Abstract
The mechanical strength of cell walls in the tip-growing cells of Vaucheria terrestris is weakened by treatment with proteolytic enzymes. To clarify the morphological characteristics of the components maintaining cell wall strength, the fine structures of the cell walls, with and without protease treatment, were observed by transmission electron microscopy (TEM) and atomic force microscopy (AFM). Observations indicated that cellulose microfibrils were arranged in random directions and overlapped each other. Most of the microfibrils observed in the inner surface of the cell wall were embedded in amorphous materials, whereas in the outer surface of the cell wall, microfibrils were partially covered by amorphous materials. The matrix components embedding and covering microfibrils were almost completely removed by protease treatment, revealing layers of naked microfibrils deposited deeply in the cell wall. Topographic data taken from AFM observations provided some additional information that could not be obtained by TEM, including more detailed images of the granular surface textures of the matrix components and the detection of microfibrils in the interior of the cell wall. In addition, quantitative AFM data of local surface heights enabled us to draw three-dimensional renderings and to quantitatively estimate the extent of the exposure of microfibrils by the enzymatic treatment.
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Abbreviations
- AFM:
-
Atomic force microscopy
- TEM:
-
Transmission electron microscopy
References
Binnig G, Quate CF, Gerber C (1986) Atomic force microscope. Phys Rev Lett 56:930–933
Carpita NC, Gibeaut DM (1993) Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. Plant J 3:1–30
Cassab GI (1998) Plant cell wall proteins. Annu Rev Plant Physiol Plant Mol Biol 49:281–309
Chi E-S, Henry EC, Kawai H, Okuda K (1999) Immunogold-labeling analysis of alginate distributions in the cell walls of chromophyte algae. Phycol Res 47:53–60
Cosgrove DJ (1993) How do plant cell walls extend? Plant Physiol 102:1–6
Cosgrove DJ (1996) Plant cell enlargement and the action of expansins. Bioessays 18:533–540
Cosgrove DJ (1997) Relaxation in a high-stress environment: the molecular bases of extensible cell walls and cell enlargement. Plant Cell 9:1031–1041
Cosgrove DJ (1999) Enzymes and other agents that enhance cell wall extensibility. Annu Rev Plant Physiol Plant Mol Biol 50:3971–3417
Davies LM, Harris PJ (2003) Atomic force microscopy of microfibrils in primary cell walls. Planta 217:283–289
Dumais J, Long SR, Shaw SL (2004) The mechanics of surface expansion anisotropy in Medicago truncatula root hairs. Plant Physiol 136:3266–3275
Emons AM, Mulder BM (2000) How the deposition of cellulose microfibrils builds cell wall architecture. Trends Plant Sci 5:35–40
Fry SC (1986) Cross-linking of matrix polymers in the growing cell walls of angiosperms. Annu Rev Plant Physiol 37:165–186
Fujino T, Sone Y, Mitsuishi Y, Itoh T (2000) Characterization of cross-links between cellulose microfibrils, and their occurrence during elongation growth in pea epicotyl. Plant Cell Physiol 41:486–494
Hayashi T (1989) Xyloglucans in the primary cell wall. Annu Rev Plant Physiol Plant Mol Biol 40:139–168
Hayashi T (1991) Biochemistry of xyloglucans in regulating cell elongation and expansion. In: Lloyd CW (ed) The cytoskeletal basis of plant growth and form. Academic, London, pp 131–144
Hörber JKH, Miles MJ (2003) Scanning probe evolution in biology. Science 302:1002–1005
Kataoka H (1982) Colchicine-induced expansion of Vaucheria cell apex. Alternation from isotropic to transversally anisotropic growth. Bot Mag Tokyo 95:317–330
Kirby AR, Gunning AP, Waldron KW, Morris VJ, Ng A (1996) Visualization of plant cell walls by atomic force microscopy. Biophys J 70:1138–1143
