 1993The plant cytoskeleton-cell wall continuumTrends Cell Biol3413417PubMedCrossRefGoogle Scholar
  93. Yu, Q, Hlavačka, A, Matoh, T, Volkmann, D, Menzel, D, Goldbach, HE, Baluška, F 2002Short-term boron deprivation inhibits endocytosis of cell wall pectins in meristematic cells of maize and wheat root apicesPlant Physiol130415421PubMedCrossRefGoogle Scholar
  94. Yu, Q, Baluška, F, Jasper, F, Menzel, D, Volkmann, D, Goldbach, HE 2003Short-term boron deprivation enhances levels of cytoskeletal proteins in maize, but not zucchini, root apicesPhysiol Plant11719CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Przemysław Wojtaszek
    • 1
    • 2
    • 3
    Email author
  • František Baluška
    • 1
    • 4
  • Anna Kasprowicz
    • 2
  • Magdalena Łuczak
    • 2
    • 3
  • Dieter Volkmann
    • 1
  1. 1.Institute of Cellular and Molecular BotanyRheinische Friedrich-Wilhelms-Universität BonnBonn
  2. 2.Department of Molecular and Cellular BiologyAdam Mickiewicz UniversityPoznań
  3. 3.Institute of Bioorganic ChemistryPolish Academy of SciencesPoznań
  4. 4.Institute of BotanySlovak Academy of SciencesBratislava

Personalised recommendations