Kutschera U (1991) Regulation of cell expansion. In: Lloyd CW (ed) The cytoskeletal basis of plant growth and form. Academic, London, pp 149–158
Masuda Y (1990) Auxin-induced cell wall loosening. Bot Mag Tokyo 103:345–370
McCann MC, Wells B, Roberts K (1990) Direct visualization of cross-links in the primary plant cell walls. J Cell Sci 96:323–334
McCann MC, Wells B, Roberts K (1991) Complexity in the spatial localizeion and length distribution of plant cell-wall matrix polysaccharides. J Microsc 166:123–136
Mine I, Okuda K (2003) Extensibility of isolated cell walls in the giant tip-growing cells of the xanthophycean alga Vaucheria terrestris. Planta 217:425–435
Morris VJ, Gunning AP, Kirby AR, Round A, Waldron K, Ng A (1997) Atomic force microscopy of plant cell walls, plant cell wall polysaccharides and gels. Int J Biol Macromol 21:61–66
Morris VJ, Gunning AP, Kirby AR (2005) Atomic force microscopy for biologists. Imperial College Press, London
Mulder BM, Emons AM (2001) A dynamical model for plant cell wall architecture formation. J Math Biol 42:261–289
Nishitani K (1997) The role of endoxyloglucan transferase in the organization of plant cell walls. Int Rev Cytol 173:157–206
Okuda K, Matsuo K, Mizuta S (1990) Characteristics of the deposition of microfibrils during formation of the polylamellate walls in the coenocytic green alga Chamaedoris orientalis. Plant Cell Physiol 31:357–365
Park YW, Tominaga R, Sugiyama J, Furuta Y, Tanimoto E, Samejima M, Sakai F, Hayashi T (2003) Enhancement of growth by expression of poplar cellulase in Arabidopsis thaliana. Plant J 33:1099–1106
Parker BC, Preston RD, Fogg GE (1963) Studies of the structure and chemical composition of the cell walls of Vaucheriaceae and Saprolegniaceae. Proc R Soc B 158:435–444
Pesacreta TC, Carlson LC, Triplett BA (1997) Atomic force microscopy of cotton fiber cell wall surfaces in air and water: quantitative and qualitative aspects. Planta 202:435–442
Rose JKC, Braam J, Fry SC, Nishitani K (2002) The XTH family of enzymes involved in xyloglucan endotransglucosylation and endohydorolysis: current perspectives and a new unifying nomenclature. Plant Cell Physiol 43:1421–1435
Round AN, Kirby AR, Morris VJ (1996) Collection and processing of AFM images of plant cell walls. Microsc Anal 55:33–35
Round AN, Rigby NM, MacDougall AJ, Ring SG, Morris VJ (2001) Investigating the nature of branching in pectin by atomic force microscopy and carbohydrate analysis. Carbohydr Res 331:337–342
Shibaoka H (1991) Microtubules and the regulation of cell morphogenesis by plant hormones. In: Lloyd CW (ed) The cytoskeletal basis of plant growth and form. Academic, London, pp 159–168
Thimm JC, Burritt DJ, Ducker WA, Melton LD (2000) Celery (Apium graveolens L.) parenchyma cell walls examined by atomic force microscopy: effect of dehydration on cellulose microfibrils. Planta 212:25–32
Updegraff DM (1969) Semimicro determination of cellulose in biological materials. Anal Biochem 32:420–424
Acknowledgments
We thank Dr. Hironao Kataoka, Tohoku University, for the gift of the algal strains and are grateful to Drs. Kazuhito Nishimura and Hideki Sasaoka, Industrial Technology Center of Kochi Prefecture, Japan, for generously providing the facilities for atomic force microscopy observations. We also thank Dr. Andy Round, University of Bristol, for critical reading of the manuscript.
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Mine, I., Okuda, K. Fine structure of cell wall surfaces in the giant-cellular xanthophycean alga Vaucheria terrestris . Planta 225, 1135–1146 (2007). https://doi.org/10.1007/s00425-006-0424-8
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DOI: https://doi.org/10.1007/s00425-006-0424-8